See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/262454624

Fermented beverages with health-promoting potential: Past and future

perspectives

Article in Trends in Food Science & Technology · August 2014

DOI: 10.1016/j.tifs.2014.05.002

CITATIONS READS

353 11,286

4 authors, including:

Alan Marsh Colin Hill

University of North Carolina at Chapel Hill University College Cork
28 PUBLICATIONS 1,107 CITATIONS 825 PUBLICATIONS 68,088 CITATIONS

SEE PROFILE SEE PROFILE

Paul Cotter
TEAGASC - The Agriculture and Food Development Authority
643 PUBLICATIONS 41,225 CITATIONS

SEE PROFILE

All content following this page was uploaded by Alan Marsh on 12 April 2018.

The user has requested enhancement of the downloaded file.

 Trends in Food Science & Technology 38 (2014) 113e124

Review

Fermented
beverages with properties is indigenous to many regions of Asia, Africa,
Europe, the Middle East and South America. Evidence
from pottery vessels show that fermented rice, honey and
health-promoting fruit beverages date as far back as 7000 B.C. in China
(McGovern et al., 2004), and there is evidence of kombu-

potential: Past and cha manufacture dating back to approximately 220 B.C.
(Dufresne & Farnworth, 2000), while recent proteomic
analysis has shown kefir-like milk to have been fermented
future perspectives some 3500 years ago in Asia (Yang et al., 2014). While
many such beverages have for quite some time been noted
for their putative health-promoting attributes, this interest is
Alan J. Marsha,b,c, Colin Hillb,c, now being harnessed by modern biotechnological tech-
niques to develop the next generation of fermented func-
R. Paul Rossa,b and tional beverages.

Paul D. Cottera,b,*
The global functional beverage market is a growing
sector of the food industry as modern health-conscious
a
Teagasc Food Research Centre, Moorepark, Fermoy, consumers show an increasing desire for foods that can
Co. Cork, Ireland improve well-being and reduce the risk of disease. Fer-
b mented milks, especially yoghurt-style products, are the
Alimentary Pharmabiotic Centre, University College
most popular functional beverages with kefir in Western
Cork, Co. Cork, Ireland (e-mail: paul.cotter@teagasc.ie)
c
Europe and North America and ymer in Denmark being
School of Microbiology, University College Cork, good examples. Notably, the global functional food and
Co. Cork, Ireland drink market increased 1.5 fold between 2003 and 2010,
and is expected to grow a further 22.8% between 2010
Fermentation is an ancient form of food preservation, which and 2014 to be worth V21.7 billion (Leatherhead, 2011),
also improves the nutritional content of foods. In many regions with other estimates predicting the market will reach
of the world, fermented beverages have become known for V65 billion by the year 2016 (Companiesandmarkets,
their health-promoting attributes. In addition to harnessing 2013). Dairy-based produce account for approximately
traditional beverages for commercial use, there have recently 43% of the functional beverage market, and is mainly
comprised of fermented products (Ozer € & Kirmaci,
been innovative efforts to develop non-dairy probiotic fer-
mented beverages from a variety of substrates, including soy 2010). It is also intriguing to note that a number of food
milk, whey, cereals and vegetable and fruit juices. On the basis companies that have been under pressure, due to the poor
of recent developments, it is anticipated that fermented bever- public perception regarding the ‘healthiness’ of the foods
ages will continue to be a significant component within the they produce, are now focussing on developing such func-
functional food market. tional products.
In this article we review the literature regarding tradi-
tional fermented beverages with reputed health benefits,
and explore recent trends and developments in this field,
Introduction as well as areas for future research.
Societies throughout the world independently discovered
the value of fermenting food as a cheap means of preserva-
Natural fermented beverages: sources and microbial
tion, improving nutritional quality and enhancing sensory
composition
characteristics. The fermentation of milk, cereals and other
Naturally fermented milks
substrates to produce beverages with health-promoting
The yoghurt and fermented milks market is currently
worth V46 billion, with North America, Europe and Asia
* Corresponding author. accounting for 77% of the market. Many communities
0924-2244/$ - see front matter Ó 2014 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.tifs.2014.05.002
114 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124

across the world produce naturally fermented milks with naturally, and has been reported to contain fewer lacto-
many of these products being of a yoghurt-style consis- cocci. Shubat is a fermented camels milk popular in
tency. Fermented milk products can be made with milk Asia, also believed to have healing properties (Rahman,
(or skimmed milk) from various sources, including cow, Xiaohong, Meiqin, & Mingsheng, 2009). In Africa, fer-
camel, goat, sheep, yak and even coconut, milk, and can mented milk beverages are quite popular, where the art
be either pasteurised or unpasteurised. They can be pro- of making fermented products is passed down through
duced through the use of defined starter cultures, back- generations. Examples of such beverages include amasi
slopping or allowed to ferment naturally. Although fer- from Zimbabwe, kivuguto from Rwanda, suusac from
mented milk beverages are predominantly composed of lac- Kenya, nyarmie from Ghana and rob and garris from
tic acid bacteria (LAB), the exact microbial content may Sudan. Considering that most of these are derived from
vary depending on the source of milk, treatment of the the spontaneous fermentation of milk by its innate micro-
milk (e.g. pasteurisation), use of starters, the nature of the biota, it is likely that the fermented milks, although known
local environmental microbes present, temperatures, hy- by different names, are actually quite similar, and can be,
giene, the type and treatment of containers used and the in combination, referred to as naturally fermented milk
length of fermentation. Many artisanal fermented milk bev- (NFM) (Narvhus & Gadaga, 2003). Nonetheless, accurate
erages are produced as a result of back-slopping, whereby a categorization remains difficult in the absence of more
small portion of already-fermented milk is used to begin a detailed microbiological and biochemical analyses. Also,
new fermentation. In this way, cultures from the LAB natu- in many countries yoghurts are diluted with water to
rally present in the raw milk are passed from household to form drinkable fermented milk, such as doogh, ayran,
household and between generations. While the consump- chaas and lassi, with the resulting microbial composition
tion of spontaneously fermented milk is common to many generally being similar to that of yoghurt. The composi-
different regions, the exact microbial differences between tion and purported health benefits associated with fer-
these products have not been ascertained. Table 1 lists a mented dairy beverages can also be read about in a
number of the most popular and best-studied fermented recent review by Shiby and Mishra (2013).
beverages from around the world, along with information
with respect to their corresponding microbial compositions. Non-dairy fermented beverages
From this, the domination of milk-based beverages fer- Another important class of fermented beverages are
mented by LAB, mainly Leuconostoc, lactobacilli and lac- those made from cereals, which are popular in tropical re-
tococci, is clear. Fermentation in colder climates promotes gions and on the continent of Africa in particular. As with
the growth of mesophilic bacteria such as Lactococcus and many milk-based products, the natural microbial compo-
Leuconostoc, whereas beverages produced at higher tem- nent is used to ferment grains including maize, millet,
peratures usually have greater counts of thermophillic bac- barley, oats, rye, wheat, rice or sorghum. The grains are
teria such as Lactobacillus and Streptococcus. The often heated, mashed and sometimes filtered. Back-
contributions of slime-producing species or acetic acid pro- slopping is again quite common, but the microbial popula-
ducing species, generally present at low abundance relative tions responsible for the fermentation of these beverages
to Lactobacillus or Lactococcus species, vary depending on are not as well characterised.
abundance. There may also be significant numbers of coli- Boza, consumed in Bulgaria and Turkey, is generated
forms present, depending on the level of hygiene employed through the fermentation of a variety of cereals including
during preparation, with high levels having been noted in barley, oats, rye, millet, maize, wheat or rice, with the spe-
some African beverages (Gran, Gadaga, & Narvhus, cific composition affecting the viscosity, fermentability and
2003). The quantity and types of yeasts involved can vary content of the final beverage (Akpinar-Bayizit, Yilmaz-
greatly, but Candida and Saccharomyces are the species Ersan, & Ozcan, 2010). The cereal is boiled and filtered,
most commonly detected. a carbohydrate source is added, and the mixture can be
Of the many fermented milk beverages, kefir, a drink left to ferment independently or with the use of back-
that originated with shepherds in the Caucasian mountains slop. Boza has yet to be commercialised and studies have
has been a notable success, gaining worldwide popularity, revealed that the microbial population varies. The function
with the market now worth V78.7 million in North Amer- of the yeast present, which is only sometimes detected, re-
ica alone (Lifeway, 2014). The microorganisms respon- mains unknown. Of several combinations, it has been sug-
sible for the fermentation are actually a symbiotic gested that fermentation by Saccharomyces cerevisiae,
combination of bacteria and yeast, bound within a poly- Leuconostoc mesenteroides and Lactobacillus confusus pro-
saccharide matrix, known as kefir ‘grains’. Koumiss, duce the most palatable beverage (Zorba, Hancioglu, Genc,
sometimes known as airag, is a popular beverage of Karapinar, & Ova, 2003).
nomadic cattle breeders in Asia and some regions of Togwa, a sweet and sour, non-alcoholic beverage, is one
Russia. This beverage is similar to kefir, but there is no of the better studied African cereal beverages. Produced
solid inoculation matrix, and this milk is fermented by from the flour of maize, sorghum and finger millet and,
back-slopping or by allowing the milk to ferment sometimes, cassava root, the chosen substrates are boiled,
 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124 115

Table 1. A compilation of various milk, cereal and other fermented beverages popular around the world, with their corresponding microbial
populations and substrates.

Product Substrates Region Microflora

Amasi Milk (cow, various) Africa (Zimbabwe) Lactococcus (L. lactis), Lactobacillus, Leuconostoc, Enterococcus.
Uncharacterised fungal component
Aryan Milk (cow, various) Turkey LAB: Lactobacillus bulgaricus, Streptococcus thermophilus
Garris Milk (camel) Africa (Sudan) Bacteria: Lactobacillus (Lb. paracasei, Lb. fermentum and Lb. plantarum),
Lactococcus, Enterococcus, Leuconostoc. Uncharacterised fungal
component
Kefir Milk (cow, various) Eastern Europe Bacteria: Lactococcus, Lactobacillus, Leuconostoc, Acetobacter;
(Caucasian region) Yeast: Naumovozyma, Kluyveromyces, Kazachstania
Kivuguto Milk (cow) Africa (Rwanda) LAB: Leuconostoc (Leu. mesenteroides, Leu. pseudomesenteroides)
and L. lactis. Uncharacterised fungal component
Koumiss/Airag Milk (horse) Asia/Russia LAB: Lactobacillus; Yeast: Kluyveromyces, Saccharomyces and
Kazachstania
Kumis Milk (cow) South America Bacteria: Lb. cremoris, L. lactis, Enterococcus (E. faecalis, E. faecium);
(Columbia) Yeast: Galactomyces geotrichum, Pichia kudriavzevii, Clavispora
lusitaniae, Candida tropicalis
Nyarmie Milk (camel) Africa (Ghana) LAB: Leu. mesenteroides, Lb. bulgaricus, Lb. helveticus, Lb. lactis,
Lactococcus lactis; Yeast: Saccharomyces cerevisiae
Rob Milk (unspecified) Africa (Sudan) LAB: Lb. fermentum, Lb. acidophilus, L. lactis, Streptococcus salivarius;
Yeast: Saccharomyces cerevisiae, Candida kefyr
Suusac Milk (unspecified) Africa (Kenya) LAB: Leu. mesenteroides, Lactobacillus (Lb. plantarum, Lb. cruvatus,
Lb. salivarius, Lb. Raffinolactis); Yeast: Candida krusei, Geotrichum
penicillatum, Rhodotorula mucilaginosa
Shubat Milk (camel) China Bacteria: Lactobacillus (Lb. sakei, Lb. Helveticus, Lb. brevis) Enterococcus
(E. faecium, E. faecalis), Leu. lactis and Weissella hellenica;
Yeast: Kluyveromyces marxianus, Kazachstania unisporus, and Candida
ethanolica
Amazake Rice Japan Fungi: Aspergillus spp
Boza Various (barley, oats, Balkans LAB: Leuconostoc (Leu. paramesenteroides, Leu. sanfranciscensis,
rye, millet, maize, (Turkey, Bulgaria) Leu. mesenteroides), Lactobacillus (Lb. plantarum, Lb. acidophilus,
wheat or rice) Lb. fermentum); Yeast: Saccharomyces (S. uvarum, S. cerevisiae), Pichia
fermentans, Candida spp.
Bushera Sorghum, millet flour, Africa (Uganda) Bacteria: Lactobacillus, Streptococcus, Enterococcus. Uncharacterised
fungal component
Koko Cereal (pearl millet) Africa (Ghana) Bacteria: Weissella confusa, Lb. fermentum, Lb. salivarius, Pediococcus
Sour Water spp. Uncharacterised fungal component
Kvass Rye bread, rye Russia LAB: Lb. casei, Leu. mesenteroides; Yeast: Saccharomyces cerevisiae
and barley malt/flour,
Mahewu Maize, sorghum/millet Africa (Zimbabwe) Unknown
Pozol Maize Mexico (Southeast) Bacteria: L. lactis, Streptococcus suis, Lactobacillus (Lb. plantarum,
Lb. casei, Lb. alimentarium, Lb. delbruekii), Bifidobacterium,
Enterococcus. Uncharacterised fungal component
Togwa Maize flour, finger Africa (Tanzania) LAB: Lactobacillus spp.; Yeast: Saccharomyces cerevisiea, Candida spp.
millet malt,
Hardaliye Grapes/mustard Turkey LAB: Lactobacillus spp. Uncharacterised fungal component
seeds/cherry leaf
Kombucha Tea China, Worldwide Bacteria: Gluconacetobacter (G. xylinus), Acetobacter, Lactobacillus;
Yeast: Zygosaccharomyces, Candida, Hanseniaspora, Torulaspora, Pichia,
Dekkera, Saccharomyces
Water Kefir Water/sucrose Mexico, Worldwide Bacteria: Lactobacillus (Lb. casei, Lb. hilgardii, Lb. brevis, Lb. plantarum),
L. lactis, Leu. mesenteroides, Zymomonas; Yeast: Dekkera (D. anomola,
D. bruxellensis), Hanseniaspora (H. valbyensis, H. vineae)
Saccharomyces cerevisiae, Lachancea fermentati, Zygosaccharomyces
(Z. lentus, Z. florentina)

cooled and fermented for approximately 12 h to form a germinated or non-germinated sorghum grains, and fer-
porridge, which is then diluted to drink (Kitabatake, mented for 1e6 days (Muyanja, Narvhus, Treimo, &
Gimbi, & Oi, 2003). Mahewu is similar in that maize or Langsrud, 2003). These beverages are often used to wean
sorghum meal is fermented with millet or sorghum malt, children, and as a high-energy diet supplement. Koko
and is available commercially (Mugochi, Mutukumira, & sour water is the fermented liquid water created in the pro-
Zvauya, 2001). Bushera is generally prepared from duction of the fermented porridge, koko. This contains a
116 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124

high portion of LAB and is used by locals to treat stomach is thought to have antioxidant properties (Amoutzopoulos
aches and as a refreshing beverage (Lei & Jakobsen, 2004). et al., 2013).
Kvass is a fermented rye bread beverage common in
Russia, which has seen much commercial success. The Health benefits
beverage can have a sparkling, sweet or sour, rye bread Originally devised as a means of food preservation, over
flavour. Its alcohol content, though usually low, can vary, time many beverages, such as kefir and koumiss, became
and has been suggested as a contributor to alcoholism popular due to their reputed abilities to improve gastroin-
(Jargin, 2009). Amazake is a sweet fermented rice beverage testinal health (Metchnikoff & Metchnikoff, 1908;
that is the non-alcoholic precursor to sake, produced in Saijirahu, 2008). However, most of the traditional fer-
Japan. Steamed rice is mixed with rice-koji (Aspergillus- mented beverages are poorly studied, with unsubstantiated
mycelia and rice) and water, and is heated to 55e60  C claims linking them to positive effects on human health.
for 15e18 h. Enzymes breakdown the rice and form Ideally, any such beverage making health claims should
glucose content of approximately 20%. Amazake is highly be backed by credible scientific evidence in the form of
nutritious and is consumed for its purported health benefits randomised, controlled and replicated human intervention
(Yamamoto, Nakashima, Yoshikawa, Wada, & Matsugo, trials. This form of evidence is rare for these beverages
2011). Pozol, which is common to south-eastern Mexico, (and particularly so for non-dairy forms), and the genera-
has quite a different method of production, in that maize tion of such data is an expensive and unappealing prospect
grains are heat-treated in an acid solution, ground and for industry, but nonetheless remains a critical area for
shaped into dough balls. These are then wrapped in banana proof-of-concept and future research. Despite this, howev-
leaves and fermented for 2e7 days, after which they are re- er, there is still a perception that many of these beverages
suspended in water and consumed as beverages. Pozol is are “healthy”, particularly in societies where the beverage
composed of a variety of microorganisms including LAB, is steeped in local tradition, which in turn contributes to
non-LAB, yeasts and other fungi (Ben Omar & Ampe, their market potential and justifies investing in related
2000). research.
In addition to milk and cereal-based fermentations, there For many of the fermented beverages, it is the strong as-
are also other forms of fermented beverages. One example sociation between the microbial content and improvement
is kombucha, which is a fermented sweetened tea that was of gastrointestinal health that is thought to be responsible
originally popular in China but is now enjoyed worldwide, for perceived health outcomes. While it is sometimes un-
and is set to be worth V363 million by 2015 in North clear what functional characteristics traditional beverages
America (BevNet, 2011). It is fermented by a symbiotic confer beyond the basic nutrition of the raw unfermented
mixture of bacteria (typically acetic acid bacteria, with ingredients, there is evidence that some fermented bever-
small quantities of LAB) and yeast, which are embedded ages provide beneficial effects through direct microbial/
within a cellulosic matrix that floats above the fermentate, probiotic action and indirectly via the production of metab-
similar to the mother cultures of vinegar. Due to the high olites and breakdown of complex proteins. Nonetheless,
acid content (as low as pH2), the functionality of kombucha natural fermented milks have been shown to have antihy-
is predominantly due to its physiochemical properties pertensive effects, enhance systemic immunity, lower
(Greenwalt, Steinkraus, & Ledford, 2000). As a result of cholesterol and to help lower blood pressure. In recent hu-
the tea content, it also contains a number of phenols and vi- man trials, they have been shown to aid in the treatment of
tamins (Dufresne & Farnworth, 2000). Water kefir is IBS and to help alleviate constipation (Tabbers et al.,
similar in concept to milk kefir in that it is fermented by 2011). Additionally, they have been shown to have modula-
a symbiosis of bacteria and yeast contained within grains. tory effects on the brain, and demonstrate anti-cancer po-
However, these grains are composed of dextran, are trans- tential (Kumar et al., 2012; Tillisch et al., 2013). Of the
lucent and crystal-like in appearance, and are thought to traditional-style beverages, kefir specifically has been
have originated in Mexico where they formed as hard gran- shown to positively impact the gastrointestinal tract, stimu-
ules fermented from sap on the pads of the Opuntia cactus. late the immune system, and have anti-inflammatory and
They ferment sweetened water, to which figs and lemon are anti-carcinogenic effects, albeit not through clinical trials
traditionally added for additional flavour and nutrients. The (De Oliveira Leite et al., 2013). Lactic fermented milks
composition of water kefir can vary, but is known to contain often contain compounds not present in regular milk,
LAB, including Lactobacillus, and Bifidobacterium such as exopolysaccharides, e.g. kefiran in kefir, and natural
(Laureys & De Vuyst, 2014). Hardaliye is a non- enrichments, including increased vitamin (e.g. B12 and
alcoholic, Turkish, fermented beverage made from red K2), folate and riboflavin content (Hugenholtz, 2013).
grapes, black mustard seeds, cherry leaf and benzoic acid. Furthermore, fermented dairy products usually possess b-
Ingredients are pressed and fermented for 5e10 days at galactosidase activity and a reduced lactose content
room temperature. Again, the microbial population has compared to milk, making them potentially suitable for
been reported to be predominantly composed of Lactoba- those suffering from lactose intolerance. Fermented pro-
cillus and unknown fungal components, and this beverage duce can also be a source of bioactive peptides, released
 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124 117

through fermentation by proteolytic cultures, and have been are naturally fermented, and thus subject to environmental
linked with many potential health benefits including diges- influences, their microbiota can differ significantly, but the
tive, endocrine, cardiovascular, immune and nervous sys- application of reliable technology can help definitively
tem affects. identify a core population (or lack thereof), responsible
The occurrence of organic acids, which lower the pH of for characteristic traits of the beverage in question. While
the beverages, may also confer health benefits. Indeed, the some molecular-based, microbial characterisation of these
presence of glucuronic acid, one of the primary metabolites beverages has taken place, most studies have relied on
in kombucha, is believed to improve detoxification by bind- low-throughput approaches, employing techniques such as
ing toxin molecules and aiding excretion through the kid- DGGE, which can only assess 1e2% of a population
neys, and it is this acidic composition that is most (Muyzer, de Waal, & Uitterlinden, 1993).
associated with the reputed health properties of kombucha, Moving forward, the availability of molecular technolo-
rather than a microbial-gut interaction (Wang et al., 2014). gies such as culture-independent, high-throughput,
Kombucha also contains increased B vitamins and folic sequencing-based microbial analyses, metabolomics and
acid in addition to a number of healthy components, such bioinformatics will prove particularly useful, and will pro-
as phenols, naturally present in tea (Dufresne & vide a more accurate picture of these populations, sur-
Farnworth, 2000). Acid content, in conjunction with anti- mounting problems associated with relying on
microbials often produced by bacteria, could result in the phenotypic-based approaches. In-depth molecular studies
beverage possessing therapeutic, antimicrobial properties. have the potential to be particularly useful when carrying
Fermented cereals can also contain a high mineral con- out analyses across different beverages with a view to
tent, and generally have a lower fat percentage than their attributing specific desirable or non-desirable sensory and
dairy-based counterparts, but grains are generally lacking organoleptic characteristics with specific microorganisms
in essential amino acids. These forms of beverages can present (Marsh, O’Sullivan, Hill, Ross, & Cotter, 2013).
also naturally provide plant-based functional components, Such approaches will also ultimately facilitate accurate
such as fibre, vitamins, minerals, flavonoids and phenolic species identification, leading to novel starter design, and
compounds, which can effect oxidative stress, inflamma- the development of beverages with different and complex
tion, hyperglycemia and carcinogenesis (Wang, Wu, & flavour profiles. It will also be possible to more effectively
Shyu, 2013). As previously mentioned, fermented foods monitor the change of proportions of different species
are particularly common in Africa, where palates are accus- throughout fermentation and storage (Cocolin,
tomed to sour foods. Providing a safe, fermented cereal Alessandria, Dolci, Gorra, & Rantsiou, 2013). Future
beverage with reliable probiotic cultures could help reduce studies will also shed light on the nature of the symbiosis
diarrhoea and malnutrition caused by contaminated tradi- of such beverages, which is so complex that in vitro synthe-
tional beverages used in weaning children, and help reduce sis of kefir grains has yet to be replicated. Currently, com-
fatalities and improve well-being (Motarjemi, K€aferstein, mercial kefir is produced by defined starters, with probiotic
Moy, & Quevedo, 1993). strains added to some products to boost reputed health
Despite the need for definitive studies demonstrating claims.
direct health benefits on consumers, in vitro and animal
studies give reason to be optimistic. In many cultures, Health-promoting microbes
alleged health benefits are the reason for consumption, As noted above, it is widely believed that the primary
and if there are indeed health benefits to be gained from reason for the functionality of these beverages is due to
consuming fermented beverages, it is most likely the result the presence of specific live microorganisms. To the con-
of a synergistic effect between substrates, delicate microbi- sumer, health claims are more important than nutritional
al content and microbial end products, the relationship be- claims (Verbeke, Scholderer, & L€ahteenm€aki, 2009), so
tween which should become clearer with further research. there has and will be a desire to augment the health-
promoting potential of these beverages through the addition
Beyond physiochemical advantages: from microbial of certified probiotics. The probiotic market was worth
content to functionality V15.7 billion in 2010, and is expected to increase to
Molecular-based microbial characterisation V22.6 billion by 2015 (BCC Research, 2011). The WHO/
Despite health claims linked to the microbial composi- FAO defines probiotics as “live microorganisms, which
tion of fermented beverages, there is a considerable lack when administered in adequate amounts confer a health
of analyses relating to the microorganisms present and benefit on the host”, and the probiotic sector is the largest
the quantities in which they exist in such beverages. In or- component of the functional food market. The physiology
der to address this, it is necessary for the application of un- of certain strains of lactobacilli and bifidobacteria make
biased, standardised techniques to assess beverages from them well-suited to both the gastrointestinal and milk envi-
different geographical regions, and to reach a consensus ronments, and thus lactic acid bacteria and bifidobacteria
on the definition of microorganisms which constitute part are the most studied and utilised probiotic organisms. It
of any particular beverage. Since many such beverages is generally considered that a minimum of 109 cells per
118 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124

daily dose are required for probiotics to be effective contribute to the final composition of the product by produc-
(Forssten, Sindelar, & Ouwehand, 2011). Within the EU, ing ethanol and carbon dioxide (Viljoen, 2001). In particular,
the term “probiotic” is now considered a health claim, studies have demonstrated that yeast can exert a positive ef-
with strict criteria surrounding its use and resulting in fect on the abundance of Lactobacillus in fermented environ-
many applications submitted to the European Food Safety ments (Gadaga, Mutukumira, & Narvhus, 2001), and this
Authority (EFSA) being rejected (Guarner et al., 2011). might be a key function in such symbioses, as well as pre-
In Europe, boosting numbers of Lactobacillus and Bifido- venting the proliferation of undesirable species. While yeast
bacterium in the gut is not deemed to be of sufficient merit only comprise <0.1% of the gut microbiota, they are 10
to be considered a health benefit; the link must be made to a times larger than prokaryotes and can thus impede colonisa-
physiological (e.g. strengthening the immune system or tion of pathogenic bacteria (Czerucka, Piche, & Rampal,
resistance to infections) benefit to the host. Proving such 2007). Success has been made in incorporating them in com-
health claims is expensive, and in the midst of unclear def- mercial fermented milk products, but excessive gas produc-
initions and guidelines, industries are currently more likely tion during storage can be an issue. Some species of
to develop and market probiotic products in other parts of Saccharomyces and Candida yeasts are common to both fer-
the world (Katan, 2012). In situations where probiotic mented beverages and the gut microbiota, such as species,
strains are added during fermentation, they must not and could be investigated with a view to their contribution
interact antagonistically with starter strains. This becomes to fermentations and optimising health-promoting potential.
less of an issue if strains are added after fermentation is However, to date, Saccharomyces boulardii is the only recog-
complete, due to the low metabolic rates at refrigerated nised probiotic yeast.
temperatures. Additionally, microencapsulation technology
may aid in the delivery of probiotic strains by protecting Rational design of starter cultures
them in non-native environments. In one instance, microen- The selection of appropriate starter strains will be key in
capsulation of Bifidobacterium successfully increased efforts to accurately reproduce the desirable characteristics
viable numbers in mahewu, without significantly impacting of traditional health-promoting beverages for mass produc-
on flavour, suggesting it could be an effective probiotic de- tion (Fig. 1). To faithfully reproduce these beverages and
livery system (McMaster, Kokott, Reid, & Abratt, 2005). traits, microbes should be sourced from the traditional fer-
A health-related role for the yeast in fermented beverages mented beverages, given that these microbes have adapted
has yet to be elucidated. The volume of studies reporting sig- over thousands of years to their respective environments,
nificant numbers of yeast in traditional fermented beverages and are more likely to function at the appropriate pH, salt
indicates their importance in these fermentations. Yeasts in concentration, temperature etc. For instance, amylolytic
dairy generate desirable aromatic compounds, proteolytic digestion of starch could be considered desirable for fer-
and lipolytic activities and can aid bacterial growth by pro- mented cereal production, and isolates from boza and pozol
ducing amino acids, vitamins and other metabolites, and have been shown to be capable of this metabolic trait. Such
Considerations

Metabolites
Lactose
Ethanol Market Health Benefits
Carbon Dioxide Consumer Acceptance Cholesterol Lowering
Organic Acids Gastrointestinal Relief
Scientific Claims
Vitamins Probiotics
Geography
Minerals Nutrient Content
History
Bioactive Peptides Immune Stimulation
Competition
Antimicrobials Others

Substrates Starter
Formulation
Selection

Milk
Soy Beverage Multistrain
Cereal Probiotic vs Qualitative
Tea Fermentation Lactobacillus
Whey Lactococcus
Juice Bifidobacterium
Others Others

Addition Monitor
Production

Fibre pH
Vitamin
Process/Control
Ethanol
Mineral Carbohydrates
Organic acids
Oil Pasteurisation
Volatile compounds
Polyphenols Homogenisation
Storage
Sterols Acidity
Sensory Evaluation
Minerals Oxygen
Probiotics

Fig. 1. An overview of the interlinked processes and considerations in fermented beverage production and development.
 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124 119

populations also have a history of safe human consumption. 28% per year (Leatherhead, 2011). Consumers’ willingness
Rational strain selection to produce the correct balance of to pay a premium price for fortified products is also a key
flavour, aroma, texture, acidification, bitterness, speed of driver for innovation. While most current functional bever-
fermentation, and the optimum quantity of organic acid, vi- ages are aimed at the high-income consumer, there is an
tamins and minerals is essential, as beverages that are too argument to be made that those who would benefit most
sour or bitter, or contain too much ethanol, will not meet from fermented beverages are from underdeveloped na-
consumers’ approval. Over recent years, genetic tools tions, where such beverages could provide a cost-effective
have become available to engineer and select superior means of delivering much-needed nutrition (Van Wyk,
starter strains, but legislation currently hinders their indus- Britz, & Myburgh, 2002).
trial use (Hansen, 2002). The inclusion of strains producing
antimicrobials, such as bacteriocins, could serve as natural Substrate exploration
preservatives and help produce a more natural product, The US, Europe and Japan markets account for over
while sequential fermentation with yeast, followed by bac- 90% of total functional foods, with the majority being func-
teria, could produce a beverage with the desired physio- tional dairy products. However, non-dairy probiotic deliv-
chemical effects, but without biostabilisation issues ery has been attracting more attention in recent years,
created by excessive gas production (Kwak, Park, & Kim, partly due to the success of bio-functional foods and the
1996). desire to expand and provide an alternative probiotic choice
As stated above, the natural fermentation of beverages to conventional dairy-based beverages. Indeed, this market
involves many different strains of bacteria, and sometimes, is projected to have an annual growth rate of 15% between
yeast. There is an understandable tendency to keep starter 2013 and 2018 (Marketsandmarkets, 2013). Non-dairy pro-
formulations simple but, as traditional beverages show, biotic beverages are particularly attractive due to their lack
there are often multiple strains involved, including different of dairy allergens, low cholesterol content and vegan-
species or even microorganisms. From a health perspective, friendly status (Prado, Parada, Pandey, & Soccol, 2008).
multistrain or multispecies probiotic beverages may pro- Furthermore, different substrates can provide different
vide greater beneficial effects than monostrain cultures. Un- combinations of antioxidants, dietary fibre, minerals and
fortunately, however, there is a lack of studies assessing the vitamins.
effects of combining several natural strains on the physio- To this end, cereal-based beverages could be marketed in
chemical and sensory characteristics of milk or other func- response to consumers’ awareness of the benefits of high
tional beverages. Without such information, it is difficult to fibre diets. They contain natural prebiotic traits due to the
accurately reproduce the characteristics of the organic presence of indigestible fibres and the presence of diacetyl
beverage with one produced by a defined combination of acetic acid aromatic compounds make them palatable, and
starters, to match the flavour and properties of the original. furthermore, could be cheaper to produce. Oats, a major
This is crucial when marketing beverages to consumers source of beta-glucan which can reduce LDL-cholesterol,
already familiar with the artisanally produced variant of are known to function as a prebiotic by boosting bifidobac-
the product, and if wishing to retain any health-promoting teria numbers in the gut (M artensson et al., 2005), and have
characteristics attributed to the original product. been investigated with a view to producing synbiotic bever-
In spite of the wide range of options available when ages. Indeed, a fermented oat drink with two Bifidobacte-
designing novel health-promoting fermented beverages, rium longum strains was shown to normalise bowel
there will always be an attraction for healthy foods derived movements in elderly patients (Pitkala et al., 2007). Malt
from natural processes. Applying the solid inoculation and barley have also been used as beverage substrates
matrices of traditional fermented beverages to new sub- (Rathore, Salmeron, & Pandiella, 2012), while emmer, an
strates provides a means of generating new beverages while ancient European cereal has also shown potential as a func-
retaining natural microbial populations. For example, kefir tional cereal beverage (Coda, Rizzello, Trani, & Gobbetti,
grains have been employed to produce whey and cocoa 2011).
pulp beverages containing potentially health-promoting There has also been a positive trend towards the con-
strains (Londero, Hamet, De Antoni, Garrote, & sumption of soy products, as evident in worldwide soy
Abraham, 2012; Puerari, Magalh~aes, & Schwan, 2012). food sales, which increased from V218 million to almost
Similarly, the cellulosic pellicle of kombucha has been suc- V2.9 billion between the years 1992 and 2008, and con-
cessfully used to ferment milk and other substrates tinues to increase (Granato, Branco, Nazzaro, Cruz, &
(Malbasa et al., 2009). Faria, 2010). Soy-based beverages contain low cholesterol
and low saturated fats, are lactose-free, are rich in isofla-
Biotechnology and beverage development vones and antioxidants, and have been shown to exert bene-
Expanding technological capabilities, especially ingre- ficial effects on the host. Soy milks are capable of
dient exploration and development, has led to increased fermentation by probiotic strains and, when fermented by
functional product innovation. The number of new products Bifidobacterium and Lactobacillus, have been shown to
with functional claims has been growing by approximately have a positive impact on the ecosystem of the intestinal
120 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124

tract (Cheng et al., 2005). Positive consumer attitudes to- vegetable juices with fermented milks as natural flavour-
wards soy have encouraged industry to develop probiotic ings to overcome undesirable flavours in otherwise prom-
derivatives with several varieties already available commer- ising beverages/products. To this end, the inclusion of
cially (Haelan951Ò and JivaÔ). sensory panel evaluations provides invaluable information
The utilisation of waste products to generate functional regarding consumer acceptance, especially for non-dairy
beverages has seen increased interest, with whey being products which are intrinsically more difficult to sell than
the most prominent example. Whey is a by-product of the their dairy counterparts. The use of direct liquid inoculation
cheese industry, which retains 55% of milk nutrients and systems to include probiotics while avoiding fermentation
contains only 0.36% fat, and has the potential for further side-effects has its own problems in ensuring cell viability
use in the human diet. In an effort to add value to whey, and stability during storage.
numerous studies have investigated its fermentation by lac-
tic acid bacteria (Streptococcus and Lactobacillus) to pro- Fermentation parameters
duce a lactic probiotic beverage, and probiotic bacteria In addition to the importance and ratio of starter selection,
have already demonstrated good survival in whey as already described, the fermentation of potentially health-
(Drgalic, Tratnik, & Bozanic, 2005). Prebiotics have also promoting beverages needs to be carefully controlled to
been successfully incorporated, including oligofructose achieve stability, sensory and safety standards. Changes in
and inulin, and hydrocolloid thickening agents added to the concentration of sugars and other compounds need to
improve viscosity and mouthfeel (Gallardo-Escamilla, be carefully monitored both during and after fermentation,
Kelly, & Delahunty, 2007). and is particularly important with respect to the production
One of the most exciting developments is the develop- of ethanol and carbon dioxide. Sensitive techniques,
ment of fruit juices, which have been shown to have consid- including high performance liquid chromatography
erable market value and consumer acceptance (Sun- (HPLC) and gas chromatography (GC), are now routine
Waterhouse, 2011). Already considered a healthy food for such analyses. Antioxidant levels may also be measured
product, fruit juices are often fortified with vitamins and by ferric reducing ability of plasma (FRAP) and 2,2-
minerals, in addition to having a high nutrient and antioxi- diphenyl-1-picrylhydrazyl (DPPH) assays. pH is obviously
dant content, and represent a new method of nutrient and crucial to the success of a fermentation and can be lowered
probiotic delivery. As an increasing number of studies are to a specified level prior to fermentation to encourage enzy-
demonstrating, sugars naturally present in juices can facil- matic activity and prevent contamination. The concentration
itate the growth of cultures with appealing taste profiles. of oxygen in the brewing environment can also be important
This is true of tomato, pomegranate, pineapple, orange depending on the homo- or hetero-fermentative nature of the
and cashew-apple juice. These microbes can impact on cultures. Metabolic engineering of fermenting microorgan-
physiochemical aspects, such as increasing the concentra- isms may eventually be accepted to boost concentrations
tions of flavanones and carotenoids in orange juice, and of desirable compounds in the final products. Other factors
have shown good survival rates during storage of the bever- to be considered include the choice of substrates, particularly
ages. While the final content of such beverages are quite the types and concentrations of carbohydrates, and the treat-
acidic and best suited to fermentation by probiotic Lactoba- ment of raw ingredients such as cereals, by homogenisation,
cillus species (Lactobacillus casei, Lactobacillus acidophi- for example, can allow for more effective metabolism and
lus, Lactobacillus plantarum, Lactobacillus paracasei and release of bioactive peptides. The time and intensity of
Lactobacillus delbrueckii), the use of microencapsulation heat during pasteurisation need to be considered. The addi-
technology could aid in the delivery of other viable probi- tion of certain compounds, such as ascorbic acid and Na-
otic microorganisms (Champagne & Fustier, 2007). The FeEDTA, can encourage the release by fermentation of
enrichment of juices with brewer’s yeast autolysate before bioactives, such as, zinc and iron, in the final beverage.
fermentation positively impacts on the nutritional content Conversely, the concentration of phytic acid, an inhibitor
of the final beverage, raising the feasibility of co- of mineral absorption, particularly with regards to cereals,
fermentation by the right combination of bacteria and yeast could lower the mineral impact of the final beverage, and
(Priya & Munishamanna, 2013). Examples of commer- the inclusion of phytases might be necessary to ensure or
cially available probiotic-containing fruit juices include augment health claims. The concentration of bulk starch
BiolaÒ and BioprofitÒ. Similar microorganisms have also and other factors will impact the consistency of the final
been shown to successfully ferment various vegetable jui- drink, providing either a thin and free-flowing product or a
ces including cabbage, beet, pumpkin, courgette and carrot thicker beverage with a smoothie-like consistency. Natural
juices supplemented with prebiotics (Martins et al., 2013). antimicrobials, such as bacteriocins, may be included to
The major challenge with any substrate/culture combi- act as preservatives and prevent the growth of spoilage or-
nation is to overcome the sensory hurdles of sour, acidic ganisms. As microbes, particularly yeast, continue to grow
fermentates, and produce a palatable beverage that would following storage, packaging must be able to withstand the
realistically be consumed regularly to avail of functional pressure generated as a consequence of gas production,
benefits. There exists the option of combining fruit or with either plastic or glass containers. Additionally, viability
 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124 121

during storage needs consideration, particularly for cereal- further extensive sensory, physical and chemical character-
type beverages that would traditionally be stored at room isation to develop a palatable flavour profile and viable
temperature. product.
Clearly, there a number of parameters and variations that In terms of traditional fermented beverages, there is still
need to be measured, controlled and experimented with to a great deal to be understood. First and foremost, there
determine the optimum conditions for fermentation, and needs to be a consensus with respect to what constitutes
proven to be consistent following up-scaling. Automated the natural microbiota of specific beverages, a description
processes such as controlled nutrient availability and stir- of which are essential for fermentation, and the contribu-
ring can influence efficiency of the fermentation. Ongoing tion of each microbe to the final beverage composition.
research into community analysis and fermentation Also important is the characterisation of the relationship
biochemistry will inform future decisions regarding the between microorganisms, particularly between bacterial
control of processes for these types of fermentations. and yeast populations. The influence of containers, sub-
strates, metabolites and enhancements on the organoleptic
Beverage enhancement qualities and fermentation kinetics need to be evaluated.
There are now a variety of enhancements that can be made Fortunately, technology is advancing such that sensitive
to both traditional and novel beverages to boost health techniques can now be used in an increasingly cost-
claims. Prebiotics, including fructooligosaccharides, inulin effective manner to provide greater insight.
and galactooligosaccharides, are often added commercially Critically, there is increasing pressure to identify and
to fermented milks to promote the growth of favourable bac- confirm proposed health claims for the consumer. The
teria (Huebner, Wehling, & Hutkins, 2007), while investiga- role of traditional beverages in the future of the fermented
tions of other prebiotics such as oligofructose and beverage industry may be to inspire the development of
polydextrose have also yielded positive results (Oliveira new products (and assess a country’s willingness to accept
et al., 2009). In addition to preventing and treating a product), whereby it is easier to develop simple, novel
intestinal-associated diseases, the incorporation of bio- beverages and directly evaluate the functional and sensory
active nutraceuticals such as u-3 fatty acids, isoflavones properties in controlled fermentations with minimum vari-
and phytosterols in fermented milks also have potential ap- ables. Indeed, this is a key hurdle in the marketing of
plications (Awaisheh, Haddadin, & Robinson, 2005). Isofla- such products, especially in light of increasing awareness
vones are powerful antioxidants, comparable to vitamin E, amongst consumers and the emergence of strict legislation.
while plant-derived phytosterols are cholesterol-lowering Considering the costs of development and clinical trials,
agents. Addition of such compounds, however, can be innovation in the functional food market may need to
complicated as u-3 fatty acids are sensitive to light, air become a collaborative effort between industry partners
and heat, and can cause undesirable flavours in the end prod- and academia (Khan, Grigor, Winger, & Win, 2013). None-
uct, while isoflavones and phytosterols have poor solubility theless, this is an exciting time for beverage development.
in water, and might be difficult to incorporate into non-fat so- Advances in probiotic (including yeast species) discovery
lutions. u-3 fatty acids can now be microencapsulated to and characterisation will advance the possibilities for health
hide fishy off-notes. claims and starter design. The milk sector has already seen
A variety of vitamins and minerals may be added, great success in this regard, and as probiotics are intrinsi-
including vitamins D, E and C, calcium and magnesium, cally linked to the health claims of many beverages it is nat-
while fortification of fermented milks with iron was shown ural to assume this will extend to other varieties of
to improve the growth of preschool children (Silva, Dias, beverages to hit the market, with success already seen
Ferreira, Franceschini, & Costa, 2008). Microorganisms with probiotic soy beverages, and exciting developments
can also provide functional metabolites, which has encour- with juice beverages. This is particularly true as the impor-
aged the screening of ecological niches, such as marine en- tance of gut health to our well-being becomes increasingly
vironments, in addition to the previously referred to gut- apparent. As our knowledge and discovery of probiotics in-
derived probiotics, for novel nutraceuticals, the likes of creases, so too will the need for alternative means of probi-
which may eventually be incorporated into functional bever- otic delivery. Additionally, as research into the fermentation
ages (Dewapriya & Kim, 2013). Finally, it may be necessary of waste and by-products products (e.g. whey) continues,
to combat or mask resulting undesirable flavours and aromas there is the potential for a significant environmental impact.
arising from the addition of functional ingredients, using As developed society becomes more health-conscious,
flavour enhancers (e.g. fruit flavours or spearmint) and natu- particularly in response to the growing obesity epidemic,
ral or artificial sweeteners. the market for functional food appears to be in a long-
term, sustainable trend (Bigliardi & Galati, 2013), with
Conclusions and future prospects for fermented beverages constituting a substantial share of this market.
beverages Aside from marketing to health-conscious (and high-
Most of the beverages described in this review are still in income) consumers, there is evidence that functional bever-
the early stages of commercial development, and require ages could function as a therapeutic product, particularly as
122 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124

a means of delivering nutrition to, and improving the health BCC Research. (2011). The probiotics market: Ingredients,
of, malnourished populations. This medicinal impact may supplements, foods. BCC Research.
Ben Omar, N., & Ampe, F.. (2000). Microbial community dynamics
also be augmented by the growing field of nutraceuticals, during production of the Mexican fermented maize dough pozol.
addition of cholesterol-controlling factors, and in terms of Applied and Environmental Microbiology, 66, 3664e3673. http://
probiotics, the alleviation of intestinal discomfort and aid- dx.doi.org/10.1128/AEM.66.9.3664-3673.2000.
ing in the recovery from antimicrobial treatment. One BevNet. (2011). The kombucha crisis: One year later. BevNet.
aspect that cannot be underestimated in the development Bigliardi, B., & Galati, F.. (2013). Innovation trends in the food
industry: the case of functional foods. Trends in Food Science and
of beverages is the need to accurately assess the market po- Technology, . http://dx.doi.org/10.1016/j.tifs.2013.03.006.
tential for the product. The obvious hurdle is consumers’ Champagne, C. P., & Fustier, P.. (2007). Microencapsulation for the
willingness to accept an unfamiliar product, and the right improved delivery of bioactive compounds into foods. Current
combination of starters and substrates, optimum nutrition Opinion in Biotechnology, . http://dx.doi.org/10.1016/
and flavour development and scientifically-supported health j.copbio.2007.03.001.
Cheng, I.-C., Shang, H.-F., Lin, T.-F., Wang, T.-H., Lin, H.-S., & Lin, S.-
benefits need to be carefully considered. It has been shown H.. (2005). Effect of fermented soy milk on the intestinal bacterial
that taste, price and base nutritional composition are more ecosystem. World Journal of Gastroenterology: WJG, 11,
important than functional properties (Falguera, Aliguer, & 1225e1227.
Falguera, 2012). Consumers perceive products that are Cocolin, L., Alessandria, V., Dolci, P., Gorra, R., & Rantsiou, K..
intrinsically healthy such as yoghurt, fruit juices and cereal (2013). Culture independent methods to assess the diversity and
dynamics of microbiota during food fermentation. International
as preferable carriers of functional foods (Annunziata & Journal of Food Microbiology, 167, 29e43. http://dx.doi.org/
Vecchio, 2011), reflected in the increase in the study of 10.1016/j.ijfoodmicro.2013.05.008.
these food types, and which may allow developers to Coda, R., Rizzello, C. G., Trani, A., & Gobbetti, M.. (2011).
exploit natural mineral and vitamin content of foods and Manufacture and characterization of functional emmer beverages
juices already perceived to be healthy. fermented by selected lactic acid bacteria. Food Microbiology, 28,
526e536. http://dx.doi.org/10.1016/j.fm.2010.11.001.
In conclusion, fermentation is an ancient form of bio- Companiesandmarkets. (2013). Functional drinks: Global industry
preservation that is common to all regions of the world. guide. Companiesandmarkets.
With traditional milk-fermented products currently enjoy- Czerucka, D., Piche, T., & Rampal, P.. (2007). Review article: yeast as
ing success in many markets, there is an increasing interest probiotics e Saccharomyces boulardii. Alimentary Pharmacology
in functional beverages from a scientific, consumer and & Therapeutics, 26, 767e778. http://dx.doi.org/10.1111/j.1365-
2036.2007.03442.x.
commercial perspective. There is a movement in the mod- De Oliveira Leite, A. M., Lemos Miguel, M. A., Peixoto, R. S.,
ern consumers’ selection of foods that offer health, social Rosado, A. S., Silva, J. T., Flosi Paschoalin, V. M., et al. (2013).
and environmental benefits, which has encouraged the Microbiological, technological and therapeutic properties of kefir:
food industry to develop new products and market strate- a natural probiotic beverage. Brazilian Journal of Microbiology,
gies. The functional beverage market is still small and frag- 44, 341e349. http://dx.doi.org/10.1590/S1517-
83822013000200001.
mented in most European countries (Siro, Kapolna, Dewapriya, P., & Kim, S.. (2013). Marine microorganisms: an
Kapolna, & Lugasi, 2008), but it is expected that this emerging avenue in modern nutraceuticals and functional foods.
area will see much success in the coming years. Indeed, Food Research International, 56, 115e125. http://dx.doi.org/
with the availability and improvements in technology, and 10.1016/j.foodres.2013.12.022.
consumers’ increasing interest in functional foods, the Drgalic, I., Tratnik, L., & Bozanic, R.. (2005). Growth and survival of
probiotic bacteria in reconstituted whey. Le Lait, . http://
outlook for fermented beverages is more promising than dx.doi.org/10.1051/lait:2005009.
ever. Dufresne, C., & Farnworth, E. (2000). Tea, kombucha, and health: a
review. Food Research International, 33(6), 409e421.
Falguera, V., Aliguer, N., & Falguera, M.. (2012). An integrated
References
approach to current trends in food consumption: moving toward
Akpinar-Bayizit, A., Yilmaz-Ersan, L., & Ozcan, T. (2010). functional and organic products? Food Control, . http://dx.doi.org/
Determination of boza’s organic acid composition as it is affected 10.1016/j.foodcont.2012.01.051.
by raw material and fermentation. International Journal of Food Forssten, S. D., Sindelar, C. W., & Ouwehand, A. C.. (2011).
Properties, 13(3), 648e656. Probiotics from an industrial perspective. Anaerobe, 17, 410e413.
Amoutzopoulos, B., L€ oker, G. B., Samur, G., Çevikkalp, S. A., http://dx.doi.org/10.1016/j.anaerobe.2011.04.014.
Yaman, M., Timur, K., et al. (2013). Effects of a traditional Gadaga, T. H., Mutukumira, A. N., & Narvhus, J. A.. (2001). The
fermented grape-based drink “hardaliye” on antioxidant status of growth and interaction of yeasts and lactic acid bacteria isolated
healthy adults: a randomized controlled clinical trial. Journal of from Zimbabwean naturally fermented milk in UHT milk.
the Science of Food and Agriculture, 93(14). International Journal of Food Microbiology, 68, 21e32. http://
Annunziata, A., & Vecchio, R.. (2011). Functional foods development dx.doi.org/10.1016/S0168-1605(01)00466-4.
in the European market: a consumer perspective. Journal of Gallardo-Escamilla, F. J., Kelly, A. L., & Delahunty, C. M.. (2007).
Functional Foods, 3, 223e228. http://dx.doi.org/10.1016/ Mouthfeel and flavour of fermented whey with added
j.jff.2011.03.011. hydrocolloids. International Dairy Journal, 17, 308e315. http://
Awaisheh, S. S., Haddadin, M. S. Y., & Robinson, R. K.. (2005). dx.doi.org/10.1016/j.idairyj.2006.04.009.
Incorporation of selected nutraceuticals and probiotic bacteria Gran, H. M., Gadaga, H. T., & Narvhus, J. A.. (2003). Utilization of
into a fermented milk. International Dairy Journal, 15, various starter cultures in the production of Amasi, a Zimbabwean
1184e1190. http://dx.doi.org/10.1016/j.idairyj.2004.11.003. naturally fermented raw milk product. International Journal of
 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124 123

Food Microbiology, 88, 19e28. http://dx.doi.org/10.1016/S0168- Marketsandmarkets. (2013). Dairy alternative (beverage) market by
1605(03)00078-3. type (soy, almond, rice), formulation (plain, flavored, sweetened,
Granato, D., Branco, G. F., Nazzaro, F., Cruz, A. G., & Faria, J.a. F. unsweetened), channel (supermarket, health store, pharmacy,
(2010). Functional foods and nondairy probiotic food convenience store) & geography e global trends & forecast to
development: trends, concepts, and products. Comprehensive 2018. Marketsandmarkets.com/.
Reviews in Food Science and Food Safety, 9, 292e302. http:// Marsh, A. J., O’Sullivan, O., Hill, C., Ross, R. P., & Cotter, P. D..
dx.doi.org/10.1111/j.1541-4337.2010.00110.x. (2013). Sequencing-based analysis of the bacterial and fungal
Greenwalt, C. J., Steinkraus, K. H., & Ledford, R. A.. (2000). composition of kefir grains and milks from multiple sources. PLoS
Kombucha, the fermented tea: microbiology, composition, and ONE, 8. http://dx.doi.org/10.1371/journal.pone.0069371.
claimed health effects. Journal of Food Protection, 63, 976e981. Martensson, O., Bi€ orklund, M., Lambo, A. M., Due~ nas-Chasco, M.,
Guarner, F., Sanders, M. E., Gibson, G., Klaenhammer, T., Irastorza, A., Holst, O., et al. (2005). Fermented, ropy, oat-based
Cabana, M., Scott, K., et al. (2011). Probiotic and prebiotic claims products reduce cholesterol levels and stimulate the bifidobacteria
in Europe: seeking a clear roadmap. British Journal of Nutrition, flora in humans. Nutrition Research, 25, 429e442. http://
106(11), 1765e1767. dx.doi.org/10.1016/j.nutres.2005.03.004.
Hansen, E. B.. (2002). Commercial bacterial starter cultures for Martins, E. M. F., Ramos, A. M., Vanzela, E. S. L., Stringheta, P. C., de
fermented foods of the future. International Journal of Food Oliveira Pinto, C. L., & Martins, J. M.. (2013). Products of
Microbiology, . http://dx.doi.org/10.1016/S0168-1605(02)00238-6. vegetable origin: a new alternative for the consumption of
Huebner, J., Wehling, R. L., & Hutkins, R. W.. (2007). Functional probiotic bacteria. Food Research International, . http://dx.doi.org/
activity of commercial prebiotics. International Dairy Journal, 17, 10.1016/j.foodres.2013.01.047.
770e775. http://dx.doi.org/10.1016/j.idairyj.2006.10.006. McGovern, P. E., Zhang, J., Tang, J., Zhang, Z., Hall, G. R.,
Hugenholtz, J.. (2013). Traditional biotechnology for new foods and Moreau, R. A., et al. (2004). Fermented beverages of pre- and
beverages. Current Opinion in Biotechnology, . http://dx.doi.org/ proto-historic China. Proceedings of the National Academy of
10.1016/j.copbio.2013.01.001. Sciences of the United States of America, 101, 17593e17598.
Jargin, S. V.. (2009). Kvass: a possible contributor to chronic http://dx.doi.org/10.1073/pnas.0407921102.
alcoholism in the Former Soviet Union e alcohol content should McMaster, L. D., Kokott, S. A., Reid, S. J., & Abratt, V. R.. (2005). Use
be indicated on labels and in advertising. Alcohol and Alcoholism, of traditional African fermented beverages as delivery vehicles for
44(5), 529. Bifidobacterium lactis DSM 10140. International Journal of Food
Katan, M. B.. (2012). Why the European Food Safety Authority was Microbiology, 102, 231e237. http://dx.doi.org/10.1016/
right to reject health claims for probiotics. Beneficial Microbes, . j.ijfoodmicro.2004.12.013.
http://dx.doi.org/10.3920/BM2012.0008. Metchnikoff, E., & Metchnikoff, I. I. (1908). The prolongation of life:
Khan, R. S., Grigor, J., Winger, R., & Win, A.. (2013). Functional food Optimistic studies. Springer Publishing Company.
product development e opportunities and challenges for food Motarjemi, Y., K€aferstein, F., Moy, G., & Quevedo, F.. (1993).
manufacturers. Trends in Food Science & Technology, 30, 27e37. Contaminated weaning food: a major risk factor for diarrhoea and
http://dx.doi.org/10.1016/j.tifs.2012.11.004. associated malnutrition. Bulletin of the World Health
Kitabatake, N., Gimbi, D. M., & Oi, Y.. (2003). Traditional non- Organization, 71, 79e92.
alcoholic beverage, Togwa, in East Africa, produced from maize Mugochi, T., Mutukumira, T., & Zvauya, R. (2001). Comparison of sensory
flour and germinated finger millet. International Journal of Food characteristics of traditional Zimbabwean non-alcoholic cereal
Sciences and Nutrition, 54, 447e455. beverages, masvusvu and mangisi with mahewu, a commercial cereal
Kumar, M., Verma, V., Nagpal, R., Kumar, A., Behare, P. V., Singh, B., product. Ecology of Food and Nutrition, 40(4), 299e309.
et al. (2012). Anticarcinogenic effect of probiotic fermented milk Muyanja, C. M. B. K., Narvhus, J. A., Treimo, J., & Langsrud, T..
and chlorophyllin on aflatoxin-B1-induced liver carcinogenesis in (2003). Isolation, characterisation and identification of lactic acid
rats. British Journal of Nutrition, . http://dx.doi.org/10.1017/ bacteria from bushera: a Ugandan traditional fermented beverage.
S0007114511003953. International Journal of Food Microbiology, 80, 201e210. http://
Kwak, H. S., Park, S. K., & Kim, D. S.. (1996). Biostabilization of kefir dx.doi.org/10.1016/S0168-1605(02)00148-4.
with a nonlactose-fermenting yeast. Journal of Dairy Science, Muyzer, G., de Waal, E. C., & Uitterlinden, A. G.. (1993). Profiling of
79(6), 937e942. complex microbial populations by denaturing gradient gel
Laureys, D., & De Vuyst, L.. (2014). Microbial species diversity, electrophoresis analysis of polymerase chain reaction-amplified
community dynamics, and metabolite kinetics of water kefir genes coding for 16S rRNA. Applied and Environmental
fermentation. Applied and Environmental Microbiology, 80(8), Microbiology, 59, 695e700.
2564e2572. Narvhus, J. A., & Gadaga, T. H.. (2003). The role of interaction
Leatherhead. (2011). Future directions for the global functional foods between yeasts and lactic acid bacteria in African fermented
market. Leatherhead Food Research. milks: a review. International Journal of Food Microbiology, .
Lei, V., & Jakobsen, M.. (2004). Microbiological characterization and http://dx.doi.org/10.1016/S0168-1605(03)00247-2.
probiotic potential of koko and koko sour water, African Oliveira, R. P. S., Florence, A. C. R., Silva, R. C., Perego, P.,
spontaneously fermented millet porridge and drink. Journal of Converti, A., Gioielli, L. A., et al. (2009). Effect of different
Applied Microbiology, 96, 384e397. http://dx.doi.org/10.1046/ prebiotics on the fermentation kinetics, probiotic survival and fatty
j.1365-2672.2004.02162.x. acids profiles in nonfat symbiotic fermented milk. International
Lifeway. (2014). Lifeway Foods Inc., financial results. Lifeway Foods Inc. Journal of Food Microbiology, 128, 467e472. http://dx.doi.org/
Londero, A., Hamet, M. F., De Antoni, G. L., Garrote, G. L., & 10.1016/j.ijfoodmicro.2008.10.012.
Abraham, A. G.. (2012). Kefir grains as a starter for whey €
Ozer, B. H., & Kirmaci, H. A.. (2010). Functional milks and dairy
fermentation at different temperatures: chemical and beverages. International Journal of Dairy Technology, 63, 1e15.
microbiological characterisation. Journal of Dairy Research, . http://dx.doi.org/10.1111/j.1471-0307.2009.00547.x.
http://dx.doi.org/10.1017/S0022029912000179. Pitkala, K. H., Strandberg, T. E., Finne-Soveri, U. H.,
Malbasa, R. V., Milanovic, S. D., Loncar, E. S., Djuric, M. S., Ouwehand, A. C., Poussa, T., & Salminen, S.. (2007). Fermented
Caric, M. D., Ili
ci
c, M. D., et al. (2009). Milk-based beverages cereal with specific bifidobacteria normalizes bowel movements
obtained by Kombucha application. Food Chemistry, 112, in elderly nursing home residents. A randomized, controlled trial.
178e184. http://dx.doi.org/10.1016/j.foodchem.2008.05.055. Journal of Nutrition Health and Aging, 11(4), 305.
 124 A.J. Marsh et al. / Trends in Food Science & Technology 38 (2014) 113e124

Prado, F. C., Parada, J. L., Pandey, A., & Soccol, C. R.. (2008). Trends Tabbers, M. M., Chmielewska, A., Roseboom, M. G., Crastes, N.,
in non-dairy probiotic beverages. Food Research International, . Perrin, C., Reitsma, J. B., et al. (2011). Fermented milk containing
http://dx.doi.org/10.1016/j.foodres.2007.10.010. Bifidobacterium lactis DN-173 010 in childhood constipation: a
Priya, P., & Munishamanna, K. B. (2013). Microbial fermentation of randomized, double-blind, controlled trial. Pediatrics, 127,
blended tomato juice by yeast and lactic acid bacteria for e1392ee1399. http://dx.doi.org/10.1542/peds.2010-2590.
nutritional improvement. Environment and Ecology, 31(1), Tillisch, K., Labus, J., Kilpatrick, L., Jiang, Z., Stains, J., Ebrat, B., et al.
181e186. (2013). Consumption of fermented milk product with probiotic
Puerari, C., Magalh~ aes, K. T., & Schwan, R. F.. (2012). New cocoa modulates brain activity. Gastroenterology, 144. http://dx.doi.org/
pulp-based kefir beverages: microbiological, chemical 10.1053/j.gastro.2013.02.043.
composition and sensory analysis. Food Research International, Van Wyk, J., Britz, T. J., & Myburgh, A. S.. (2002). Arguments
48, 634e640. http://dx.doi.org/10.1016/j.foodres.2012.06.005. supporting kefir marketing to the low-income urban African
Rahman, N., Xiaohong, C., Meiqin, F., & Mingsheng, D. (2009). population in South Africa. Agrekon, 41(1), 43e62.
Characterization of the dominant microflora in naturally Verbeke, W., Scholderer, J., & L€ahteenm€aki, L.. (2009). Consumer
fermented camel milk shubat. World Journal of Microbiology and appeal of nutrition and health claims in three existing product
Biotechnology, 25(11), 1941e1946. concepts. Appetite, 52, 684e692. http://dx.doi.org/10.1016/
Rathore, S., Salmer on, I., & Pandiella, S. S.. (2012). Production of j.appet.2009.03.007.
potentially probiotic beverages using single and mixed cereal Viljoen, B. C.. (2001). The interaction between yeasts and bacteria in
substrates fermented with lactic acid bacteria cultures. Food dairy environments. International Journal of Food Microbiology,
Microbiology, 30, 239e244. http://dx.doi.org/10.1016/ 69, 37e44. http://dx.doi.org/10.1016/S0168-1605(01)00570-0.
j.fm.2011.09.001. Wang, C.-Y., Wu, S.-J., & Shyu, Y.-T. (2013). Antioxidant properties of
Saijirahu, B.. (2008). Folk medicine among the mongols in Inner certain cereals as affected by food-grade bacteria fermentation.
Mongolia. Asian Medicine, 4(2), 338e356. Ournal of Bioscience and Bioengineering, .
Shiby, V. K., & Mishra, H. N.. (2013). Fermented milks and milk Wang, Y., Ji, B., Wu, W., Wang, R., Yang, Z., Zhang, D., et al. (2014).
products as functional foods e a review. Critical Reviews in Food Hepatoprotective effects of kombucha tea: identification of
Science and Nutrition, 53, 482e496. http://dx.doi.org/10.1080/ functional strains and quantification of functional components.
10408398.2010.547398. Journal of the Science of Food and Agriculture, 94, 265e272.
Silva, M. R., Dias, G., Ferreira, C. L. L. F., Franceschini, S. C. C., & http://dx.doi.org/10.1002/jsfa.6245.
Costa, N. M. B.. (2008). Growth of preschool children was Yamamoto, S., Nakashima, Y., Yoshikawa, J., Wada, N., &
improved when fed an iron-fortified fermented milk beverage Matsugo, S.. (2011). Radical scavenging activity of the Japanese
supplemented with Lactobacillus acidophilus. Nutrition Research, traditional food, Amazake. Food Science and Technology
28, 226e232. http://dx.doi.org/10.1016/j.nutres.2008.02.002. Research, . http://dx.doi.org/10.3136/fstr.17.209.
Siro, I., Kapolna, E., Kapolna, B., & Lugasi, A. (2008). Functional food. Yang, Y., Shevchenko, A., Knaust, A., Abuduresule, I., Li, W., Hu, X.,
Product development, marketing and consumer acceptance d A et al. (2014). Proteomics evidence for kefir dairy in Early Bronze
review. Appetite, 51(3), 456e467. Age China. Journal of Archaeological Science, 45, 178e186.
Sun-Waterhouse, D. (2011). The development of fruit-based Zorba, M., Hancioglu, O., Genc, M., Karapinar, M., & Ova, G..
functional foods targeting the health and wellness market: a (2003). The use of starter cultures in the fermentation of boza, a
review. International Journal of Food Science & Technology, 46, traditional Turkish beverage. Process Biochemistry, 38,
899e920. http://dx.doi.org/10.1111/j.1365-2621.2010.02499.x. 1405e1411. http://dx.doi.org/10.1016/S0032-9592(03)00033-5.

View publication stats