Food Research International 151 (2022) 110842

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Food Research International

journal homepage: www.elsevier.com/locate/foodres

Consumer’s acceptability and health consciousness of probiotic and

prebiotic of non-dairy products
Fernanda Cosme, António Inês, Alice Vilela *
Chemistry Research Centre-Vila Real (CQ-VR), Dep. of Biology and Environment, School of Life Sciences and Environment, University of Trás-os-Montes and Alto Douro,
Vila Real, Portugal

A R T I C L E I N F O A B S T R A C T

Keywords: Human gut microbiota is a protective agent of intestinal and systemic health, and its modulation is of great
Gut microbiota interest for human wellbeing. In the world of biotics, besides probiotics, prebiotics, and synbiotics, also appears
Fermented cereals the denomination of “postbiotics” and “psychobiotics”. Fermented dairy products are, traditionally, the major
Fermented fruits
source of probiotics. Nevertheless, due to the increasing number of lactose-intolerant individuals and strict
Fermented vegetables
Saccharomyces boulardii
vegetarians, there is a need for innovative non-dairy products. Non-dairy biotics are being included in the normal
Lactic acid bacteria diet and due to technological advances, many products are created using non-conventional food matrices like
kombucha tea, herbal tea, baking mix, and cereal-based products.
The microorganisms most used as probiotics in many of the non-dairy products are strains belonging to the
genera Bifidobacterium, Enterococcus, Lactobacillus, Lactococcus, Streptococcus, and Bacillus, and some yeast strains
namely Saccharomyces cerevisiae var. boulardii. Recently, several other yeasts have been described as having
probiotic properties. This review describes gut-derived effects in humans of possible microorganisms, such as
yeasts, and bacteria, isolated from non-dairy fermented and non-fermented foods and beverages. The microor­
ganisms responsible for the processing of these non-dairy fermented products, together with the prebiotics, form
a class of nutrients that have been proven to be beneficial for our gut health.

1. Introduction approach to improve gut function and overall health. Probiotics are
classified as “live strains of strictly selected microorganisms that, when
Human gut microbiota is a protective agent of intestinal and systemic administered in adequate amounts, confer a health benefit on the host”
health, comprised of a huge number of microorganisms in an intricate (Satokari, 2019). The microorganisms most used as probiotics are strains
ecosystem. Microbiota dysbiosis (alterations in the composition, di­ belonging to the genera Bifidobacterium, Enterococcus, Lactobacillus,
versity, and temporal stability) is associated with several intestinal and Lactococcus, Streptococcus, and Bacillus (Markowiak & Śliżewska, 2017;
systemic conditions, and its modulation for human health is of great Sanders, Merenstein, Merrifield, & Hutkins, 2018; Zommiti, Feuilloley,
interest. & Connil, 2020), and some yeast strains belonging to the genus
The human intestinal microbiota is a vastly diverse population of Saccharomyces, namely S. cerevisiae var. boulardii (Lazo-Vélez, Serna-
microorganisms consisting of archaea, bacteria, fungi, viruses, and Saldívar, Rosales-Medina, Tinoco-Alvear, & Briones-García, 2018).
protozoa, and has a key contribution to human health (Lavelle & Hill, Without condescending the attractive rheological and sensory charac­
2019). Microbiota dysbiosis has been linked with several gastrointes­ teristics of fermented products, S. cerevisiae var. boulardii can release and
tinal and systemic conditions. Consequently, modulation of the intesti­ modify secondary metabolites which can increase the nutraceutical
nal microbiota maintaining a favorable balance in the ecosystem, which qualities of food and beverage (Lazo-Vélez et al., 2018; Ryan et al.,
will improve human health, is of enormous interest (Lavelle & Hill, 2011).
2019). Fructo-oligosaccharides and galactooligosaccharides are two
Markowiak and Śliżewska (2017) published a review article where important groups of prebiotics; however, some other compounds have
they evaluated the evidence and discussed the options of using pro­ been described as having similar actions such as resistant starch, inulin,
biotics, prebiotics, and their combinations, synbiotics, as a nutritional lactulose, pyrodextrins, sugar alcohols, levans, and lactosucrose (Farias,

* Corresponding author at: Quinta de Prados, UTAD, Portugal.

E-mail address: avimoura@utad.pt (A. Vilela).

https://doi.org/10.1016/j.foodres.2021.110842
Received 10 June 2021; Received in revised form 1 November 2021; Accepted 27 November 2021
Available online 3 December 2021
0963-9969/© 2021 Elsevier Ltd. All rights reserved.
F. Cosme et al. Food Research International 151 (2022) 110842

de Araújo, Neri-Numa, & Pastore, 2019; Guimarães et al., 2020). components and functional compounds, depending on the organism and
Beneficial intestinal microorganisms ferment these prebiotic compounds growth conditions (Molina-Tijeras, Gálvez, & Rodríguez-Cabezas,
and obtain their energy from degrading indigestible units of them (Peng, 2019). An example of a promising next-generation probiotic is Akker­
Tabashsum, & Anderson, 2020). As a result, prebiotics can selectively mansia muciniphila (Fatemeh et al., 2019). This species is known to
influence gut microbiota (Davani-Davari et al., 2019). On the other produce extracellular vesicles, which may contribute to alleviating in­
hand, the gut microbiota affects intestinal functions, such as metabolism testinal inflammation and reinforcing epithelial integrity and function­
and intestine integrity. Furthermore, lactic acid-producing genera ality (Cani & de Vos, 2017; Molina-Tijeras et al., 2019). Extracellular
(Bifidobacterium and Lactobacillus), by inducing a variety of immuno­ vesicles can be used as biotherapeutic agents to avoid the risks associ­
modulatory molecules, can suppress pathogens in healthy individuals ated with the use of live bacteria in individuals with compromised im­
(Ayivi et al., 2020). Probiotics have also been shown to regulate fat munity (Wiklander, Brennan, Lötvall, Breakefield, & El Andaloussi,
storage and stimulate intestinal angiogenesis, among other health ben­ 2019).
efits (Kerry et al., 2018). In the world of biotics, besides probiotics, prebiotics, and synbiotics,
Synbiosis is the interaction between probiotics and prebiotics. Pan­ also appears the denomination of “postbiotics” and “psychobiotics”.
igrahi et al. (2017) demonstrated, in a clinical trial with 4556 in­ Postbiotics are the newest members of the biotics family. The name
dividuals, that a synbiotic mix containing a strain of Lactiplantibacillus refers to bioactive compounds produced during a fermentation process
plantarum (formerly Lactobacillus plantarum) and a prebiotic, fructooli­ by food-grade microorganisms. Postbiotics include microbial cells, cell
gosaccharides, reduced by 40 % neonatal sepsis and death amongst in­ constituents, and metabolites (Wegh, Geerlings, Knol, Roeselers, &
fants in rural India. Moreover, prebiotic-based nutritional approaches Belzer, 2019), such as extracellular polysaccharides, cell lysates, func­
seem extremely attractive in targeting particularly oxygen-sensitive tional proteins, short-chain fatty acids, secreted polysaccharides, tei­
commensals species such as Faecalibacterium prausnitzii (Verhoog choic acid, peptidoglycan-derived muropeptides, and pili-type
et al., 2019). The consumption of dietary fiber or prebiotics such as structures (O’Grady, O’Connor, & Shanahan, 2019).
inulin may increase the abundance of F. prausnitzii which presents anti- Postbiotics can be divided into two categories: (i) paraprobiotics
inflammatory properties and is found to be reduced in individuals with (also called ghost or inactivated probiotics) that are “nonviable micro­
inflammatory bowel disease (Sokol et al., 2008). The utilization of these bial cells (intact or broken), or crude cell extracts (i.e., with complex
synbiotic systems seems to be the next probiotic generation. Screening chemical composition), which, when administered (orally or topically)
for properties such as adherence to the intestinal epithelium, immuno­ in adequate amounts, confer a benefit on the human or animal con­
modulation, and the production of extracellular vesicles, has been the sumer” (Shripada, Gayatri, & Sanjay, 2020), Fig. 1. One example is
aim of many works that try to discover the next generation of probiotics S. boulardii, that by activation of α2β1 integrin collagen receptors, can
(Macia, Nanan, Hosseini-Beheshti, & Grau, 2019; Markowiak & enhance barrier function against bacterial species, and improves
Śliżewska, 2017). Several Lactobacillus and Bifidobacterium strains have angiogenesis in vitro and in vivo in intestinal epithelial cells (Terciolo,
been found to produce extracellular vesicles, which can carry different Dapoigny, & Andre, 2017); (ii) probioceuticals/probiotaceuticals which

Fig. 1. Schematic representation of various health benefits of postbiotic molecules. Postbiotic molecules have been studied due to their known chemical structure,
long storage stability, and ability to activate various mechanisms in controlling inflammation, anti-adhesion of pathogens to the intestinal tract, and antagonistic
effect against pathogens. In the plate in the middle of the image it is possible to observe the inhibitory effect of CFS (Cell-Free Supernatant) of probiotic lactobacilli
against BM S. aureus a) L. reuteri, b) L. plantarum, c) L. acidophilus and d) L. casei (Soleimani, Kermanshahi, Yakhchali, & Sattari, 2010). Moreover, postbiotic
molecules can help us to control obesity, hypertension, coronary artery diseases, cancer, and oxidative stress (Nataraj et al., 2020).

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F. Cosme et al. Food Research International 151 (2022) 110842

defines probiotic resulting factors such as reuterin from Limosilactoba­ vegetables. Recently, Le Roy and co-workers (2020), performed a study
cillus reuteri -formerly Lactobacillus reuteri (Nataraj, Ali, & Behare, 2020; that showed that moderate red wine intake (one glass a day) could be
Rebeca & Philippe, 2019; Zheng et al., 2020). beneficial for our gut health; Our gut microbiomes can be affected by
Psychobiotics are probiotics that confer mental health benefits to the alcoholic beverages including beer, cider, spirits, and both red and white
host (Sarkar et al., 2016). Rapid innovation in the medical therapy of wines, namely due to de microorganisms they contain but, also, due to
depression attracts high enthusiasm in the microbiome and dietary the presence of prebiotics. In this review, we describe gut-derived effects
research and psychobiotics. They act through the microbiota-gut-brain in humans of possible microorganisms, such as wine-yeasts and bacteria,
axis and can modify neural circuits relevant to emotional, cognitive, isolated from wine and other non-dairy fermented and non-fermented
and social behaviors (Tian et al., 2021). There are mechanisms through foods and beverages. The microorganisms responsible for the process­
which the gut microbiota can signal to the brain: (i) activation of the ing of these non-dairy fermented products, together with the prebiotics,
vagus nerve; (ii) production of antigens that engage immune B cell re­ such as polyphenols, that they contain (Vilela, Cosme, & Inês, 2020)
sponses; (iii) production of metabolites like short-chain fatty acids; (iv) could be beneficial for our gut health.
enteroendocrine signaling from gut epithelial cells. Across these paths of
communication, the microbiota-gut-brain axis controls behavior, 2. Probiotics in non-dairy fermented foods
neurotransmission, neurogenesis, neuroinflammation, and neuroendo­
crine signaling that are all implicated in stress-related responses, Fig. 2 2.1. Yeasts as probiotics/synbiotics in non-dairy fermented foods
(Foster, Rinaman, & Cryan, 2017; Tian et al., 2021). However, some
studies evidence the impact of physical stressors and psychological For yeast to be classified as a probiotic, must present some charac­
environmental on gut microbiota composition and function (Karl et al., teristics needed to survive and function in the gastrointestinal tract
2018; Sarkar et al., 2020). So, a feedback complex mechanism occurs; a (viability at 36–38 ◦ C; resistance to gastric acid, bile salts, and digestive
healthy and not stressful life will help our microbial gut microflora enzymes), be considered safe when administered (absence of hemolytic
maintain its balance, on the other hand, they will provide through the and mucolytic activities, and susceptibility to antimicrobial drugs) and
microbiota-gut-brain axis a correct emotional, social, and cognitive be beneficial to Humans (protect against infection, or be able to co-
state. aggregate – entrapment- pathogenic agents) (Fijan, 2014). Saccharo­
The major source of probiotics is fermented dairy products, however, myces cerevisiae var. boulardii is the first yeast described as a probiotic, at
there is a need for innovative non-dairy probiotics, due to the increasing least since 1982–83 (Ducluzeau & Bensaada, 1982; Massot, Desconclois,
number of lactose-intolerant individuals tied with the adverse effect of & Astoin, 1983; Tempé et al., 1983). This yeast (S. boulardii) has
cholesterol contained in fermented dairy products aside from the extraordinary physiological properties like optimal growth temperature,
increasing number of strict vegetarians. Vegetarian and vegan diets are resistance to the gastric environment, and viability at low pH (Pais,
great allies of a healthy lifestyle, with a growing intention to buy new Almeida, Yılmaz, & Teixeira, 2020).
products, so there is a growing need to serve this consumer market. The S. boulardii presents the potential to inhibit pathogen’s growth
increasing number of adherents to these types of diets drives the food (Kunyeit, Anu-Appaiah, & Rao, 2020). The mechanism of elimination of
industry to diversify elevating the variety of probiotic products based on the pathogenic bacteria is mainly attributed to the adhesion proteins of

Fig. 2. Microbiota–gut-brain axis main communication pathways. SCFAs - short-chain fatty acid; CCK – cholecystokinin; GABA γ-aminobutyric acid; GLP glucagon-
like peptide; PYY - peptide YY; TNF - tumor necrosis factor; IL – interleukin. Adapted from Foster et al. (2017).

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S. boulardii (Vilela et al., 2020) or secreted metabolites such as short- Table 1

chain fatty acids that inhibit the adhesion and morphological transi­ Saccharomyces and non-Saccharomyces yeasts strains, non-dairy environment
tion of several pathogens like Candida species (Kunyeit et al., 2020) - see from which they were isolated, and main probiotic properties.
Fig. 1. S. boulardii also possesses the capacity to degrade pathogen Environment Yeast strain Main probiotic Reference
toxins, modulate normal microbiota preserving normal intestinal phys­ properties
iology, and increase secretory IgA (sIgA) levels acting as an immune Fermented food Kluyveromyces Bile salt and acid Hsiung et al.
regulator by changing cytokine levels (Mourey et al., 2020; Stier & products and marxianus JYC2614 tolerance, cell (2021)
Bischoff, 2016). beverages surface
collected in hydrophobicity, and
Over the years, several clinical trials, in vivo and in vitro have been
Taiwan such as β-galactosidase
made aiming to assess the efficacy and safety of Saccharomyces cerevisiae kombucha, rice activity. Can survive
var. boulardii in the management of several intestinal disorders (Kele­ wine, sweet in a gastrointestinal
sidis & Pothoulakis, 2012). This yeast was seen to improve the conse­ wine, and environment.
quence of several diarrhea diseases, as pediatric diarrhea, antibiotic- Taiwanese
kimchi.
associated diarrhea, acute diarrhea, traveler’s diarrhea, and enteral Antarctica Rhodotorula Protected mice Coutinho
nutrition-related diarrhea (Dinleyici, Kara, Ozen, & Vandenplas, 2014; mucilaginosa against Salmonella et al. (2021)
McFarland, 2010, 2017). Clinical trial data also indicates a possible role UFMGCB 18377 infection presenting
of S. boulardii in reducing treatment relapses (Dinleyici et al., 2014; a higher survival and
reduced weight loss,
McFarland, 2010, 2017) and improving the clinical condition in patients
bacterial
suffering from Irritable Bowel Syndrome (IBS) symptoms (Pineton de translocation to the
Chambrun et al., 2015). liver, sIgA intestinal
In 2020, Mourey and co-workers performed a work where a total of levels, and intestinal
100 infants, 3–36 months of age, with acute diarrhea, received medical and hepatic
myeloperoxidase
care according to the World Health Organization (WHO) guidelines on
(MPO) and
the management of acute diarrhea in children and were randomly eosinophil
assigned to the probiotic group (S. boulardii CNCM I-3799 at a daily dose peroxidase (EPO)
of 5 billion CFU twice daily) or to the placebo group. The administration activities
Brazilian Saccharomyces Resistance to 37 ◦ C, Simões et al.
of S. boulardii CNCM I-3799 was associated with beneficial effects on the
fermented table cerevisiae CCMA pH 2.0, and bile (2021)
duration and severity of diarrhea. The time of recovery from diarrhea olives 1746, Pichia salts. Hydrophobic
was significantly shorter in the probiotic group compared with the guilliermondii CCMA cell surface
placebo group (65.8 ± 12 h vs. 95.3 ± 17.6 h, p = 0.0001). Faster 1753, (42.5–92.2%), auto-
remission in the probiotic group was also demonstrated by a shorter Candida orthopsilosis aggregation capacity
CCMA 1748, (41.0–91.0%) and
time before the first episode of semisolid stool [− 23.5 h, diff (95%
Candida tropicalis adhesion to Caco-2
confidence interval): − 7.99 (− 31.49 to − 15.51), p = 0.0001] and the CCMA 1751, (62.0–82.8%) and
faster normalization of stool consistency. Moreover, S. boulardii CNCM I- Meyerozyma HT-29 (57.6–87.3%)
3799 was well tolerated (Mourey et al., 2020). caribbica CCMA epithelial cell lines.
1758, Antimicrobial
Though S. boulardii possesses a Food Grade status (Czerucka, Piche,
Debaryomyces activity against
& Rampal, 2007) and has been used as a probiotic without the reporting hansenii CCMA Salmonella Enteritidis
of many adverse effects, fungemia (a systemic infection characterized by 1761. as well as the ability
the presence of fungal species in the blood) and sepsis are possible to co-aggregate and
concerns, particularly in immunocompromised patients (Sen & Mansell, reduce the adhesion
of this pathogen to
2020). Also, gut colonization of S. cerevisiae has been reported as being
intestinal cells.
responsible for a condition called “auto-brewery syndrome”, in which Isolated and Rhodosporidiums Inhibit the growth of Yun et al.
yeast ferment sugars to ethanol in the anaerobic gut environment purified from sphaerocarpum Vibrio cells when a (2021)
(Hafez, Hamad, Fouad, & Abdel-Lateff, 2017; Tameez-Ud-Din, Alam, farming water YLY01 small quantity of
carbon source was
Tameez-Ud-Din, & Chaudhary, 2020), leading to toxicity. Reduction of
added into farming
the probability of colonization may be by controlling the dosages and by water. In addition, a
the administration of consortia, with other probiotic yeasts or bacteria, nutrition
rather than monocultures of S. boulardii. composition assay
Consequently, the search for yeasts capable of acting as probiotics is showed the contents
of protein, fatty
an ongoing process. In Table 1 some of the yeast strains isolated from
acids, and total
non-dairy environments, and their main or para-probiotic properties are carotenoids of the
summarized. The data is from works between 2019 and 2021. For yeast YLY01 were
instance, Coutinho et al. (2021) select presumed para-probiotic yeasts 30.3%, 3.2%, and
isolated from different habitats of Antarctica by using in vitro and in vivo 1.2 mg/g of dry cell
weight, respectively.
assays. Nowadays, the Antarctic due to its extreme environment has All these results
been highlighted in the search for microorganisms, mainly those that indicated that the
can produce bioactive metabolites. Many of the Antarctica fungi, namely marine red yeast
yeasts, previously described are characterized by being cold-adapted, YLY01 has a great
potential to be used
mesophiles, and psychrophiles, endemic or not (Rosa et al., 2019).
as a versatile
The results from Coutinho et al. (2021) suggested that yeast species of probiotic in
the genus Rhodotorula, namely the strain R. mucilaginosa UFMGCB aquaculture and to
18377, isolated from this extreme environment, is a potential candidate be developed as a
to be used as a probiotic. The yeast was able to capture, in in vivo trials, microbial agent for
high-ammonia tail
the bacteria Salmonella in a co-aggregation experiment and produced water treatment.
anti-inflammatory substances.
(continued on next page)
Notwithstanding the promising results of Coutinho and co-workers

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F. Cosme et al. Food Research International 151 (2022) 110842

Table 1 (continued ) Table 1 (continued )

Environment Yeast strain Main probiotic Reference Environment Yeast strain Main probiotic Reference
properties properties

Bollo, a S. cerevisiae These isolates Pereira, annuum L.) H. opuntiae IPNFG2 gastrointestinal
traditional DABRP5 exhibited tolerance Jadhav, Fermentation W. anomalus conditions and
Goan to high bile salt Baghela, and IPNFG3 human body
fermented food concentration and Barretto temperature. high
in which coarse acidic pH and (2021) auto-aggregation
wheat/wheat resistance to various abilities. co-
and finger antibiotics and aggregation against
millet are antibacterial activity gram-negative
leavened with against the test bacteria, such as E.
toddy. pathogens coli and
Pistachio fruit Diutina rugosa 14 Good Fernández- S. typhimurium. high
(Pistacia vera). and D. rugosa 8 gastrointestinal Pacheco et al. adhesion to mucin,
resistance and (2021) absence of
adhesion properties. associated virulence
Able to assimilate factors; ability to
some carbon reduce cholesterol
sources, which may
be a desirable
capability for a (2021), most of the scientific works that aim to isolate probiotic yeasts
probiotic from non-dairy origin occurs in less extreme environments. Some are
microorganism.
Nigerian Pichia kluyveri Strain-specific Ogunremi,
isolated from fruits like lemon - Debaryomyces hansenii strain L2 (Reyes-
traditional LKC17, Issatchenkia growth at 37 ◦ C, Sanni, and Becerril et al., 2012), others from fermented table olives - Saccharomyces
fermented orientalis OSL11, P. survived at acidic pH Agrawal cerevisiae CCMA 1746, Pichia guilliermondii CCMA 1753, Candida
foods kudriavzevii OG32, (2.0), tolerance to up (2015), orthopsilosis CCMA 1748, Candida tropicalis CCMA 1751, Meyerozyma
(burukutu, P. kudriavzevii to 2% bile salts Ogunremi,
caribbica CCMA 1758 and D. hansenii CCMA 1761 - isolated and studied
kunun-zaki and ROM11, Candida concentration, Agrawal, and
ogi) tropicalis BOM21 potentials of Sanni (2020). by Simões et al. (2021); isolated from fish - Yarrowia lipolytica D1 (Reyes-
surviving passage Becerril, Alamillo, & Angulo, 2021); fermented food and beverages
through the GI tract including traditional fermented foods - Kluyveromyces marxianus
after exposure to JYC2614 (Hsiung et al., 2021); Pichia kluyveri LKC17, Issatchenkia ori­
simulated conditions
during the gastric
entalis OSL11, Pichia kudriavzevii OG32 and P. kudriavzevii ROM11
and intestinal (Ogunremi et al., 2015, 2020).
passage, adhere to Besides presenting beneficial or para-probiotic properties, yeasts
epithelial cells, and used in the fermentation of non-dairy products (fruits, vegetables, and
mucosa surfaces,
grains), must also be able to give to the finish fermented products
good aggregation
ability and secrete pleasant sensory properties. Though S. cerevisiae strains are commonly
bioactive used in fruit/cereals fermentation, nowadays there is a rising interest in
compounds with combining non-Saccharomyces and Saccharomyces yeasts in wine or
antioxidant wine-like fermentation (Lu, Huang, Lee, & Liu, 2015; Vilela, 2020).
properties.
Brazilian P. kluyveri They tolerate low Menezes et al.
Overall, yeasts with extracellular enzymatic properties can improve the
spontaneous pH, bile salts, and (2020) technological and sensory properties of fruit wine products.
fermentations 37 ◦ C temperatures. In recent literature, yeast strains described as having beneficial or
(cocoa) High percentages of probiotic properties (Table 1) such as Pichia kluyveri, Metschnikowia
hydrophobicity,
pulcherrima, and K. marxianus also showed pectinolytic activity (Belda
auto-aggregation,
coaggregation with et al., 2016). The former authors concluded that the use of
E. coli, and adhesion M. pulcherrima NS-EM-34 with S. cerevisiae improved wine limpidity and
to Caco-2 cells, and increased anthocyanin content and color intensity in comparison to
their cells showed wines fermented with pure S. cerevisiae. K. marxianus also produces a
high antioxidant
activity. In addition,
more complex volatile profile, namely in Albariño wines with stronger
these yeasts were floral, citric, balsamic, and spicy aroma was found when compared with
able to produce wines produced with a commercial pectic enzyme (Sieiro, Villa, Da
phytase, an Silva, García-Fraga, & Vilanova, 2014). Pichia kudriavzevii and
important enzyme
M. pulcherrima possess β-glucosidase activity, helping to increase the
for nutrient
availability in plant- wine fruity and floral notes, thereby adding more complexity to the
based foods. flavor profile (Zhang, Zhuo, Hu, & Zhang, 2020). Furthermore, non-
Isolated from Lachancea Ability to survive at Agarbati et al. Saccharomyces yeast strains such as Wickerhamomyces anomalus (Belda
natural thermotolerans close to human body (2020) et al., 2016) and Debaryomyces hansenii with extracellular high protease
environments (B13), temperature (37 ◦ C),
and Metschnikowia antioxidant activity,
activity prevent haze-forming due to their protease activity (Toy, Lu,
spontaneous ziziphicola (B27), S. resistant strain in the Huang, Matsumura, & Liu, 2020). Recently, Canonico, Zannini, Ciani,
processed foods cerevisiae (10c, 8, 6, gastric juice and Comitini (2021) studied the potential use of Lachancea thermoto­
2PV, 7).Torulaspora. simulated lerans previously isolated by Agarbati et al. (2020) from a natural un-
delbrueckii (1.1 t2, conditions,
anthropized environment (oakmoss in wood) in the production of craft
7.3 t2, 35, c7.4, antibacterial activity
j401, tdvcsff) beer. Active sour notes and fruity/ester, together with an increase of
Guajillo Pepper P. kudriavzevii The yeasts were able Lara-Hidalgo aromatic notes were found in the final fermented product. Moreover, the
(Capsicum IPNFG1 to survive in these et al. (2019) low ethanol content exhibited by L. thermotolerans pure cultures was also
simulated relevant to producing low alcohol beer. The yeast strain Kazachstania

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F. Cosme et al. Food Research International 151 (2022) 110842

unispora, isolated by artisanal sourdough exhibited, in the same study and other constituents) with increased availability due to the process of
performed by Canonico et al. (2021), an effective and peculiar aroma fermentation. Also, many fermented foods contain live microorganisms
potential. As the authors concluded, this trend could be useful to obtain that may improve gastrointestinal health and provide other health
a craft beer marked by low ethanol content and at the same time with benefits (as shown in Fig. 1) including lowering the risk of type two
distinctive aromatic notes. diabetes and cardiovascular diseases (Rezac et al., 2018). Although
considerable variation based on geographical region and sampling time
may be found in counting (per mL or gram) of viable LAB in food
2.2. Lactic acid bacteria (LAB) as probiotics in non-dairy foods samples, usually dairy products presented higher values, however, the
values and the species found in other fermented food matrices of plant
Foods such as water kefir, sourdough bread, miso soup, puddings, and animal origin constitute a good source of live lactic acid bacteria,
juices, puree, sauerkraut, sour pickles, olives, tempeh, sausages are ex­ including species that reportedly provide human health benefits (Rezack
amples of fermented foods, being sources of LAB probiotics (Aspri, et al., 2018).
Papademas, & Tsaltas, 2020; Inês et al., 2008, 2009; Inês, 2007), Fermented sausages composed of pork and/or beef (many types of
Table 2. LAB are fundamental in the production of fermented foods and dry fermented sausages, many types of salami, chorizo, and alheiras
several strains are regarded as probiotics. Pasolli et al. (2020) in an among others) are produced in the United States and many countries of
extensive study of metagenomic evaluating thousands of LAB genomes Europe, containing the sausages produced in Europe high levels of LAB
from human stool and fermented foods microbiomes samples, demon­ (>108 cfu/g) due to the more artisan system of production.
strated that closely related LAB strains occur in both food and gut en­ Fermented vegetables including olives, sauerkraut, mustard pickles,
vironments and provides unprecedented evidence that fermented foods pickles, and kimchi are produced in many countries worldwide, are also
can be indeed regarded as a possible source of LAB for the gut a rich source of LAB species. Kimchi, traditional Korean food made by
microbiome. the fermentation of vegetables, the most common of which is baechu
The importance of fermented foods and beverages in the human diet (cabbage, Brassica rapa) kimchi (>70% of kimchi) has become popular
is due to their enhanced shelf-life, safety, functionality, sensory, and globally because of its sensory, beneficial, and nutritional properties
nutritional properties (the presence of bioactive molecules, vitamins, (Park, Kim, & Jeong, 2017). Heterofermentative LAB belonging to the
genera Leuconostoc, Lactobacillus, and Weissella are likely to be key
Table 2 players in kimchi fermentation (Jung, Lee, & Jeon, 2014). According to
Examples of non-dairy probiotic foods. Park et al. (2017), it presents many health benefits, and kimchi LAB
Food/beverages Applications Reference
exhibit antioxidative, anticancer, immune-stimulatory effects, and an­
product tiobesity, and other probiotic activities. In a European Project PRO­
BIOLIVES, a total of 597 strains of LAB were screened for probiotic
Sauerkraut (salted white It contains minerals, Peñas, Martinez-
cabbage fermented vitamins, and antioxidants Villaluenga, and Frias properties by in vitro tests, and 38 strains were found to possess probiotic
using lactic acid which are important for eye (2017) characteristics, specifically 9 strains belonging to Lactiplantibacillus
bacteria) health and other disease pentosus (formerly Lb. pentosus), Lactiplantibacillus plantarum (previously
prevention.
Lb. plantarum) and Lacticaseibacillus paracasei (formerly Lb. paracasei
Pickles They are the warehouse of Behera, El Sheikha, and
valuable nutrients and Hammami (2020)
subsp. paracasei) in Greece, 4 Lactiplantibacillus pentosus (formerly Lb.
antioxidants. It helps in pentosus), strains in Spain, 17 Lactiplantibacillus plantarum (formerly Lb.
protection from diabetes. plantarum), and Leuconostoc mesenteroides in Italy, 3 Lactiplantibacillus
Tempeh (soybean It is rich in vitamin B12 Murata, Ikehata, and plantarum (formerly Lb. plantarum), Lactiplantibacillus paraplantarum
product fermented by which is mostly found in Miyamoto (1967)
(formerly Lb. paraplantarum), Lactiplantibacillus pentosus (formerly Lb.
lactic acid bacteria) animal products.
Fruit juices (cranberry, They are also rich in Aspri et al. (2020), pentosus), in Portugal and 5 Lactiplantibacillus plantarum (formerly Lb.
sweet lime, grapes, vitamins, antioxidants, Perricone, Bevilacqua, plantarum) (Zheng et al., 2020; http://www.lactobacillus.uantwerpen.
olive, pineapple, fibers (prebiotics); Sensory and Altieri (2015), be/) strains in Tunisia.
strawberry, mango, and nutritional aspects. Amorim, Piccoli, and
Xia, Meng, Zhang, Lei, and Liu (2021) isolated and identified 61
carrot, cashew apple, Duarte (2018)
oranges, and beetroot)
strains of LAB from spontaneously fermented rose jams and submitted
Fermented cereal food The organic acids produced Prado, Parada, and them to through a series of in vitro probiotic tests, including resistance to
(Bushera, Boza, Pozol, during the fermentation of Pandey (2008), Reddy low pH, bile salts, simulated gastric, and simulated pancreatic digestion,
Togwa, and Mahewu) cereals increase the (2015). as well as antibiotic susceptibility. The best 5 strains (MP3, MP11,
availability of various
MP13, MP16, and MY8) with the highest probiotic activity were iden­
minerals such as iron,
phosphorus, and calcium. tified as Pediococcus pentosaceus. MP13 strain revealed like or even
This can also be due to the better probiotic characteristics than the reference probiotic Lactiplanti­
presence of phytases and bacillus plantarum (formerly Lb. plantarum), ATCC 8014 as well a better
other microbial enzymes. technological performance, reflected in increased total phenols, total
The presence of dietary
fibers that can act as
flavonoids, and anthocyanins content, and DPPH, and improved flavor
prebiotics. of the rose jam.
Fermented meat Fermented sausages are Aspri et al. (2020) Numerous worldwide traditional non-dairy fermented beverages
products (Swiss generally considered to be such as Boza, Pozol, Bushera, Mahewu, and Togwa, among others,
salami, Italian salami, the best vehicles for the
whose raw materials include cereals, millets, legumes, fruits, and veg­
sturgeon fermented survival and growth of
sausage, mutton probiotic bacteria. They etables are good sources of probiotics and prebiotics (Krishnamoorthy &
fermented sausage, protect the bacterial cells Arjun, 2012; Vasudha & Mishra, 2013).
Hungarian salami, and from the extreme Boza is a cereal beverage that is obtained from the fermentation of
Norwegian salami) environment in the whole grains such as maize and wheat (Kivanc, Yilmaz, & Demir, 2011)
gastrointestinal tract such
as low pH and bile salts.
or flour. It is popular in Turkey, Kazakhstan, Kyrgyzstan, Albania,
Plant sterol (PS)- Elevation of phytosterol Gonzalez-Larena, Bulgaria, Macedonia, Montenegro, Bosnia and Herzegovina, and parts of
enriched beverages oxidation products (POPs) Garcia-Llatas, Clemente, Romania and Serbia. There are also similar beverages produced in East
Barbera, and Lagarda European countries (braga or brascha), the Balkans (busa), and Egypt
(2015)
(bouza) (Petrova & Petrov, 2017). From this fermented food, Kivanc

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F. Cosme et al. Food Research International 151 (2022) 110842

et al. (2011) isolated many strains of Lactiplantibacillus plantarum Lb. crustorum) (1). Most strains presented immunomodulatory effects,
(formerly Lb. plantarum), that showed antagonistic activity against and some exhibited high acid tolerance properties and good bile acid
pathogenic bacteria, both gram-positive (Listeria monocytogenes, Bacillus tolerance. Due to its high cell adhesion, the strain P. acidilactici (PA5)
cereus, B. subtilis) and gram-negative (Yersinia enterocolitica, Escherichia was revealed to be a putative candidate as a probiotic for further food
coli, Pseudomonas aeruginosa, Salmonella enterica subsp. enterica Serovar industry applications.
Typhimurium and Klebsiella pneumoniae). In addition to Lactiplantiba­ Palm wine is a traditional alcoholic beverage made using the sap
cillus plantarum (formerly Lb. plantarum), many more LAB species mak­ collected from different palm tree species according to their geographic
ing part of the microbiome of boza have been isolated and identified. origin. This beverage is consumed in countries of Africa (Cameroon and
According to Petrova and Petrov (2017), they are distributed by: (i) Côte d’Ivoire), America (Mexico), and Asia (Borneo, India) thus being
formerly genus Lactobacillus (Lactiplantibacillus paraplantarum, Lacti­ known with local and different designations (Astudillo-Melgar, Ochoa-
plantibacillus pentosus, Lactobacillus acidophilus, Lacticaseibacillus casei, Leyva, Utrilla, & Huerta-Beristain, 2019; Fossi, Goghomu, Tongwa,
Lacticaseibacillus paracasei, Lacticaseibacillus rhamnosus, Levilactobacillus Ndjouenkeu, & Cho Ngwa, 2017; Kouamé, Aké, & Assohoun, 2020).
brevis, Lentilactobacillus buchneri, Lentilactobacillus parabuchneri, Limosi­ Astudillo-Melgar et al. (2019) disclosed that Fructobacillus was the
lactobacillus fermentum, Loigolactobacillus coryniformis, Latilactobacillus principal genus in all the samples followed by Leuconostoc inside the LAB
graminis, Fructilactobacillus sanfranciscensis); (ii) genus Leuconostoc group during the fermentation process of Tuba (palm wine) from com­
(Leuconostoc citreum, Leuc. lactis, Leuc. mesenteroides, Leuc. mesenteroides mercial and laboratory-controlled conditions samples. For the identifi­
subsp. dextranicum, Leuc. mesenteroides subsp. mesenteroides, Leuc. par­ cation of the strains and evaluation of bacterial diversity and population
amesenteroides, Leuc. raffinolactis); (iii) genus Weissella (Weissella oryzae, dynamics, the authors used a molecular approach by next-generation
W. confusa); (iv) genus Lactococcus (Lactococcus lactis); (v) genus Oeno­ sequencing of the V3–V4 regions of the 16S rRNA gene. Also, with
coccus (O. oeni); (vi) genus Enterococcus (Ent. faecium); (vii) genus Ped­ 16S rRNA gene sequencing and typification by (GTG)5-PCR finger­
iococcus (Pediococcus spp., Pd. pentosaceus, Pd. parvulus, Pd. printing, Kouamé et al. (2020) identified their palm wine LAB isolates as
ethanolidurans). Leuconostoc mesenteroides (45.66%), Fructobacillus durionis (40.33%),
Kunu-zaki is a Nigerian traditional fermented non-alcoholic drink and with Leuconostoc pseudomesenteroides, Lacticaseibacillus paracasei
made from non-germinated sorghum and millet cereal grains (Agarry, (formerly Lb. paracasei), Limosilactobacillus fermentum (formerly Lb. fer­
Nkama, & Akoma, 2010; Oluwajoba, Akinyosoye, & Oyetayo, 2013). mentum), Weissella cibaria, Enterococcus casseliflavus and Lactococcus
The latter authors isolated probiotic LAB strains belonging to Lactoba­ lactis occurring occasionally. Fossi et al. (2017) isolated 3 bacter­
cillus, Pediococcus, and Lactococcus species with antimicrobial activity iocinogenic LAB strains identified as Levilactobacillus brevis (formerly Lb.
against strains of Staphylococcus aureus, Escherichia coli, Pseudomonas brevis), Lactiplantibacillus plantarum (formerly Lb. plantarum), and Lacti­
aeruginosa, and Enterococcus faecalis. caseibacillus rhamnosus (formerly Lb. rhamnosus) that showed high
Limosilactobacillus fermentum (formerly Lb. fermentum) KKL1 was the antimicrobial activity against gram-positive bacteria (Staphylococcus
main LAB strain isolated in Haria, one of the most popular traditional aureus, and Listeria monocytogenes) and gram-negative (Escherichia coli,
rice beers, consumed in certain areas of India (Gosh et al., 2015). These Salmonella enterica, Salmonella enterica subsp. enterica Serovar
authors emphasize that traditional fermented foods prepared from the Typhimurium).
most common types of available cereals (rice, wheat, corn, or sorghum, Pulque is a traditional Mexican alcoholic beverage produced from
etc.) present higher nutritional value, shelf-life, and digestibility the fermentation of the fresh sap known as aguamiel (mead) extracted
compared to unfermented raw material. from several species of Agave (maguey) plants (Escalante et al., 2008,
Hardaliye is another non-alcoholic fermented beverage, but from 2016; Rocha-Arriaga et al., 2020). Escalante et al. (2008) characterized
Turkey, produced from a mixture of red grapes (Vitis vinifera) juice with for the first time by a polyphasic approach utilizing both culture and
the addition of different concentrations of whole/ground or heat-treated non-culture-dependent methods, the bacterial community present dur­
crushed mustard seeds (Sinapis alba) and dried sour cherry leaves ing the fermentation of pulque. Concerning to LAB population, the
(Prunus cerasus) (Coskun, 2017). In 2001, Arici and Coskun were able to species identified belong to formerly Lactobacillus (Lactobacillus spp., Lb.
isolate and identify 15 strains as Lacticaseibacillus paracasei subsp. par­ acidophilus, Lentilactobacillus hilgardii, Secundilactobacillus para­
acasei (formerly Lb. casei subsp. pseudoplantarum), 6 as Limosilactoba­ collinoides, Fructilactobacillus sanfranciscencis), Lactococcus (Lactococcus
cillus pontis (formerly Lb. pontis), 3 as Levilactobacillus brevis (formerly Lb. spp., Lactococcus lactis, Lactococcus lactis subsp. cremoris), to Leuconostoc
brevis), 3 as Lactobacillus acetotolerans, 3 as Fructilactobacillus san­ (Leuconostoc kimchi, Leuc. citreum, Leuc. gasicomitatum, Leuc. mesenter­
franciscensis (formerly Lb. sanfransisco), and 3 as Paucilactobacillus vac­ oides, Leuc. pseudomesenteroides) genera, Pediococcus urinaeequi, and
cinostercus (formerly Lb. vaccinostercus). The results obtained by Streptococcus devriesei.
Amoutzopoulos et al. (2013) confirmed the predominance of a LAB Currently, beyond probiotic fermented foods and beverages, there
population constituted exclusively by Lactobacillus species. are many LAB probiotics formulations available, commercialized mostly
Water kefir is a sour, alcoholic, and fruity fermented beverage plenty in capsules, tablets, powder, and liquid forms (Nagashima, Pansiera,
rich in LAB species. By using molecular approaches Lacticaseibacillus Baracat, & Gómez, 2013; Sreeja & Prajapati, 2013) and may be incor­
casei/paracasei (formerly Lb. casei/paracasei), Schleiferilactobacillus har­ porated in dietary supplements and functional foods (Forssten, Laitila,
binensis (formerly Lb. harbinensis), Lentilactobacillus hilgardii (formerly Maukonen, & Ouwehand, 2020), other “dry” food matrices which are
Lb. hilgardii), Bifidobacterium psychraerophilum/crudilactis (Laureys & De expected to have up to 24 months of stability at ambient temperature
Vuyst, 2014), Liquorilactobacillus nagelii (formerly Lb. nagelii), Liq­ and humidity (Fenster et al., 2020). The number of LAB strains in each
uorilactobacillus hordei/mali (formerly Lb. hordei/mali), Bifidobacterium formulation is variable (from 1 to 13 strains) within each trademark.
aquikefiri, and a novel Oenococcus species related to Oenococcus oeni and Table 3 presents some examples of the many LAB formulations available
Oenococcus kitaharae under the name of Candidatus Oenococcus aquikefiri worldwide.
were identified (Verce, De Vuyst, & Weckx, 2019). We should emphasize the reduced expression of other bacterial
Makgeolli or takju is a turbid rice wine, a traditional Korean alco­ groups as probiotics, with only strains of Bacillus coagulans appearing in
holic beverage, that is brewed by fermenting a mixture of steamed rice Probiotic Lister + formulation, Bacillus subtilis appearing in formulations
and nuruk (wheat or grits fermented with fungi, yeast, and lactic acid of Prebiotech Healthcare and Lallemand, as well as, just one trademark
bacteria) (Kim, Jun, Lee, Hwang, & Rhee, 2018). From this beverage (Digest Ultra Probiotics) association with yeasts, namely with Saccha­
Park et al. (2015), isolated 17 different LAB strains identified as Ped­ romyces boulardii strains, which can also be traded alone as probiotics
iococcus acidilactici (8), P. pentosaceus (6), Latilactobacillus curvatus (Vilela et al., 2020).
(formerly Lb. curvatus (2), and Companilactobacillus crustorum (formerly A few examples of the clinical trials with the most used bacterial

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F. Cosme et al. Food Research International 151 (2022) 110842

Table 3 Table 3 (continued )

Examples of LAB probiotics formulations available in the world market. Formulations LAB strains References
Formulations LAB strains References
Lactobacillus acidophilus, Accessed 24 April 2021;
Protexin Balance Lacticaseibacillus casei Lacticaseibacillus paracasei Drago & De Vecchi, 2009; Cao
(formerly Lb. casei) PXN 37 subsp. paracasei (formerly Lb. et al., 2020
Lacticaseibacillus rhamnosus paracasei subsp. paracasei),
(formerly Lb. rhamnosus) PXN Lactiplantibacillus plantarum
54 subsp. plantarum (formerly Lb.
Streptococcus thermophilus plantarum), Ligilactobacillus
PXN 66 salivarius (formerly Lb.
Bifidobacterium breve PXN 25 salivarius), Bacillus coagulans,
Lactobacillus acidophilus PXN Lactococcus lactis,
Protexin 35 Saccharomyces boulardii
Protect Bifidobacterium longum PXN Isolated strains Lacticaseibacillus rhamnosus Lallemand Retrieved from
30 (formerly Lb. rhamnosus) https://www.lallemand.com.
Lactobacillus delbrueckii subsp. Prebiotech Healthcare. Rosell-11ME; Lactobacillus Accessed 24 April 2021
Protexin bulgaricus (formerly Lb. Retrieved from helveticus Rosell-52 ME;
Restore bulgaricus) PXN 39 http://prebiotech.com. Bifidubacterium longum Rosell-
(TVC: 200 million CFU TVC: 2 Accessed 24 April 2021 175 ME; Bacillus subtilis
× 108 CFU) Rosell-179
Protexin ProBiotics Lister Lactobacillus acidophillus, LISTER + Retrieved from
Vitality The same 7 strains + Lacticaseibacillus rhamnosus https://www.listermais.com.
(TVC: 2 billion CFU/daily (formerly Lb. rhamnosus), Accessed 2 September 2021
dose 2 × 109 CFU plus Garlic Bifidobacterium bifidum,
Protexin concentrate 60.00 mg) B. lactis plus Bacillus coagulans
Biokult and inulin
The same 7 strains except UREX; Lacticaseibacillus rhamnosus Chr. Hansen Retrieved from
Bifidobacterium longum PXN (formerly Lb. rhamnosus) GR-1 https://www.chr-hansen.
35 and Limosilactobacillus reuteri com. Accessed 24 April 2021
(TVC: 1 billion CFU TVC: 1 × RC-14
109 CFU plus Bifidobacterium VSL3 Streptococcus thermophilus, VSL3 Retrieved from
infantis (child-specific) PXN Bifidobacterium breve, B. https://www.vsl3.com.
27 longum, B infantis, Accessed 24 April 2021
Lactobacillus acidophilus,
The same 7 strains except Lactiplantibacillus plantarum
Bifidobacterium longum PXN subsp. plantarum (formerly Lb.
35 plantarum), Lacticaseibacillus
(TVC: 200 million CFU TVC: 2 paracasei subsp. paracasei
× 108 CFU plus (formerly Lb. paracasei subsp.
Bifidobacterium infantis (child- paracasei), Lactobacillus
specific) PXN 27 delbrueckii subsp. bulgaricus
(formerly Lb. bulgaricus)
The same 7 strains
(plus Bacillus subtilis PXN 21;
Bifidobacterium bifidum PXN strains worldwide as probiotics that have scientifically proven the health
23; Bifidobacterium longum benefits of their consumption are exemplified below.
PXN 30; Lactiplantibacillus
A study performed by Sanborn, Azcarate-Peril, Updegraff, Mander­
plantarum subsp. plantarum
(formerly Lb. plantarum) PXN ino, and Gunstad (2020) with a total of 145 participants (aged 52–75) in
47; Lactobacillus helveticus a double-blind, placebo-controlled, randomized clinical trial, during a
PXN 45; Ligilactobacillus three-month intervention involved daily consumption of probiotic or
salivarius (formerly Lb. placebo, showed that Lacticaseibacillus rhamnosus (formerly Lb. rham­
salivarius) PXN 57;
Lactococcus lactis ssp. lactis
nosus) GG strain probiotic supplementation was associated with
PXN 63) improved cognitive performance in middle-aged and older adults with
Ultrabiotique Lactobacillus helveticus UBi Laboratoires Nutrisanté. cognitive impairment. Based on these results, the authors defend that
Equilibre 30 114, Lacticaseibacillus Retrieved from https://www. probiotic supplementation may be a novel method for protecting
jours rhamnosus (formerly Lb. nutrisante.fr/en/home/.
cognitive health in aging.
rhamnosus) UBi 125, Accessed 24 April 2021
Lactiplantibacillus plantarum The efficacy of Lacticaseibacillus rhamnosus (formerly Lb. rhamnosus)
subsp. plantarum (formerly Lb. GR-1 and Limosilactobacillus reuteri (formerly Lb reuteri subsp. reuteri)
plantarum) UBi 176, RC-14 probiotic strains prepared in capsules and administered orally
Bifidobacterium breve UBi 263 was assessed by Vujic, Jajac Kne, Despot Stefanovic, and Kuzmic
Zumub Bifidobacterium infantis, ZUMUB. Retrieved from
Advanced Bifidobacterium lactis, https://www.zumub.com.
Vrbanovic (2013) to evaluate their potential in the treatment of bacte­
Probioticare Enterococcus faecium, Accessed 24 April 2021 rial vaginosis and other vaginal infections. Their clinic study involved
Bifidobacterium bifidum, 544 women older than 18 years of age, diagnosed with vaginal infection.
Lactobacillus acidophilus, The results obtained allowed the authors to conclude that oral probiotics
Lacticaseibacillus casei
could be an alternative, side-effect-free treatment for one of the most
(formerly Lb. casei),
Lacticaseibacillus rhamnosus common indications in gynaecology, combining the good aspects of both
(formerly Lb. rhamnosus), metronidazole and vaginal capsules.
Streptococcus thermophilus, In a randomized, double-blind, placebo-controlled clinical trial, fifty-
Ligilactobacillus salivarius three patients with Non-alcoholic fatty liver disease (NAFLD) were
(formerly Lb. salivarius)
Digest Ultra Bifidobacterium infantis, B. Eladiet. Retrieved from
randomly assigned to receive either a synbiotic (Bacillus coagulans plus
Probiotics lactis, B. longum, E. faecium, https://www.eladiet.com. inulin) or a placebo capsule for 12 weeks (Abhari et al., 2020). The
authors observed a reduction in steatosis score in Fibroscan exam of

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F. Cosme et al. Food Research International 151 (2022) 110842

patients, concluding that this treatment with a probiotic and a prebiotic its importance as a food preservative; (5) similarly as some other strains
is beneficial for the treatment of NAFLD and its related inflammation of lactobacilli and bifidobacteria wine LAB induce the production of
without any significant effects on related cardiovascular risk factors. cytokines by monocytes and lymphocytes, thus its intake may be useful
in the prevention or treatment of inflammatory bowel diseases or atopic
2.3. The special case of malolactic bacteria (MLB) as a source of LAB disease.
probiotics García-Ruiz et al. (2014) evaluated the probiotic properties of 11
enological LAB strains of Lactobacillus, Pediococcus, and Oenococcus oeni
Malolactic bacteria are responsible for Malolactic Fermentation and two probiotic reference strains, Limosilactobacillus fermentum
(MLF), a secondary fermentation that takes place after alcoholic (formerly Lb. fermentum) CECT5716 and Lactiplantibacillus plantarum
fermentation in the process of grape wine production. There are many (formerly Lb. plantarum) CLC 17. Amongst the evaluated probiotic fea­
LAB species able to perform this biological deacidification of wine in tures such as saliva and acid resistance, bile tolerance, and exopoly­
which L-malic dicarboxylic acid is converted to L-lactic monocarboxylic saccharides production, were Lactobacillus and Pediococcus strains that
acid. According to a recent publication of Inês and Falco (2018), it is exhibited higher resistance to lysozyme (conditions simulating the in
possible to find the following groups of MLB species: (1) Hetero­ vivo dilution by saliva) and ability to survive at low pH values of 1.8 and
fermentative cocci (Leuconostoc citrovorum, Leuc. mesenteroides subsp. bile salts (simulating stomach and small intestine, respectively),
dextranicum, Leuc. mesenteroides subsp. mesenteroides, Leuconostoc spp., revealing thus good adaptation of the wine strains to gastrointestinal
Weissella confusa, W. paramesenteroides, Weissella spp., W. uvarum, conditions.
Oenococcus oeni); (2) Homofermentative cocci (Pediococcus acidilactici, They also evaluated the capacity of the wine strains to adhere to the
Pc. damnosus, Lapidilactobacillus dextrinicus (formerly Pc. dextrinicus), Pc. intestinal mucosa and to prevent the adhesion of Escherichia coli strains
inopinatus, Pc. parvulus, Pc. pentosaceus, Pediococcus spp., Lactococcus to human intestinal cells, using Caco-2 cells. In this study even when
lactis, Lactococcus spp., Enterococcus spp.); (3) Homofermentative bacilli compared to probiotic reference strains, a Pediococcus pentosaceus strain
(Lactobacillus delbrueckii, Lb. jensenii, Liquorilactobacillus mali (formerly revealed a higher percentage of adhesion to intestinal cells and high
Lb. mali), Liquorilactobacillus vini (formerly Lb. vini); (4) Facultative anti-adhesion activity against E. coli, thus supporting that this specific
heterofermentative bacilli - Lacticaseibacillus casei (formerly Lb. casei), wine MLB strain has a high potential to be used as a probiotic.
Loigolactobacillus coryniformis (formerly Lb. coryniformis), Lat­ In another study, only with O. oeni strains, Su et al. (2015) also
ilactobacillus curvatus (formerly Lb. curvatus), Fructilactobacillus fructi­ observed good survival abilities at low pH values (pH 1.8) and bile salts
vorans (formerly Lb. homohiochii), Lacticaseibacillus paracasei (formerly (1%) thus assuming good adaptation to gastrointestinal conditions and
Lb. paracasei), Lactiplantibacillus pentosus (formerly Lb. pentosus), Lacti­ high bile resistance abilities of those strains. The authors also verified
plantibacillus plantarum (formerly Lb. plantarum), Latilactobacillus sakei their effectiveness in the defense against in vitro oxidative stress, so
(formerly Lb. sakei), Lacticaseibacillus zeae (formerly Lb. zeae), Liq­ putatively serve as defensive agents in the intestinal microbial
uorilactobacillus nagelii (formerly Lb. nagelli), Lentilactobacillus diolivorans ecosystem and overcome endogenous and exogenous oxidative stress.
(formerly Lb. diolivorans); (5) Heterofermentative bacilli (Levilactoba­ Foligné et al. (2010) advocate that the potential of MLB strains as
cillus brevis (formerly Lb. brevis), Lentilactobacillus buchneri (formerly Lb. probiotics should be better exploited as a supplement rather than in
buchnerii), Secundilactobacillus collinoides (formerly Lb. collinoides), functional food.
Limosilactobacillus fermentum (formerly Lb. fermentum), Fructilactoba­ According to the data collected by Industry Arc, Market Research,
cillus fructivorans (formerly Lb. fructivorans), Lentilactobacillus hilgardii and Research and Market, companies, and made available on their sites,
(formerly Lb. hilgardii), Apilactobacillus kunkeei (formerly Lb. kunkeei), the global probiotics market is estimated to be valued at USD 61.1
Fructilactobacillus sanfranciscensis (formerly Lb. sanfrancisensis), billion in 2021 and is projected to reach USD 95.25 billion by 2028, at a
(formerly Lactobacillus spp.), Paucilactobacillus vaccinostercus (formerly compound annual growth rate (CAGR) of 7.2% during the forecast
Lb. vacinostercus). period. Factors affecting the growth of the probiotics market are health
Given the high diversity of LAB species present in this beverage, we benefits associated with probiotic-fortified foods and technological ad­
can infer that wine constitutes an excellent source of LAB to be used as vancements in probiotic products. Increasing consumer awareness about
probiotic cultures. Moreover, as can be seen, many of these LAB species healthy diets and the aging population in some regions of the world
isolated and identified in wine are already present in the formulations of (Asia countries) also reflects the market’s growth of probiotics.
the probiotics previously presented in Table 3. On the other hand, the Yeasts are expected to be the fastest-growing ingredients of pro­
high diversity observed, will also make it possible to assess the potential biotics, namely Saccharomyces boulardii, due to the increasing demand
of other strains and species not yet explored as probiotics. for products incorporating this yeast species. However, Lactobacillus-
It should also be noted that according to some authors, as wine is an based probiotic supplements continue to exert stronger consumer appeal
adverse environment (acid, ethanol, and phenolic compounds) the iso­ and vaginal probiotic supplements based on Lactobacillus have been
lated strains, present natural tolerance towards these conditions, char­ gathering significant adhesion by consumers over the years. An increase
acteristics that enhance their use as live probiotics (Su et al., 2015). in the adoption of Bifidobacterium and Streptococcus-based probiotic
The pioneering work on the putative use of MLB as probiotics was supplements is to be seen in the neighboring future. As an example,
carried out by Foligné et al. (2010). The authors underline a set of Japanese consumers have available already in supermarkets, a wide
characteristics that MLB strains may have even “beneficial” or “unsuit­ variety of products containing strains of Lactobacillus and Bifidobacte­
able” for winemaking may have health-promoting potential. Indepen­ rium genera, ranging from fortified drinks to candies.
dently of their suitability for winemaking, the authors underline a set of
characteristics that MLB strains may have that contribute to their health- 3. Non-dairy unfermented or fermented foods as a source of
promoting potential. The main characteristics of wine LAB are (1) high prebiotics
resistance to an acidic and alcoholic environment and sulfur dioxide
stress; (2) the ability by some strains to produce exopolysaccharides Worldwide consumers are more and more alert to the relation be­
(EPS), that may confer resistance to bile salts and low pH, and also allow tween nutrition and health. Consumers attribute great importance to
adhesion to intestinal epithelial cells and to reduce biofilm formation of their health; therefore, they not only search for tasty and attractive foods
pathogens (this characteristic is observed in probiotic strains used for but even more for safe and healthy foods (Lai, Yang, & Liu, 2017). The
colitis attenuation); (4) the ability by some strains to produce and major segment of this market includes foods designed to increase gut
excrete bacteriocins with activities against enterococci and Listeria health such as prebiotics. The concept of prebiotics was introduced and
monocytogenes thus playing a role in animal and human health, as well as defined for the first time in 1995 by Gibson and Roberfroid (Gibson &

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F. Cosme et al. Food Research International 151 (2022) 110842

Roberfroid, 1995) as “non-digestible food constituents that beneficially prebiotics on bowel function, however, prebiotics, such as inulin, can
affect the host by selectively stimulating the growth and/or activity of improve bowel function in patients with chronic constipation by posi­
one or a limited number of bacterial species already resident in the tively influencing intestinal biota. Yurrita, Martín, Ciudad-Cabañas,
colon”. However, in 2010 the International Scientific Association for Calle-Purón, and Cabria (2014) performed a meta-analysis of random­
Prebiotics and Probiotics (ISAPP) prolonged the definition to comprise ized controlled clinical trials involving 252 subjects and they found a
also the functionality of the prebiotics: “a selectively fermented ingre­ significant overall effect of inulin on stool frequency, stool consistency,
dient that results in specific changes in the composition and/or activity transit time, and hardness of the stool. Micka, Siepelmeyer, Holz, Theis,
of the gastrointestinal microbiota, thus conferring benefit(s) upon host and Schön (2017) studied the effect of Inulin on stool frequency in forty-
health” (Gibson et al., 2010). Nevertheless, in December 2016, spe­ four healthy subjects with constipation. Consumption of Inulin signifi­
cialists of the ISAPP suggested the new definition of a prebiotic, “a cantly increased stool frequency compared to placebo, improving bowel
substrate that is selectively utilized by host microorganisms conferring a function.
health benefit” (Gibson et al., 2017). The best-known sources of prebiotics are found in different foods,
There are several kinds of prebiotics, being many of them carbohy­ such as root and tuber crops as well as some fruit crops, while the
drate generally non-digestible oligosaccharides, that are low molecular prebiotic-rich grain crops include barley, chickpea, lentil, lupin, wheat,
weight carbohydrates of intermediate in nature between simple sugars rye-flour, well as asparagus, leeks, onions, soybeans, oats, Jerusalem
and polysaccharides (Davani-Davari et al., 2019). In non-digestible ol­ artichokes, garlic, chia seeds, dandelion greens, flaxseeds, bananas, and
igosaccharides, the anomeric C atom (C1 or C2) of the monosaccharide chicory (Davani-Davari et al., 2019; do Prado, Castro-Alves, Ferreira, &
units has a configuration that makes their osidic bounds non-digestible Fabi, 2019; Van-Loo, Coussement, & de Leenheer, 1995). The prebiotics
to the hydrolytic activity of the human digestive enzymes (Roberfroid & content, in most of these foods, is around 0.3% and 6% of fresh weight;
Slavin, 2010). Prebiotics are recognized for their ability to sustain gut for chicory, this content is between 5% and 10% while in Jerusalem
microorganisms existing in the gastrointestinal tract and substantially artichoke they can reach up to 20%.
improve their metabolic activity, increasing nutrient absorption ability, The two most important groups of prebiotics with valuable effects on
digestion, and the immune system while decreasing the growth of human health are non-digestible oligosaccharides fructans [fructooli­
pathogenic microorganisms (Lockyer & Stanner, 2019). These important gosaccharides (FOS) and inulin and galactans (galactooligosaccharides
enhancements show a positive result on human health (Mohr, Jäger, & (GOS)] (Gibson et al., 2017). These oligosaccharides are preferentially
Carpenter, 2020). Therefore, given the importance of these results for metabolized by bifidobacteria as they have β-fructanosidase and
public health, it is suitable to reiterate accurately and supporting in­ β-galactosidase enzymes, respectively (Rastall & Gibson, 2015; Roberf­
formation on their clinical application and use, which is shown in roid et al., 2010).
several clinical trial research using prebiotics (Sanders, Merenstein, The fructose-based carbohydrates, also known as fructans, inulin,
Reid, Gibson, & Rastall, 2019). For example, in the defense against and fructooligosaccharides (FOS) are the most studied prebiotics (Louis,
pathogens, the establishment of a stable population of commensal mi­ Flint, & Michel, 2016). Fructans, in general, is a term used for any
croorganisms will reduce nutrient availability for invading microor­ carbohydrate in which fructosyl-fructose links constitute most of the
ganisms, inhibiting colonization. Also, in studies of elderly healthy glycosidic bonds. They are not hydrolyzed by the human gastrointestinal
individuals, 10 weeks of daily galactooligosaccharide consumption tract enzymes, therefore when they reach the colon, they beneficially
significantly decrease in less beneficial bacteria and a significant in­ stimulate the growth and consolidation of specific bacteria in the in­
crease in beneficial bacteria, especially bifidobacteria, and induced an testine producing short-chain fatty acids (acetate, propionate, butyrate,
increase in immune function, increase in phagocytic activity, and ac­ lactate, etc.) (Olvera, Centeno-leija, & López-munguía, 2007; Voragen,
tivity of natural killer cells (Vulevic et al., 2008, 2015). Concerning 1998). All fructans are resistant to hydrolysis by human digestive en­
immune modulation, the most supportive data come from studies in zymes (α-glucosidase, maltase, isomaltase, and sucrase), due to the
infants (Cuello-Garcia et al., 2016). Prebiotics – non-digestible oligo­ β-configuration of the anomeric C2 of the fructose monomers, which are
saccharides that stimulate the growth of probiotic bacteria – have been specific for α-glycosidic bonds, and are thus classified as non-digestible
stated to modulate immune responses and their supplementation has oligosaccharides based on both in vitro and in vivo data (Cummings,
been recommended in the prevention of allergy (Wawryk-Gawda, Macfarlane, & Englyst, 2001). As defined, the prebiotic effect of fructans
Markut-Miotła, & Emeryk, 2021). Consequently, galacto- and long-chain is to stimulate selectively the growth of bifidobacteria and lactobacilli in
fructooligosaccharides in infant formula administered in a double-blind, the gut and, thereby, increase the body’s natural resistance to invading
randomized, placebo-controlled trial in 259 infants was associated with pathogens (Cummings et al., 2001). They comprise linear fructose
a reduction in the incidence of atopic dermatitis to less than 50% of the chains in β (2 → 1) linkage, frequently with a terminal glucose unit in β
incidence in non-prebiotic formula-fed infants (Ivakhnenko & Nyan­ (2 → 1) linkage as in sucrose (Fig. 3 A and B) (Sabater-Molina, Larqué,
kovskyy, 2013; Moro et al., 2006). Studies have also shown that con­ Torrella, & Zamora, 2009; Voragen, 1998). Inulin usually has chain
sumption by young adolescents of a mixture of fructooligosaccharides lengths with a degree of polymerization from 2 to 60 monomers of
and inulin (Abrams, Griffin, & Hawthorne, 2007; Bakirhan & Kar­ fructose, whereas FOS presented a degree of polymerization lesser than
abudak, 2021) or galactooligosaccharides (Whisner et al., 2013) can 10 (Louis et al., 2016). FOS can be synthesized enzymatically or pro­
result in calcium absorption increases. Whisner et al. (2014) observed duced from inulin by partial hydrolysis (Gibson et al., 2010). However,
that a moderate daily intake of soluble maize fiber resulted in an in­ several prebiotic carbohydrates existent in the usual diet. Fructooligo­
crease in calcium absorption and retention in children. Mineral ab­ saccharides are existent in a concentration from 0.15% to 0.75% of FOS
sorption takes place in the small intestine by active transport in natural food such as in asparagus, Jerusalem artichoke, chicory, leak,
mechanisms (Diaz de Barboza, Guizzardi, & Tolosa de Talamoni, 2015) sugar beet, onion, garlic, barley, wheat, honey, banana, tomato, and rye
and prebiotics have been shown to increase calcium absorption in the (Shigwedha, Hiwilepo-Van Hal, Jia, Sichel, & Zhang, 2016; Yadav &
lower intestines of both preclinical and human models (Whisner & Shukla, 2017). Namely, barley and tomato contain 0.15 %, banana has
Castillo, 2018). Whisner et al. (2016) proposed that the bacterial 0.30 %, and honey has 0.75 % of FOS (Flamm, Glinsmann, Kritchevsky,
fermentation of prebiotics leads to the production of short-chain fatty Prosky, & Roberfroid, 2001). FOS is the main soluble carbohydrate
acids reducing the gut luminal pH, which may increase calcium solu­ found in the dry matter of onion and demonstrates outstanding prebiotic
bility and transcellular absorption. The use of fructooligosaccharides is properties by improving gut microflora (Galdón, Rodríguez, Rodríguez,
also described, to improve the absorption of minerals and trace elements & Romero, 2009). Total FOS ranged from nd-0.89 g/100 g fresh weight
appearing to be beneficial with evidence corroborating in studies with of an edible sample of 32 fruits and nd-3.32 g/100 g fresh weight of an
humans (Costa et al., 2021). There are few studies on the effect of edible sample of 41 vegetables (Jovanovic-Malinovska, Kuzmanova, &

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Fig. 3. (A) Inulin, a fructan-type polysaccharide, consists of (2 → 1) linked β-d-fructosyl residues (n = 2–60), usually with a (1 → 2) α-d-glucose end group. (B)
Examples of foods high in inulin.

Winkelhausen, 2014), being the total content of fruits oligosaccharides (0.5–1.0 g/100 g), and garlic (9–16 g/100 g) (Fig. 4 A). In cereals, for
in a decreasing order nectarine > watermelon > pear > raspberry > example, wheat has lower concentrations of inulin-type fructans (1–4 g/
blueberry and for vegetable, scallion > onion > garlic > leek > spring 100 g) (Carpita, Kanabus, & Housley, 1989; Van-Loo et al., 1995) they
garlic. Fructans isolated from plants have a wide variety of uses. Fruc­ are the main source of fructan intake in the United Kingdom (66%)
tans with a large degree of polymerization form emulsions with a fatlike [inulin (66.2%±16.5) and oligofructose (69.2%±15.5)] (Dunn, Datta, &
texture and neutral taste whereas, fructans with a small degree of Kallis, 2011).
polymerization have a sweet taste, the food industry also shows a great Galactooligosaccharides are oligosaccharides composed of diverse
interest in using these fructans as low-calories and as ingredients of galactosyl residues (2–9 units) and terminal glucose linked by β-glyco­
nutraceutical food (Vijn & Smeekens, 1999). Garlic fructan is an sidic bonds, such as β(1 → 2), β(1 → 3), β(1 → 4), and β(1 → 6) (Illanes,
important constituent of garlic, accounting for around 75% of its dry Vera, & Wilson, 2016). They comprised raffinose family oligosaccha­
weight, and has been described to have prebiotic characteristics influ­ rides, which are based on the extension of sucrose with galactose resi­
encing gut microbiota (Zhang, Huang, Zeng, Wu, & Peng, 2013). Inulin dues (Fig. 4 A and B), normally comprise between two and 10 molecules
is the non-digestible prebiotic found in chicory root, which is the poly­ of galactose and one molecule of glucose and are other naturally
mer of fructose linked through the β (2 → 1) glycosidic linkage, and it occurring non-digestible oligosaccharides. Shorter chain gal­
aids in nourishing probiotic bacteria (El-Kholy, Aamer, & Ali, 2020). actooligosaccharides, such as raffinose, stachyose, and verbascose, are
Fresh chicory contains inulin (68%), sucrose (14%), protein (6%), cel­ commonly found in pulse (Brummer, Kaviani, & Tosh, 2015).
lulose (5%), ash (4%), and other compounds (3%) compared to dried Resistant starch is the fraction of starch that resists digestion in the
chicory, which contains inulin (98%) and other compounds (2%) upper gut due to its physicochemical properties, it is found in both
(Nwafor, Shale, & Achilonu, 2017). According to Van-Loo et al. (1995), processed and whole starch-containing foods, such as bread, grains,
inulin-type fructans were detected in chicory root (35.7–47.6 g/100 g), pasta, cereals, beans and legumes, potatoes, and rice, example of values
Jerusalem artichoke (16–20 g/100 g), wheat (1.0–3.8 g/100 g), raw found in cereal grains (7.2–25.2 g/100 g dry matter) and legumes
onion pulp (1.1–7.5 g/100 g), raw asparagus (2.0–3.0 g/100 g), barley (17.7–35.4 g/100 g dry matter) (Fuentes-Zaragoza et al., 2011; Lunn &

Fig. 4. (A) Galactooligosaccharides: Raffinose family oligosaccharides α-(1 → 6)-galactosyl derivatives of sucrose (α-D-glucopyranosyl-(1 → 2)-β-D-fructofurano­
side); (B) α-Galactooligosaccharides occur naturally in legumes such as lentils, chickpeas, and beans (Kao, Harty, & Burnet, 2016).

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Buttriss, 2007). The quantity of resistant starch differs between diverse (Hervert-Hernández & Goñi, 2011). The main dietary polyphenols are
foods (such as cereals, legumes, and potatoes), and food processing can phenolic acids, flavonoids, tannins, stilbenes, and diferuloylmethanes
also affect resistant starch content. There are currently 5 types of (Kinger, Kumar, & Kumar, 2018). These dietary polyphenols are natural
resistant starch (RS), R1 - physically inaccessible starch (whole- or partly compounds present in many foods and plant-based beverages, namely in
milled grains and seeds, legumes), R2 – ungelatinized resistant granules vegetables, fruits, cereals, coffee, tea, and wine, among others. Wine
with type B crystallinity, slowly hydrolyzed by α-amylase (high-amylose phenolic compounds have been suggested to modulate gut microbiota
maize starch, raw potato, raw banana starch, some legumes, high inducing prebiotic-like effects of the growth of beneficial bacteria and
amylose corn), R3 - retrograded starch (cooked and cooled starchy the inhibition of pathogenic bacteria (Cueva et al., 2013, 2017). Also,
foods, potatoes, bread, cornflakes, food products with repeated moist intestinal bacteria metabolize wine phenolic compounds into bioavail­
heat treatment), R4 - chemically modified starches (cross-linked starch able metabolites. The beneficial actions designated for wine have been
and octenyl succinate starch, bread, cakes) and R5- amylose–lipid recognized to these phenolic microbial-derived metabolites rather than
complex (stearic acid-complexed high-amylose starch) (Raigond, for the initial precursors present in wine (Cueva et al., 2017).
Ezekiel, & Raigond, 2014). Resistant starch can also promote health by Non-dairy prebiotic fermented beverages (Table 4), using cereals
producing a high level of butyrate; so, it has been suggested to be also (oats, wheat, maize, rye, millet, sorghum, barley, or rice), soy milk, fruit,
classified as a prebiotic (Fuentes-Zaragoza et al., 2011). and vegetable juices, have become known for their health-promoting
Xylooligosaccharides is prebiotic with health benefits, and they are qualities (Nissen et al. 2021, 2019, 2020; Salmerón, 2017; Schwan &
composed of sugar oligomers of xylose units linked by β (1 → 4) bonds, Ramos, 2019). Water-soluble and insoluble arabinoxylans, β-glucan,
with DP ranging from 2 to 10, from natural sources like fruits, vegeta­ oligosaccharides, and resistant starch are cereal indigestible but
bles, bamboo shoots, wheat bran, barley hulls, gram husk, almond fermentable dietary carbohydrates, which are used as fermentation
shells, corn cob, straw, brewery spent grains and honey (Mano et al., substrates for probiotic lactic acid bacteria and could be used to get the
2018; Poletto et al., 2020). Primary sources of raffinose oligosaccharides beneficial effect of both the probiotic organisms and confer prebiotic
are seeds of legumes, peas, lentils, beans, mustard, and chickpeas. effects (Achi & Asamudo, 2019; Jovanovic-Malinovska et al., 2014;
Arabinooligosaccharides are one more class of oligosaccharides that Ripari, 2019; Tangyu, Muller, Bolten, & Wittmann, 2019). These fer­
hold the potential of being considered as prebiotics. The source is ara­ mented beverages are principally attractive due to their low cholesterol
binan polysaccharide a branched pectic polysaccharide presenting content, absence of dairy protein and lactose, thus avoiding allergic and
linkage of 1,3 and 1,5 αn L-arabinofuranosyl residue (Vogel, 1991). intolerance reactions by consumers, and they are vegan friendly (Gon­
Arabinose occurs in arabinans, arabinoxylans, or arabinogalactans from cerzewicz, Misiewicz, Owczarek, Jasińska, & Skąpska, 2016; Sethi,
the plant’s cell wall. This resistance of cell walls polysaccharides con­ Tyagi, & Anurag, 2016). Cereal-based beverages have natural prebiotics
cerning intestinal hydrolysis confer them the potential to be used as due to the presence of indigestible fibers, for example, oats fermented
prebiotics, however, their efficacy is structure-dependent (Yoo, Kim, & beverages, are an important source of β-glucans which can decrease LDL
Park, 2012). cholesterol (Lam & Chi-Keung, 2013; Rathore, Salmeron, & Pandiella,
Beta-glucans are soluble fibers placed in the endosperm cell walls of 2012) barley and malt have also been used as beverage substrates
cereal grains, they are linear polysaccharides composed of D-glucopyr­ (Mugula, Nnko, Narvhus, & Sørhaug, 2003; Phiri et al., 2019).
anosyl units with a mixture of β (1 → 3) and β (1 → 4) glycosidic link­ Prebiotic ingredients global market size was USD 5,568.7 Billion in
ages, and are also present in foods like mushrooms, algae, and other 2020 and estimated to reach USD 11,48 Billion in 2028, growing at a
marine plants (Fig. 5 A and B). The highest sources of beta-glucans are compound annual growth rate (CAGR) of 9.3% during the forecast
oat (3.5–5.7% of the dry matter) and barley (3.5–5.9% of the dry matter) period 2020–2028. This growing awareness is related to the health
(Cloetens, Ulmius, Johansson-Persson, Akesson, & Onning, 2012). benefits associated with consuming prebiotics among consumers are
According to the new definition of prebiotics (Gibson et al., 2017), major factors leading to a global market increase (Research and Markets,
polyphenols and fatty acids could be also considered as prebiotics 2021). Prebiotics Ingredients Market in 2020 was dominated by the Asia
together with some peptides catabolized by bacteria into active in­ Pacific due to the increasing consumer awareness and due to the de­
gredients. Even inorganic materials (i.e., micronutrients essential for the mographics aging. Nevertheless, Europe is forecasted to grow at a higher
growth of bacteria) used outside and inside could be considered as CAGR from 2021 to 2026. Inulin held the largest share in the Prebiotics
prebiotics. Therefore, besides dietary fibers, recent studies (preclinical Ingredients Market in 2020 and is forecasted to grow at a CAGR of 8.0%
and clinical) suggest that plant phenolic compounds can also meet the during the period 2021–2026. Fructooligosaccharide is estimated to
criteria of prebiotics, as it has been shown the interaction between register the higher CAGR over the period 2021–2026 (Industry ARC,
phenolic compounds and the gut microbiota (Duda-Chodak, Tarko, 2021).
Satora, & Sroka, 2015; Kawabata, Yoshioka, & Terao, 2019). They are
naturally occurring secondary metabolites of plants that comprise
several compounds that are classified mainly based on structure

Fig. 5. Beta-glucan structure and oatmeal, a β-glucan-rich cereal.

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F. Cosme et al. Food Research International 151 (2022) 110842

Table 4 Table 4 (continued )

Health benefits of non-alcoholic fermented cereal beverages. Beverage Sensory Health benefits Cereals Reference
Beverage Sensory Health benefits Cereals Reference characteristics
characteristics
bacteriostatic Jean-Pierre et al.
Amazake cloudy improves digestion; rice koji Maruki-Uchida, activities (2003)
appearance, anti-hypertension, Sai, Yano, Morita, Shalgam red color; sour antiseptic; probiotic wheat Altay et al. (2013)
sour–sweet taste anti-obesity; anti- and Maeda taste; food; regulates the
amnesia, alleviates (2020), Ajiro et al. pH digestive
liver cirrhosis (2017), systems; diuretic
Kawakami et al. Tobwa opaque and antimicrobial maize, Kitabatake,
(2020), Oguro, brownish color; activity; finger Gimbi, and Oi
Nishiwaki, sweet, enteropathogenic millet, (2003), Waters,
Shinada, occasionally sour inhibition of sorghum Mauch, Coffey,
Kobayashi, and taste Campylobacter jejuni Arendt, and
Kurahashi (2017) and Escherichia coli; Zannini (2015)
Bors sour-bitter taste; respiratory wheat Nicolau and eases diarrhea and
“bran”, “yogurt”, diseases, digestive bran, Gostin (2015), prevents
“goat milk- problems, effective cornflour Pasqualone, malnutrition
cheese”, management of Summo,
“pungent/sour”, liver and bile Laddomada,
“ripe/fermented diseases, potentially Mudura, and
fruit” beneficial in cancer Coldea (2018), 4. Market, consumer trends, and current research in non-dairy
treatment Grosu-Tudor et al. products
(2019)
Boza a thick liquid, improves wheat, Altay,
The global synbiotic product market size was valued at USD 700,6
pale yellow color; gastrointestinal millet, Karbancioglu-
sweet or sour health, stimulates maize, and Güler, Daskaya- million in 2019 and is anticipated to grow in the next years (Fig. 6).
taste the immune system, other Dikmen, and Nowadays the growing awareness about the correlation between diet
reductions of cereals Heperkan (2013), and health is leading the consumers’ choices of food and beverages.
cholesterol level Sahu and Panda Consumers also are showing a growing interest in microbiome health:
(2018),
From 2014 to 2019, Google searches for “microbiome” increased by
Ramakrishnan,
Ravichandran, 267% (Mintel, 2019). o, consumers understand the role of probiotics in
and Antony microbiome health. According to a survey, at least 54% of consumers,
(2019) globally, are already aware that probiotics can promote good digestive
Gowé brown/white certain lactic acid malted Adinsi et al.
health (Kerry Global Consumer Survey, 2019). The health benefits
color; sweet, bacteria strains can and non- (2015), Adinsi
acidic, cereal help in preventing malted et al. (2017) offered by probiotic microorganisms, namely lactic acid bacteria and
taste; soft texture infections by sorghum, S. boulardii, have now resulted in their increased usage in dairy and non-
urogenital maize dairy foods. This has increased the sale of probiotics in foods exponen­
pathogens; tially, worldwide, forming the largest segment of functional foods (Dixit,
antimicrobial value
Wagle, & Vakil, 2016).
Kunun- low viscosity, offers micro-and wheat and Agarry et al.
Zaki creamy macronutrients, sorghum/ (2010), Nkama, Non-dairy probiotic/synbiotics are being included in the normal diet
appearance; increased millet, Agarry, and and due to technological advances, many non-dairy products are created
sweet–sour taste; nutritional status wheat, Akoma (2010), using non-conventional food matrices (kombucha tea, herbal tea, and
malted Wartu, Whong,
baking mix- Mishra, Chakravarty, & Mandavgane, 2021). Moreover,
rice Abdullahi, Ameh,
and Musa (2015),
there are various cereal-based products available globally (cereal,
Olufunke (2014) granola, and breakfast bars) (Aspri et al., 2020), and big companies like
Kvass slightly cloudy modulates extruded Jargin (2009), Danone, General Mills, and Nestle are now researching and developing
appearance, metabolism, rye, Baschali, new products with synbiotic properties (Kearney & Gibbons, 2018;
light–dark brown deceased flatulence, malted Tsakalidou,
Mishra et al., 2021). These products, present in the market, show the
color; sweet or lessens hyperacidity barley Kyriacou,
sour taste Karavasiloglou, variance of non-dairy products and that there is still scope for the
and Matalas development of new products. One of the most seen on the supermarket
(2017), shelf is plant-based milk alternatives. These like-milk beverages are
Dlusskaya,
fluids derived from the maceration of plant material soaked in water
Jänsch, and
Schwab (2008),
making a suspension with particles with a size range of 5–20 µm, such
Gambus et al. that mammalian milk is simulated in appearance and consistency
(2015) (Kundu, Dhankhar, & Sharma, 2018). Soy milk and almond milk are two
Mahewu creamy color, bacteriostatic and maize, Olusanya, of the most common examples of these types of beverages. They have the
sour taste; bactericidal sorghum, Kolanisi, van
appearance of a rich creamy and milky white liquid and can be utilized
properties against millet, Onselen, Ngobese,
enteric pathogens malt, or and Siwela in many products like soy cheese, soy yogurt, and tofu. Almond is a
wheat (2020), Salvador, concentrated source of nutrients such as α-tocopherol which plays a
flour McCrindle, Buys, pivotal role in the prevention of oxidative stress. They also present a
and Steenkamp
high content of monounsaturated fatty acid (MUFA) which is potentially
(2016), Fadahunsi
and Soremekun
beneficial for heart health (Oliveira et al., 2020).
(2017) Today’s consumers hold high standards for the foods they consume.
Pozol yellow–brown reduces cholesterol maize Marsh, Hill, Ross, They demand foods that taste great, are fat- and/or calorie-reduced, and
color; levels; improves and Cotter are also interested in such foods that provide added health benefits.
sweet–sour; gastrointestinal (2014), ben Omar
Therefore, it is necessary to develop prebiotic-rich crops to promote
slightly acidic health; bactericidal, and Ampe (2000),
taste bacteriolytic; human health. A paradigm shift in breeding programs is needed to
achieve this goal and to ensure that newly bred crop cultivars are
nutritious, safe, and health-promoting. However, during the

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F. Cosme et al. Food Research International 151 (2022) 110842

Fig. 6. Estimation of U.S. synbiotic products market size, by product, between 2016 and 2027 (USD Million). Retrieve from https://www.grandviewresearch.
com/industry-analysis/synbiotic-product-market. Assessed 05 April 2021.

development of the non-dairy products, the functional properties, sta­ olives - Saccharomyces cerevisiae CCMA 1746, Pichia guilliermondii CCMA
bility, consumers’ sensory acceptance, and the price is to be kept in 1753, Candida orthopsilosis CCMA 1748, Candida tropicalis CCMA 1751,
attention, as these factors show a key role in their successful commer­ Meyerozyma caribbica CCMA 1758 and CCMA 1761; fish: Yarrowia lip­
cialization (Min, Bunt, Mason, & Hussain, 2019). olytica D1; and traditional fermented foods: Kluyveromyces marxianus
Safety issues of probiotic products have been reported frequently in JYC2614; Pichia kluyveri LKC17; Issatchenkia orientalis OSL11,
recent years due to several issues. The most cited are (i) inaccurate la­ P. kudriavzevii OG32, P. kudriavzevii ROM11) and tested regarding their
beling due to incorrect taxonomic identification of probiotic strains probiotic application.
(Weese & Martin, 2011); (ii) contamination with other microorganisms Non-dairy foods such as water kefir, sourdough bread, miso soup,
or external chemicals (Patro et al., 2016); (iii) probiotic genome varia­ puddings, juices, puree, sauerkraut, sour pickles, olives, tempeh, sau­
tion that may affect probiotic functionality (Sybesma, Molenaar, Wv, sages are examples of fermented foods, being sources of LAB probiotics.
Venema, & Kort, 2013); (iv) antimicrobial resistance genes and viru­ Moreover, fermented vegetables including olives, sauerkraut, mustard
lence factors that are harmful to humans (Llor & Bjerrum, 2014); (v) pickles, pickles, and kimchi are produced in many countries worldwide,
bacterial toxic metabolites, harmful to humans that most of the times are are also a rich source of probiotic bacteria, mainly distributed by six
forgotten and not screened (hemolysins, D-lactic acid, biogenic amines, genera, Lactobacillus, Leuconostoc, Weissella, Lactococcus, Oenococcus,
nitroreductase, amino acid decarboxylase enzyme, and azoreductases) and Pediococcus. Currently, there are many LAB probiotic formulations
(Pradhan, Mallappa, & Grover, 2020; Wang et al., 2021). commercialized in capsules, tablets, powder, and liquid forms that can
Oncobiosis which is the abnormal composition of the microbiome in be incorporated in dietary supplements and functional foods.
neoplastic diseases (Sári et al., 2020) is also a cause of health concern. In wines, malolactic bacteria responsible for wine malolactic
Studies have provided evidence that the microbiome secretes cytostatic fermentation are present in a huge diversity of species, so, we can infer
metabolites that inhibit the proliferation, movement, and metastasis that wine constitutes an excellent source of LAB to be used as a probiotic.
formation of cancer cells (Banerjee et al., 2018; Howe et al., 2018). In a Moreover, many wine-LAB species are already present in the probiotic
study performed by Sári et al. (2020) bacterial indole biosynthesis formulations available in the market.
showed a correlation with lymphocyte infiltration to tumors of breast Worldwide consumers are more and more alert to the relation be­
cancer cells in humans. Bacterial metabolites like lithocholic acid, short- tween nutrition and health and prebiotics “substrates that are selectively
chain fatty acids or cadaverine, and indole propionic acid (IPA) have a utilized by host microorganisms conferring a health benefit” are usually
pivotal role in regulating the progression but not the initiation of the included in the daily diet.
disease. Prebiotics possess the ability to sustain gut microorganisms existing
in the gastrointestinal tract and improve their metabolic activity,
5. Final remarks boosting nutrient absorption, digestion, and the improve the human
immune system whilst decreasing the growth of pathogenic microor­
Human gut microbiota contains a huge number of microorganisms in ganisms. Prebiotics can be found in different food sources, such as roots,
a complex ecosystem and microbiota dysbiosis, or microbial imbalance, tubers, and grain crops and the prebiotic content in some of these foods
is associated with several intestinal disorders, so its modulation is of can reach up to 20%. The most important groups of prebiotics with
great interest for human health. Probiotics, prebiotics, and their com­ beneficial effects on human health are non-digestible oligosaccharides
binations – synbiotics - are used as natural approaches to improve gut fructans and galactans which are preferentially metabolized by
function and overall wellbeing. bifidobacterial.
Yeasts can be used as probiotic if they possess some characteristics:
able to survive and function in the gastrointestinal tract (viability at
36–38 ◦ C; resistance to gastric acid, bile salts, and digestive enzymes); Declaration of Competing Interest
are considered safe when administered (absence of hemolytic and
mucolytic activities, and susceptibility to antimicrobial drugs, protect The authors declare that they have no known competing financial
against infection, or be able to co-aggregate – entrapment-pathogenic interests or personal relationships that could have appeared to influence
agents). Saccharomyces cerevisiae var. boulardii was the first yeast the work reported in this paper.
described as a probiotic. Nowadays the search for new beneficial or
potential probiotic yeasts is an ongoing process, and several yeasts have
Acknowledgments
been isolated from extreme environments (Antarctica) like the strain
Rhodotorula mucilaginosa UFMGCB 18377; and from non-dairy origin
Funding: This study was funded by the CQ-VR [grant number UIDB/
products (lemon - Debaryomyces hansenii strain L2; fermented table
00616/2020 and UIDP/00616/2020], FCT - Portugal, and COMPETE.

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