Food Research International 51 (2013) 764–770

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Food Research International

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Review

Products of vegetable origin: A new alternative for the consumption of

probiotic bacteria
Eliane M. Furtado Martins a,⁎, Afonso Mota Ramos b, Ellen Silva Lago Vanzela b, Paulo César Stringheta b,
Cláudia Lúcia de Oliveira Pinto c, José Manoel Martins a
a
Food Science and Technology Department, Federal Institute of Education, Science and Technology of Southeast of Minas Gerais, Dr. José Sebastião da Paixão Avenue, w/n., Lindo Vale,
36180–000, Rio Pomba, Minas Gerais State, Brazil
b
Food Technology Department, Federal University of Viçosa. P.H. Rolfs Avenue, w/n., 36570-000, Viçosa, Minas Gerais State, Brazil
c
Agricultural Research Company of Minas Gerais. Vila Gianetti, 46, Campus of Federal University of Viçosa, 36570-000, Viçosa, Minas Gerais State, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Consumers are more aware and concerned about their lifestyle than ever before. This has increased demand
Received 15 August 2012 for foods that promote health and wellness, such as functional products containing probiotic microorganisms,
Accepted 22 January 2013 which have a beneficial effect on the balance of intestinal microbiota. Among probiotic microorganisms,
those of the Lactobacillus genus are the most commonly used by the food industry. Fermented dairy products
Keywords:
are generally good food matrices for probiotics, but the consumption of these products is limited due to growing
Functional food
Fruit
vegetarianism and the large number of individuals who are lactose intolerant or on cholesterol-restricted diets.
Vegetable Thus, the development of non-dairy probiotic products, including food matrices based on fruit, vegetables and
Cereal cereals, has been widely studied. This paper reviews the main applications of probiotic microorganisms
Non-dairy probiotic products in products of vegetable origin and the characteristics that enable the use of these food matrices as potential
carriers of probiotic bacteria.
© 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 764
2. Application of probiotic bacteria in vegetable products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 765
2.1. Probiotic products from fruit and vegetable . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 765
3. Characteristics of fruits and vegetables that make them a promising carrier matrix for probiotic microorganisms . . . . . . . . . . . . . . 767
4. Clinical trial of probiotic bacteria in vegetable products and the mechanisms of action of probiotic bacteria on host function . . . . . . . . . . 767
5. Future prospects for the use of probiotic bacteria in vegetable products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 768
6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 768
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 768
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 768

1. Introduction
In recent years, consumers have increasingly sought diets that pro-
mote health and wellness. Among the foods that meet this demand,
those with functional properties have attracted the attention of con-
sumers and the food industry.
The term “functional foods” was introduced by the Japanese govern-
ment in the mid-1980s (Chonan, 2011). These foods are products used as
part of a normal diet with effects beyond their basic nutritional functions,
⁎ Corresponding author. Tel.: +55 32 3571 5742; fax: +55 32 3571 5710.
E-mail address: eliane.martins@ifsudestemg.edu.br (E.M.F. Martins).
such as providing physiological benefits and reducing the risk of chronic
diseases (Cenci & Chingwaru, 2010; Stringheta et al., 2007). They have
attracted the attention of researchers worldwide due to their diversity
of bioactive compounds. Moreover, consumers are attracted to functional
foods, which contain prebiotics and probiotics, due to their health benefits
over traditional products (Ares, Giménez, & Gámbaro, 2009).
Prebiotics benefit the host by promoting the growth of select
probiotic microorganisms and activating bacterial metabolism in the
intestinal tract (Charalampopoulos & Rastall, 2011; Gibson, Probert,
Loo, Rastall, & Roberfroid, 2004; Roberfroid, 2007), once they are
fermented by beneficial bacteria from the colon (Forssten, Sindelar, &
Ouwehand, 2011; WGO, 2008).

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http://dx.doi.org/10.1016/j.foodres.2013.01.047
 E.M.F. Martins et al. / Food Research International 51 (2013) 764–770 765

In addition, probiotics have positive effects on the composition of
intestinal microbiota and overall health. As a result, their consumption
has increased (Granato, Branco, Nazzaro, Cruz, & Faria, 2010). Inter-
nationally, probiotics are defined as microorganisms that provide
health benefits to the host when administered in appropriate amounts
(FAO/WHO, 2001).
The most common probiotic microorganisms used and marketed in
food worldwide belong to the genera Lactobacillus and Bifidobacterium
(Champagne, Ross, Saarela, Hansen, & Charalampopoulos, 2011;
Saulnier, Spinler, Gibson, & Versalovic, 2009). Fermented dairy products
generally provide good carrier matrices of probiotic microorganisms.
However, other food matrices have also been studied as potential
carriers for these microorganisms. The increasing number of individuals
with lactose intolerance, dyslipidemia, and vegetarianism reinforces the
importance of development of non-dairy probiotic products such as
fruit and vegetables (Peres, Peres, Hernández-Mendoza, & Malcata,
2012; Ranadheera, Baines, & Adams, 2010).
Prado, Parada, Pandey, and Soccol (2008) reported that beverages
such as fruit and vegetable juices may be the next category of food matri-
ces to serve as carriers of probiotic bacteria, as supported by published
studies (Nicolesco & Buruleanu, 2010; Nualkaekul & Charalampopoulos,
2011; Pereira, Maciel, & Rodrigues, 2011; Sheela & Suganya, 2012).
Besides, probiotic foods containing fruit ingredients are increas-
ingly preferred by consumers (Espírito-Santo, Perego, Converti, &
Oliveira, 2011) and in addition to fruits, raw and fermented vegeta-
bles and cereals have been used as substrates for probiotic bacteria
once these foods contain nutrients easily assimilated by probiotics
(Kourkoutas, Kanellaki, & Koutinas, 2006; Peres et al., 2012; Soccol
et al., 2010). Strains of Lactobacillus acidophilus, Lactobacillus casei,
Lactobacillus plantarum, Lactobacillus rhamnosus and Bifidobacterium
lactis are the most utilized in the formulation of new vegetable probiotic
products.
Espírito-Santo et al. (2011) related that there are scarce studies
that point out the effects of fruity food matrices on probiotic survival.
Then, this article presents an overview of the application of probiotic
microorganisms in products of vegetable origin and highlights the
reasons for these products to be considered suitable food matrices for
probiotic bacteria.
2. Application of probiotic bacteria in vegetable products
Products containing probiotic bacteria comprise much of the avail-
able functional food, including dairy products such as yogurt, cheese,
ice cream, butter (Soccol et al., 2010) and mousses (Buriti, Castro, &
Saad, 2010), as well as non-dairy products prepared from cereal, baby
food formulas and soy products (Singh, Kallali, Kumar, & Thaker,
2011). Products made from fruits and vegetables, such as drinks, purées,
fermented vegetables, table olives (Peres et al., 2012) and minimally
processed fruit (Rößle, Auty, Brunton, Gormley, & Butler, 2010; Rößle,
Brunton, Gormley, Ross, & Butler, 2010) have also been used. Moreover,
products containing probiotic bacteria have an ever-expanding world
market due to consumer demand as a result of their potential health
benefits (Champagne et al., 2011).
According to Khurana and Kanawjia (2007), the expansion of the
dairy industry leads to the introduction of hybrid dairy products, made
by combining the dairy and fruit drink markets to offer healthier, more
convenient and more flavorful products.
Fermented milk enriched with fruit is responsible for more than
half of this market segment of the dairy industry. Prepared fruits, in
the form of pieces, pulp and even flour prepared from processing
the peel, have been successfully incorporated with probiotic yogurts
as sources of prebiotic fibers and nutrients that stimulate the growth
and activity of intestinal microbiota (Espírito-Santo, Perego, Converti,
& Oliveira, 2012; Espírito-Santo et al., 2011).
2.1. Probiotic products from fruit and vegetable
Most probiotic products are marketed in the form of yogurt and
fermented milk. However, there is a growing interest in developing
non-dairy probiotic products (Ranadheera et al., 2010). According to
Granato et al. (2010), the consumption of probiotic products is limited
by growing vegetarianism, the high number of individuals with lactose
intolerance and consumers with cholesterol-restricted diets. Economic
and cultural factors may also negatively affect the consumption of
probiotic dairy products, since most are fermented foods. Thus, the
development of non-dairy probiotic products, including food matrices
from fruit, vegetables and cereals (Table 1), has a promising future
(Peres et al., 2012).
Besides, previous studies have reported the use of probiotic bacteria
with high amount of cells in fruit juices, fruit smoothies, minimally
processed fruit, fermented vegetables, snack products, olive, and cereal
beverage to provide probiotic food free of cholesterol, lactose and aller-
gens present in dairy products (Table 2).
Champagne and Gardner (2008) evaluated the viability of nine strains
of Lactobacillus genus in a commercial fruit drink stored at 4 °C for up to
80 days. Lactobacillus brevis LB6, L. rhamnosus LB24 and L. acidophilus

Table 1
Recent studies related to the use of vegetable food matrices for carrying probiotic bacteria.

Food matrix Probiotic microorganism Food product Reference

Apple Lactobacillus rhamnosus GG Minimally processed product Rößle, Auty, et al. (2010)
Cocoa Bifidobacterium longum Chocolate Possemiers, Marzorati, Verstraete,
Lactobacillus helveticus and Wiele (2010)
Cashew Lactobacillus johnsonii Juice Vergara, Honorato, Maia, and Rodrigues (2010)
Orange, grapefruit, black currant, pineapple, Lactobacillus plantarum Juice Nualkaekul and Charalampopoulos (2011)
pomegranate, cranberry and lemon
Apple L. rhamnosus GG Minimally processed product Alegre, Viñas, Usall, Anguera, and Abadias (2011)
Yam Lactobacillus acidophilus Fermented yam Lee, Ganesan, Ahn, and Kwak (2011)
Pomegranate L. plantarum, Lactobacillus delbrueckii, Juice Mousavi, Mousavi, Razavi, Emam-Djomeh,
L. acidophilus and Lactobacillus paracasei and Kiani (2011)
Shalgam L. plantarum Drink Tanguler and Erten (2012)
(black carrot, turnip) L. paracasei
Pear L. acidophilus Juice Ankolekar, Pinto, Greene, and Shetty (2012)
Plum Lactobacillus kefiranofaciens, Candida kefir Juice Sheela and Suganya (2012)
and Saccharomyces boluradii
Olive L. plantarum Table olives Hurtado, Reguant, Bordons, and Rozès (2012)
Apple Lactobacillus casei Drink Ellendersen, Granato, Guergoletto, and
Wosiacki (2012)
Soybean L. acidophilus Soybean bar Chen and Mustapha (2012)
Barley, tomato pulp and whey powder L. acidophilus Food mixture Jood, Khetarpaul, and Goyal (2012)
Cabbage L. plantarum Sauerkraut Yu et al. (2012)
766 E.M.F. Martins et al. / Food Research International 51 (2013) 764–770

Table 2
Viability of probiotic cultures in fruit and vegetable products.

Food product Probiotic microorganism Viability of the probiotic in the product Reference

Tomato juice Lactobacillus acidophilus LA39, Lactobacillus 106–108 CFU·mL−1 Yoon, Woodams, and Hang (2004)
casei A4, Lactobacillus delbrueckii D7 and
Lactobacillus plantarum C3
Beet juice L. acidophilus LA39, L. casei A4, L. delbrueckii 106–108 CFU·mL−1, except for L. acidophilus Yoon, Woodams, and Hang (2005)
D7 and L. plantarum C3
Cabbage juice L. casei A4, L. delbrueckii D7 and L. plantarum C3 107 CFU·mL−1 of L. plantarum and Yoon, Woodams, and Hang (2006)
105 CFU·mL−1 of L. delbrueckii. L. casei did not
survive
Fruit smoothies Lactobacillus acidophilus LA-5 and 107 CFU·g−1 Rodgers (2007)
Bifidobacterium animalis ssp. lactis BB-12
Orange, pineapple and cranberry juice L. casei DN 114 001, Lactobacillus rhamnosus Above 107 CFU·mL−1 of L. casei, L. rhamnosus Sheehan, Ross, and Fitzgerald
GG, Lactobacillus paracasei NFBC 43338, and and L. paracasei in orange juice and above (2007)
Bifidobacterium lactis Bb-12 106 CFU·mL−1 in pineapple juice. B. lactis
showed concentrations above 106 CFU·mL−1
in both juices
Minimally processed apple and papaya B. lactis BB-12 Above 106 CFU·g−1 Tapia et al. (2007)
Fruit cocktail from carrot, celery and apple L. acidophilus LA-5 Above 107 CFU·mL−1 Nicolesco and Buruleanu (2010)
Minimally processed symbiotic apples L. rhamnosus GG 107–108 CFU·g−1 Rößle, Brunton, et al. (2010)
Olive L. paracasei IMPC2.1 107 CFU·g−1 De-Bellis, Valerio, Sisto, Lonigro,
and Lavermicocca (2010)
Cataloupe juice L. casei NRRL B-442 Above 108 CFU·mL−1 Fonteles, Costa, Jesus, and
Rodrigues (2011)
Honeydew melon juice L. casei NCIMB 4114 Above 108 CFU·mL−1 Saw, Chen, Wong, Tan, and Goh
(2011)
Cashew juice L. casei NRRL B 442 Above 108 CFU·mL−1 Pereira et al. (2011)
Turşu L. plantarum BC 7321 Above 107 CFU·mL−1 Çetin (2011)
Defatted soy flour L. paracasei BCRC 14023 and Bifidobacterium Above 109 CFU·g−1 of L. paracasei and Chen, Wei, and Chi (2011)
longum BCRC 14661 B. longum
Snack product from apple, mandarin and Lactobacillus salivarius spp. salivarius Above 107 CFU·g−1 Betoret et al. (2012)
pineapple grape juice CETC4063 and Lactobacillus acidophilus
CECT903
Beverage from rice, barley, oats, wheat, L. plantarum 6E and M6 Above 108 CFU·g−1 Coda, Lanera, Trani, Gobbetti, and
soy flour and red grape juice Dicagno (2012)
8 −1
Malt beverage L. plantarum NCIMB 8826 and L. acidophilus Above 10 CFU·mL of L. plantarum and Rathore, Salmerón, and Pandiella
NCIMB 8821 L. acidophilus (2012)

LB45 had viability patterns similar to L. fermentum LB32, L. reuteri, LB38
and L. plantarum LB42, respectively. Both strains of L. rhamnosus showed
good viability patterns. The strains of L. rhamnosus LB11, L. plantarum
LB42 and L. reuteri LB38 had concentrations above 107 CFU·mL−1 over
80 days of storage. The authors also observed that microorganisms are
stable at drink conditions and that stability varies according to the
species and strains used. Ranadheera et al. (2010) related that food
can influence the growth, survival, viability and functionality of
probiotics, which determine their effectiveness. Hence, care should be
taken in choosing the strain best suited for each type of product
(Soccol et al., 2010).
Mousavi et al. (2011) observed that L. plantarum and L. delbrueckii
fermented pomegranate juice with optimal probiotic growth and
maintained their viability during the first two weeks of storage at
4 °C, whereas L. acidophilus and L. paracasei lost their viability. The
authors observed that the citric acid (an organic acid present in the
main pomegranate juice) was rapidly consumed by all the probiotic
microorganisms, indicating that this juice may be a potential substrate
for producing probiotic beverages.
Another product, such as olives, also has been reported as a promise
vehicle of probiotic culture. According to Peres et al. (2012), the probiotic
Lactobacillus genus has been recently tested in the fermentation of table
olives. Some of the strains tolerate the relative acidity and salt of
fermented vegetables, binding effectively to the surface of olives. As a re-
sult, desirable sensory changes and an extension of the product shelf life
are observed.
Cereal grains, from whole grain to flour, have also been evaluated
as potential carriers of probiotic cultures in beverages, bread, biscuits,
cereal bars, breakfast cereals, and others (Lamsal & Faubion, 2009)
because they contain native prebiotic substances that protect probiotic
microorganisms from the adverse conditions of the gastrointestinal
tract.
Furthermore, cereals can also be used to encapsulate probiotics
and maintain the viability and functionality of these microorganisms.
Considering that the acidic conditions of the stomach can reduce the
number of viable cells that reach the intestine, microencapsulation
can increase probiotic survival during the gastrointestinal transit.
The fermentation of cereals, such as oats, maize and wheat by pro-
biotic microorganisms is beneficial because it provides better digestibility
of food products. This is associated with a reduction in non-digestible
carbohydrates such as polysaccharides and oligosaccharides, the avail-
ability of B complex vitamins and the release of minerals such as calcium,
zinc, iron, among others (Soccol et al., 2010).
Charalampopoulos and Pandiella (2010) studied the survival of
L. plantarum NCIMB 8826 in extracts of malt, wheat and barley pro-
duced in a flour and water suspension. The fermentation was conducted
for 24 h at 37 °C and the product was stored at 4 °C for 70 days. The re-
searchers observed that the probiotic survived best under refrigeration
in malt extract medium and attributed this finding to the higher
concentration of sugar and other unidentified compounds that protect
bacterial cells.
Besides, fermentation is known to increase the nutritional value
and improve the acceptability of soy products. The soybean is rich in
high quality proteins and contains oligosaccharides such as raffinose
and stachyose, which are not digested by the human body, causing
flatulence (Soccol et al., 2010). Thus, the fermentation of hydrosoluble
soybean extract by probiotic bacteria results in multiple benefits, since
it reduces the sugars that cause flatulence and better preserves the
product (Champagne, Gardner, & Roy, 2005).
There is no consensus regarding on the minimum amount of pro-
biotic microorganisms to be ingested to ensure their functionality.
Some researchers recommend minimal concentrations from 106 to
107 CFU·g−1 (Dave & Shah, 1997; Vinderola & Reinheimer, 2000),
while others suggest higher concentrations. According to Prado et al.
 E.M.F. Martins et al. / Food Research International 51 (2013) 764–770
(2008), probiotics must be ingested daily in high numbers, usually
more than 10 9 cells per dose, to ensure continuing health benefits.
Doses of food products (100 g) containing 10 8–109 CFU probiotic mi-
croorganisms (106–107 CFU∙g−1 of food product) resulted in favor-
able changes in the intestinal microbiota composition in vivo, with
a physiologically maintained active probiotic intestinal concentration
of 106–107 CFU·g−1 (Shah, 2000). According to Shah (2007), the daily
intake should be approximately of 108 CFU∙g−1 in order to compensate
for possible reductions in probiotic concentration during passage through
the intestine.
The latest recommendation from the Brazilian National Agency of
Sanitary Surveillance (ANVISA) is that probiotic microorganisms must
be ingested in concentrations of around 108–109 CFU·day−1. As indi-
cated by ANVISA, this concentration was calculated based on the daily
portion of viable probiotic microorganisms that must be ingested
to obtain functional effects (BRAZIL, 2008).
3. Characteristics of fruits and vegetables that make them a
promising carrier matrix for probiotic microorganisms
Plant tissue is formed by a multi-phase system, with a microstruc-
ture comprised of intricate internal cells, intercellular spaces, pores
and capillaries. The plant cell wall, when intact, is an efficient physical
barrier against the action of microorganisms (Brackett & Splittstoesser,
2001), since the pores are too small (0.1 to 5.0 μm) to allow bacterial
access (Alzamora et al., 2005).
However, microorganisms can enter the plant by means of lenticels
and tissue lesions, become entrapped and attach to trichomes. In addi-
tion, nutrient release may occur depending on the holes formed in plant
tissue, thus facilitating microbial growth due to easy access to nutrients
(Reina, Fleming, & Júnior, 2002).
Microorganisms tend to be located in pores, holes or irregularities
naturally occurring on the surface of intact fruit. Those sites favor
microbial binding and protection. Bacteria may also adhere to cut and
damaged vegetable surfaces. Thus, plant tissue often provides condi-
tions favorable to microbial internalization (Sapers, 2001).
Oliveira, Souza, Bergamini, and Martinis (2011) reported that the
steps of minimally processing vegetables, such as peeling and cutting,
promote the release of cellular content rich in minerals, sugars, vitamins
and other nutrients, creating ideal conditions for microbial growth.
Moreover, Rößle, Auty, et al. (2010) indicated that this characteristic
allows the use of fruit and vegetable food products as probiotic carriers.
According to Soccol et al. (2010), processed fruits and vegetables are con-
sidered good matrices and can provide ideal substrates for probiotics,
since they contain minerals, vitamins, antioxidants and fibers.
Intercellular spaces, commonly called pores, may play an impor-
tant role regarding bacterial entry in fruits and vegetables; in apples,
bacterial entry is common in parenchymal tissue, which occupies
20–25% of total apple volume (Alzamora et al., 2005). According to
these authors, the pores are large enough to allow microbes to enter
vegetable products. In this way, mature cells of apple parenchyma
present pore sizes ranging from 50–500 μm in diameter. In addition,
during senescence fruits exhibit significant changes in cell wall com-
position, with disintegration of the middle lamella and enlargement
of intercellular spaces, allowing bacterial entry (Castillejo, Fuente,
Iannetta, Botella, & Valpuesta, 2004).
Fresh fruits and vegetables contain mostly cellulose, which is not
digested by the gastrointestinal system. Some studies regarding the
use of vacuum impregnation technology for probiotic bacteria were
done with apples, showing promising results (Alzamora et al., 2005;
Betoret et al., 2003). Thus, fruit matrices are certainly an important
area of research and development with great potential for the function-
al food market. According to Kourkoutas et al. (2006), fruits contain
requirements necessary for probiotic adhesion to plant tissue. In this
way, fruits such as apples and pears, due to their cellulose content,
may exert a protective effect on the probiotic microorganisms during
767
passage through the intestinal tract. As a result, the bacterial integrity
of probiotics, such as L. casei, is maintained, allowing these microorgan-
isms to reach the colon and benefit the host.
Studies conducted by our research group showed that fruits, such
as apple, guava, banana and melon, have potential as carriers for pro-
biotic bacteria. The results of scanning electron microscopy showed a
positive interaction between the probiotic microorganisms and the
fruity tissues, since bacteria strongly adhered to the fruit surface.
Ranadheera et al. (2010) reported that some strains of lactic acid
bacteria isolated from fermented vegetables may be used as probiotics.
These authors suggest that the survival of these strains in fermented
products prepared from plants, such as olives and artichokes, can be
compared to the results observed for dairy products, in some cases
even having better results than dairy products. This can be attributed
to the microstructure and format of the plants that protect microorgan-
isms, allowing bacteria to survive. Additionally, the cell wall of the lactic
acid bacteria naturally present in plants is more resistant, allowing
bacterial adaptation to environmental conditions of carrier matrices of
plant origin, such as low moisture and the presence of antimicrobial
compounds (Masuda, Kimura, Okada, & Yasui, 2010).
Therefore, the intrinsic characteristics of the plant surface
microarchitecture, due to the presence of ridges and natural prebiotic
compounds (such as oligosaccharides), protect probiotic microorgan-
isms from the acidic environment of the stomach and are a source of nu-
trients, which positively influences bacterial survival (Ranadheera et al.,
2010). However, Ijabadeniyi (2010) indicated the need for further work
on the mechanism of internalization of microorganisms in plants. In
particular, the way microorganisms fit into openings naturally present
on the vegetable surface, such as stomata and lenticels, and in tissue
damaged by processing.
When comparing vegetable matrices with dairy matrices, the pro-
tective effect of the latter, especially from milk proteins on probiotics
in the digestive system, has been discussed in the literature. Saxelin,
Korpela, and Mäyra-Mäkinen (2003) related that proteins are sources
of bioactive peptide precursors, which resist passage through the diges-
tive tract. Furthermore, according to these authors, milk has a physico-
chemical composition rich in protein and with considerable amounts of
lipids, resulting in a protective matrix for probiotics. These characteris-
tics favor the survival of probiotics against the adverse conditions of the
digestive system. Moreover, Ritter, Kohler, and Von Ah (2009) reported
that milk proteins are used as a suitable carrier matrix for probiotic
bacteria, which acts effectively along the stomach to the intestine,
allowing probiotic bacteria to reach their site of action.
Although it is challenging to incorporate probiotic bacteria into
processed fruits, it is highly advantageous to do so, since this is a food cat-
egory rich in nutrients, intended for consumption by all individuals and
widely accepted among consumers (Saad, Komatsu, Granato, Branco, &
Buriti, 2011). Although there is a lack of studies demonstrating the
effects of fruits as carrier matrices on the survival and activity of probiotic
microorganisms, recent studies indicate a neutral or even positive effect
on probiotic microorganisms, as well as their hosts (Espírito-Santo et al.,
2011).
4. Clinical trial of probiotic bacteria in vegetable products and the
mechanisms of action of probiotic bacteria on host function
The selection of a carrier matrix of vegetable origin to ensure the
viability of probiotic microorganisms is important. However, it is
essential to evaluate the product containing probiotics by means of
clinical trials to ensure probiotic bacterial adhesion to the intestine.
In this way, many in vitro studies have been conducted; however,
few clinical trials have been done on experiments in vivo.
Ouwehand, Kurvinen, and Rissanen (2004) evaluated an oat cereal
bar inoculated with B. lactis BB-12 and its detection in human feces of
nine individuals over seven days. The authors identified the probiotic
768 E.M.F. Martins et al. / Food Research International 51 (2013) 764–770

microorganism in the feces of five individuals, indicating that results as probiotic microencapsulation (Lamsal & Faubion, 2009) have been
regarding probiotics in this kind of food product are promising. the focus of research, being used successfully to maintain the viability
Valerio et al. (2006) demonstrated that artichokes can carry probiotic and functionality of these microorganisms since they can increase
bacteria, such as L. paracasei IMPC2.1. Results showed that L. paracasei probiotic survival during processing and target delivery in the gastroin-
IMPC2.1 was recovered from fecal samples of four healthy volunteers testinal tract (Anal & Singh, 2007). According to Gaggia, Gioia, Baffoni,
that consumed artichokes inoculated with this probiotic microorganism. and Biavati (2011), microencapsulation technology deals with mate-
Chiu, Tsai, Hsih, and Tsen (2008) evaluated the potential activity rials packaged in miniature capsules that release their content under
of two probiotic strains, Pedioccus pentosaceus MP12 and L. plantarum specific conditions.
LAP6, isolated from pickled vegetables against invasion of Salmonella
spp. in the liver and spleen of mice. The strains showed a strong
5. Future prospects for the use of probiotic bacteria in
antagonistic effect against Salmonella spp. Moreover, L. plantarum
vegetable products
LAP6 was able to adhere to epithelial cells of mice. Furthermore, by
using REP-PCR Valerio et al. (2011) found that the profile of probiotic
Research to propose new matrices using non-dairy products for
L. paracasei LMGP22043 carried in artichoke transiently colonized the
probiotic carriers has been conducted. Fermented dairy products
intestines of 17 individuals who consumed artichokes containing the
have high cholesterol, lactose, and proteins which may limit their con-
probiotic strain. The authors concluded that the strain successfully
sumption by some population groups. Thus, the use of vegetables have
colonized the intestines of tested individuals and had a positive effect
been widely discussed as an alternative for individuals, including veg-
on intestinal microbiota.
etarians and individuals with cholesterol restricted diets, lactose intol-
Probiotic bacteria have multiple and diverse influences on the host,
erance and milk protein allergies; since fruits and vegetables have
such as suppressing the number of viable cells by producing compounds
nutrients which promote the growth of probiotic microorganisms
with antimicrobial activity, and competing for nutrients and adhesive
and do not offer to consumers the drawbacks of dairy products. Studies
sites. They also alter microbial metabolism by increasing or decreasing
have shown that fruits and vegetables have potential to serve as carrier
enzymatic activity and stimulate the immunity of the host by increasing
food matrices to create probiotic foods with high cell viability as a func-
antibody levels and macrophage activity (Fuller, 1989; Ng, Hart, Kamm,
tion of the intrinsic characteristics of certain vegetables. These intrinsic
Stagg, & Knight, 2009).
characteristics protect probiotic microorganisms as they pass through
The antimicrobial activity of the probiotic microorganisms occurs
the gastrointestinal tract. Probiotic foods of vegetable origin include
by reducing the pH in the lumen due to the production of acetic and
fermented juices and vegetables, minimally processed fruits and vege-
lactic acids, bacteriocins and other antimicrobial compounds, blocking
tables, fruit purée, among others.
bacterial adhesion to the epithelial cells, decreasing the pathogen
Currently, probiotic products from fruits and vegetables are already
population (Ng et al., 2009; Zhang et al., 2011). As the probiotics act
available on the American and European markets. Commercial products
on the intestinal microbiota by adhesion and colonizing the mucous,
include fermented and unfermented fruits and vegetables, organic pro-
this action impedes the adhesion and consequent toxin production or
biotic drinks and dried fruit enriched with these microorganisms. These
invasion of the epithelial cells by pathogenic bacteria, depending on its
products have a healthy appeal, which attracts consumers.
pathogenic mechanism (Saad, Bedani, & Mamizuka, 2011; Walker, 2008).
Technologies such as microencapsulation, vacuum impregnation and
The modulation of intestinal microbiota by probiotic microorgan-
immobilization have been used to incorporate bioactive compounds,
isms occurs through the mechanism of competitive exclusion, which
such as probiotics, into food carrier matrices with positive results. How-
impedes the colonization of the intestinal mucous by potentially
ever, future studies should be done to assess probiotic adherence and
pathogenic bacteria through competition at the sites of adhesion, of
viability in the human intestine by means of in vivo clinical trials.
the competition for nutrients and the production of antimicrobial
These studies would demonstrate the interaction of probiotics carried
compounds (Guarner & Malagelada, 2003).
by products of vegetable origin.
The increase in mucous and of the integrity of the intestinal barrier
against pathogens are also mechanisms of action of the probiotics
(Ng et al., 2009). Moreover, these microorganisms promote the in- 6. Conclusions
crease of bioavailability of certain nutrients such as short-chain
fatty acids, proteins, minerals such as calcium and have beneficial The rise of vegetarianism and consumer concerns regarding an al-
effects on bone metabolism. ternative diet to dairy products with high nutritional value and free of
According to Saulnier et al. (2009), probiotics may improve the cholesterol and lactose is of great interest to researchers. As a result,
hosts' defense system against pathogenic microorganisms in different new food matrices have been tested for use as probiotic carriers. In
ways. The epithelial cell barrier of mucous is the first line of defense this way, food products such as fruit and vegetable juices, minimally
against pathogens that may be enhanced by the promotion of mucin processed fruits, raw and fermented vegetables, olives, artichokes and
production or the reduction of intestinal permeability. According to cereals, have been inoculated with probiotic microorganisms and show
Ng et al. (2009), the mechanism by which the probiotics increase the promising results.
function of the intestinal mucous barrier is not clear; however, it may
be related to alterations in the secretion of mucous or chloride. Acknowledgments
The immunomodulation or modulation of the immunological
system of the host occurs by the stimulation of the immune system The authors thank the Coordenação de Aperfeiçoamento de Pessoal de
by means of increasing the levels of antibodies and of the activity of Nível Superior (CAPES) and the Conselho Nacional de Desenvolvimento
the macrophages, increasing the level of pro and anti-inflammatory Científico e Tecnológico (CNPq) for financial support.
cytokines and increasing the activity of the natural killer (NK) cells
(Saad, Bedani, & Mamizuka, 2011).
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