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Prebiotic in fruit juice: processing challenges,

advances, and perspectives
Thatyane Vidal Fonteles and Sueli Rodrigues

Prebiotics are non-digestible food ingredients or chemically also render many other health benefits in the large intes-
stable structures that modulate gut microbiota and so, the tine such as reduction of cancer risk and increase calcium
overall consumer’s health. The prebiotic fortification of fruit and magnesium absorption. It is not the prebiotic by itself
juices has increased, and the scarce literature suggests that the but the qualitative changes on microbiota that is respon-
food matrix can influence prebiotic stability. This review sible for its effects. The most important bacterial genera
presents the main aspects of the design of fruity prebiotic juices target for selective stimulation are the indigenous bifido-
covering the effects of processing on prebiotic structure and bacteria and lactobacilli; the health effect is a phenome-
properties. The use of fruit juice as a substrate to synthesize non named bifidogenic effect [4,5].
prebiotics oligosaccharides are also covered.
According to Global Market Insights, Inc. (Delaware,
Address
USA), the global prebiotic market is increasing, and this
Federal University of Ceará, Food Engineering Department, food ingredient is expected to surpass USD 8.5 billion by
Biotechnology Laboratory, CEP 60440-900, Fortaleza, CE, Brazil 2024. From the technological point of view, the addition
of prebiotic to foods improves sensory characteristics such
Corresponding author: Fonteles, Thatyane Vidal (sueli@ufc.br) as taste and texture and enhances the stability of foams,
emulsions, and mouthfeel in a vast range of food applica-
Current Opinion in Food Science 2018, 22:55–61 tions like dairy and baking products [6]. Fruit juices are
This review comes from a themed issue on Innovations in food
suitable for the development of functional foods because
science they are rich in bioactive compounds and meets the
Edited by Adriano Cruz
consumer’s claims for healthy, tasty and practical foods
[7]. This paper reviews the design of fruity prebiotic
juices covering the effects of processing on prebiotic
structure and properties.
doi:10.1016/j.cofs.2018.02.001
2214-7993/ã 2018 Elsevier Ltd. All rights reserved. Types and sources of prebiotics
Prebiotics are manufactured by three different methods:
isolation from plant resources, microbiological production or
enzymatic synthesis, and enzymatic hydrolysis of polysac-
charides [8,9]. Inulin is an example of a prebiotic that can be
directly extracted from plant sources, mainly chicory root
Introduction and Jerusalem artichoke. Some foods, such as asparagus,
Prebiotics are non-digestible food ingredients that impart leek, onions, banana, wheat, and garlic are sources of inulin.
health benefits by selectively stimulating the growth and However, in a commercial scale, inulin is obtained through
activity of one or a limited number of bacteria in the colon, the hydrolysis of longer-chain polysaccharides [10]. Inulin is
thereby improving host health [1]. The development of a plant reserve polysaccharide, which the human digestive
prebiotics is focused on nondigestible oligosaccharides system [11] cannot break down. The ‘nondigestible
such as inulin, fructooligosaccharides (FOSs) and galactoo- oligosaccharides’ (NDO) are resistant to digestion and
ligosaccharides (GOS), although, potentially, any dietary absorption, they, therefore, reach the large bowel, where
component that reaches the colon intact is a potential they might be fermented by the local microbiota [10,11].
prebiotic, [2]. Singh et al. [3] included in the prebiotic Some prebiotic carbohydrates are currently used by the food
definition the chemically stable structures that signifi- industry as additives, such as fructooligosaccharides (FOSs).
cantly enhance growth and functionality of gut microflora. FOSs are obtained by partial hydrolysis of inulin or from
Figure 1 depicts the prebiotic action in the host. sucrose by the action of fructosyltransferases [12]. Besides
their prebiotic properties, FOS can be used to partially
The non-digestible oligosaccharides have bioactive prop- replace sucrose in fruit juices without affecting physical
erties so their use as food ingredients has increased in the characteristics of the product.
last years. Such properties include non-cariogenicity, low
caloric value and the modulation of bowel microbiota. Another example of controlled hydrolysis includes
Prebiotics are fermented by beneficial bacteria in the the production of xylooligosaccharides from xylan
intestines producing short chain fatty acids. Prebiotics [13]. Others prebiotics such as lactulose as lactulose,

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56 Innovations in food science

Figure 1 Figure 2

Prebiotic

Gut Microbiota

Fermentation
End Products

Short Chain Fatty

pH drop
Acids (SCFAs)

Colonic and Systemic

Health Effects

Current Opinion in Food Science

Mode of action of prebiotics on host.

galactooligosaccharides, isomaltooligosaccharides, and

glucooligosaccharides are obtained using transglycosyla-
tion [14–19]. Figure 2 shows the chemical structure of the
most studied and applied prebiotic oligosaccharides.

Beyond the NDO, polyphenolic compounds could be

considered prebiotic ingredients. Li et al. (2015) [20]
reported the prebiotic effect of pomegranate ellagitannins
are due to the ellagic acid produced by the gut microbiota
hydrolysis. Alqurashi et al. [21] examined the prebiotic
potential of digested açai pulp and found inhibition in the
growth of harmful gut bacteria such as Bacteroides, Pre-
votella and Clostridium histolyticum when digested açai was
incorporated into culture media.

There are two different way of applying prebiotic oligo-

saccharides in fruit juices: by adding the prebiotic carbo-
hydrate to the food matrix or by synthesizing the prebiotic
carbohydrate directly into the fruit juice. The first
approach is most reported one and requires the use of
purified oligosaccharides, increasing the production costs. Current Opinion in Food Science
Table 1 shows some suppliers of prebiotic oligosacchar-
ides used as food ingredients. The synthesis directly into Chemical structure of the most studied prebiotic oligosaccharides.
the fruit juice suppress the purification steps and uses the
natural sugars of the fruit juice. This latter approach also
reduces the sugar content by turning simple sugars into
prebiotic carbohydrates. The direct synthesis into fruit also, to have attractive sensory characteristics, making
juice was successful for orange juice, cashew apple juice, them well accepted and often consumed by a significant
acerola, lemon, pineapple and melon [22–25]. portion of the population [7]. However, the incorporation
of prebiotics into fruit juices presents some technological
Processing effects challenges. The compatibility of these ingredients with
Fruit juices may represent an ideal vehicle for prebiotic the products regarding physico-chemical, sensory, and
delivery because they are rich in functional components, nutritional properties must be well established [26].

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 Challenges of processing prebiotic fruit juices Fonteles and Rodrigues 57

Table 1

Prebiotic suppliers.

Supplier Product Application Commercial brand Website

Baltic Dairy Board Galactoligosaccharides Infant formula, yogurt, pastry, GOS www.bdbproteins.eu
musli bars, soups and others
Best Ground Inulin from agave Bakery, beverages, processed Agave Inulin www.bestground.com
International foods, food supplements and
desserts
Cargill Health Inulin from chichory Bakery, beverages, Oliggo-Fiber Chicory www.helmmexico.com
food confectionary, dairy products Root Fiber
Helm Polidextrose Bakery, beverages, dairy Sta-Lite III Polidextrose http://www.helmmexico.com
products, cereal, supplements
and snacks
Danisco Soluble and insoluble soy fiber Bakery, extruded snacks and Fibrim Soy Fiber www.danisco.com
cereals
Danisco Polydextrose Bakery, bars, beverages, Litesse www.danisco.com
confectionary, culinary, dairy,
frozen desserts and fruit
processing
Hayashibara Isomaltodextrin Food ingredient Fibryxa www.hayashibara.co.jp
Hayashibara Lactosucrose Food ingredient Nyuka Oligo www.hayashibara.co.jp
Lonza Arabinogalactan (AG) Supplement ResistAid www.lonza.com
Beneo Inulin Bakery, baby foods, beverages, Oraft Inulin www.beneo.com
breakfast cereals, candy, dairy
products, fillings, frozen
desserts and fruit processing
Beneo Fructooligosaccharides Bakery, baby foods, beverages, Orafti L60; Orafti L85; www.beneo.com
breakfast cereal, candy, dairy Orafti L90; Orafti L92;
products, fillings, frozen dessert, Orafti L95 and Orafti P95
fruit processing
Ingredion Resistant starch Food ingredient Hi-Miaze 260 www.ingredion.us
Ingredion Galactooligosaccharide Food ingredient, infant formula BIOLIGOTMGL www.ingredion.us
Ingredion Fructooligosaccharide Food ingredient Nutraflora FBP95; www.ingredion.us
Nutraflora LP95 and
Nutraflora L95S
TICGums Inulin Food ingredient TIC Pretested Inulin LV www.ticgums.com
110

Furthermore, prebiotics had to be stable during food beverages stored at refrigerated temperature in compari-
processing mainly processes involving high temperatures, son with those stored at ambient temperatures.
low pH, or a combination of those factors, favors the
Maillard reactions, which can potentially reduce the The fructooligosaccharides have attracted particular
prebiotic activity of the carbohydrate if the prebiotic attention because of their sweet taste similar to that of
compound is a reducing sugar [27]. sucrose. However, inulin and FOS have been suggested
to be less stable than other oligosaccharides at conditions
A considerable amount of information on the stability of of low pH and high temperatures. The combination of
prebiotics, in particular, GOS, FOS, and inulin are avail- low pH and high temperature is characteristic of fruit
able from experiments using model systems. Also, to a juice processing due to thermal processing. FOS decom-
lesser extent, experiments with real foods; especially position showed a first-order kinetic rate for the hydrolysis
considering the negative impact on organoleptic proper- of FOS and sucrose, but with a much lower activation
ties and maintaining stability during food processing, energy for FOS than for sucrose, indicating that less
have been reported [27,28]. energy is required to hydrolyze FOS [30].

Renuka et al. [29] evaluated the fortification of-of selected GOS are in general very stable to acidic conditions and
fruit juice beverages (pineapple, mango and orange juice) high temperatures, and for this reason, they can be
with fructooligosaccharides (FOSs). The authors potentially added to a variety of acid or heated foods,
observed that fruit juice beverages could successfully such as processed fruit juices [28]. In very acidic condi-
be fortified with FOS with a shelf life of 4 months and tions, the b(2-1) bonds between the fructose units in
6 months at ambient and refrigerated temperature, FOS, can be partially hydrolyzed [31]. Voragen [32]
respectively. At the end of 6 months of storage, a signifi- reported that the heating of an acid FOS solution (pH
cant amount of FOS was retained in the fruit juice 3.5) at 145  C for 10 s resulted in the hydrolysis of

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58 Innovations in food science

Table 2

Literature review on processing effects on prebiotic structure and function.

Processing Fruit juice Prebiotic Key findings Reference


Pasteurization (80–90 C for 5– Apple Oligosaccharides No changes observed after processing and López-Sanz
15 min) derived from during stability (4  C for 90 days) et al. [40]
lactulose (OsLu)
Ultrasound (US) followed by high- Cranberry FOS HPP or the combination of non-thermal Gomes
pressure processing (HPP) technologies (US + HPP) are viable et al. [7]
processes for the treatment of prebiotic
juices. A conservative prebiotic content
was obtained despite the slight changes
inferred during the processing.
Atmospheric cold plasma and ozone Orange Oligosaccharides Both processes promoted a partial Almeida
degradation of the oligosaccharides in the et al. [35]
juice. However, the juice maintained
enough amount of oligosaccharides to be
classified as a prebiotic food. The phenolic
content and antioxidant capacity of the
treated samples was also well preserved as
the pH and color.
Pasteurization Fruit-milk drink gal-xylitol The minimum of 97% of the initial amount of Klewicki [34]
(84–99  C for 30 s–25 min) pH ranging from gal-sorbitol gal-polyols remains in an unchanged form
2.7 to 4.2 lactitol after thermal preservation, while FOSs are
GOS hydrolyzed during pasteurization. The
FOS degree of hydrolysis of these saccharides is
higher the lower the pH and the longer the
pasteurization time. The pasteurization of a
black currant drink (pH = 3.1; 95  C 30 s
+ 84  C 10 min) causes the loss of 50% of
tetrasaccharide and up to 30% of
trisaccharides
Simulated heat and pH stability — Arabinoxylooligosaccharides (AXOS) The short
during storage XOS chain
FOS
oligosaccharides, XOS and FOS, Courtin et al. [41]
were more sensitive to alkaline
decomposition than were the longer
chain AXOS. At pH 2.0 and 3.0,
hydrolysis of oligosaccharide
linkages took place, with FOS being
the most acid-sensitive component
Simulated food processing — FOS and inulin Prebiotic activity was stable for treatments Huebner
conditions: low pH (pH 3–6), heat of low pH and Maillard reaction conditions. et al. [33]
at low pH (30 min at 85  C, pH 4– By contrast, heating at low pH resulted in a
7), and Maillard reaction reduction in prebiotic activity
conditions (up to 6 h at 85  C with
1% glycine, pH 7)
Atmospheric cold plasma (ACP) and Orange FOS HPP showed the highest FOS degradation Almeida
HPP overall percentage. Higher FOS et al. [39]
depolymerization was found in orange juice
compared to the same processing with only
FOS in water evidencing the importance of
the food matrix interaction
HHP (500 MPa for 90 s) at ambient Apple puree Inulin In general, HHP resulted in greater retention Keenan
temperature (20  C), and thermal FOS of the prebiotic compared to sous vide et al. [38]
processing sous vide processing, but there was no evidence of
loss of prebiotic during chill storage.
Atmospheric cold plasma (ACP) — FOS Atmospheric cold plasma (direct or indirect Alves Filho
(direct or indirect application), application), high-pressure processing et al. [30]
HPP and US + HPP (HPP) and ultrasonic treatment followed by
HPP did not significantly change the
concentration of FOS solution and had not
hydrolyzed the FOS molecules.

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 Challenges of processing prebiotic fruit juices Fonteles and Rodrigues 59

approximately 10% of FOS. Huebner et al. [33] reported studied FOS non-thermal processing. Atmospheric cold
that the heating (85  C for 30 min) at low pH caused a plasma (direct or indirect application), HPP and US
significant reduction in prebiotic activity of inulin and followed by HPP did not impart significant FOS degra-
FOS. dation, keeping the concentration and the degree of
polymerization significantly for FOS solution in water
Klewicki [34] compared the stability of gal-xylitol and gal- [30]. On the other hand, ACP and HPP of prebiotic
sorbitol (synthesized with b-galactosidase from lactose orange juice caused some FOS depolymerization [39],
and polyols) with the stability of lactitol, galactooligosac- which supports that changes in DP degree could also be
charides (GOSs) and fructooligosaccharides (FOSs) in the attributed to the interaction between the FOS and the
conditions of pasteurization of juices and fruit drinks (pH juice compounds, aside from the low pH of orange juice.
ranging from 2.7 to 4.2). The galactosyl derivatives of
polyols demonstrate high stability in the pasteurization Understand the behavior of prebiotic during processing is
conditions. It is comparable to the heating resistance a crucial issue for their food applications once the chemical
characteristic of GOSs and lactitol. The minimum of structures of oligosaccharides must be kept to claim the
97% of the initial amount of gal-polyols remains in an food as prebiotic. The number and the type of sugar
unchanged form after thermal preservation, while FOSs moieties and the position and conformation of the carbo-
are hydrolyzed during pasteurization. The presence of b hydrate linkages may affect the not only fermentation
type bonds in the carbohydrate structure is a significant properties of probiotic microorganisms but also the carbo-
factor for the occurrence of the thermostability of trans- hydrate integrity during the processing and storage [14].
galactosylation products obtained using b-galactosidase.
Future perspectives
Some chemical properties of prebiotics influence their The consumers choice for healthier foods has targeted the
stability such as the presence of b-linkages, which are food industry to the development of foods containing
very stable to hydrolysis, although other factors, such as prebiotics and other functional ingredients. The advan-
the sugar residues, the ring form and the anomeric con- tages of regular prebiotic intake are tailoring the food
figuration can play a role too [32,34]. Non-thermal tech- industry to the seek for prebiotic carbohydrates that
nologies, on the other hand, might be a feasible alterna- present low cost, high stability and minimal effect on
tive for processing of prebiotic juices. Prebiotic orange the food properties and taste. Taking into the account the
juice with glucooligosaccharides synthesized by dextran- global market rise for functional foods, the use of fruit
sucrase acceptor reaction was produced and evaluated the juice as a vehicle for prebiotic is a promising field. Studies
effects of atmospheric cold plasma (ACP) and ozone on the carbohydrate stability are crucial to assure the
processing on oligosaccharides [35]. Both non-thermal functional properties of the final product.
technologies have partially degraded glucooligosacchar-
ides, but the juice still kept a sufficient amount of
Conflict of interest
oligosaccharides to be classified as a prebiotic food.
The authors declare no conflict of interest.
The authors pointed out that ozone can cause polysac-
charides depolymerization (DP) producing other poly-
saccharides with shorter chains. Dextransucrase produced Acknowledgments
by L. mesenteroides present a-1,6 glycosidic bonds [36,37]. This review did not receive any specific grant. However, we must
acknowledge the Brazilian funding agencies that usually supports our
research and laboratory (CNPq, CAPES, and FUNCAP). It is also necessary
FOS hydrolysis with a degree of 27.2% and 17.1% for to acknowledge CAPES support for the access to the scientific publications.
apple puree processed by sous vide thermal processing and
high-pressure processing (HHP), respectively was References and recommended reading
reported by [38]. On the other hand, that high-pressure Papers of particular interest, published within the period of review,
have been highlighted as:
processing (HPP) and ultrasound (US) or the combination
of non-thermal technologies (US + HPP) impart only  of special interest
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 Challenges of processing prebiotic fruit juices Fonteles and Rodrigues 61

processed apple purees enriched with prebiotic inclusions. pasteurization, making these technologies suitable and promising for
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