Bioactive Carbohydrates and Dietary Fibre 28 (2022) 100325

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Bioactive Carbohydrates and Dietary Fibre

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

Jerusalem Artichoke (Helianthus tuberosus L.) inulin as a suitable bioactive

ingredient to incorporate into spreadable ricotta cheese for the delivery
of probiotic
Irene A. Rubel a, *, Carolina Iraporda a, Guillermo D. Manrique a, Diego B. Genovese b, c
a
Departamento de Ingeniería Química y Tecnología de los Alimentos, Facultad de Ingeniería, Universidad Nacional del Centro de la Provincia de Buenos Aires. Av. Del
Valle 5737, Olavarría, 7400, Argentina
b
Departamento de Ingeniería Química, Universidad Nacional del Sur (UNS), Av. Colón 80, 8000, Bahía Blanca, Argentina
c
Planta Piloto de Ingeniería Química – PLAPIQUI (UNS-CONICET), Camino La Carrindanga Km 7, 8000, Bahía Blanca, Argentina

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

Keywords: In this work, inulin from Jerusalem artichoke (Helianthus tuberosus L.) tubers or commercial inulin from chicory
Spreadability roots were employed for the development of spreadable ricotta cheese as a basis matrix for the delivery of the
Functional dairy products probiotic strain Lacticaseibacillus paracasei BGP1. The samples of spreadable ricotta cheese containing probiotics
Ricotta cheese
and inulin from Jerusalem artichoke, presented stable physicochemical characteristics for a very high moisture
Probiotics
product. Also, this spreadable cheese preserved the probiotic viability and survival after the gastrointestinal
stress conditions and extended the product’s shelf-life up to 28 days. The results described the successful
application of inulin obtained from alternative plant source, contributing to the diversification of functional
dairy products.

1. Introduction polymerization (DP, between 10 and 60) determines the preponderant

Functional foods provide specific biological functions, improve the
general state of health, reduce the risk of suffering some diseases, and
act as nutrient sources (Rodríguez et al., 2006). The functional food
market has rapidly increased in recent years and is dominated by dairy
food products with the application of probiotic bacteria and prebiotics
as “food additives” (Min, Bunt, Mason, & Hussain, 2019). Probiotics are
live microorganisms that confer a health benefit on the host when
administered adequately (Hill et al., 2014). In particular, its benefits are
related to protecting the human body against infections, especially
through the colonization of mucosal surfaces throughout the gastroin­
testinal tract and their interaction with the immune system (Plaza-Diaz
et al., 2019).
On the other hand, prebiotics are defined as substrates that are used
selectively by human microorganisms, providing a health benefit
(Gibson et al., 2017). In particular, inulin has been extensively
employed as prebiotic in the food industry and thoroughly studied for its
nutritional and technological properties (Karimi et al., 2015). Inulin is a
soluble fiber that consists of a fructose polymer linked by β (2→1)
linkages, with a D-glucose molecule at an extreme and a degree of
technological properties (Leyva-Porras et al., 2015). Inulin is naturally
found as a reserve polysaccharide of different certain vegetal species
(Mudannayake et al., 2015). Currently, chicory roots (Cichorium intybus)
represent the primary inulin industrial source employed to formulate
functional foods (Ahmed & Rashid, 2019). Moreover, Jerusalem arti­
choke (Helianthus tuberosus L.) is an annual plant native from North
America with scarce cultivation requirements and high environmental
conditions resistance, that has emerged as an alternative source of
fructans like inulin (Lv et al., 2019). Jerusalem artichoke tubers (JAT)
store inulin, reaching up to 30% of its fresh weight (Kays & Nottingham,
2008). Although the inulin content in chicory roots or Jerusalem arti­
choke tubers may be similar, some advantages may render the Jerusa­
lem artichoke as a better source of polymers with lower DP (between DP
3–5) compared with the traditional production from chicory (Bedzo
et al., 2020). Different types of commercial inulin are available in the
market and they primarily differ in origin, physical form, average DP,
sweetness, and functionality (Fallourd & Viscione, 2009). The charac­
teristics and functionality of inulin depends on the degree of polymeri­
zation; long-chain inulin is more stable, viscous and less soluble as
opposed to short-chain inulin. Also, short-chain inulin molecules have

* Corresponding author. Facultad de Ingeniería, UNCPBA. Av. Del Valle, 5737, Olavarría, Pcia. Bs. As, Argentina.
E-mail address: irubel@fio.unicen.edu.ar (I.A. Rubel).

https://doi.org/10.1016/j.bcdf.2022.100325
Received 11 February 2022; Received in revised form 3 May 2022; Accepted 18 May 2022
Available online 25 May 2022
2212-6198/© 2022 Elsevier Ltd. All rights reserved.
I.A. Rubel et al.
functional qualities similar to sugar or glucose syrups and therefore
enhance flavor, and sweetness. Meanwhile, long-chain inulin is
commonly employed as fat replacer that considerably improve creami­
ness, mouthfeel and smoothness; also, as gelling agent, viscosity modi­
fier, and texture modifier of different products (Ahmed & Rashid, 2019;
Helal et al., 2018; Illippangama et al., 2022; Shoaib et al., 2016). The
employment of Jerusalem artichoke inulin at the food industry has not
extensively been exploited yet, however some applications in various
food matrices are reported (Rubel et al., 2021).
Dairy products are foods widely consumed worldwide, being the
dairy sector the most significant functional food market (Ali et al.,
2021), with a projected growth to a global level. Also, some authors
mentioned that the regular consumption of safe and live microbes confer
health promoting properties to mitigate or reduce risk of diseases (Di
Marco et al., 2020).
The most common functional products are milk-based (Siro et al.,
2008), however, the development of functional foods based on whey are
scarce.
Ricotta cheese is obtained by enzymatic or heat-induced whey pro­
tein coagulation, unripened product that presents a moisture content
around 75%. It consists of a compact mass with a gel-like structure
composed of whey proteins (mainly α-lactalbumin and β-lactoglobulin),
with a uniform yellowish-white color and a characteristic granular
texture responsible for limited acceptability by consumers (Pintado
et al., 2001). Ricotta cheese also represents a versatile food matrix of
massive consumption, either fresh or as part of fresh and/or cooked meal
fillings. Cheeses have been extensively studied as alternative for pro­
biotic delivery (Homayouni et al., 2020). Several studies have reported
that the intrinsic conditions of cheeses could affect the viability of
probiotic microorganism (Buriti et al., 2007; Rolim et al., 2020). In this
sense, ricotta cheese presents physicochemical characteristics favorable
Fig. 1. Flow diagram for spreadable ricotta cheese elaboration with addition of L. paracasei BGP1 and commercial inulin or Jerusalem artichoke inulin.
2
Bioactive Carbohydrates and Dietary Fibre 28 (2022) 100325
for formulating a probiotic food (da Cruz et al., 2009). Given the po­
tential of Jerusalem artichoke (Helianthus tuberosus L.) as a bioactive
ingredient and the high nutritional value of the dairy industry
by-products such as whey proteins, this work aimed to the diversifica­
tion of functional dairy products based on ricotta cheese. With this
purpose, Lacticaseibacillus paracasei BGP1 combined with Jerusalem
artichoke (Helianthus tuberosus L.) inulin, were incorporated into
spreadable ricotta cheese and the effect on the physicochemical char­
acteristics of the functional product and the probiotic properties of the
strain were evaluated.
2. Materials and methods
2.1. Probiotic culture and Jerusalem artichoke inulin
The probiotic bacterial culture Lacticaseibacillus paracasei BGP1
(Clericci, Sacco, Italy) was stored in MRS broth (Britania, Argentina)
with 20% w/v glycerol at − 20 ◦ C. For its activation, a portion of the
frozen stock was inoculated in MRS broth and incubated at 37 ◦ C in
aerobiosis for 24 h. Periodic transfers were carried out in fresh MRS
broth at 1% to obtain active cultures for incorporation into the
spreadable ricotta cheese formulations.
Inulin was obtained from Jerusalem artichoke tubers, purified and
discolored as described by Rubel et al. (2014 and 2018). Commercial
chicory inulin, with an average polymerization degree ≥10 (GR, Beneo
Orafti, Belgium) kindly donated by Saporiti S.A. (Argentina) was also
employed.
I.A. Rubel et al.
2.2. Elaboration of spreadable ricotta cheese with addition of inulin and
probiotic
A fresh ricotta cheese kindly donated by Lácteos La Casiana
(Argentina) was employed as base matrix, for the functional spreadable
product development (Fig. 1). The final humidity of the spreadable
ricotta cheeses was fixed to 79% w/w. Firstly, an aqueous solution of
0.06% w/w potassium sorbate, 0.4% w/w gelatin 250 H4 (Rousselot,
Argentina) was prepared to be incorporated into the fresh ricotta. In the
corresponding formulations, inulin powder from Jerusalem artichoke
(JAI) or chicory inulin (CI) at 4% w/w, was also added in this step. The
ingredients were introduced into a batch system, heated to 78 ◦ C and
were mechanically treated with domestic mixer (2 min, 1000 rpm) in
order to reduce the particle size, thus generating the spreadable product.
Then, this mixture was rapidly cooled until 55 ◦ C for the incorporation
of the probiotic suspension (1010 CFU/mL) that was previously prepared
in an aliquot of the moisture adjustment water. The spreadable ricotta
cheeses samples were immediately aseptically packed in plastic con­
tainers with the previous spraying of natamycin solution (0.5 g/mL) on
the container and product surfaces. The formulations of spreadable
ricotta cheeses (SRC) were named SRC-C (control), SRC-P (with pro­
biotic), SRC-JAI + P (with probiotic and Jerusalem artichoke inulin),
and SRC-CI + P (with commercial inulin and probiotic). Finally, the
samples were stored at 4 ◦ C for 28 days.
2.3. Physicochemical analysis
2.3.1. Determination of pH and moisture
For all spreadable ricotta cheese formulations developed, the mois­
ture was measured using an infrared balance (Kern DBS, Germany). The
pH was measured using a pH meter (Hanna Instruments, USA) at the
beginning and after 7, 14, 21 and 28 days of refrigerated storage.
2.3.2. Color measurement
The spreadable ricotta cheese samples were homogenized and placed
in plastic containers (0.5 cm height and 3 cm ID). The surface color was
measured using a spectrophotometric colorimeter (Chroma Meter CR-
410, Konica Minolta, Japan). Three measurements of each sample
were carried out. The results were expressed as the parameters of the CIE
scale L* a* b*: where L * (Luminosity: 0 black, 100 white), a* [greenness
(− ), redness (+)] and b* [blueness (− ), yellowness (+)].
2.3.3. Syneresis analysis
The induced syneresis of spreadable ricotta cheeses was determined
as the volume of liquid exuded after centrifugation at 10000×g for 15
min (Sorvall™ Legend™ X1, Thermo Scientific, US). The results were
expressed as a percentage (v/w) (Aichinger et al., 2003). Each measure
was realized in triplicate, from independent samples, during the
refrigerated storage.
2.4. Probiotic viability in the spreadable ricotta cheeses
The viability of the probiotic was analyzed in the spreadable ricotta
samples at 0, 7, 14, 21, and 28 days of refrigerated storage. At each time,
5 g of sample were suspended in 45 mL of saline solution. Then, suitable
decimal dilutions were spread on MRS agar plates (Britania, Argentina)
and incubated for 48 h at 37 ◦ C. The results obtained were expressed as
log CFU per gram of spreadable ricotta cheese.
2.5. Probiotic resistance to the simulated gastrointestinal treatment
The resistance of the probiotic incorporated into the spreadable
ricotta cheese samples to the simulated gastrointestinal conditions was
assesed as described by Grimoud et al. (2010), with modifications. The
spreadable ricotta samples were 10-fold diluted in saline solution. A 2.5
mL aliquot of this suspension was mixed with 2.5 mL of 2-fold
3
Bioactive Carbohydrates and Dietary Fibre 28 (2022) 100325
concentrated simulated gastric solution (NaCl 125 mM, KCl 7 mM,
NaHCO3 45 mM, pepsin 3 g/L, pH adjusted to 2.5) and incubated for 90
min at 37 ◦ C. Then 5 mL of 2-fold concentrated simulated intestinal
solution (NaCl 22 mM, KCl 3.2 mM, NaHCO3 7.6 mM, pancreatin 0.1%
w/v, bovine bile salts 0.15% w/v, final pH adjusted to 8.0) were added
and incubated for 180 min at 37 ◦ C. After these incubations, serial
decimal dilutions were seeded on MRS agar plates (Britania, Argentina),
and the plates were incubated at 37 ◦ C for 48 h. The survival percentage
of the probiotic was calculated according to the following formula:
/
CFU
% survival = Log after GIT Log CFU before GIT x 100
g
g
where CFU/g after GIT and CFU/g before GIT represent cell viability
after and before the simulated gastrointestinal treatment, respectively.
2.6. Shelf-life of spreadable ricotta cheese
The counts of mold and yeasts present in the spreadable ricotta
cheese samples stored 28 days at 4 ◦ C were analyzed. For the assay, 5 g
of sample were placed in 45 mL of saline solution. Then, serial decimal
dilutions were seeded on Sabourade agar plates (Britania, Argentina)
and incubated at 25 ◦ C for 5 days. Results were expressed as Log CFU/g
of sample.
2.7. Statistical analysis
For the statistical analysis of the results obtained, the Software
Infostat Version 2008 was used (Córdoba, Argentina). The results were
expressed as the average ± standard deviation. A variance analysis
(ANOVA) was performed, followed by the LSD Fisher test to compare
multiple means employing a value of α = 0.05.
3. Results and discussion
3.1. Physicochemical properties of functional spreadable ricotta cheese
during storage
Different formulations of spreadable ricotta cheese with incorpora­
tion of L. paracasei BGP1 and inulins were prepared and their physical
and stability properties were compared. The proximal composition of
the fresh ricotta cheese informed by the manufacturer presented
(expressed as a percentage on a dry basis) was the following: lipids,
32.18 ± 1.40; proteins, 41.31 ± 0.64, ashes 6.28 ± 0.08; and carbohy­
drates, 23. This ricotta was employed as base for the spreadable matrix
development. Since moisture is a parameter that influences cheese
texture, in the present work, the moisture of the spreadable ricotta
samples was adjusted to 79% to obtain a softer product that can be
considered a very high moisture cheese. Sant’Ana et al. (2013) reported
that cheeses with higher moisture content have a weaker protein
network, resulting in softer cheeses. Also, this moisture content is in
agreement with previous studies on ricotta cheese (Hesarinejad et al.,
2021; Rubel et al., 2018). Other authors developed ricotta cheeses with
similar moisture contents describing a high spreadability and homoge­
neous appearance by sensory analysis (Miele et al., 2021).
The interconnected molecular protein network of the ricotta matrix
retains fat and water, and confers elasticity and rigidity to the system
(Hesarinejad et al., 2021; Luyten et al., 1991). The strength of in­
teractions depends on pH, calcium-binding, ionic strength, and covalent
bonds via disulfide bridges between casein and whey proteins (Lucey,
Johnson, & Horne, 2003). The control sample (SRC-C), presented initial
pH values of 6.92 ± 0.16 that remained relatively constant during 28
days of storage at 4 ◦ C, with a final pH value of 6.65 ± 0.05. Meanwhile,
the ricotta samples with the probiotic strain showed final pH values
lower than the control sample (Fig. 2a). This fact could be related to the
natural process caused by the production of lactic acid and other organic
I.A. Rubel et al. Bioactive Carbohydrates and Dietary Fibre 28 (2022) 100325

Fig. 2. (a) pH values of spreadable ricotta cheeses during storage at 4 ◦ C. (•)
SRC-C: Spreadable ricotta cheese control. (•)SRC-P: Spreadable ricotta cheese
with probiotic. (•) SRC-P + CI: Spreadable ricotta cheese with probiotic and
commercial inulin. (o) SRC-P + JAI: Spreadable ricotta cheese with probiotic
and Jerusalem artichoke inulin.
Fig. 2. (b) Percentage of syneresis (mL/100 g) of spreadable ricotta cheeses
during storage at 4 ◦ C. (•) SRC-C: Spreadable ricotta cheese control. (■) SRC-P:
Spreadable ricotta cheese with probiotic. (▴) SRC-P + CI: Spreadable ricotta
cheese with probiotic and commercial inulin. (▾) SRC-P + JAI: Spreadable
ricotta cheese with probiotic and Jerusalem artichoke inulin.
inulin. This result evidenced that inulin molecules dispersed among the
casein micelles, serum proteins and gelatin, may be interfering with the
formation of the protein-hydrocolloid network, in agreement with re­
sults obtained by Paseephol et al. (2008). Guven et al. (2005) reported
that whey separation and consistency of low-fat yoghurt, increased with
the concentration of long-chain inulin added. According to Monteiro
et al. (2009), in a matrix of high humidity, such as the spreadable ricotta
cheese, the protein-water interactions are strongly affected by the pH
values, showing that at lower pH, the protein-water interactions
diminish, producing a progressive expulsion of serum from the
protein-network.
In the case of the ricotta control sample, there was an increase in
syneresis between days 14 and 28 of storage. The ricotta samples with
inulin presented higher initial syneresis values, but then this was
reduced and/or stabilized, and at the end of 28 days, it was similar to the
control. This might be because of the inulin reabsorbed the water
released from the protein-network, taking into account its ability to
immobilize large amounts of water, as suggested by Mensink et al.
(2015) and Meyer et al. (2011). As observed in the present work,
Pimentel et al. (2012) reported an increased in the water retention of
dairy products related to the production of exopolysaccharides by pro­
biotic strains. The exopolysaccharides also increased the viscosity, and
their interaction with other components of the dairy matrix results in an
increased cohesiveness and higher stickiness (Pimentel et al., 2012).
Color is an important parameter in the development of new foods
since it is directly related to the product’s appearance and can strongly
affect the general acceptability of the consumers. In this work, the SRC
samples’ color attributes were not significantly different from the con­
trol formulation. In general, the color parameters of all the samples did
not present significant differences at each storage time (Table 1).
However, significant variations in the color parameters were observed in
Table 1
Color parameters (L* a* b*) of the different spreadable ricotta cheese samples
stored at 4 ◦ C.
Days of storage
0 7 14 21 28

SRC-C L* 89,5 ± L* 90,82 ± L* 91,0 ± L* 90,9 ± L* 90,8

acids by the probiotic microorganism that metabolize lactose and sugars
2,0 B a 0,8 A a 0,6 A a 0,4 A a ± 0,5 A ab
presents in the dairy matrix, as reported by other authors in fresh a* − 3,1 a* − 2,97 ± a* − 2,7 ± a* − 2,5 ± a* − 2,3
cheeses (Buriti et al., 2005 and 2007). Moreover, it was observed that ± 0,7 C a 0,5 BC a 0,2 AB a 0,2 A a ± 0,2 A a
the ricotta sample with commercial inulin, presented the lowest final pH b* 13,0 b* 14,79 ± b*14,8 ± b* 14,8 ± b* 14,6
value (5.51 ± 0.01), probably because of the differential ability of the ± 1,8 B b 0,3 A a 0,3 A a 0,6 A a ± 0,2 A c
SRC-P L* 89,8 ± L* 90,28 ± L* 90,7 ± L* 90,4 ± L* 90,5
probiotic strain to ferment inulin from different origin in favor to 0,6B a 0,9 AB a 0,2 A a 0,2 AB b ± 0,2 A b
commercial inulin, as reported by Rubel et al. (2014). Also, de Almeida a*-3,2 ± a* − 3,11 ± a* 2,8 ± a* − 2,9 ± a* − 2,6
et al. (2018) showed an increased acidity and decreased pH values in 0,7 B a 0,7 AB a 0,2 AB a 0,2 AB c ± 0,4 A b
mascarpone-type cheeses with addition of bifidobacteria and inulin b* 14,7 b*14,89 ± b* 14,9 ± b* 14,6 ± b* 15,2
± 0,8 A a 0,5 A a 0,8 A a 1,3 A a ± 0,9 A b
during the storage at 5 ◦ C.
SRC-P L* 91,1 ± L*91,09 ± L* 91,1 ± L* 90,71 L* 90,9
A mechanical treatment was applied during the spreadable ricotta þ CI 0,1 A a 0,1 AB a 0,1 A a ± 0,2 C ab ± 0,1 B a
cheese elaboration process to obtain the desired spreadability; however, a* − 2,6 a* − 2,72 ± a* − 2,8 ± a* − 2,62 a* − 2,1
this step may also lead to a matrix destabilization due to structural ± 0,04 B a 0,04 BC a 0,1 C a ± 0,1 B ab ± 0,1 A a
changes. The induced syneresis was evaluated as an indicator of the b* 15,1 b* 14,84 ± b* 14,7 ± b* 14,83 b* 15,9
± 0,03 Aa 0,2 Aa 0,6 Aa ± 0,2 A a ± 0,1 Aa
ricotta cheese stability (Fig. 2b). The SRC-C presented syneresis values of SRC-P L* 90,8 ± L* 90,7 ± L* 90,9 ± L* 90,5 ± L* 90,9
28.4 ± 4.1% during the storage, showing high stability for this kind of þ 0,04 A a 0,1 A a 0,1 A a 0,3 B b ± 0,1 A ab
product. The probiotic incorporation did not affect the stability of the JAI a* − 2,6 a* − 2,6 ± a* − 27,9 ± a* − 2,7 ± a* − 2,3
samples and did not show significant differences in the syneresis values ± 0,03 B a 0,1 B a 0,03 B a 0,1 B bc ± 0,1 A a
b* 14,7 b* 14,9 ± b* 14,77 ± b* 14,1 ± b* 14,8
with respect to the control during storage. Moreover, the combined
± 0,1 A a 0,2 A a 0,2 A a 0,2 B a ± 0,2 A bc
addition of probiotic and the two types of inulins, slightly increased the
syneresis values for the spreadable ricotta samples obtained after 21 SRC-C: Spreadable ricotta cheese control. SRC-P: Spreadable ricotta cheese with
days, without significant differences. Meanwhile, no significant differ­ probiotic. SRC-P þ CI: Spreadable ricotta cheese with probiotic and commercial
inulin. SRC-P þ JAI: Spreadable ricotta cheese with probiotic and Jerusalem
ences were found at 28 days of storage. It is important to mention the
artichoke inulin.
naturally dynamic physical events that may occur during the storage of a
The different superscripts with uppercase letters indicate significant differences
high moisture cheese added with a probiotic strain and inulin. Along the (p < 0.05) between each SRC samples at the different times. The different su­
first 14 days of storage, the syneresis percentage resulted lower for the perscripts in lowercase letters indicate significant differences (p < 0.05) be­
spreadable ricotta cheese samples without inulin, concerning those with tween the SRC samples at each time.

4
I.A. Rubel et al.
each sample during the period of storage at 4 ◦ C. The luminosity
parameter (L*) showed high values and remained relatively stable
during the 28 days of storage for all the samples. Meira et al. (2015)
informed that the luminosity of goat milk ricotta containing probiotics
was lower than the luminosity for the ricotta developed without pro­
biotics, in coincidence with the results found in the present work after 21
days of storage. The negative a* values of the SRC samples developed
indicated a tendency to a green color, in agreement with results obtained
by Fritzen-Freire et al. (2013) for ricotta-cream cheese. The positive b*
values obtained for the SRC samples indicated a tendency towards a
yellowness, and these values remained practically constant during 28
days of storage. The same behavior was described by Fritzen-Freire et al.
(2013) for ricotta-cream cheese with probiotics during the same period
of storage; however, an increase in the b* value was described for longer
storage times. Also, Fresno and Alvarez (2012) informed a rise in the
yellowness of goat cheeses stored 90 days. According to these authors,
there is a positive correlation between total solids and b* values. In
agreement with this statement, in the present study, the content of total
solids and the values of the parameter b* remained practically constant.
The low yellowness and the high luminosity values of the SRC samples
obtained suggest a potential high acceptability of the product. Finally, in
line with the results obtained in the present work, other authors reported
that incorporating probiotics in cheeses promotes color changes during
storage (García et al., 2012; Rohm & Jaros, 1996).
3.2. Probiotic counts in spreadable ricotta cheeses during storage
Dairy products traditionally represent the ideal matrices for devel­
oping probiotics foods; however, it is necessary to guarantee in each case
the maintenance of bacterial viability at the recommended minimal
limit of 6 Log CFU/g during their storage (Granato et al., 2010). The
viability of probiotics in a dairy matrix is related to various barriers
existing in the processing. L. paracasei BGP1 counts in spreadable ricotta
cheese samples was analyzed during storage at 4 ◦ C (Fig. 3). After 21
days of storage, all SRC samples presented counts around 8 Log CFU/g,
indicating that this matrix presented favorable conditions for the sur­
vival of probiotic cells. Silva Meira et al. (2015) informed that the
probiotic strains Lactobacillus acidophilus La-05 and Bifidobacterium
animalis subsp lactis Bb-12 maintained their viability in goat ricotta
during 7 days of storage. Buriti et al. (2007) reported the counts of the
probiotic L. paracasei subsp. paracasei incorporated into fresh cream
cheese were in the order of 7 Log CFU/g along 21 days of storage. These
authors showed that the incorporation of inulin in this product did not
affect the viability of the strain. In contrast, other authors have reported
that inulin-type prebiotics can benefit the survival of probiotic micro­
organisms during the processing and storage of dairy products (Capela
et al., 2006; Desai et al., 2004; Özer et al., 2005). In the present study,
higher counts of L. paracasei BGP1 were found in the SRC samples
Fig. 3. Bacterial viability (Log CFU/g) of L. paracasei BGP1 in spreadable
ricotta cheeses during storage at 4 ◦ C. (■) SRC-P: Spreadable ricotta cheese
with probiotic. (▴) SRC-P + CI: Spreadable ricotta cheese with probiotic and
commercial inulin. (▾) SRC-P + JAI: Spreadable ricotta cheese with probiotic
and Jerusalem artichoke inulin.
5
Bioactive Carbohydrates and Dietary Fibre 28 (2022) 100325
containing either of the two inulins after 28 days of storage. Desai et al.
(2004) observed an increase in the viability of Lactobacillus strains when
cultivated in reconstituted low-fat milk supplemented with 5% (w/v)
inulin. In contrast, Özer et al. (2005) evaluated the viability of Lacto­
bacillus delbrueckii subsp. bulgaricus, and Lactobacillus acidophilus in
yoghurt supplemented with inulin at 0.5 and 1% (w/v) with no effect on
the viability of these cultures. Furthermore, Capela et al. (2006) re­
ported that the addition of commercial fibers inulin and FOS at 2%
(w/v) improved the viability of L. acidophilus 33200, L. casei 279, Bifi­
dobacterium longum 536 and L. rhamnosus GG in fresh yoghurt, in com­
parison with control yogurt (without added fiber), during 28 days of
storage at 4 ◦ C. The differences in the probiotic behavior may be related
to specific features of the strains, the ability to ferment the soluble fibers
such as inulin-type fructans, and the storage time (Makras et al., 2005).
3.3. Probiotics survival after simulated gastrointestinal conditions
In developing potentially probiotic food, it must be guaranteed that
the microorganisms added into the matrix can tolerate the digestive
stress. The results obtained in the present work showed that after the
simulated gastrointestinal treatment, the percentage of survival of
L. paracasei BGP1 incorporated into spreadable ricotta cheeses were
higher than 55% (Fig. 4). It is worth to mention that the SRC-P and SRC-
P + CI, presented final counts of L. paracasei of 6.3 and 6.6 Log CFU,
respectively, with no significant differences. Besides, the final count in
SRC-P + JAI was 5.3 Log CFU. These results demonstrate that the
spreadable ricotta cheese is a suitable matrix for incorporating this
probiotic strain. The buffering capacity of the ricotta matrix, most likely
may resist the change in pH resulting in an improved survival of pro­
biotic microorganisms (Kisan et al., 2021; Silva Meira et al., 2015).
Moreover, the total solid content of the ricotta cheese may enhance the
probiotic protection, resulting in higher survival of the microorganism
after the gastrointestinal stress. The water activity of the matrix may also
influence the capacity of microorganisms to resist low pH conditions, so
the high-water activity of ricotta cheese might be helpful to decrease the
stress imposed during gastrointestinal transit (da Cruz et al., 2009). de
Oliveira et al. (2014) described that semi-hard goat cheese presented a
protective effect on probiotic strains when challenged with artificial
digestion. Meanwhile, da Cruz et al. (2009) also described a high
Fig. 4. Percentage of survival of L. paracasei BGP1 included in the spreadable
ricotta cheeses stored 21 days at 4 ◦ C, after the gastrointestinal simulated
treatment. Different letters indicate significant differences (p < 0.05). (•) SRC-
P: Spreadable ricotta cheese with probiotic. (•) SRC-P + CI: Spreadable ricotta
cheese with probiotic and commercial inulin. (•) SRC-P + JAI: Spreadable
ricotta cheese with probiotic and Jerusalem artichoke inulin.
I.A. Rubel et al.
probiotic survival in other cheese types after exposure to the gastroin­
testinal conditions. Other authors showed a higher resistance of pro­
biotic microorganisms when incorporated in ricotta matrix obtained
from goat and buffalo milk, compared with their resistance in MRS
medium (Kisan et al., 2021; Silva Meira et al., 2015). Desai et al. (2004)
indicated that the incorporation of inulin also improves bacterial sur­
vival both during the food processing and during the passage through
the gastrointestinal tract in vitro, allowing to reach higher final counts of
viable microorganisms at the colon level, as observed in the present
work for the SRC sample with commercial inulin. However, this effect
was not observed in the SRC sample with Jerusalem artichoke inulin.
This difference may be attributed to the weaker structure obtained with
Jerusalem artichoke inulin, generating greater susceptibility to the
rupture and so, the exposure of the probiotic to the environmental
gastrointestinal simulated conditions. Other authors report that the
presence of inulin in mascarpone-type cheese, was not the major factor
in the survival or bifidobacteria during the gastrointestinal stress.
Various authors have described that the inulin incorporation to dairy
matrices improves the probiotic strains’ tolerance to the simulated
gastrointestinal conditions (Casarotti et al., 2015; Padilha et al., 2016;
Zhang et al., 2021). At the same time, added to the fact that the dairy
components contribute to maintaining the viability of the probiotic
strains, the addition of growth promoters (e.g., sugar, prebiotics) in the
food may also enhance the delivery and viability of the microorganisms
in the intestinal environment (Terpou et al., 2019).
3.4. Shelf-life of spreadable ricotta cheese
Spreadable ricotta cheese is a product with an expected short shelf-
life due to its high moisture (79%) and nutrients content, such as min­
eral salts and lactose. Regarding the microbiological quality of the
ricotta cheeses developed in the present work, the mold and yeast counts
were evaluated after 28 days of refrigerated storage. The SRC control
(SRC-C) sample showed a mold and yeasts level >5 Log CFU/g. Mean­
while, the SRC sample containing L. paracasei BGP1 (SRC-P) presented a
mold and yeasts level of 2.9 Log CFU/g; and the samples with both inulin
types (SRC-P + CI and SRC-P + JAI) presented levels above 2.7 Log CFU/
g. These results are lower than the reference limit value allowed for the
Argentinean legislation of 3.7 Log CFU/g. As suggested by de de Vuyst
et al., 2004 probiotic bacteria may contribute to the food preservation
due to their potential antimicrobial activity, given by the production and
delivery of different compounds synthesized by these bacteria into the
food matrix. These results showed that the incorporation of the probiotic
and inulin contributed to extending the shelf-life of the ricotta-based
spreadable product, possibly due to the competence or the production
of antimicrobial compounds. In line with the results obtained in the
present work, Hegab et al. (2021) reported that the shelf-life of Karish
cheese was extended up to 28 days when supplemented with
L. plantarum and inulin. In the same way, the addition of Lactobacillus
rhamnosus IMC 501® and Lactobacillus paracasei IMC 502® allowed the
extension of shelf-life longer than original foods (Coman et al., 2012).
4. Conclusion
In this work inulin was incorporated into spreadable ricotta cheese to
develop a suitable matrix for the delivery of the probiotic strain Lacti­
caseibacillus paracasei BGP1. The spreadable ricotta cheese obtained
presented physicochemical characteristics of a very high moisture
cheese. Furthermore, this matrix was suitable for incorporating the
probiotic strain Lacticaseibacillus paracasei BGP1 in combination with
inulin. The probiotic strain showed high viability during storage. Also,
the spreadable ricotta cheese matrix showed to be effective as a potential
protective matrix for the probiotic against the stressful conditions
imposed by the gastrointestinal tract conditions. In particular, the
spreadable ricotta cheese containing L. paracasei BGP1 together with
Jerusalem artichoke inulin presented stable physicochemical
6
Bioactive Carbohydrates and Dietary Fibre 28 (2022) 100325
parameters during storage and preserved the viability of the probiotic at
the recommended levels to provide consumers with health benefits.
Moreover, spreadable ricotta added with the probiotic and inulin
extended their shelf-life, contributing to limit the use of other chemical
preservatives, responding to the demands of products with clean labels.
Besides, to the best of our knowledge, this study presents a novelty
application of Jerusalem artichoke inulin, giving rise to a final product
with promissory features, contributing to the future development of new
functional dairy foods and also respond to the growing demand for food
products with bioactive properties.
CRediT authorship contribution statement
Irene A. Rubel: have made substantial contributions to conception
and performed the experimental assays, design, acquisition, Formal
analysis, analysis and interpretation of data, Writing – original draft,
manuscript writing. Carolina Iraporda: have made substantial contri­
butions to conception and performed the experimental assays, design,
acquisition, Formal analysis, analysis and interpretation of data, Writing
– original draft, manuscript writing. Guillermo D. Manrique: have
been involved in drafting the manuscript and revising it critically for
important intellectual content and final approval of the version to be
published. Diego B. Genovese: have been involved in drafting the
manuscript and revising it critically for important intellectual content
and final approval of the version to be published.
Declaration of competing interest
The authors confirm that they have no conflicts of interest with
respect to the work described in this article.
Acknowledgments
The authors thank the financial support through National Agency
Promotion Science and Technology (ANPyCT, Argentina) research pro­
jects PICT 2019-1220 and PICT 2019-0211, research projects form the
Faculty of Engineering National of the University of the Center of Buenos
Aires Province (FIO i + D + I, UNCPBA) and National Council of Sci­
entific and Technical Research (CONICET, Argentina).
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