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International Journal of Food Science and Technology 2023, 58, 145–153 145

Original article
Development of bigel based dysphagia-oriented products,
structured with collagen and carnauba wax: characterisation and
rheological behaviour

Viktorija Eisinaitė,* Ina Jasutienė, Rimantė Vinauskienė & Daiva Leskauskaitė


Kaunas University of Technology, Department of Food Science and Technology, Radvilenu pl 19, Kaunas LT-50254, Lithuania
(Received 13 June 2022; Accepted in revised form 31 October 2022)

Summary The aim of the study was to design composition of the bigels with required rheological properties that
responds the needs of the dysphagia patients. Bigels were prepared with carnauba wax and different collagen
concentrations in the hydrogel phase (40, 60%) as well as by changing oleogel to hydrogel ratio from 40:60
to 60:40. The stability, physical and rheological properties of obtained bigels were evaluated after their
preparation and after 14 days storage. All obtained bigels were stable without phase separation and had a
pleasant taste and good mouth-feel, exept bigels with the higher oleogel fraction. Viscosity values at 50 s−1
divided formulated bigels into two groups: honey-like and spoon thick. An increase of oleogel fraction
caused an increase in the consistency index and elastic modulus. Higher firmness and cohesiveness values
were obtained in the samples with the higher collagen concentration. It was also obtained that all rheological
parameters increased after 14 days of storage. The present work develops a novel bigel-based product with
strong shear-thinning behaviour and high protein concentration (16–36%). It is believed that such product
could not only ensure the safe swallowing process but also reduce the risk of malnutrition development.
Keywords bigel, dysphagia, food design, rheology.

for the longer response of the muscles that are respon-


Introduction
sible for swallowing (Dewar & Joyce, 2006; Nishinari
Dysphagia is a swallowing dysfunction, causing diffi- et al., 2019). Viscosity is a fundamental property as it
culty in transferring a liquid or food bolus from is used in the categorization of dysphagia-oriented
mouth to stomach (Clave & Shaker, 2015; Taguchi products: thin (1–50 cP), nectar-like (51–350 cP),
et al., 2022). The most prevalent and severe stage is honey-like (351–1750 cP), and spoon thick (>1750 cP)
oropharyngeal dysphagia that already affecting 8% of (NDD, 2002). It was also previously reported that
the population (Chen, 2009). Dysphagia may be such categorization facilitates palliative care proce-
caused by many disorders and diseases such as stroke, dures for different types of patient needs. There are a
Parkinson disease, cerebral palsy, head and neck can- number of publications about dysphagia-oriented food
cer, and etc. It was also reported that ageing is associ- products, most of which are focused on liquids whose
ated with a slowing of the swallow response and viscosity has been changed by using thickeners (syn-
tongue pressure decline that could cause presbyphagia. thetic or natural) or already existing solid or semi-
The state of presbyphagia does not give rise to patho- solid products that have been modified to purre consis-
logical changes in swallowing as such, but it is a risk tency (for example blending) (Choppe et al., 2010;
factor that can lead to oropharyngeal dysphagia (de Vieira et al., 2020; Vieira et al., 2021; Wei et al., 2021).
Stefano et al., 2020). Untreated dysphagia can lead to It is clear that safe swallowing could be only achieved
malnutrition, dehydration, aspiration, and higher mor- by modifying and obtaining the desired structure of
tality rates among patient populations (East the product. In our opinion, novel biphasic gelled sys-
et al., 2014). tems could be successfully used for that purpose.
Patients with this disorder should receive specially Bigels are two-phase semi-solid systems usually com-
thickened foods in order to increase the bolus passage prising of the gelled oil phase (oleogel) and gelled
time from the mouth to the oesophagus, allowing time water phase (hydrogel) (Shakeel et al., 2019). Due to
unique structure bigels has the advantages of both
*Correspondent: E-mail: viktorija.eisinaite@ktu.lt emulsion and gel systems and have been favourable as

doi:10.1111/ijfs.16181
Ó 2022 Institute of Food, Science and Technology (IFSTTF).
13652621, 2023, 1, Downloaded from https://ifst.onlinelibrary.wiley.com/doi/10.1111/ijfs.16181 by Kaunas University Of, Wiley Online Library on [16/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
146 Bigel based dysphagia-oriented products V. Eisinaitė et al.

more stable delivery systems for lipophilic and hydro- olive pomace oil was purchased from the local super-
philic compounds and controlled bioactive compounds market (Basso, San Michele di Serino, Italy) and used
release (Shakeel et al., 2021). All those advantages as such. This oil contains saturated (10.8 g/100 mL),
caught our attention and make us believe that by using monounsaturated (32.8 g/100 mL) and polyunsatu-
such double gellation technology is possible to create rated (48.3 g/100 mL) fatty acids. Carnauba wax
specifically intended products to the dysphagia diets. (melting point 82°C–84°C) obtained from Sigma-
In recent years, there were several attempts to apply Aldrich (St. Louis, Missouri) was used as an oil struc-
bigels in cosmetics and farmaceuticals (Choppe turing agent. Emulsifier soy lecithin was kindly offered
et al., 2010; Martı́n-Illana et al., 2022). To our knowl- by Alvas Group (Kaunas, Lithuania).
edge, bigels were never applied for the dysphagia-
oriented food products. Preparation of bigels
It was previously reported that bigel properties highly The oil phases (oleogels) were prepared by dissolving
depend on the gelator type, concentration, oleogel, and carnauba wax (as a gelator) and lecithin (as emulsifier)
hydrogel ratio as well as preparation conditions (Faso- (quantities are given in Table 1) in a mixture of sun-
lin et al., 2021). In order to tailor physical properties of flower oil and olive pomace oil in water bath at 85°C
these systems, ingredients used in the production must until complete solubilisation (~30 min). The most suit-
be chosen very carefully especially considering their fur- able concentrations of the lipophilic compounds were
ther purpose. Various biopolymers such as guar gum selected after many preliminary experiments. The
(Singh et al., 2014), xanthan gum (Moschakis water phases (hydrogels) were prepared by dispersing
et al., 2016), alginate (Martins et al., 2019), pectin (Lupi different collagen concentrations (quantities are given
et al., 2016), hydroxypropyl-methylcellulose (Ibrahim in Table 1) into distilled water and were kept in water
et al., 2013), and agar-gelatin mixture (Wakhet bath at 85°C for 30 min. To obtain bigels, both phases
et al., 2015) were previously used in the bigel formula- were mixed and homogenised with rotor-stator homo-
tion to obtain hydrogel phase. As was previously geniser Ultra-Turrax (IKA T-18, basic, Staufen, Ger-
reported, a thermo-reversible gelatin gel tend to melt many) for 3 min at 11 000 rpm in a water bath
below human body temperature resulting unique melt- (85°C). Immediatelly after homogenization mixtures
in-the-mouth property that is highly desirable for good were transfered to the icy water in order to induce
human consumption perception (Huang et al., 2019). gelation of both phases and were kept at 4°C for 24 h
Whereas gelatin is denatured collagen, it was decided to and 14 days prior to characterisation. The oil-in-water
use collagen for the bigel preparation in order to obtain bigels were formed in the samples where oleogel
double functionality. First, thermally treated collagen hydrogel ratio were 40:60 and 50:50. After increasing
will act as a gelator for the hydrogel phase and in addi- oleogel content to 60% bigels demonstrated water-in-
tion to that it will be used as a source of proteins in the oil type.
dysphagia-oriented food products. The protein content
in such type of products should be as high as possible,
Methods
as the protein consumption of the elderly should be
between 1.0 and 1.5 g protein/kg/day (Nowson & Textural properties
O’Connell, 2015). Firmness and cohesiveness were used to characterise
Therefore, the aim of the study was to design com- textural properties of the bigels and were obtained by
position of the bigels with required rheological proper-
ties that responds the needs of the dysphagia patients Table 1 The composition (% w/w) of bigel samples prepared
by changing concentration of collagen in hydrogel and with different oleogel:hydrogel ratio and collagen concentra-
ratio between oleogel and hydrogel. The stability, tions
physical and rheological properties of obtained bigels
were evaluated after their preparation and after Oleogel:Hydrogel ratio
14 days storage.
40:60 50:50 60:40

Concentration in hydrogel, (% w/w)


Materials and methods
Collagen 40 60 40 60 40 60
Water 60 40 60 40 60 40
Materials Concentration in bigel, (% w/w)
Collagen (bovine, I and III type mixture; 90% of pro- Collagen 24 36 20 30 16 24
Carnauba wax 3.2 3.2 4 4 4.8 4.8
tein) was obtained from MyProtein (Manchester, UK)
Lecithin 0.2 0.2 0.25 0.25 0.3 0.3
and used together with an ultra-pure water for the
Oil 31 31 41 41 51 51
water phase (hydrogel) preparation. For the oil phase Water 41.60 29.60 34.75 24.75 27.90 19.90
(oleogel) preparation a mixture of sunflower oil and

International Journal of Food Science and Technology 2023 Ó 2022 Institute of Food, Science and Technology (IFSTTF).
13652621, 2023, 1, Downloaded from https://ifst.onlinelibrary.wiley.com/doi/10.1111/ijfs.16181 by Kaunas University Of, Wiley Online Library on [16/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Bigel based dysphagia-oriented products V. Eisinaitė et al. 147

backward extrusion mode. Measurements were per- Results and discussion


formed with a TA-XT2 texture analyser (Stable Micro
Systems, TA.XT Plus, Godalming, UK) equipped with All obtained bigels were homogenous with an opaque
a 30 kg load cell. About 100 g of bigel was formed in appearance, had milky-yelowish colour and did not
a 150 mL glass beaker (50 mm in diameter and show phase separation. It is required that no phase
85 mm height) and penetrated to a distance of 10 mm separation occur throughout the swallowing process in
at a speed 1 mm/s with a 20 mm aluminium cylindri- order to avoid aspiration of food into the pulmonary
cal plunger and then returned to a starting point. airways (Germain et al., 2006). Preliminary tests of
acceptance showed that bigels had a pleasant taste and
Colour good mouth-feel, except bigels with the higher oleogel
Bigel colour measurement was performed with a Min- fraction as an excessive amount of fat was felt. It was
olta Chroma Meter colorimeter (Model CR-310, Japan) also visually visible that samples with 40% of the col-
according to CIE standards, and the values of L, a* and logen in the hydrogel phase had a more liquid consis-
b* were recorded. The colour parameters L*, a*, and b* tency.
represented lightness, redness/greenness, and yellow-
ness/blueness, respectively. The colorimeter was cali- Colour
brated with a standardwhite plate. Whiteness index
(WI) that is the measure of degree of whiteness of a pro- Results indicated a change in the colour of the samples
duct was calculated from the following equation (Barros mainly due to different formulations. Evaluating oleo-
et al., 2020): gel and hydrogel ratio it could be seen (Table 2) that
h i1=2 lightness (L* value) and redness (a* value) decrease
WI ¼ 100 ð100L Þ2 þ a2 þ b2 (1) and yelowness (b* value) increase were obtained in
bigels with relatively higher oleogel fractions; this
directly related with the higher amount of yellow oil
Rheological properties addition. However, the colour parameters were mainly
All rheological measurements were performed with a influenced by the collagen concentration in the hydro-
Physica MCR502 rheometer (Anton Paar, Graz, Aus- gel phase, especially L* and b* values. This is associ-
tria) at 25°C usingcone-plate geometry (D 25 mm, angle ated to the lower amount of water in those systems.
2°, truncation 99 μm) with 0.1 mm gap. In order to cre- Thus, the same reason caused decrease in whiteness
ate controlled initial state in the samples all samples index (WI) from the 73.24–75.74 to 57.53–61.08 and
were pre-shared at a shear rate of 100 s−1 for 1 min, fol- these differences were observed directly by the eye.
lowed by a rest period at 5 min (Dinkgreve et al., 2016). It is desirable that relevant changes of the colour do
The flow behaviour of bigel samples were measured not appear during period of product shelf life as col-
in a shear rate range from 0 to 400 s−1. Apparent vis- our plays a significant role on product acceptability.
cosity values at a fixed shear rate of 10 s−1 (indicator The colour parameters remained relatively constant
of oral shear rate according to Cutler et al. (1983)), when the systems were kept for 14 days at 4°C
50 s−1 (used as a reference by the National Dysphagia (Table 2). We could make assumption that minor
Diet – (NDD, 2002) and 400 s−1 (representative value changes could be related with changes in rheological
to which a liquid food is subjected during the swallow- and structural properties of the samples as a fraction
ing process according to Meng et al., 2005)) were eval- of the light waves is absorbed by the bigel and there-
uated for the different bigel formulations. fore less light is reflected from the surface (Chantra-
Oscillatory measurements were performed at a fre- pornchai et al., 2001).
quency sweep between 0.1 and 100 Hz within the lin-
ear viscoelastic region (strain 0.05%). Based on the
frequency sweep data, the complex viscosity at 50 rad/ Rheological properties
s, storage (G’), loss (G") modulus and loss tangent The first step in the evaluation of rheological proper-
(tan δ) at a fixed frequency of 1 Hz were evaluated. ties is to measure apparent viscosity at 50 s−1 as it is a
crucial parameter for the dysphagia-oriented products
Statistical analysis (Wood, 1968) (Fig. 1). However, such parameters as
apparent viscosity at 10 s−1 and 400 s−1, complex vis-
All analyses were carried out in triplicate. The results cosity at 50 rad/s, G’ (elastic modulus), G" (loss mod-
are presented as the mean  standard deviation. A P- ulus), tan δ, consistency coeficient (κ), flow index (n)
value of <0.05 was used to indicate significant differ- and cohesiveness could give extra information about
ences between the mean values determined by an anal- the product consistensy (Vieira et al., 2020) (Tables 3
ysis of variance (ANOVA) using Statistica 12.0 and 4). The power-law model was fitted to the data to
(StatSoft, Inc., 2013). obtain rheological properties (Vieira et al., 2021):

Ó 2022 Institute of Food, Science and Technology (IFSTTF). International Journal of Food Science and Technology 2023
13652621, 2023, 1, Downloaded from https://ifst.onlinelibrary.wiley.com/doi/10.1111/ijfs.16181 by Kaunas University Of, Wiley Online Library on [16/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
148 Bigel based dysphagia-oriented products V. Eisinaitė et al.

Table 2 Colour coordinates and textural properties of the bigels of different formulations after preparation and after 14 days of
storage at 4°C temperature

After preparation After 14 days of storage

40% collagen in hydrogel


O:H ratio 40:60 50:50 60:40 40:60 50:50 60:40
L* 86.04  0.56b 85.84  0.83b 84.36  0.56a 85.39  0.51b 84.13  1.44a 84.20  0.62a
a* −1.87  0.08c −2.48  0.08b −2.91  0.11a −1.48  0.09c −2.08  0.04b −2.60  0.13a
b* 19.75  0.06a 20.70  0.27b 21.51  0.34c 20.95  0.09a 22.21  0.37b 22.38  0.40b
WI 75.74  0.28c 74.79  0.30b 73.24  0.12a 74.41  0.22b 72.59  0.51a 72.47  0.13a
Firmness, N 0.08  0.00a 0.08  0.00a 0.08  0.01a 0.08  0.01a 0.08  0.00a 0.09  0.01a
Cohesiveness (−) 0.04  0.01a 0.04  0.00a 0.07  0.01b 0.10  0.01a 0.09  0.00a 0.09  0.01a
60% collagen in hydrogel
O:H ratio 40:60 50:50 60:40 40:60 50:50 60:40
L* 69.43  0.98b 64.31  0.52a 64.66  0.76a 68.75  0.87c 65.07  1.06a 65.06  0.81b
a* −1.43  0.17c −1.78  0.07b −2.82  0.05a −1.70  0.12c −1.88  0.10b −2.11  0.04a
b* 24.03  0.69a 24.30  0.47a 25.38  0.42b 23.80  0.61a 25.80  0.40b 26.31  0.24b
WI 61.08  0.36c 56.79  0.31a 57.53  0.40b 60.68  0.33c 56.52  0.76a 57.78  0.49b
Firmness, N 0.90  0.07b 0.73  0.08a 0.89  0.06b 2.79  0.27b 1.38  0.20a 1.59  0.07a
Cohesiveness (−) 1.01  0.09b 0.64  0.05a 0.63  0.06a 1.21  0.00b 1.07  0.01ab 0.97  0.02ab

Values represent the mean of triplicate  standard deviation. Data labelled with different letters showed statistically significant differences
(P < 0.05) between bigel formulations with different oleogel hydrogel ratio.

Figure 1 Viscosity at a fixed shear rate of 50 s−1 immediately after preparation (IMP) and after 14 days of storage (14D) at 4°C temperature.
40% or 60% indicates the amount of collagen in the hydrogel phase. Data labelled with different letters showed statistically significant differ-
ences (P < 0.05) between different bigels formulation. *Statistically significant differences (P < 0.05) during storage. The dashed line separates
honey like (below) and spoon-thick (above) viscosity according to National Dysphagia Diet.

σ ¼ k∙γn guarantee the safety of the new product for dysphagia


patients (Hadde et al., 2021).
where: σ – shear stress (Pa), k – consistency index All bigels presented shear-thinning behaviour which
(Pa*sn), γ – shear rate (s−1), n – flow index. implies viscosity decrease with an increase in shear
It follows that a complete rheological analysis apply- rate. This was also confirmed by the flow index n < 1
ing different shear rates/frequencies is essential to (0.474–0.832) that could be compared to the most high

International Journal of Food Science and Technology 2023 Ó 2022 Institute of Food, Science and Technology (IFSTTF).
13652621, 2023, 1, Downloaded from https://ifst.onlinelibrary.wiley.com/doi/10.1111/ijfs.16181 by Kaunas University Of, Wiley Online Library on [16/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Bigel based dysphagia-oriented products V. Eisinaitė et al. 149

Table 3 Rheological characteristics of the bigels of different formulations after preparation

40% collogen 60% collogen

O:H ratio 40:60 50:50 60:40 40:60 50:50 60:40

Apparent viscosity 0.854  0.057 a


1.503  0.085 b
2.173  0.206 c
32.700  2.710 b
2.493  0.903 a
4.400  0.690a
at 10 s−1 (mPas)
Apparent viscosity 0.500  0.027a 0.539  0.011a 0.612  0.031b 2.290  0.740b 1.243  0.272a 1.250  0.180a
at 400 s−1 (mPas)
Complex viscosity η* 0.53  0.00a 1.06  0.04a 7.50  0.49b 67.40  8.63a 94.45  20.44a 578.33  30.66b
at 50 rad/s
κ (Pasn) 1.457  0.113a 3.127  0.326b 5.147  0.157c 1.200  0.05a 2.710  0.779a 7.039  0.560b
n 0.832  0.005c 0.712  0.011b 0.654  0.027a 0.474  0.008a 0.811  0.088c 0.684  0.027b
R2 0.99698 0.99894 0.99386 0.8316 0.88783 0.91123
tan δ (1 Hz) 1.37  0.16b 2.20  0.15c 0.55  0.03a 1.45  0.29b 0.64  0.02a 0.33  0.00a
G’ at 1 Hz (Pa) 0.38  0.01a 0.57  0.08a 25.40  2.69b 95.00  38.18a 267.50  55.05b 2626.67  156.31c
G" at 1 Hz (Pa) 0.53  0.04a 1.24  0.08a 13.80  0.71b 107.03  30.40a 171.75  35.22b 871.67  48.68c

Values represented as mean  standard deviation. Data labelled with different letters showed statistically significant differences (P < 0.05) between
bigel formulations with different oleogel hydrogel ratio.
R2 – coefficient for rheological Hershel-Bulkley model.

Table 4 Rheological characteristics of the bigels of different formulations after 14 days storage at 4°C temperature

40% collogen 60% collogen

40:60 50:50 60:40 40:60 50:50 60:40

Apparent viscosity 1.41  0.18a 2.22  0.18b 2.38  0.17b 36.37  0.61c 3.11  0.44a 5.38  0.01b
at 10 s−1 (mPa*s)
Apparent viscosity 0.79  0.16b 0.67  0.03ab 0.68  0.04ab 3.74  0.26b 0.83  0.08a 0.68  0.37a
at 400 s−1 (mPa*s)
Complex viscosity η* 0.65  0.03a 1.45  0.03b 13.90  1.27c 60.40  1.56a 118.50  2.12b 922.00  72.12c
at 50 rad/s
k 3.319  0.158a 5.314  0.293b 5.951  0.187c 3.56  0.87a 11.898  1.645b 13.483  1.191c
n 0.762  0.024c 0.660  0.016b 0.636  0.009a 0.551  0.052b 0.553  0.081b 0.493  0.114a
R2 0.99752 0.9805 0.99577 0.94561 0.81687 0.94855
tan δ (1 Hz) 1.56  0.18c 1.97  0.11c 0.43  0.06a 2.08  0.11b 0.57  0.04a 0.32  0.00a
G’ at 1 Hz (Pa) 0.43  0.09a 1.05  0.04a 60.40  5.94b 34.50  2.83a 366.00  9.90b 4640.00  445.48c
G" at 1 Hz (Pa) 0.66  0.06a 2.07  0.04a 25.17  4.48b 71.35  2.05a 215.00  1.41b 1460.00  127.28c

Values represented as mean  standard deviation. Data labelled with different letters showed statistically significant differences (P < 0.05) between
bigel formulations with different oleogel hydrogel ratio.
R2 – coefficient for rheological Hershel-Bulkley model.

molecular weight polymers, used for the liquids thick- It should be noticed that viscosities of the stored
ening (Mandala et al., 2004). The apparent viscosity bigels were reasonably higher than those of measured
values at 50 s−1 (refered by the NDD) are shown in after preparation. Furthemore, bigels showed a signifi-
Fig. 1. It is clearly seen that all prepared bigels could cant (P < 0.05) increase in viscosity at higher collagen
be divided into two groups by the viscosity values: concentration (Fig. 1). This could be explained by the
honey-like and spoon thick. Nectar-like, honey like multiple noncovalent intermolecular interactions,
and spoon thick consistency are recommended in the which effectively bind large transient networks of asso-
palliative care of dysphagia patients (Zargaraan ciated protein molecules that resist flow and hence
et al., 2013). That shows potential of the pseudoplastic exhibit higher viscosity (Conley et al., 2012).
bigel consistency to be used in such patients nutrition An increase of oleogel fraction caused an increase in
as the non-Newtonian fluids reduced risk of aspiration the consistency index (κ) of formed bigels from 1.457
by giving the neuromuscular system a longer reflex to 5.147 Pasn (40% collagen in hydrogel phase) and
response time to close the epiglottis (Meng et al., 2005; from 1.200 to 7.039 Pasn (60% collagen in hydrogel
Nakauma et al., 2011; Nishinari et al., 2019). phase). The same tendency was observed in other

Ó 2022 Institute of Food, Science and Technology (IFSTTF). International Journal of Food Science and Technology 2023
13652621, 2023, 1, Downloaded from https://ifst.onlinelibrary.wiley.com/doi/10.1111/ijfs.16181 by Kaunas University Of, Wiley Online Library on [16/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
150 Bigel based dysphagia-oriented products V. Eisinaitė et al.

authors study whereas an increase in viscosity of the collagen concentration; thus stronger network forma-
bigels has been observed after oil content was tion. This indicates that both gelling agents affect the
increased from 20% to 40% (Cui et al., 2022). It was increase of phases consistency andhave an impact on
also previously reported that compared to hydrogel, the system stability, despite the fact that have different
the presence of oleogel could impart better rheological structuring mechanisms. Carnauba wax formed
properties for bigels (Shakeel et al., 2019). As pre- platelet-like crystals, which in the presence of van der
dicted, apparent viscosity values at 10 s−1 and 400 s−1 Waals interactions cause immobilisation of the liquid
changed in the same way as apparent viscosity at oil in the three-dimensional structure. Denser network
50 s−1; the highest viscosity values (32.700 and formation reported in the samples with the higher
2.290 mPa*s) obtained in the bigels with the highest oleogelator concentrations (Pan et al., 2021), as well as
added collagen concentration (36%) (Table 3). in our studies. Meanwhile, collagen form hydrogel
It is believed that viscoelastic parameters provided through self-assembly of collagen fibrils. We assume
sample behaviour closer way to physiological condi- that absence of the “self-standing" bigel structure and
tions because measurements performed without more specifically bigel’s ability to flow after some force
destroying the sample (Payne et al., 2011). Complex applied related with the collagen gel dominance.
viscosity at 50 rad/s is associated to the stability and In general, higher elasticity and higher complex vis-
sensory consistency (sliminess in the mouth) of the cosity as well as lower tan δ values are desired and
analysed food (Richardson et al., 1989; Farahmandfar potentially relevant for the swallowing process (Choi
et al., 2017), while elastic modulus (G’) associated to & Yoo, 2009; He et al., 2016) and have been suggested
the bolus formation (Jo et al., 2018). As seen, complex as a rheological criterion for the safe swallow (Jo
viscosity and elastic modulus (G’) increased with et al., 2018).
increasing oleogel fraction while tan δ decreased As could be seen from the Tables 3 and 4 all rheo-
(Table 3). Furthermore, formulations with the higher logical parameters increased after 14 days of storage.
amount of oleogel represent structured gel-like beha- This also related with protein transformation during
viour (G’ > G" and tanδ <1). However, the G’ and storage time. Such phenomenon is desirable to a cer-
G" were frequency-dependent, which indicated a weak tain level whereas it is much more important to avoid
nature of the obtained gel (Fig. 2). It could be a decrease in rheological parameters during storage as
assumed that increase in elastic behaviour (higher G’) very low viscosity (fluid-like consistency) could be
induced by increase in carnauba wax as well as unsuitable for the dysphagia diet.

Figure 2 Elastic modulus (closed symbols), viscous modulus (open symbols) as a function of frequency of the bigels with (a) 40% of collagen
in the hydrogel phase and (b) at 60% of collagen in the hydrogel phase at oleogel/hydrogel ratio (●) – 40:60, (▲) – 50:50; (■) – 60:40 (after
preparation).

International Journal of Food Science and Technology 2023 Ó 2022 Institute of Food, Science and Technology (IFSTTF).
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Bigel based dysphagia-oriented products V. Eisinaitė et al. 151

Higher frequency dependence was observed in sam- One more important advantage of the prepared bigels
ples with the lower oleogel fraction as well as collagen is high added concentration of the protein collagen (16–
concentration (40% in the hydrogel phase). As seen, 36%). Higher amount of the protein is cruicial in the diet
both values (G’ and G") shift to higher values with the of the elderly with dysphagia as it helps to prevent malnu-
increase in collogen concentration in hydrogel phase, trion developing. It also worth mentioning that carried
indicating an enhanced mechanical strength. In bigel out study is the first step in the dysphagia-oriented bigel
formulations the network backbone composed from analysis. Extensional analysis in consumer acceptance,
the carnauba wax (oil structuring) and collagen (water matrix suitability for encapsulation and in vitro digestion
structuring) thus lack of those components resulted should be done in future studies.
weaker gel formation. That was also confirmed by the
lower elastic modulus (G’) values (Fig. 2).
Acknowledgment
This project has received funding from European
Textural properties
Social Fund (project No 09.3.3-LMT-K-712-23-0050)
Texture analysis was performed in order to mimic under grant agreement with the Research Council of
behaviour of the sample during chewing process; firm- Lithuania (LMTLT).
ness and cohesiveness were chosen as the main param-
eters. Firmness related to the energy, required to make
food bolus ready for the swallowing (Xing Author contributions
et al., 2022), while cohesiveness shows the ability to Viktorija Eisinaite: Formal analysis (equal); investigation
maintain internal structure against deformation (Nishi- (equal); methodology (equal); writing – original draft
nari et al., 2019). Significantly higher firmness and (equal). Ina Jasutiene: Methodology (equal). Rimante
cohesiveness values were obtained in the samples with Vinauskiene: Resources (equal). Daiva Leskauskaitë:
the higher collagen concentration (Table 2), confirming Supervision (equal); writing – review and editing (equal).
our previous hypothesis about collagen domination in
the bigel structure formation. Furthermore, there was
no relationship between carnauba wax concentration Conflict of interest
(Table 1) and firmness values (Table 2). We declare that we do not have any commercial or
Higher cohesiveness values are desired as stronger associative interest that represents a conflict of interest
internal bonds prevent food bolus destabilisation (de- in connection with the work submitted.
composition into several parts) during swallowing pro-
cess (Xing et al., 2022) and ensure easy swallowing
without stick to the pharynx. Ethical approval
In the following, firmness and cohesiveness values Ethics approval was not required for this research.
increased during storage but only in the samples with
60% of collagen in the hydrogel phase and that was
also related with the structural changes of collagen. Peer review
Unlike cohesiveness, an increase in firmness is not The peer review history for this article is available at
desirable as in that case patient needs more energy for https://publons.com/publon/10.1111/ijfs.16181.
the food bolus formation. However, in our study sam-
ples even with higher firmness values easily slided off
the spoon with a very gentle flick applied. Data availability statement
The data that support the findings of this study are
Conclusions openly available in [repository name e.g. “figshare”] at
[https://doi.org/10.1111/ijfs.16181].
The present work develops a novel bigel-based product
with strong shear-thinning behaviour oriented to the dys-
phagia diet. Structural properties and visual appearance References
of the bigels were greatly affected by collagen concentra- Barros, R.F.D., Torres, F.R., Silva, P.H.F.D. et al. (2020). Lutein as
tion and oleogel/hydrogel ratio. Higher viscosity, vis- a functional ingredient in sheep milk yogurt: development, charac-
coelasticity and cohesiveness values were obtained in the terization and extraction recovery. Food Science and Technology,
samples with the highest collagen concentration. It should 40, 683–669.
be noted that all formulations considered as suitable for Chantrapornchai, W., Clydesdale, F.M. & Mcclements, D. (2001).
Influence of relative refractive index on optical properties of emul-
the easier swallowing. However, samples that contained sions. Food Research International, 34, 827–835.
60% of oleogel fraction were less sensually acceptable Chen, J. (2009). Food oral processing – a review. Food Hydrocol-
because of the higher fat and wax content. loids, 23, 1–25.

Ó 2022 Institute of Food, Science and Technology (IFSTTF). International Journal of Food Science and Technology 2023
13652621, 2023, 1, Downloaded from https://ifst.onlinelibrary.wiley.com/doi/10.1111/ijfs.16181 by Kaunas University Of, Wiley Online Library on [16/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
152 Bigel based dysphagia-oriented products V. Eisinaitė et al.

Choi, H.M. & Yoo, B. (2009). Steady and dynamic shear rheology Mandala, I.G., Savvas, T.P. & Kostaropoulos, A.E. (2004). Xanthan
of sweet potato starch–xanthan gum mixtures. Food Chemistry, and locust bean gum influence on the rheology and structure of a
116, 638–643. white model-sauce. Journal of Food Engineering, 64, 335–342.
Choppe, E., Puaud, F., Nicolai, T. & Benyahia, L. (2010). Rheology Martı́n-Illana, A., Notario-Pérez, F., Cazorla-Luna, R. et al. (2022).
of xanthan solutions as a function of temperature, concentration Bigels as drug delivery systems: from their components to their
and ionic strength. Carbohydrate Polymers, 82, 1228–1235. applications. Drug Discovery Today, 27, 1008–1026.
Clave, P. & Shaker, R. (2015). Dysphagia: current reality and scope Martins, A.J., Silva, P., Maciel, F. et al. (2019). Hybrid gels: influ-
of the problem. Nature Reviews Gastroenterology & Hepatology, ence of oleogel/hydrogel ratio on rheological and textural proper-
12, 259–270. ties. Food Research International, 116, 1298–1305.
Conley, S.M., Stuck, M.W. & Naash, M.I. (2012). Structural and Meng, Y., Rao, M.A. & Datta, K. (2005). Computer simulation of
functional relationships between photoreceptor tetraspanins and the pharyngeal bolus transport of Newtonian and non-Newtonian
other superfamily members. Cellular and Molecular Life Sciences, fluids. Food and Bioproducts Processing, 83, 297–305.
69, 1035–1047. Moschakis, T., Panagiotopoulou, E. & Katsanidis, E. (2016). Sun-
Cui, H., Tang, C., Wu, S. et al. (2022). Fabrication of chitosan- flower oil organogels and organogel-in-water emulsions (part I):
cinnamaldehyde-glycerol monolaurate bigels with dual gelling microstructure and mechanical properties. LWT - Food Science and
effects and application as cream analogs. Food Chemistry, 384, Technology, 73, 1–2.
132589. Nakauma, M., Ishihara, S., Funami, T. & Nishinari, K. (2011).
Cutler, A.N., Morris, E.R. & Taylor, L.J. (1983). Oral perception of Swallowing profiles of food polysaccharide solutions with different
of viscosity in fluid foods and model systems. Journal of Texture flow behaviors. Food Hydrocolloids, 25, 1165–1173.
Studies, 14, 377–395. National Dysphagia Diet Task Force (2002). Dysphagia diet task,
de Stefano, A., Di Giovanni, P., Kulamarva, G. et al. (2020). and AD association. In: National Dysphagia Diet: Standardiza-
Oropharyngeal dysphagia in elderly population suffering from mild tion for Optimal Care. Chicago, IL: American Dietetic Associa-
cognitive impairment and mild dementia: understanding the link. tion.
American Journal of Otolaryngology, 41, 102501. All necesarry information about dysphagia diet and all requirements
Dewar, R.J. & Joyce, M.J. (2006). Time-dependent rheology of for the dysphagia patients (Textural property considerations of foods
starch thickeners and the clinical implications for dysphagia ther- for dysphagia; Practice applications of the National Dysphagia Diet;
apy. Dysphagia, 21, 264–269. National Dysphagia diets; Food preparation for dysphagia diets in
Dinkgreve, M., Paredes, J., Denn, M.M. & Bonn, D. (2016). On dif- patient care facilities; Hydration and the use of commercial thick-
ferent ways of measuring “the” yield stress. Journal of Non- eners; Discussions for consideration: developing standards for thick-
Newtonian Fluid Mechanics, 238, 233–241. ened liquids and dietary textures used in dysphagia management;
East, L., Nettles, K., Vansant, A. & Daniels, S.K. (2014). Evaluation Doctor notification of National Dysphagia Diet; Resources and tools
of oropharyngeal dysphagia with the Videofluoroscopic swallowing for implementing a dysphagia diet).
study. Journal of Radiology Nursing, 33, 9–13. Nishinari, K., Turcanu, M. & Nakauma, M.Y. (2019). Role of fluid
Farahmandfar, R., Asnaashari, M., Salahi, M.R. & Rad, T.K. cohesiveness in safe swallowing. npj Science of Food, 3, 5.
(2017). Effects of basil seed gum, cress seed gum and quince seed Nowson, C. & O’Connell, S. (2015). Protein requirements and rec-
gum on the physical, textural and rheological properties of ommendations for older people: a review. Nutrients, 7, 6874–6899.
whipped cream. International Journal of Biological Macromolecules, Pan, J., Tang, L., Dong, Q., Li, Y. & Zhang, H. (2021). Effect of
98, 820–828. oleogelation on physical properties and oxidative stability of
Fasolin, L.H., Martins, A.J., Cerqueira, M.A. & Vicente, A.A. camellia oil-based oleogels and oleogel emulsions. Food Research
(2021). Modulating process parameters to change physical proper- International, 140, 110057.
ties of bigels for food applications. Food Structure, 28, 100173. Payne, C., Methven, L., Fairfield, C. & Bell, A. (2011). Consistently
This pubication was very informative and used in order to better inconsistent: commercially available starch-based dysphagia prod-
understand bigel structure formation and properties as well as it ucts. Dysphagia, 26, 27–33.
application in food products. Richardson, R.K., Morris, E.R., Ross-Murphy, S.B., Taylor, L.J. &
Germain, I., Dufresne, T. & Gray-Donald, K.A. (2006). Novel dys- Dea, I.C.M. (1989). Characterization of the perceived texture of
phagia diet improves the nutrient intake of institutionalized elders. thickened systems by dynamic viscosity measurements. Food
Journal of the American Dietetic Association, 106, 1614–1623. Hydrocolloids, 3, 175–191.
Hadde, E.K., Mossel, B., Chen, J. & Prakash, S. (2021). The safety Shakeel, A., Farooq, U., Alejandro, D.G., Marangoni, G. & Lupi,
and efficacy of xanthan gum-based thickeners and their effect in F.R. (2021). Bigels and multi-component organogels: an overview
modifying bolus rheology in the therapeutic medical management from rheological perspective. Food Hydrocolloids, 111, 106190.
of dysphagia. Food Hydrocolloids for Health, 1, 100038. Shakeel, A., Farooq, U., Iqbal, T., Yasin, S., Lupi, F.R. & Gabriele,
He, Q., Hort, J. & Wolf, B. (2016). Predicting sensory perceptions of D. (2019). Key characteristics and modelling of bigels systems: a
thickened solutions based on rheological analysis. Food Hydrocol- review. Materials Science and Engineering:C, 97, 932–953.
loids, 61, 221–232. Singh, V.K., Banerjee, I., Agarwal, T., Pramanik, K., Bhattacharya,
Huang, T., Tu, Z.C., Shangguan, X. et al. (2019). Fish gelatin modi- M.K. & Pal, K. (2014). Guar gum and sesame oil based novel
fications: a comprehensive review. Trends in Food Science and bigels for controlled drug delivery. Colloids and Surfaces B: Bioint-
Technology, 86, 260–269. erfaces, 123, 582–592.
Ibrahim, M.M., Hafez, S.A. & Mahdy, M. (2013). Organogels, Taguchi, K., Wakabayashi, H., Fujimoto, M. et al. (2022). Associa-
hydrogels and bigels as transdermal delivery systems for diltiazem tion between malnutrition severity and swallowing function in con-
HCL. Asian Journal of Pharmaceutical Sciences, 8, 46–54. valescent rehabilitation wards: a multi-center cohort study in
Jo, W., Bak, J.H. & Yoo, B. (2018). Rheological characterizations of malnourished patients with Sarcopenic dysphagia. The Journal of
concentrated binary gum mixtures with xanthan gum and galac- Nutrition, Health & Aging, 26, 469–476.
tomannans. International Journal of Biological Macromolecules, Vieira, J.M., Andrade, C.C.P., Santos, T.P. et al. (2021). Flaxseed
114, 263–269. gum-biopolymers interactions driving rheological behaviour of
Lupi, F.R., Shakeel, A., Greco, V., Oliviero Rossi, C., Baldino, N. oropharyngeal dysphagia-oriented products. Food Hydrocolloids,
& Gabriele, D. (2016). A rheological and microstructural charac- 111, 106257.
terisation of bigels for cosmetic and pharmaceutical uses. Materials These three publications contained a lot of information about dys-
Science and Engineering C, 69, 358–365. phagia-oriented food products. There are a lot of explanations about

International Journal of Food Science and Technology 2023 Ó 2022 Institute of Food, Science and Technology (IFSTTF).
13652621, 2023, 1, Downloaded from https://ifst.onlinelibrary.wiley.com/doi/10.1111/ijfs.16181 by Kaunas University Of, Wiley Online Library on [16/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Bigel based dysphagia-oriented products V. Eisinaitė et al. 153

such products structure formation and final rheological and textural gia management: Carboxymethylated curdlan, konjac glucomannan
properties. and their mixtures compared to xanthan gum. Food Hydrocolloids,
Vieira, J.M., Oliveira, D.B., Maffezzolli, G.P., de Mello, J.D.B., 110, 106198.
Vicente, A.A. & Cunha, R.L. (2020). Rheology and soft tribology Wood, G.N. (1968). Centric occlusion, centric relation, and the
of thickened dispersions aiming the development of oropharyngeal mandibular posture. The Journal of Prosthetic Dentistry, 20, 292–306.
dysphagia-oriented products. Current Research in Food Science, 3, Xing, X., Chitrakar, B., Hati, S. et al. (2022). Development of black
19–29. fungus-based 3D printed foods as dysphagia diet: effect of gums
These three publications contained a lot of information about dys- incorporation. Food Hydrocolloids, 123, 107173.
phagia-oriented food products. There are a lot of explanations about Zargaraan, A., Rastmanesh, R., Fadavi, G., Zayeri, F. & Moham-
such products structure formation and final rheological and textural madifar, M.A. (2013). Rheological aspects of dysphagia-oriented
properties. food products: a mini review. Food Science and Human Wellness,
Wakhet, S., Singh, V.K., Sahoo, S. et al. (2015). Characterization of 2, 173–178.
gelatin–agar based phase separated hydrogel, emulgel and bigel. These three publications contained a lot of information about dys-
Journal of Materials Science: Materials in Medicine, 26, 118. phagia-oriented food products. There are a lot of explanations about
Wei, Y., Guo, Y., Li, R., Ma, A. & Zhang, H. (2021). Rheological such products structure formation and final rheological and textural
characterization of polysaccharide thickeners oriented for dyspha- properties.

Ó 2022 Institute of Food, Science and Technology (IFSTTF). International Journal of Food Science and Technology 2023

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