Evaluation of the physical changes of different soluble fibres produced during an in vitro digestion

Journal of Functional Foods 62 (2019) 103518

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Evaluation of the physical changes of different soluble fibres produced during an in vitro digestion

T

Natalia Vera C.a, Laura Lagunab, Liliana Zurac, Luis Puentea, Loreto A. Muñozc,

⁎

a

Universidad de Chile, Departamento de Ciencias de los Alimentos y Tecnología Química, Santos Dumont 964, Independencia, Santiago, Chile Institute of Agrochemistry and Food Technology (IATA), C/Catedrático Agustín Escardino Benlloch, 7, 46980 Paterna, Spain c Universidad Central de Chile, Escuela de Ingeniería, 8330601 Santiago, Chile b

ARTICLE INFO

ABSTRACT

Keywords: Soluble fibre In vitro digestion Chia mucilage Xanthan gum Guar gum Pectin

Some dietary fibres, especially soluble, due to their ability to modify the physical properties of digestive content, are associated with positive physiological effects. In this study, the effect of digestion on apparent viscosity and fragmentation/aggregation degree of different soluble fibres (guar gum, xanthan gum, pectin, and chia seed mucilage) were evaluated during in vitro digestion. All fibres showed pseudoplastic behaviour independent of the concentration and digestion stage, but xanthan gum and mucilage retained more viscosity compared with the other fibres. Particle size during digestion showed that pectin and guar gum had different degree of fragmentation at the intestinal level, while xanthan gum exhibited aggregation at the gastric stage and the chia mucilage remained unchanged during the digestion. The ability of xanthan gum and mucilage to conserve their structure and viscosity during digestion could help to modulate the digestive process, delay gastric emptying and enhance the functionality of foods.

1. Introduction In recent years, the consumption of dietary fibre, both soluble and insoluble, has received great attention from consumers, researchers and the food industry, but the majority is from health institutions around the world due, mainly, to the health benefits associated with its consumption (EFSA, 2010; FAO/WHO 2003). The high dietary fibre intake has been widely associated with improving health outcomes in many major non-communicable diseases (European Heart Network, 2011; Marlett, McBurney, & Slavin, 2002). In particular, the beneficial effects have been associated with lowering blood lipid levels (Anderson et al., 2009), reduction in risk of cardiovascular disease (Theuwissen & Mensink, 2008), improved glycaemia control (Goff, Repin, Fabek, El Khoury, & Gidley, 2018), an increase in satiety (Clark & Slavin, 2013), the production of short-chain fatty acids by fermentation in the large intestine with anti-carcinogenic properties (Lattimer & Haub, 2010), among others. According to many authors, the beneficial properties of soluble fibres have been strongly related with their significant role in human physiological function, among the beneficial effects are: the increase in the total transit time by delaying gastric emptying, which affect fullness and satiety; the effect on microbiota improving the production of shortchain fatty acids which can improve the lipid homeostasis; decrease the ⁎

glucose absorption which helps for prevention of diabetes type 2; cholesterol lowering effects, between others (Brownlee, 2011; Chawla & Patil, 2010; Mackie, Bajka, & Rigby, 2016; Perry & Ying, 2016; Rana, Kumar Bachheti, Chand, & Barman, 2011; Tan et al., 2016). For instance, soluble fibres such as gums, chia mucilage and pectin can increase the viscosity in the gastrointestinal tract due the capacity to form swollen hydrated networks (Brownlee, 2011; Fabek, Messerschmidt, Brulport, & Goff, 2014). These kinds of fibres, when hydrated, produce viscous, gel-forming solutions which can decrease the rate of gastric emptying, reduce the rate of macronutrient absorption, reduce postprandial glucose responses, and can have a positive influence on certain blood lipids (Tan et al., 2016; Vuksan, Rogovik, Jovanovski, & Jenkins, 2009). The physiological effects of dietary fibre depend mainly on their physicochemical properties, such as water holding capacity, binding and bulking ability (that effect the viscosity), and fermentability; these properties also impact textural and rheological properties of food products (Mudgil & Barak, 2013). Thus, the goal of the present work was first to study comparatively the physicochemical properties of four different soluble fibres with different structures: xanthan gum with a β-(1-4)-D-glucopyranose glucan backbone with side chains of –(3-1)-α-D-mannopyranose-(2-1)β-D-glucuronic acid-(4-1)-β-D-mannopyranose on alternating residues (Sworn, 2009); pectin with a complex structure with an α-(1-4)-D-

Corresponding author. E-mail address: [email protected] (L.A. Muñoz).

https://doi.org/10.1016/j.jff.2019.103518 Received 8 May 2019; Received in revised form 13 August 2019; Accepted 13 August 2019 1756-4646/ © 2019 Elsevier Ltd. All rights reserved.

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galacturonic acid polysaccharide backbone (Wüstenberg, 2014); guar gum which is a linear chain of (1-4)-β-D-mannopyranosyl units with (16)-α-D-galactopyranosyl residues (Mudgil, Barak, & Khatkar, 2014) and chia seed mucilage, which has been tentatively identified as a polymer of β-D-xylopyranosyl, α-D-glucopyranosyl, and 4-Ο-methyl-α-D-glucopyranosyl uronic acid (Lin, Daniel, & Whistler, 1994). The second goal was to investigate the rheological properties and the degree of fragmentation/aggregation of each fibre at different concentrations during in vitro digestion.

Instruments Inc. The supernatant was discarded, and the swollen sample was weighed. Finally, the WAbC was determined by placing the swollen sample in four tubes and adding different quantities of water; 1.5 ml and 0.5 ml greater than the original weight; 1.5 ml and 0.5 ml less than the original weight. Water absorbed was calculated following Eq. (1) and expressed as g water absorbed per g of sample:

WAb C = sf

where sf is the swollen samples weight, and s0 is initial samples weight. 2.3.1.2. Water and oil holding capacity (WHC/OHC). Both, water and oil holding capacities were determined according to the methods described by Timilsena, Adhikari, Kasapis, and Adhikari (2016). Samples of 0.25 g were weighed in test tubes, after 10 ml of distilled water or, separately in another sample set, sunflower oil (density: 0.92 g/ml, Natura Oil, Chile) was added. The samples were stirred for 2 h and subsequently kept overnight at room temperature (20 °C) for complete hydration. The samples were centrifuged at 1600g for 10 min and the supernatant was discarded. The swollen sample was weighed and WHC/OHC were expressed as g of water or oil held per g of sample.

2. Materials and methods 2.1. Materials The high methoxyl (HM) pectin from apple (93854), xanthan gum from Xanthomonas (G1253) and guar gum (G4129) were purchased from Sigma-Aldrich. Crude chia mucilage was obtained from chia seeds by using the method proposed by Muñoz, Cobos, Diaz, and Aguilera (2012). The chia seeds with no previous treatment were provided by Benexia (Functional Products Trending S.A. Santiago, Chile). α-Amylase from human saliva (1000–3000 U/mg of solid A0521), pepsin from porcine gastric mucosa (2000 U/mg of solid P6887), bovine bile extract, pancreatin (800 U/ml from solid, based on lipase activity) were purchased from Sigma-Aldrich, St. Louis MO, USA. Reagents, sodium dihydrogen phosphate (99%), disodium hydrogen phosphate (99%), sodium chloride (99.8%), potassium chloride (99%), calcium chloride (99%), potassium dihydrogen phosphate (99.5%), sodium bicarbonate (99.5%), magnesium chloride hexahydrate (99%) and ammonium carbonate (99.5%) were purchased from Merck©.

2.3.1.3. Solubility. The solubility was measured by modifying the method described by Cortés-Camargo et al. (2018). 10 ml of each DSF in triplicate were prepared at 1% w/w and were kept in constant agitation in a water bath for 30 min at 30, 37, 60, 70, and 80 °C. The suspensions were centrifuged at 2000g for 15 min, 3 ml of the supernatant was dried in an air convection oven (BOV-V70F, Biobase) at 125 °C, overnight. The solubility was calculated using Eq. (2):

%Solubility =

2.2. Dispersions preparation

2.3.1. Water adsorption capacity (WAdC) The water adsorption capacity was determined using the method described by Segura-Campos, Ciau-Solís, Rosado-Rubio, Chel-Guerrero, and Betancur-Ancona (2014). Samples of 0.1 g, in triplicate, were introduced into a desiccator with an equilibrium microenvironment at 98% relative humidity provided by potassium sulphate solution saturated. The samples were left until they reached a constant weight (72 h). The water adsorption capacity was expressed as g of water per g of sample.

=k

where η is the shear viscosity (Pa s), k is the consistency index (Pa s ), is the shear rate (s−1) and n is the fluid behaviour index (dimensionless) 2.5. Particle size analysis The particle size distribution before and at each stages of the in vitro digestion of each hydrocolloid was determined in six-fold, by laser light scattering with a Malvern Mastersizer 2000 (Malvern Instruments) in a range of 0.01 to 1000 µm using water at 20 °C as solvent and analysed by the software Mastersizer 2000 version 5.60. The refractive indices used were 1.33 to the water and 1.333; 1.333; 1.334 and 1.331 to mucilage, xanthan gum, guar gum and pectin, respectively. The results were quantified and expressed as relative volume of particles in size bands presented as size distribution curves.

Table 1 Concentrations used for the preparation of each hydrocolloid dispersions (%w/ w).

Pectin Guar gum Xanthan gum Mucilage from chia seed

Concentration (% w/w) High

1 1 0.3 0.3

2 2 0.5 0.5

4 3 1 1

(3)

n 1 n

2.3.1.1. Water absorption capacity (WAbC). The water absorption capacity was determined according to the AACC method 88-04 (AACC, 1989). Samples of 0.1 g, in triplicate, were weighed, and distilled water was added until saturation (approximately 5 ml), with constant agitation. Then, the samples were centrifuged at 2000g for 10 min in a centrifuge model DSC-200 SD, Digisystems Laboratory

Medium

(2)

Rheological measurements were carried out using a steady shear test with a Rotational Rheometer, RheolabQC (Anton Paar GmbH, Austria-Europe), with a double gap concentric cylinder and a Peltier temperature plate, set at 37 °C, simulating body temperature. The apparent viscosity of each hydrocolloid dispersion was determined without digestion, in triplicate, as a control, before and after each digestion stage, by applying an increasing shear rate from 0.1 to 100 s−1 (Alpizar-Reyes et al., 2018). The flow behaviour index (n) and consistency index (k) values were obtained by fitting to the Power Law model (Eq. (3)):

2.3. Functional properties of the selected hydrocolloids

Low

Wf 10 100 Wi 3

2.4. Rheological measurements

The dietary soluble fibre (DSF) dispersions were prepared at low, medium, and high concentrations (% w/w) in distilled water at room temperature (20 °C), with constant agitation for 2 h to reach a complete hydration, in triplicate (Table 1).

Hydrocolloids

(1)

s0

2.6. Static in vitro digestion Suspensions of low, medium, and high concentrations of each DSF were subjected to in vitro human digestion, simulating oral, gastric, and 2

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intestinal conditions by using the standardised static in vitro digestion protocol, suggested by international consensus within the framework of Infogest COST Action (Minekus et al., 2014). The simulated digestive fluids were prepared according to Minekus et al. (2014), included simulated salivary fluid (SSF), simulated gastric fluid (SGF), and simulated intestinal fluid (SIF). In the oral phase, 5 ml of each sample was mixed with 3.5 ml of SSF, 0.5 ml of 1500 U/ml α-amylase fabricated in SSF solution, 25 µl 0.3 M CaCl2, and 975 µl of water to achieve a final ratio of 50:50 v/v. The oral bolus was incubated at 37 °C for 2 min in a thermostatic bath (NB-304, N-Biotek) with agitation. Subsequently, the oral bolus was mixed with 7.5 ml of SGF and 1.6 ml 2000 U/ml porcine pepsin prepared with SGF solution, 5 µl 0.3 M CaCl2, 0.2 ml 1 M HCl (to achieve pH 3.0), and 0.695 µl of water reaching 50:50 v/v. The mix was then incubated at 37 °C for 2 h in a thermostatic bath with agitation. Finally, the gastric chime was mixed with 11 ml of SIF, 5.0 ml of 800 U/ ml pancreatin solution prepared in SIF solution, 40 µl 0.3 M CaCl2, 0.15 ml 1 M NaOH (to achieve pH 7), and 1.31 ml of water to obtain a final ratio of 50:50 v/v. The mix was incubated at 37 °C for 2 h in a thermostatic bath with agitation. Samples were taken at each stage of digestion and rapidly cooled to 4 °C for further analysis during the same day.

(2015) where freeze-dried chia seed mucilage was analysed, while Segura-Campos et al. (2014) reported lower values, probably because of the differences in extraction methodologies (Segura-Campos et al., 2014; Velázquez-Gutiérrez et al., 2015). The values of WAdC of xanthan gum and guar gum agree with those previously determined by Torres, Moreira, Chenlo, and Vázquez (2012). Thus, xanthan gum would spontaneously adsorb water when exposed to an atmosphere of constant relative humidity compared to the other hydrocolloids in this study (Segura-Campos et al., 2014). This behaviour can result from glucuronic acids and acetic acid esters present in its structure, which gives greater polarity and a higher water affinity (Torres et al., 2012). Opposed to this, the values obtained for guar gum agree with the results found by Torres et al. (2012). Guar gum is formed by mannose and galactose monomers without acid or ionic groups and the presence of hydroxyl groups allows water molecules to link by hydrogen bonds (Mudgil et al., 2014). Finally, the values of WAdC obtained for pectin (0.42 ± 0.01 g/g) are also like those previously reported by EinhornStoll, Benthin, Zimathies, Görke, and Drusch (2015). 3.1.2. Water absorption capacity (WAbC) Table 2 shows water absorption capacity of each dietary soluble fibre (DSF). Overall, the xanthan gum, guar gum, and chia seed mucilage show higher values of WAbC, compared with the HM pectin (p < 0.05). The low WAbC observed in the pectin could be due its linear structure and the behaviour in aqueous suspensions, where molecules are not stable but highly dependent on factors such as chemical structure, particle size, temperature and solvent properties (Lopes da Silva & Rao, 2006). The WAbC values obtained in this study for the isolated chia seed mucilage (50.12 ± 0.54 g/g) were higher than obtained by SeguraCampos et al. (2014) and significantly higher than fibre-rich fractions of chia seed obtained by solvent extraction and pressing, respectively (Capitani, Spotorno, Nolasco, & Tomás, 2012). With guar gum and xanthan gum, the values of WAbC were almost the double of those obtained by Sciarini, Maldonado, Ribotta, Perez, and Leon (2009), probably due to the different origin, degree of purity, particle size, solubilizing protocol and differences in the methodology. Functional properties of the hydrocolloids are associated with how they interact with water in relation to their structures. The differences observed between the DSF can be attributed to the branched structures of guar gum, xanthan, and chia seed mucilage, as the decisive factor to their variation of water absorption capacity compared with pectin (Li, Hou, & Chen, 2016).

2.7. Statistical analysis The data obtained was expressed as the mean ± standard deviation, each calculated by triplicate for all the analysis except for particle size distribution that was calculated by six-fold. The comparisons among means were performed using one-way ANOVA. The effect of solubility, type of fibre, temperature, and percentage were calculated by multi-factor ANOVA. Least significant differences were calculated by the Tukey test and the significance at p < 0.05 was determined. All these tests were performed using the software, Statgraphics Centurion XV.I. 3. Results and discussion 3.1. Functional properties of the selected hydrocolloids 3.1.1. Water adsorption capacity (WAdC) The hygroscopic nature of the hydrocolloids is an important factor; predicting moisture exchange between food materials and surroundings is relevant, as it influences the physicochemical properties; water molecules progressively and reversibly combine with the dry hydrocolloid by different via chemisorption, physical adsorption, and multilayer condensation (Vishwakarma, Shivhare, & Nanda, 2011). Table 2 shows the functional properties of the pectin, xanthan gum, guar gum and chia seed mucilage. The WAdC between groups showed significant differences (p < 0.05), where the xanthan gum registered the higher value (0.65 g/g of sample), followed by guar gum, pectin and chia seed mucilage (0.48, 0.42 and 0.41 g/g of sample, respectively). Similar results for chia seed mucilage were obtained by Velázquez-Gutiérrez et al.

3.1.3. Water and oil holding capacity (WHC/OHC) In general, DSF are strongly hydrophilic, the water is attracted to the hydrophilic sites on the fibre itself or is held within void spaces in the molecular structure. Its WHC depends not only on functional groups of the polysaccharide fractions which are hydrophilic but also, on protein fraction present in the gums (Mudgil & Barak, 2013; Sarkar et al., 2018). Water and oil holding capacities of each DSF is shown in Table 2. Guar and xanthan gum exhibit higher WHC with 39.84 ± 0.18 and 39.65 ± 0.1 g of water/g of sample respectively, while the chia seed mucilage shows a WHC of 33.62 ± 0.6 g water/g sample. These results are comparable with those obtained for chia seed mucilage by Lazaro, Puente, Zúñiga, and Muñoz (2018); higher to those reported by Timilsena et al. (2016) for chia seed mucilage and guar gum; also higher to those described for xanthan gum by Sarkar et al. (2018). A high WHC is normally associated with an increase in volume which also produce an increase in the intestinal content when the DSF is ingested which can prevent the constipation (Rana et al., 2011). The low WHC observed to HM pectin (0.31 ± 0.08 g/g) compared with the values reported by Gannasin, Ramakrishnan, Adzahan, and Muhammad (2012) to apple pectin, could be due to the different origin, degree of methylation, and previous treatment. In this study, the chia seed mucilage exhibits the highest OHC

Table 2 Functional properties of the selected hydrocolloids. Sample

WAdC* (g water/g sample)

Pectin Xanthan gum Guar gum Mucilage

0.42 0.65 0.48 0.41

± ± ± ±

0.01a 0.02c 0.01b 0.01a

WAbC* (g water/g sample)

WHC* (g water/g sample)

OHC* (g oil/g sample)

1.51 ± 0.29a 50.25 ± 0.42b 50.19 ± 0.46b 50.12 ± 0.54b

0.31 ± 0.08a 39.65 ± 0.1c 39.84 ± 0.18c 33.62 ± 0.6b

2.51 1.76 1.73 9.06

± ± ± ±

0.06b 0.08a 0.05a 0.36c

WAdC: Water adsorption capacity; WAbC: Water absorption capacity. WHC/ OHC: Water/oil holding capacity. Different letters indicate significant differences (p < 0.05) according to the Tukey’s test. 3

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seed mucilage, xanthan gum, and pectin, indicate the negative charge which confers higher solubility compared to neutral polysaccharides like guar gum (Salarbashi & Tafaghodi, 2018). The solubility of the DSFs was studied as isolated ingredients at specific temperatures, but when the DSF is added into the food matrix more considerations should be included, such as the thermic process to which the food is subjected and the interaction between other components. 3.2. Rheological measurements The steady flow behaviour, consistency, and flow index behaviour of the DSF at low, medium, and high concentration, before and during the in vitro digestion can be seen in Fig. 2 and Table 3, respectively. The low, medium and high concentrations to xanthan gum and mucilage from chia seeds were selected on the basis of similar monosaccharide composition and functional groups such as hydroxyl, aliphatic, carboxylic and aromatic ester (Muñoz, 2012); while the concentrations for guar gum and pectin were selected on the basis of differences in apparent viscosity measured at 20 °C. All dispersions exhibited similar flow behaviour at all concentrations and digestion stages, showing a non-Newtonian behaviour (Fig. 2), with decreasing viscosity with increasing shear rate, also known as pseudoplasticity or shear-thinning behaviour (Barnes, Hutton, & Walters, 1989). As expected, the viscosity of DSFs without digestion (Fig. 2a, b, and c) at low, medium, and high concentrations shows a directly proportional relationship with the concentration (Gómez-Díaz & Navaza, 2003). In the samples without digestion k increases as the concentration increases, as expected in a pseudoplastic fluid. Among the different fibres used, guar gum had the highest viscosity at all concentrations, followed by xanthan gum and the chia seed mucilage, which showed no significant differences between them, with pectin exhibiting the lowest viscosity of all. In agreement with Mudgil and Barak (2013) which relate the ability of DSFs to absorb water and form gelatinous masses with the viscosity and gel-forming capacity, this viscous behaviour could be associated with the water absorption capacity which increase the stool bulk and prevents the constipation. During the digestion at different stages, overall the pseudoplasticity or shear-thinning behaviour depends on the concentration. The apparent viscosity of all DSFs decreases from the oral to the intestinal stage, caused by the increase in volume produced by the incorporation of digestive fluids, in agreement with the observed by Tamargo, Cueva, Laguna, Moreno-Arribas, and Muñoz (2018) and Fabek et al. (2014). In addition, the simulated conditions of the digestive tract can also affect the rheological properties of each DSF, in agreement with those previously described by Repin, Cui, and Goff (2018) there are specific conditions of the human gastrointestinal tract, including ionic strength, presence of cations, enzymes, pH, and temperature that can affect the conformation and behaviour in solution of the polysaccharide molecule and the interaction between them. At an oral level, the same trend was found, as happened in the samples before digestion (the most viscous fibres were, guar gum > xanthan gum > chia seed mucilage > pectin). However, an important reduction in viscosity was observed in guar gum at the oral stage compared with the sample without digestion. This behaviour is confirmed with the strong decrease in k value during the digestion, even at high concentration (Table 3). According to previous studies, this reduction in viscosity could be explained as decreased irreversible structural breakdown, because of less molecular alignment in the dispersion (Marcotte, Taherian Hoshahili, & Ramaswamy, 2001; Zhang, Zhou, & Hui, 2005). As guar gum is non-ionic it is not affected by ionic strength, but pH changes along the gastrointestinal process affect the viscosity. This behaviour is also confirmed by the drastic decrease of k from oral to gastric stages comparing the lower with the higher concentration, in agreement to previously observed studies by Fabek et al. (2014). Otherwise, the flow behaviour of xanthan gum from the oral to

Fig. 1. Hydrocolloids solubility (%) as a function of temperature.

(9.06 ± 0.36 g oil/g sample) slightly lower than that reported by Segura-Campos et al. (2014), possibly because of the differences in the extraction process. This is followed by pectin, with a value of 2.51 ± 0.06 g oil/g sample, similar to previous results by RodríguezGutiérrez, Rubio-Senent, Lama-Muñoz, García, and Fernández-Bolaños (2014). In this study, guar gum and xanthan gum show the lowest OHC, however higher than reported by Sarkar et al. (2018). According to Cortés-Camargo et al. (2018), these low values of OHC obtained for pectin, guar and xanthan gum can be attributed to the absence of nonpolar chains on the proteins within the structure, and its conformational features that allow them to bind to hydrocarbon units of oil. 3.1.4. Solubility Solubility has a strong effect on functionality, the relative stability of the ordered and disordered structures determine if the polysaccharide will be totally, partially or not dissolve (Guillon & Champ, 2000). Fig. 1 shows the solubility of pectin, xanthan gum, guar gum, and chia seed mucilage in water at 30, 37, 60, 70 and 80 °C. For xanthan gum and chia seed mucilage, the solubility depends significantly on the temperature (p < 0.05), while pectin and guar gum show no significant dependence. Xanthan gum and chia seed mucilage increased solubility firstly with the increasing temperature from 30 to 37 °C; the xanthan gum continues increasing the solubility to reach the maximum at 70 °C, while mucilage decrease its solubility from 37 °C to 60 to later increase from 60 to 70 °C, however the magnitude of this increment varied among the samples with changes 0.68% and 23.28% respectively. The highest solubility of xanthan gum and chia seed mucilage was reached at 70 °C. Similar results have been described by Capitani, Ixtaina, Nolasco, and Tomas (2013) and can explain that the H bonds between the polysaccharide molecules are broken down by increasing temperature, allowing the OH groups easier access to the structure, increasing the solubility (Sharifian-Nejad & Shekarchizadeh, 2019). When the temperature increases over 70 °C the solubility of xanthan gum and chia seed mucilage decreases, this behaviour has been previously explained as the gelling effect associated with some polysaccharides at such a temperature. These results agree with those previously given by Sciarini et al. (2009) for xanthan gum, and Capitani et al. (2013) for chia seed mucilage. Alternatively, pectin showed the greater solubility, reaching the maximum at 30 °C (97.7 ± 0.5%) and the minimum (72.79 ± 0.5%) at 37 °C, then the solubility increases until reaching 97.0 ± 0.2% at 60 °C to decrease again at temperature up to 60 °C. This behaviour can be explained with the high esterification degree (≥50%) and its negative charge close to neutral pH, revealing a polyelectrolyte nature (Razavi et al., 2009). Finally, the maximum solubility of guar gum was achieved at 30 °C (68.71 ± 0.5%), in agreement to Pollard et al. (2007). This can occur because of high galactose substitution (DS Gal:0.5), decreasing the hydroxyl groups available to the intra- and inter-chain hydrogen bond formation, providing steric interruption to chain associations, thus improving solubility (Kontogiorgos, 2019). High amounts of uronic acids in the DSFs composition, as with chia 4

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N. Vera C., et al. (b)

Control: Low Concentration

10

10

10

0,1

0,01

Aparent viscosity (Pa.s)

100

1

1

0,1

0,01

0,001 1

10

0,1

0,01

10

1

100

(e)

Oral Level: Low Concentration

(f)

Oral Level: Medium Concentration

100

10

10

10

0,1

0,01

Aparent viscosity (Pa.s)

100

1

1

0,1

0,01

0,001 100

0,001 1

10

Shear rate (1/s)

100

1

(h)

Gastric Level: Low Concentration

Aparent viscosity (Pa.s)

10

1

0,1

0,01

(i)

10

100

10

10

1

0,1

0,01

1

100

1

0,1

0,01

0,001 10

100

1

(k)

Intestinal Level: Low Concentration

(l)

Intestinal Level: Medium Concentration

Intestinal Level: High Concentration

10

10

10

0,1

1

0,1

0,01

0,01

0,001

0,001 10

Aparent viscosity (Pa.s)

100

Aparent viscosity (Pa.s)

100

1

1

0,1

0,01

0,001 1

100

100

Shear rate (1/s)

100

1

10

Shear rate (1/s)

Shear rate (1/s)

(j)

Gastric Level: High Concentration

100

0,001

0,001

100

Shear rate (1/s)

Gastric Level: Medium Concentration

100

1

10

Shear rate (1/s)

Aparent viscosity (Pa.s)

(g)

1

0,1

0,01

0,001 10

100

Oral Level: High Concentration

100

1

10

Shear rate (1/s)

Shear rate (1/s)

Aparent viscosity (Pa.s)

Aparent viscosity (Pa.s)

(d)

1

0,001 1

100

Shear rate (1/s)

Aparent viscosity (Pa.s)

Control: High Concentration

100

0,001

Aparent viscosity (Pa.s)

(c)

Control: Medium Concentration

100

Aparent viscosity (Pa.s)

Aparent viscosity (Pa.s)

(a)

10

100

1

10

Shear rate (1/s)

Shear rate (1/s)

100

Shear rate (1/s)

Fig. 2. Apparent viscosity during in vitro digestion of different fibres (▲ pectin, ● guar gum, ◊ xanthan gum, and ■ mucilage), on the top file the control at three different concentrations (increasing from left to right).

gastric stage was less affected by the pH changes and ionic environment (Table 3), but at intestinal level a decrease of viscosity was observed. This decrease in viscosity of xanthan gum has been explained as the effect of salt ions in solution, protecting the ionic charges on the

polymer chain from each other (Wyatt & Liberatore, 2009). Also, this decrease can be because of the increase in volume produced by the incorporation of digestive fluids, as described above. In addition, as has been previously described, xanthan gum in

Table 3 Power of Law parameters. Hydrocolloids

Concentration

Control (before digestion)

After digestion Oral

n Pectin Guar gum Xanthan gum Mucilage

1 2 4 1 2 3 0.3 0.5 1 0.3 0.5 1

0.656 0.785 0.937 0.318 0.171 0.116 0.319 0.219 0.081 0.306 0.309 0.339

a a a b c c b bc d b b b

k

R2

n

0.025 c 0.032 b 0.078 b 6.632 a 54.798 a 215.998 a 0.844 b 2.283 b 9.479 b 0.592 bc 0.960 b 5.173 b

0.9202 0.6863 0.9846 0.9967 0.9177 0.9681 0.9994 0.9998 0.9076 0.9978 0.9989 0.9302

0.236 0.293 0.312 0.466 0.291 0.350 0.399 0.376 0.208 0.224 0.363 0.429

Gastric

b a b a a ab a a c b a a

k

R2

n

0.381 b 0.463 b 1.145 c 0.888 a 10.925 a 4.546 a 0.318 b 0.391 b 2.441 b 0.308 b 0.235 b 0.230 c

0.9876 0.9775 0.9565 0.9969 0.9953 0.9952 0.9976 0.9983 0.9506 0.9970 0.9963 0.9991

0.315 0.387 0.301 0.636 0.531 0.394 0.249 0.379 0.314 0.201 0.320 0.379

Intestinal k

b a a a a a bc a a c a a

0.149 0.130 0.227 0.163 0.647 2.845 0.254 0.226 0.507 0.320 0.096 0.180

c b c bc a a ab b b a b c

R2

n

0.9910 0.9756 0.9721 0.9736 0.9868 0.9920 0.9880 0.9710 0.9980 0.9903 0.9839 0.9801

0.249 0.163 0.334 0.244 0.672 0.556 0.333 0.351 0.355 0.178 0.337 0.278

R2

k a b b a a a a b b a b b

0.255 0.179 0.183 0.261 0.072 0.289 0.074 0.185 0.270 0.069 0.130 0.160

a a a a a a b a a b a a

0.9923 0.9754 0.9931 0.9844 0.9823 0.9923 0.9063 0.9888 0.9960 0.9406 0.9733 0.9836

k corresponds to the consistency index (Pa sn) and n is the fluid behaviour index (dimensionless). Different letters signify difference across hydrocolloids for one concentration (low, medium or high). 5

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chia seed mucilage (more viscosity retention), and HM pectin (increase of viscosity) would improve the functionality of foods and help management of the digestive process (Chesson, 2006). It is important to mention that static in vitro digestion is useful when you want to evaluate an isolated food ingredient, but has some limitations when a food matrix is evaluated. For example, it is not possible to determine the pH changes induced by the fibre intake, transport kinetics or bioaccesibility of nutrients along the gastrointestinal tract. Future research should complement these results with a dynamic digestion that includes, among others, all the stages of digestion (mouth, stomach, small intestine, and ascending, transverse and descending colon) and microbiota.

solution exhibits two different conformation states depending on the ionic content of the solvent: an ordered, helical conformation and disordered conformation as a broken or imperfect helix. In aqueous solutions, the xanthan molecule is disordered and greatly extended, because of electrostatic repulsion between charges on the side chain, presenting chains as relatively stiff, but retaining some flexibility. This explains its lower viscosity compared to guar gum (Wyatt & Liberatore, 2009). The behaviour observed in chia seed mucilage was like xanthan gum, where the apparent viscosity decreases along the digestion, but this DSF has the ability to retain more viscosity compared with the other DSFs. This capacity of viscosity retention can suggest a better physiological response increasing the viscosity luminal contents, delaying the gastric emptying, slowdown the rate of diffusion of substrates and digestive enzymes and decreasing the post-prandial glycemic response, among others (Mudgil & Barak, 2013; Repin et al., 2018). At an oral level, HM pectin shows the lower viscosity at all the concentrations, but at gastric and intestinal stages the viscosity increases, even with the dilution effect caused by the addition of digestive fluids. In addition, comparing the HM pectin control with the oral stage, an increase in apparent viscosity was observed. Similar behaviour was seen in orange pectin by Logan, Wright, and Goff (2015) where the HM pectin had a significantly higher apparent viscosity after the intestinal stage. This increase in viscosity can be explained, as the HM pectin has a high degree of esterification and thus low overall charge, it can react with the pH changes between the gastric and intestinal stages. Otherwise, the decrease of pH reduces the electrostatic repulsion between the chains, which promotes hydrogen bonding and leads to aggregation (Logan et al., 2015). According to the same author, this behaviour has been related with the ability of this DSF to increase the feeling of satiety. All the fibres studied provided viscosity in the gastrointestinal tract. As it can be observed in Table 4, the effect of each fibre, the concentration and the digestion phase, and its interaction has a significant effect in the rheological parameters. This shows how the fibre viscosity along the gastrointestinal tract depend on its concentration type and digestion stage, According to Chesson (2006), many of the presumed and known beneficial effects of soluble fibre appear to be a direct consequence of the ability to increase or retain viscosity in the digestive tract. These potential beneficial effects are related to slower digestion of carbohydrates and lipids, the ability to adsorb bile acids which helps to reduce plasma cholesterol, the maintenance of gastrointestinal health, attenuating blood glucose and finally increasing satiety (Rana et al., 2011). Many of the mechanisms suggested to these effects are related with the viscosity and the ability of the DSFs to bind endogenous compounds (enzymes or bile acids) and help the decrease of absorption rate attributable to the entanglement with the intestinal mucus (Mackie et al., 2016). Therefore, considering these statement, xanthan gum and

3.3. Particle size analysis Fig. 3 shows the particle size distribution during the in vitro digestion at the three concentrations of each DSF, which were only dispersed in distilled water and no other components, and during the three stages of the digestion. During human digestion, foods are disintegrated or fragmented, reducing the particle size, first in the mouth followed by the stomach, because of chemical reactions and physical forces such as peristaltic movements (Kong & Singh, 2008, 2009). Particle size of dietary fibre also changes during digestion because of chewing, grinding in the stomach, bacterial degradation and the action of enzymes and digestive fluids (Guillon & Champ, 2000). In this study, the measurement of particle size distribution is an estimate of fragmentation and/or aggregation of each DSF produced during the different stages of in vitro digestion. The results shown in Fig. 3, show significant changes in particle size distribution in guar gum and xanthan gum, slight changes in pectin (p < 0.05). While in chia seed mucilage the particle size and pattern distribution between the three concentrations, and the three stages of digestion remained unchanged. For the three concentrations of pectin, between the oral and gastric stage, no changes in the distribution were observed (Fig. 3), but during the intestinal stage the distribution changed from monomodal to bimodal, even more so at medium and high concentrations. This behaviour can be explained, as HM pectin has high esterification, and thus low overall charge, consequently the pH is less effective than if the sample were a LM pectin (Logan et al., 2015). Also, this behaviour relates with the increase in apparent viscosity observed at the same stages. For guar gum samples no significant change in particle size distribution was observed, compared with the control during oral and gastric stages, but at the intestinal stage a different distribution pattern emerges. At the intestinal level, guar gum shows a partial fragmentation decreasing the particle size. Xanthan gum samples, during the oral stage, show no significant changes in particle size distribution, but during the gastric stage the distribution pattern change shows increasing size of particles. The changes in the bimodal size distribution observed in xanthan gum could be attributed to its partial disintegration, a result of the breakdown of this DSF structure with prolonged exposure to acidic conditions releasing particles with different sizes after digestion. The changes in particle size distribution could be attributed to changes in pH and ionic strength produced by enzymes, the gastric, and intestinal juices.

Table 4 Interactions among variables. Parameter Fibre Concentration Digestion phase Interactions Fibre*Concentration Fibre*Digestion Concentration*Digestion Fibre*Concentration*Digestion

n

k

F value p-value F value p-value F value p-value

33.46 0.001 4.15 0.02 4.77 0.004

1884.03 0.001 984.99 < 0.0001 1867.24 0.001

F value p-value F value p-value F value p-value F value p-value

11.63 0.001 59.78 0.001 5.04 0.001 6.92 0.001

801.55 0.001 1594.63 0.001 908.31 0.001 777.29 0.001

4. Conclusions The knowledge of the physicochemical properties of the DSF is a useful tool to predict the potential functionality and structuring properties of these fibres. The results suggest that the physical changes and differences in apparent viscosity observed among the DSFs at the different concentrations during digestion, were primarily determined by the fibre type, concentration, and their physicochemical properties; not by changes in pH, presence of ions, or enzymes. Subsequently, in the following stages of digestion these differences could be determined by the dilution effect induced by the digestive juices, changes in pH and 6

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LOW CONCENTRATION

MEDIUM CONCENTRATION (b)

10 9 8 7 6

Control Oral Gastric Intestinal

5 4 3 2 1 0 10

100

1000

Oral Gastric Intestinal

0,01

0,1

1

10

Particle Size (µm)

(d)

(e)

Guar gum

10 9 8 7 6 5 4 3 2 1 0

Control

Volume (%)

Gastric Intestinal

0,1

1

10

100

Volume (%)

Oral

0,01

1000

Gastric Intestinal

100

Volume (%)

Volume (%)

Oral

10

Oral Gastric Intestinal

0,1

1

10

Gastric Intestinal

Volume (%)

Volume (%)

Oral

(i)

Gastric Intestinal

0,1

1

10

100

100

Oral Gastric Intestinal

0,1

1

100

1000

Control Oral Gastric Intestinal

(l) Oral Gastric Intestinal

10

10

Xanthan gum

0,01

Control

1

1000

Control

10 9 8 7 6 5 4 3 2 1 0

1000

Mucilage

0,1

100

0,1

1

10

100

1000

Particle Size (µm)

10 9 8 7 6 5 4 3 2 1 0

1000

10

Particle Size (µm)

Oral

0,01 10

1

Guar gum

0,01

Control

(k) Control

1

0,1

10 9 8 7 6 5 4 3 2 1 0

1000

Xanthan gum

0,01

1000

Mucilage

0,1

Intestinal

Particle Size (µm)

10 9 8 7 6 5 4 3 2 1 0 0,01

100

10 9 8 7 6 5 4 3 2 1 0

Particle Size (µm)

(j)

Gastric

0,01

Control

0,01

Control

1

Oral

(f)

Guar gum

(h)

Xanthan gum

0,1

Control

Particle Size (µm)

10 9 8 7 6 5 4 3 2 1 0 0,01

1000

10 9 8 7 6 5 4 3 2 1 0

Particle Size (µm)

10 9 8 7 6 5 4 3 2 1 0

Particle Size (µm)

(g)

100

Pectin

Particle Size (µm)

Volume (%)

1

Control

Volume (%)

0,1

10 9 8 7 6 5 4 3 2 1 0

100

Particle Size (µm)

1000

Volume (%)

0,01

HIGH CONCENTRATION (c)

Pectin

Volume (%)

Pectin

Volume (%)

Volume (%)

(a)

Mucilage

10 9 8 7 6 5 4 3 2 1 0

Control Oral Gastric Intestinal

0,01

0,1

1

10

100

1000

Particle Size (µm)

Particle Size (µm)

Fig. 3. Particle size distribution.

the ability of these fibres to increase, maintain or decrease their solubility. Because xanthan gum and chia seed mucilage retained viscosity more than the other soluble fibres, and HM pectin can increase the viscosity along the gastrointestinal tract, it could be suggested that including these types of soluble fibres can be used as a strategy to modulate the digestive process delaying the gastric emptying and enhance the functionality of foods. Further studies should include the interactions of these DSFs into the food matrix and potential synergistic effects between them.

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5. Ethics statement The authors declare did not include any human subjects and animal experiments. Declaration of Competing Interest The authors of the manuscript declare have no conflict of interest. Acknowledgements This work was carried out with the financial support of FONDECYT Project 11150307 from the Chilean National Commission for Science and Technological Research (CONICYT), Chile and CYTED Program, Project 119RT0567, Spain. The authors would also like to thank Dr Phillip John Bentley for his English revision of the paper. References AACC (1989). Approved methods of the American Association of Cereal Chemists. St. Paul, Minnesota, USA: American Association of Cereal Chemists, Inc.

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