Controlling the rheological properties of wheat starch gels using Lepidium perfoliatum seed gum in steady and dynamic shear

Journal Pre-proofs Controlling the rheological properties of wheat starch gels using Lepidium perfoliatum seed gum in steady and dynamic shear A.R. Yousefi, K. Ako PII: DOI: Reference:

S0141-8130(19)36441-4 https://doi.org/10.1016/j.ijbiomac.2019.09.153 BIOMAC 13430

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International Journal of Biological Macromolecules

Received Date: Revised Date: Accepted Date:

13 August 2019 24 August 2019 22 September 2019

Please cite this article as: A.R. Yousefi, K. Ako, Controlling the rheological properties of wheat starch gels using Lepidium perfoliatum seed gum in steady and dynamic shear, International Journal of Biological Macromolecules (2019), doi: https://doi.org/10.1016/j.ijbiomac.2019.09.153

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Controlling the rheological properties of wheat starch gels using Lepidium perfoliatum seed gum in steady and dynamic shear Yousefi1*, A.R. and Ako2*, K. 1

Department of Chemical Engineering, Faculty of Engineering, University of Bonab, Bonab, Iran 2

UGA, LRP, F-38000 Grenoble, France; CNRS, LRP, F-38000 Grenoble, France

*

Corresponding authors e-mail: [email protected], [email protected] 1

Address: East Azerbaijan, Velayat highway, University of Bonab, Bonab, Iran

2

Address: 363, rue de la Chimie, 38400 Saint-Martin-d'Hères, Université Grenoble Alpes, Grenoble, France 1

Tel.: +98 4137745000; 1Fax: +98 4137740800; 1P.O. Box: 55517-61167 2

Tel.: +33 456520194; 2Fax: +33 456520197; 2P.O. Box: 38041

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Abstract In the present work, the influence of Lepidium perfoliatum seed gum (LPSG) addition in varied concentrations (0%, 0.25%, 0.5%, 0.75% and 1%, w/w) on dynamic and steady shear rheological properties of wheat starch dispersion (4%, /w) was examined. Comparison of the values of dynamic (G′, G″, τy, τf, tan δ), shear-dependent (ηa,50, η0, 𝜂∞ , τ, m) and time-dependent (ηa,3s, k, η0, 𝜂∞ ) rheological parameters of the WS-LPSG mixtures with WS alone, indicated that the viscoelastic and flow properties of the mixtures were greatly affected by the addition of LPSG. According to the standard method provided by the National Dysphagia Diet (NDD), the WS and WS-LPSG gels were placed in the category of nectar-like (WS), honey-like (WS-0.25%LPSG, WS-0.5%LPSG and WS-0.75%LPSG) and spoon-thick (WS-1%LPSG) viscosity. In the simulated oral condition (SOC), the presence of saliva caused the increase of k value (10-81%), whilst decreased the values of η0 (43-95%) and 𝜂∞ (68-96%). As the concentration of LPSG increased, less decrease in value of ηa,3s in the SOC was observed. The results of present study demonstrated the feasibility of manipulating the viscosity of the WS gels by addition of LPSG to be suitable for the individuals with varying degrees of swallowing difficulty. Keywords: Starch; Lepidium perfoliatum seed gum; Rheology; Saliva; Dysphagia

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1. Introduction Disorder in swallowing of foods and/or liquid, dysphagia, influence the quality of eating or drinking [1]. It is reported that this disorder may take place as a result of neurological disease, some types of cancer such as head and neck and tongue, or stroke and neuromuscular disorders [2, 3]. For individuals with dysphagia (from the newborns to the elderly), inadequate managing of the disorder results in a reduction in their life quality [4]. Bolus flow properties like viscosity affect its transition behaviour during swallowing. The transition time will be slower if the viscosity of bolus is increased enough, giving the patient more time to prepare for the onset of pharyngeal swallow and engage airway protective mechanism [5]. On the other hands, if bolus is very thick (with high viscosity) it may cause some physiological problems (e.g. the risk of being aspirated for oropharynx) as well as some sensory defects (e.g. low palatability) [6, 7]. The National Dysphagia Diet (NDD) has provided a standard in associated with the dietary texture modification for management of dysphagia. For this reason, based on the bolus viscosity, NDD has proposed the following terms for liquid or liquid-like foods (a) thin (1-50 mPa.s), (b) nectarlike (51-350 mPa.s), (c) honey-like (351-1750 mPa.s) and (d) spoon-thick (> 1750 mPa.s). It is stated that only bolus with a viscosity higher than 350 mPa.s could be easily swallowed by the people with dysphagia [8]. Many of thickeners used in food systems are carbohydrate polymers which can bind water and make a thick solution. Starch composed of amylose and amylopectin are of those carbohydratebased thickeners that has widely been used in human diets (e.g. gel-like foods) [9, 10]. Many researchers have used native and modified starch as thickeners to prepare some suitable foods/beverages for patients with dysphagia [11-15]. Despite of some good properties of this thickener, it is found that starch is sensitive to salivary α-amylase and in the presence of saliva it 3

breaks down into simple carbohydrates and water, reducing the force required for extrusion or stirring [16, 17]. Moreover, it has been stated that the viscosity of some starch-based foods could be lessened by more than half when mixed with saliva for 1-10 s. In this case, gum-based thickeners could efficiently be used in starch-based foods, because they are not affected by αamylase. Furthermore, addition of such food gums that are also known as dietary fiber may result in a lower glycemic index for starch during gastrointestinal digestion [18, 19]. Consequently, application of such gum thickeners in starch-based foods is useful for the patients with dysphagia who also suffer from diabetes. Xanthan gum [20-23], guar gum [24-26] and locust bean gum [27, 28] are of the main food gum thickeners that have recently been applied in various foods for management of dysphagia. Lepidium perfoliatum seeds have been used in Iranian traditional medical prescription from a long time ago. The gum extracted from this seeds has a good alternative potential to some commercial food gums as thickening and stabilizing agent in food systems [29]. Lepidium perfoliatum seed gum (LPSG) in some food systems could attract large amount of water, make high viscosity, modify texture and stabilize product consistency [30, 31]. Many commercial food thickeners used for managing dysphagia are instant thickeners and prepared by the agglomeration methods, but they are useful for thickening beverages or providing very weak gels for the patient with dysphagia. To provide much stronger gels like some gel-foods such as custards and porridges, we can suppose that mixture of food thickeners-fully gelatinized starches are more suitable. To the best of our knowledge, this is the first study done to show the potential of LPSG as an emerging food thickener for management of dysphagia. For this reason, a simple food system/bolus containing wheat starch (WS) and water was selected and LPSG was added to this

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system at different concentrations (0%, 0.25%, 0.5%, 0.75% and 1%, w/w). The objective of this research can be stated as follows: (a) to find out the effect of the addition of LPSG on rheological properties (dynamic and steady shear behaviour) of native wheat starch gels, (b) to understand the impact of corresponding shear rate for mastication (50 s-1) and saliva addition on the final viscosity of obtained bolus (digesta) at the end of mastication and exactly before swallowing in a simulated oral condition (SOC), and (c) to know the influence of LPSG concentration and saliva addition on rheological (time independent and/or time-dependent) parameters of the bolus, the WS-LPSG mixtures, which is supposed to be used for management of dysphagia.

2. Materials and methods Lepidium perfoliatum seeds were purchased locally from a medical plant supplier in Tabriz, Iran. The seeds were cleaned manually to remove any kind of impurity such as dust, dirt, stones, chaff, immature and broken seeds. The used wheat starch in this research with 20 ± 0.2% amylase content and the molecular weight (Mw) of 1.95 × 107 kDa was supplied from Merck Company (Darmstadt, Germany). The other chemical materials applied had analytical grade of purity.

2.1. Preparation of LPSG The gum extraction procedure was carried out based on the method described by Koocheki, Taherian, Razavi and Bostan [32]. For this reason the cleaned seeds were drenched in distilled water (48 °C) and by regarding the ratio of 30:1. The pH also was checked and controlled regularly (by adding 0.1 M HCl and/or NaOH) to be 8. The slurry of water-seed was manually stirred during 1.5 h of the extraction process. Eventually, the seeds were taken from the water and the mucilages were collected and dried in a laboratory oven (50 °C, 36 h) and then milled 5

and sieved by a sifter with mesh size of 100. The chemical compositions of the obtained gum powder, on averagely (d.b.), were 88.23% total sugar, 4.6% proteins, 6.0% moisture, 0.18% ash and 0.0% fat [33].

2.2. Preparation of the WS-LPSG gels For this reason, the WS dispersions (4%, w/w) were made in distilled water (21.5 °C) and then various amounts of LPSG (0%, 0.25%, 0.5%, 0.75% and 1%, w/w) were added to the dispersions (300 rpm, 21.5 °C). For complete gelatinization of WS, the mixed dispersions were heated at 100 °C for 20 min [34], and then cooled to room temperature for 30 min prior to start any experiment.

2.3. Saliva collection Saliva was collected from a healthy individual donor (aged 35 years) according to the method described by Yousefi, Razavi and Norouzy [9]. Briefly, Tree times rinsing were asked from the donor to remove any debris from its mouth cavity. Then, a sterile piece of nylon sheet (~5×5 cm2) was given to the donor for chewing and stimulating the secretion of saliva and then the saliva was obtained through spitting in a falcon tube and then kept freshly in room temperature before use in any test.

2.4. Rheological measurements 2.4.1. Oscillatory shear Small-deformation oscillatory measurements were carried out by a DHR3 Controlled stress/strain rheometer (TA Instruments, New Castle, England) equipped with a parallel-plate

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geometry (60 mm diameter and 500 µm gap). A sufficient amount of prepared WS-LPSG gels were taken and placed on Peltier plate at 25 °C and the surplus material was removed with a spatula. Afterwards, all gel samples were allowed to rest at this temperature for 20 s before any measurements. When the gap was adjusted, two pieces of transparent plastic caps were put on the upper surface of the probe to prevent any evaporation during measurements.

2.4.1.1. Strain sweep test The dynamic measurements were implemented in the linear viscoelastic region (LVE). To acquire a strain corresponding to LVE region, amplitude sweep tests (0.01-200%) in controlled shear stress and controlled shear rate modes were performed at 25 °C and 1 Hz. Accordingly, a 0.3% strain was exactly within the LVE range for all gels and it was applied for all dynamic measurements.

2.4.1.2. Frequency sweep test Frequency sweep test was carried out by subjecting the gel samples to oscillatory measurements at a frequency range of 0.01-10 Hz and a constant strain of 0.3% at LVE region. Then, the mechanical spectra obtained were analyzed by values of G′ and G″ (Pa) as a function of frequency at 25 °C. TA Instruments Trios (version 4.0.1.29891) data analysis software was used to determine the dynamic rheological parameters including the storage modulus (G′), loss modulus (G″) and loss tangent (tan δ), and to analyze the rheological results at 25 °C.

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2.4.2. Steady shear The steady shear flow properties of the WS-LPSG gels were investigated at 25 °C, and also under the simulated oral condition (SOC) (at 37 °C and in the presence of 1.5 ml saliva). According to the viscosity of the dispersions, a concentric bob and cup geometry (cup inner diameter: 30 mm; bob outer diameter: 28 mm; gap: 2 mm) was applied for viscosity measurements using the same rheometer. Viscous flow behaviour was obtained at straincontrolled mode with shear rates within the range 0.1-100 s-1, so that 0.1 s-1 refers to the shear rate applied for gentle manipulation and 100 s-1 is corresponding to the shear rate applied for the muscular and health swallow in clinical practice [20]. Moreover, the WS-LPSG samples were sheared at 50 s-1, the shear rate supposed to apply in mouth cavity [8], in the SOC and the shear stress and the viscosity were obtained in the presence and absence of saliva as a function of shearing time.

2.5. Rheological modeling 2.5.1. Frequency dependent models It has been stated that the frequency dependency of G′ and G″ values shows a power-law relation (Eqs. 1 and 2) for a physical gel [35]: 𝐺 ′ = 𝑘 ′ × 𝜔𝑛

′

𝐺 ′′ = 𝑘 ′′ × 𝜔𝑛

(1) ′′

(2)

where, G′ is the storage modulus, G′' is the loss modulus, ω is the oscillation frequency, and k′ and k′' are model constants. The constant n′ and n′' are the slope in a log–log plot of G′ and G′' versus ω.

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2.5.2. Shear-dependent models Five common viscous flow models consisting power-law, Herschel-Bulkley, Bingham, Sisko and Cross were fitted to the experimental shear stress-shear rate or viscosity-shear rate data to find out the shear dependent characteristics of the gel samples. The fitting results showed that the Cross model (Eq. 3) was the best one to exhibit the shear dependence behaviour of the gel samples [36]:

𝜂 = 𝜂∞ +

𝜂0 −𝜂∞ 1+(𝜏𝛾)̇𝑚

(3)

where, 𝜂0 (Pa.s) is the viscosity when shear rate is close to zero, 𝜂∞ (Pa.s) is the viscosity when shear rate is infinity, m (dimensionless) is the flow behaviour index and τ (sm) is the consistency index. This model is capable to predict the flow properties over broad range of shear rate, because both terms of limiting low shear rate and high shear rate viscosities are included in this model.

2.5.3. Time-dependent models For this reason, first-order stress decay model, second-order structural kinetic model and Weltman model were applied as the most common time-dependent models for description of the thixotropic behaviour of the gel samples (bolus) during digestion in the SOC. Among the models, second-order structural kinetic (SOSK) model (Eq. 4) was found to be the best one, which predicted the closest results with those of experimental data [8]:

(𝜂−𝜂∞ ) 1−𝑛

[𝜂

0 −𝜂∞

]

= (𝑛 − 1)𝑘𝑡 + 1

(4)

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where, 𝜂0 (Pa.s) is the initial viscosity (at t = 0) and 𝜂∞ (Pa.s) is the final viscosity (t→∞); k (s-1) is the rate constant of the thixotropic breakdown; n (dimensionless) is the breakdown order.

2.6. Statistical analysis For statistical analysis, one-way analysis of variance (ANOVA) at a constant level of confidence (α = 0.05) was done using SPSS 17 (SPSS Inc., Chicago, IL, USA) and the rheological data means were compared using Duncan test. The experimental data were acquired in triplicate and presented as the mean ± standard deviation. In addition, the appropriateness of model fitting was identified using the statistical parameter of the determination coefficient (R2).

3. Results and discussion 3.1. Dynamic flow behaviour of the WS-LPSG gels 3.1.1. Strain sweep measurements Linear viscoelastic region in which G′ and G″ are constant and nonlinear domain in which G′ and G″ start to decrease, for all WS-LPSG gels were obtained by applying oscillation strain ramp (0.01-200%). As it can be found from Fig. 1, G′ started to diminish sharply in a particular strain at the end of linear region. In fact, this strain is associated with deformability of the WS-LPSG gels. Strain sweep results have been used to discern the structural strength of gels (week or strong) and it has been stated the LVE region is much broader for a stronger gel compared to a weak gel [37]. It has been reported that the strain value at the LVE region for most of soft solid foods are in the range of 0.1-2%, whilst for colloidal and natural biopolymer gels this value is commonly lower than 0.1 and higher than 1, respectively [38].

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From the results of strain sweep measurements, the values of loss-tangent (tan δLVE), yield stress (τy) at the limit of the LVE range and flow-point stress (τf) with corresponding modulus (Gf: G′ = G″), for all WS-LPSG gels were determined (Table 1). It can be observed that tan δLVE (the ratio of the G″LVE to G′LVE), which indicates the physical behaviour of a system, decreased from 0.69 to 0.21 with increasing the amount of incorporation of LPSG into the WS gels. All the values of tan δLVE for the WS and WS-LPSG gels were within the range 0.20-0.69, implying predominantly elastic behaviour of the samples at LVE domain. Based on the strain sweep test results, we can obtain the maximum deformation that a gel system can resist without structural breakdown. For this reason, the critical strain obtained, which shows the limit of LVE domain and can be considered as a criterion of structural strength and shape retention factor against the mechanical stresses [39]. The stress corresponding to this strain, τy (the non-linear region immediately begins after the mentioned stress), is considered to be the start point of the weakening of the gel strength [40]. The results revealed that the gel strength (defined as much resistant to the applied stress) was enhanced with increasing LPSG concentration. Yield stress is a useful rheological property of a food thickener which can be used to show its ability to keep food constituents in place [34]. As can be seen in Table 1, the values of yield stress at flow point (τf) were raised with increasing LPSG concentration, indicating more tendency to flow at lower concentrations of LPSG. Consequently, the WS and WS-1%LPSG samples were, respectively, less (τf = 0.70 Pa) and much (τf = 57.45 Pa) resistant gels to flow among the others. Hesarinejad, Koocheki and Razavi [41] observations proved that both the τy and τf values for Lepidium perfoliatum seed gum were increased with increasing concentration from 1.5 to 3%. For all WSLPSG gel samples in the LVE region, G′LVE was about 50-450% higher than G″LVE, implying the presence of a network structure or gel-like behaviour [42].

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3.1.2. Frequency sweep measurements The changes in storage modulus (G′) and loss modulus (G″) of the WS-LPSG gel samples as a function of frequency are shown in Fig. 2A,B. It is stated that different types of dispersion including dilute solution, concentrated solution, week gel and strong gel can be obtained based on the frequency sweep results [37]. The results observed from the mechanical spectra revealed that for all samples, except for WS, G′ was always higher than G″ without any crossover point in the range of frequency tested (0.01-10 Hz). Irrespective of LPSG concentration, as the frequency increased the magnitude of G′ and G″ were enhanced with a small dependency, demonstrating typical weak gel-like behaviour [43]. It implies that the WS-LPSG gels behave more like soft gels, so the deformations will not be completely elastic and recoverable. The same behaviour also has been reported for blends of tapioca starch-xanthan gum [44], and maize starch-guar gum [45]. It was found that the dependency of G' and G″ to the frequencies of 0.01-1 Hz were lesser than that in the range 1-10 Hz, indicating the behaviour of week gel properties for the WS-LPSG samples [46]. In fact, for week gels the rheological attributes are like those for the materials between solutions and real gels. As long as deformation is small, weak gels mechanically behave like real gels, while as deformation increases, the tree-dimensional networks undergo a progressive failure into smaller cluster and the behaviour becomes like that of weak gels [47]. Increase in LPSG concentration resulted in increase in both values of G' and G″. As the LPSG concentration was raised from 0% to 1%, at the frequency of 1 Hz, the G' and G″ modulus were steadily enhanced (P < 0.05) from 0.80 Pa to161.09 Pa, and from 0.82 Pa to 31.24 Pa, respectively (Fig. 2A,B). This observation as a result of increment in concentration may due to formation of increasingly complex structure at higher level of incorporation of LPSG. Similar results have been reported in case of the addition of guar gum and xanthan gum to colocasia

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starch [48], and also locust bean gum to the resistant corn starch [49]. Loss tangent (tan δ), defined as (G″/ G'), is of the most common dynamic rheological parameters used for description of viscoelastic behaviour, and the values of tan δ < 1 and tan δ > 1 are dedicated to the concepts of predominantly elastic and viscous behaviours, respectively. As presented in Fig. 2C, the tan δ value of the WS gel was enhanced sharply, while this value for the WS-LPSG gel samples, especially at higher concentration of LPSG, enhanced steadily throughout the frequency range tested. This result indicates less frequency dependence of the WS-LPSG mixtures compared to the WS gel. The values of tan δ for the WS-LPSG gel samples were within the range 0.17-0.49, showing an intermediate behaviour between a weak and a strong elastic gel. One the contrary, at frequency range of 1-10 Hz, the WS gel had the tan δ values greater than unity, which indicated the behaviour of weak gel. Similar observations have been reported on a tapioca starch-gum arabic mixture study [50], where there was a decreasing pattern of tan δ values with increasing concentration (0.6-1%), showing that the mixtures had a more solid-like behaviour than the control tapioca starch. The parameters calculated from the power-law equations (Eq. 1 and 2) for all gel samples are given in Table 2. The K′ and K′′ values of the WS-LPSG mixtures were much greater (P < 0.05) than those of the WS gel because of this fact that the addition of LPSG provides stronger gels. The values of n′ and n′′ = 0 are related to a true (covalent) gel, while for a physical gel n′ and n′′ values are > 0 [41]. When the n′ and n′′ values are low, the system exhibits the characteristic of an elastic gel, whereas for n′ and n′′ values close to 1, the system behaves like a viscous gel. Based on the fitting results obtained, the frequency dependency of G′ and G″ decreased with increasing LPSG concentration, indicating more elastic behaviour of the gels at higher concentration of LPSG (n′ = 0.121-0.187, n′′ = 0.154-0.277) than the WS gel (n′ = 0.353 and n′′ = 0.601). These findings for both parameters of power-law equations were in good

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agreements with those reported for the xanthan gum-rice starch [51], and flaxseed gum-maize starch mixtures [52].

3.2. Shear flow behaviour of the WS-LPSG gels Flow curves of the WS and all WS-LPSG gels (Fig. 3) showed the gels produced shear thinning behaviour, which was in agreement with the results obtained for many gel-like foods [8, 53]. Increase in shear rate from 1 s-1 to 20, 60 and 100 s-1, decreased the extent of apparent viscosity of the WS gel up to 72%, 86% and 89%, respectively. At the same increasing of shear rate, the reduction observed for the WS-0.25%LPSG and WS-1%LPSG gels was 88%, 94%, 96% and 90%, 95%, 96%, respectively. The apparent viscosity of the WS-LPSG mixtures was increased with the increasing of LPSG content. This might be attributed to the interaction between the LPSG and WS molecules during pasting. This trend was in good agreement with the behaviour observed for Lesquerella fendleri seed gum-maize starch [54] as well as flaxseed gum-maize starch [52] mixtures. The results attained from the rheological modeling demonstrated that the Cross model was precisely fitted to the experimental data (R2 = 0.999). The parameters of Cross model for all gels tested are tabulated in Table 3. With increasing the concentration of LPSG added to WS, the extents of m and τ parameters, respectively, were lowered (12-37%) and increased (20-7558%). As a result, the extent of this diminution and increment was more remarkable at higher concentration of LPSG (P < 0.05). In case of η0 and 𝜂∞ parameters, as expected both the viscosities were, respectively, increased to 162.658 Pa.s and 0.632 Pa.s, due to the increase in shear thinning behaviour as a result of raise in LPSG concentration (P < 0.05). In agreement with this result, Yadav, Yadav, Yadav and Dangi [48] found that as the concentration of guar gum and xanthan gum added to colocasia starch increases from 1 to 2%, the apparent

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viscosity and consistency coefficient of mixtures enhances. The results of Abbastabar, Azizi, Adnani and Abbasi [55] demonstrated that Cross model was fitted well to the rheological data, and with increasing concentration of quince seed gum from 0.1% to 0.70%, τ and m values were increased and decreased up to 750% and 32%, respectively. According to the apparent viscosities obtained at the shear rate of 50 s-1 (ηa,50) and the standard method provided by NDD, the WS and WS-LPSG gels were placed in the category of nectar-like (WS), honey-like (WS-0.25%LPSG, WS-0.5%LPSG and WS-0.75%LPSG) and spoon-thick (WS-1%LPSG) viscosity. Cho and Yoo [20] expressed that the viscosity of cold thickened beverages could be controlled by addition of xanthan-based gum food thickeners to be suitable for patient with dysphagia. In another research, Vilardell, Rofes, Arreola, Speyer and Clavé [21] found that both modified starch and xanthan gum food thickeners similarly improved safety of swallowing in chronic post-stroke oropharyngeal dysphagia patients. Heightening the ηa,50 of food bolus used for individuals with dysphagia using other gum-based food thickeners such as locust bean gum and carrageenan gum [3], and also guar gum and tara gum [26] have been reported. Review of the recent literatures show that at least three levels of viscosity including 51350 mPa.s (nectar-like), 351-1750 mPa.s (honey-like) and > 1750 mPa.s (spoon-thick) have been recommended for management of dysphagia [56]. It has been expressed that the nectar-like liquid is used for mild dysphagia, whilst the honey-like and spoon-thick liquids are useful for managing more severe forms of swallowing difficulties [3]. Accordingly, the results of present study reveal that the addition of 0.25-1% LPSG to WS (4%, w/w) leads to reach to the viscosity that it is appropriate for the individuals with more intense forms of dysphagia.

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3.3. Flow behaviour of the WS-LPSG gels in the SOC Typical experimental results attained from the time-dependent steady shear tests in the SOC for the WS-LPSG gels are shown in Fig. 4. As it can be seen, as shearing time increased the apparent viscosity for all gel samples diminished, exhibiting the characteristics of thixotropic materials. For instance, for the WS-0.5%LPSG gel, increment in shearing time from 1 s to 10, 100, 300 and 700 s, respectively, resulted in a 41%, 69%, 70% and 71% decrement in apparent viscosity. The second-order structural kinetic model predicted the data with the close approximate to the exponential data of shear stress-time for all sample tested (R2 = 0.986-0.998). The thixotropic breakdown rate constant (k) increased affected by the addition of LPSG to the WS gel, and WS-0.25%LPSG (0.119 s-1) and WS-0.5%LPSG (0.143 s-1) samples had greater amount than that of the others (P < 0.05). Moreover, as the concentration of LPSG was raised from 0% to 1%, both the η0 (from 0.007 to 0.389 Pa.s) and 𝜂∞ (from 0.003 to 0.093 Pa.s) values were significantly enhanced (P < 0.05). Dolz, Hernandez, Delegido, Alfaro and Munoz [57] demonstrated that the relative thixotropic behaviour of food emulsions containing modified starch were intensified in the presence of greater amounts of xanthan gum and locust bean gum. To investigate the impact of saliva on rheological behaviour of the WS and WS-LPSG gels, the flow curves of the WS, WS-0.25%LPSG and WS-0.75%LPSG gels were compared in the presence and absence of saliva conditions (Fig. 5). The results exhibited much pronounced reduction in apparent viscosity in the presence of saliva. For example, at the shearing times of 10, 100, 300 and 700 s, the extent of diminution of apparent viscosity as a result of saliva presence was within the range 95-96%, 88-91% and 47-68% for the WS, WS-0.25%LPSG and WS-0.75%LPSG samples, respectively. Yousefi and Razavi [8] findings demonstrated that the apparent viscosity of native and chemically modified wheat starch were pronouncedly lowered in

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the presence of saliva condition compared to the one without saliva. It was found that the impact of saliva presence on reduction of apparent viscosity was much attenuated as concentration of LPSG was enhanced. It has been stated that gum-based thickeners exhibit no significant reduction in viscosity in comparison with starch-based thickeners upon contact with human saliva during digestion in simulated oral conditions [21, 58]. More reduction in apparent viscosity for the WS gel and WS-LPSG gels with lower extent of LPSG can be explained by this fact that the hydrolysis of starch components is greater than that of mixtures with higher levels of LPSG, owing to more resistance of LPSG against salivary amylase [59]. Similar observations have been expressed for other food gums, particularly galactomannans, when they pass through the upper phase of digestion [60]. With comparison of the rheological parameters for the WS, WS-0.25%LPSG and WS-0.75%LPSG gel samples, it can be deduced that the presence of saliva significantly affected the rheological parameters of SOSK model (P < 0.05) (Fig. 6). As a result, it caused the increase of k value (10-81%), while decreased the values of η0 (43-95%) and 𝜂∞ (68-96%). In accordance with our results, the viscosity of starch thickened beverages drastically decreased in the presence of saliva, but its final viscosity (𝜂∞ ) remained still higher than that of water at room temperature [7]. Chen and Lolivret [61] determined the oral resistance time, defined as the time from the ingestion till the completion of swallowing, for a wide range of fluid foods. Based on their results and the ones obtained for the apparent viscosity of the WS-LPSG gels in the present work, the oral residence time of 3 s was selected for all gels. Accordingly, the values of apparent viscosity after 3 s shearing (ηa,3s) in the SOC were obtained, which are depicted in Fig. 7. It is evident that the extent of the ηa,3s in comparison with the ηa,50 has been drastically decreased (P < 0.05). These reductions were approximately 97%, 95%, 91%, 89% and 87% for the WS, WS-

17

0.25%LPSG, WS-0.5%LPSG, WS-0.75%LPSG and WS-1%LPSG gel samples, respectively. In the other words, in the SOC the viscosity of nectar-like, honey-like and even spoon-thick gels were altered to thin (for the WS and WS-0.25%LPSG gels) and nectar-like (for the WS0.5%LPSG, WS-0.75%LPSG and WS-1%LPSG gels) states. Higher structural breakdown and lower viscosity for starch custards compared to carboxymethylcellulose ones in the presence of saliva have been reported by Sanz and Luyten [62]. Hanson, Cox, Kaliviotis and Smith [7] findings proved that the addition of human saliva to a maize starch thickened bolus, reduced the viscosity to less than 1% of its original value.

4. Conclusions The present study dealt with investigating the influence of Lepidium perfoliatum seed gum (LPSG) addition upon flow properties of wheat starch (WS) gel used for management of dysphagia. Significant differences were found for dynamic rheological parameters (G′, G″, τy, τf, tan (δ)) and steady flow ones (ηa,50, ηa,3s, k, η0, 𝜂∞ , τ, m) affected by different concentrations (01%) of added LPSG (P < 0.05). Moreover, saliva had a pronounced impact on the flow behaviour of the WS-LPSG mixtures during their shearing in the simulated oral condition. The results showed that the WS-LPSG mixtures with incorporation of 0.25-0.75% and 1% were, respectively, good candidates for the patients with mild and severe dysphagia. Based on the observations of the present study it can be concluded that the addition of LPSG to WS enhances apparent viscosity and, most importantly, extremely reinforces the resistance of starch against high level of digestion (structural breakdown) by saliva, both of which are important for management of dysphagia.

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Figure captions Fig.1. Strain sweep dependence of storage modulus (G′) and loss modulus (G″) for (A) WS, WS0.25%LPSG and WS-0.5%LPSG; and (B) WS-0.75%LPSG and WS-1%LPSG gels, (f = 1 Hz, 25 °C). Fig. 2. Frequency dependence of (A) storage modulus (G′); (B) loss modulus (G″), and (C) loss tangent (tan δ) for the WS and WS-LPSG gels, (0.3% strain, 25 °C). Fig. 3. Shear-dependent flow curve of the WS and WS-LPSG gels at different concentrations (25 °C). Fig. 4. Time-dependent flow curve of the WS-LPSG gels at different concentrations in the simulated oral condition (SOC). Fig. 5. Influence of saliva addition on flow curves of the WS and WS-LPSG gels at different concentrations (37 °C, 50 s-1). Fig. 6. Rheological parameters of SOSK model for the WS and WS-LPSG gels at different concentrations (A) in the presence and (B) absence of saliva, (37 °C, 50 s-1). Fig. 7. Apparent viscosity of the WS and WS-LPSG gels at different concentrations at shear rate of 50 s-1 at 25 °C (ηa,50), and after 3 s shearing in the presence of saliva at 37 °C (ηa,3s).

22

Fig.1.

23

Fig. 2.

24

Fig. 3.

Fig. 4.

25

Fig. 5.

26

Fig. 6.

27

Fig. 7.

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Table 1. The rheological parameters related to the linear viscoelastic region (LVR) for the WS and WSLPSG gels at different concentrations (f = 1 Hz, 25 °C) Parameters

Gel samples WS

WS-0.25%LPSG

WS-0.5%LPSG

WS-0.75%LPSG

WS-1%LPSG

tan (δLVE)

0.69 ± 0.04A*

0.38 ± 0.02B

0.21 ± 0.01C

0.20 ± 0.02C

0.21 ± 0.01C

τy††

0.22 ± 0.02D

1.07 ± 0.05C

4.73 ± 0.07B

5.71 ± 0.16A

5.86 ± 0.04A

τf†††

0.70 ± 0.04D

12.93 ± 0.22C

54.17 ± 0.48B

52.07 ± 0.19B

57.45 ± 0.13A

†

†

Loss-tangent at the limit of the LVE range Yield stress at the limit of the LVE range (Pa) ††† Flow-point stress (Pa) * Different capital letters in each row indicate significant difference (P < 0.05) ††

Table 2. Power-law parameters of storage modulus (G′) and loss modulus (G″) for the WS and WS-LPSG gels at different concentrations (0.3% strain, 25 °C)

WS

G′ = K′ (ω)n′ K′ (Pa.s ) n′ e* 0.844 ± 0.011 0.353 ± 0.038a

WS-0.25% LPSG

17.964 ± 0.024d

WS-0.50% LPSG

R 0.996

G′′ = K′′ (ω)n′′ K′′ (Pa.s ) n′′ d 0.909 ± 0.018 0.601 ± 0.042a

R2 0.988

0.187 ± 0.021b

0.998

6.488 ± 0.037c

0.277 ± 0.048b

0.983

77.451 ± 0.208c

0.139 ± 0.017d

0.994

18.461 ± 0.125b

0.202 ± 0.023c

0.989

WS-0.75% LPSG

132.142 ± 0.544b

0.152 ± 0.026c

0.993

34.119 ± 0.311a

0.206 ± 0.036c

0.991

WS-1% LPSG

161.780 ± 0.461a

0.121 ± 0.033e

0.996

32.932 ± 0.587a

0.154 ± 0.019d

0.955

Sample

n

*

2

n

Different small letters in each column indicate significant difference (P < 0.05)

29

Table 3. Rheological parameters of Cross model determined for the WS and WS-LPSG gels at different concentrations (25 °C) Sample η0 (Pa.s) 𝜂∞ (Pa.s) τ m R2 WS

0.798 ± 0.062e*

0.082 ± 0.012e

0.064 ± 0.006e

1.297 ± 0.089a

0.999

WS-0.25% LPSG

3.441 ± 0.040d

0.126 ± 0.009d

0.077 ± 0.006d

1.125 ± 0.051b

0.999

WS-0.50% LPSG

72.901 ± 0.081c

0.261 ± 0.016c

1.301 ± 0.108c

1.147 ± 0.092b

0.999

WS-0.75% LPSG

100.723 ± 1.132b

0.362 ± 0.014b

4.107 ± 0.257b

0.834 ± 0.019c

0.999

WS-1% LPSG

162.658 ± 3.247a

0.632 ± 0.020a

4.901 ± 0.345a

0.817 ± 0.022d

0.999

*

Different small letters in each column indicate significant difference (P < 0.05)

Table 4. Rheological parameters of second-order structural kinetic model determined for the WS and WS-LPSG gels at different concentrations during digestion in the simulated oral condition (SOC) Sample k (s-1) η0 (Pa.s) R2 𝜂∞ (Pa.s) WS

0.086 ± 0.004d*

0.007 ± 0.002e

0.003 ± 0.001e

0.996

WS-0.25% PLSG

0.119 ± 0.007b

0.046 ± 0.005d

0.017 ± 0.002d

0.986

WS-0.50% PLSG

0.143 ± 0.009a

0.115 ± 0.008c

0.029 ± 0.004c

0.997

WS-0.75% PLSG

0.105 ± 0.011c

0.239 ± 0.015b

0.065 ± 0.007b

0.994

WS-1% PLSG

0.107 ± 0.008c

0.389 ± 0.016a

0.093 ± 0.005a

0.998

*

Different small letters in each column indicate significant difference (P < 0.05)

30