Physicochemical and morphological properties of resistant starch type 4 prepared under ultrasound and conventional conditions and their in-vitro and in-vivo digestibilities

Ultrasonics - Sonochemistry 53 (2019) 110–119

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Physicochemical and morphological properties of resistant starch type 4 prepared under ultrasound and conventional conditions and their in-vitro and in-vivo digestibilities

T

Seid Reza Falsafia,b, Yahya Maghsoudloua, , Mehran Aalamia, Seid Mahdi Jafaria, Mojtaba Raeisic,d ⁎

a

Faculty of Food Science and Technology, University of Agricultural Sciences and Natural Resources, Gorgan, Iran Niksa, Design and Development Company, Avadis Holding Group, 1917734795, Tehran, Iran Department of Nutrition, Faculty of Health, Golestan University of Medical Sciences, Iran d Cereal Health Research Center, Golestan University of Medical Sciences, Gorgan, Iran b c

ARTICLE INFO

ABSTRACT

Keywords: Resistant starch type 4 Cross-linking Ultrasound In-vitro digestibility Glucose response

In the present work, cross-linked resistant starch (RS4) was prepared under sonication and conventional conditions at various levels of pH (9–12) and cross-linker concentration (sodium trimetaphosphate/sodium tripolyphosphate 99:1, 5–15%). It was found that phosphorous and resistant starch content was generally increased by increasing the cross-linker concentration, pH and application of sonication. The damage to the surface of sonicated granules was revealed by scanning electron micrographs. The presence of cross-linked phosphorous groups was demonstrated by FT-IR results through the appearance of a new peak at wave numbers of 1248–1252 cm−1 that was more conspicuous in sonicated cross-linked samples. Sonicated cross-linked starches showed higher gelatinization temperatures and lower degrees of crystallinity, while no changes was detected in terms of A-type crystalline pattern. The development of viscosity was diminished prominently by the extreme cross-linking reactions in both sonicated and conventional cross-linked starches. The least glycemic index value was obtained for sonicated cross-linked starches which was negatively correlated to their higher RS content measured in-vitro. These results provide novel information on the preparation of cross-linked resistant starch under sonication conditions.

1. Introduction Starch is the most abundant carbohydrate in human diet which plays an important role in defining the final physicochemical and nutritional properties of foods. In order to enhance the starch applications, it is often modified using different physical, enzymatic and chemical methods [1]. Cross-linking has been the most commonly used method for preparation of chemically modified starches during which, multifunctional reagents (e.g. phosphorous oxychloride (POCl3), epichlorohydrin, sodium trimetaphosphate (STMP) and sodium tripolyphosphate (STPP)) enter the starch granule and create covalent bonds with at least two hydroxyl groups of adjacent anhydroglucose [2]. These novel binding structures tend to enhance the granules resistance against shear, temperature, retrogradation and acidic conditions. Moreover, it has been reported that cross-linking increases the resistant starch (RS) and slowly digestible starch (SDS) content of the starch [3]. RSs are the starch fractions not hydrolyzed by human digestive enzymes and remain intact within the small intestine.

⁎

This fraction is further fermented by microorganisms inhabit the large bowel. Different physiological benefits of RS has been reported in the literature mainly including the reduction of blood glucose, generation of short-chain fatty acids in particular butyric acid, decrement of colonic pH, facilitation of stool transit through the large intestine and reduction of the risk of colon cancer and type 2 diabetes [4]. However, only a small number of cross-links could remarkably change the physicochemical properties of starch, but it rarely affects the starch digestibility. In the case of POCl3 as a fast reacting reagent, reaching enough of crosslinks to induce resistance to digestion is not achievable as it is permitted up to a maximum of 0.1% in food products [5]. Woo and Seib [3] reported that starches modified at 0.1% level of POCl3 almost contained no dietary fiber. Recently, mixture of STMP/STPP has widely been used for preparation of dietary fibers as it is allowed up to 0.4% in food products [5]. Nevertheless, comparing to POCl3, STMP/STPP is relatively slower in reaction rate and rather time-consuming. Furthermore it has been reported that STMP/STPP are less capable of production of distarch monophosphate

Corresponding author. E-mail addresses: [email protected] (S.R. Falsafi), [email protected] (Y. Maghsoudlou), [email protected] (S.M. Jafari).

https://doi.org/10.1016/j.ultsonch.2018.12.039 Received 23 October 2018; Received in revised form 27 December 2018; Accepted 27 December 2018 Available online 28 December 2018 1350-4177/ © 2018 Published by Elsevier B.V.

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(DSMP) that plays the main role as the resistant starch particularly at lower pH, temperatures and times of reaction [2,3,6]. Numerous attempts have been made to elevate the incorporation of cross-linking agents into the starch granules and accelerate their reaction rate. Han & BeMiller [7] applied combinations of starch chemical modification methods and showed that the hydroxypropylation followed by cross-linking attained the highest amount of RS content (25.6%) which caused by the fact that the bulky hydroxypropyl groups loose the internal compact structures of the granules and facilitate the entrance of crosslinking reagents. Some other researchers employed reactive extrusion to prepare starch phosphates and stated that mixing the starch-phosphate blends under the high shears and temperatures during the extrusion, effectively enhanced the included phosphorus groups by 3–4 times as compared to normal procedure [8–10]. Kim et al. [11] developed a new method for preparation of cross-linked corn starch using ultra-high pressures (Pressure = 100–400 MPa) and suggested that both conventional and UHP methods have the same influence on the starch characteristics while, UHP reduced the cross-linking reaction time from 2 h to 15 min. Their results indicated that probably more DSMP complexes could be formed during the application of UHP treatment. Sonication has been introduced as an environmental friendly method of starch modification and proved to have many benefits as diminishing the process time, enhancing the chemical reaction efficiency and selectivity. During sonication, the expansion of cavitation bubbles created by high energy sound waves results in spots of very high shear, pressure (1000–2000 atm) and temperature (5000 K) which can induce drastic changes in the ambient media [12,13]. Many researchers have studied different chemical reactions of starch under sonication condition such as enzymatic or acid hydrolysis of starch [14,15], starch acetylation [16] and starch oxidation [17]. In all of the aforementioned studies, involvement of sonication in reactions, effectively enhanced their efficacy mainly caused by creating turbulent flow in the mixture and alteration in starch granular and/or molecular structure. In a most recent research, Udoetok et al. [18] studied the preparation of cross-linked cellulose under conventional process and a parallel process using ultrasonication. They reported that, cross-linked cellulose prepared under ultrasonication contained more cross-linkers and ascribed it to the facilitation of process by acoustic cavitation effect due to sonication. Although numerous researches on the fabrication and characterization of chemically modified resistant starch have been conducted [2,3,19,20], no research has investigated the synthesis of RS4 under ultrasound condition. In the present work, cross-linked RS4 preparation was assisted with sonication and the RS4 production process was further optimized using response surface methodology (RSM). The ultrasonically prepared resistant starch was compared to the conventionally prepared RS4 sample in terms of in-vitro and in-vivo digestibility and various physicochemical and morphological properties.

Table 1 The experimental design and the obtained data for phosphorous (P) and RS content of starch samples cross-linked under conventional and sonication conditions.a,b Treatment

1 2 3 4 5 6 7 8 9 10 11 12 13 14

pH

9.00 12.00 9.00 12.00 9.75 11.25 9.75 12.00 9.00 10.50 10.50 10.50 11.25 10.50

Cross-linker concentration (%)

Conventional conditions

Sonication conditions

P content (%)

RS (%)

P content (%)

RS (%)

5.0 5.0 15.0 15.0 12.5 12.5 7.5 10.0 10.0 5.0 10.0 15.0 7.5 10.0

0.02a 0.17b 0.04b 0.34b 0.04b 0.23b 0.03a 0.26b 0.02b 0.05b 0.11b 0.13b 0.15b 0.09b

2.9A 18.1B 3.4A 54.3B 4.1A 21.2B 3.7A 36.4B 3.1A 4.3A 5.5A 7.4B 12.7B 6.3A

0.03a 0.21a 0.08a 0.46a 0.09a 0.31a 0.05a 0.35a 0.05a 0.11a 0.15a 0.21a 0.2a 0.17a

1.7A 31.3A 2.0A 75.9A 2.4B 27.7A 1.9B 52.5A 2.1A 4.1A 5.3A 10.1A 16.2A 6.4A

a Means with different lowercase letters represent significant differences (P < 0.05) in phosphorous content within each row. b Means with different uppercase letters represent significant differences (P < 0.05) in RS content within each row.

was prepared in a glass beaker and placed approximately at the center of an ultrasound bath (Eurosonic 4D, Euronoda SPA, Vicenza, Italy) which was modified for laboratory application with overall dimensions of 315 * 255 * 165 mm (L * H * D) and an output power of 500 W. The temperature of the ultrasound bath and reaction media was adjusted to 45 ± 0.5 °C and kept constant at this temperature using the circulation of ice water through the bath. The pH of this solution was quickly adjusted to the specified values shown in Table 1 using the addition of appropriate amounts of 0.5 M NaOH solutions. Different amounts of STMP/STPP mixtures (99:1% w/w) were added into the solution to give the final concentrations shown in Table 1. The sonication process was performed for 60 min. The termination of the reaction was accomplished using the addition of 0.1 M HCL until neutrality. Starch samples were recovered by centrifugation (LMC-4200R, Biosan SIA., Latvia) at 1500g for 15 min. The starch pellet was washed three times with distilled water, oven dried at 40 °C, grinded and sifted to pass a 210 µm sieve for further analysis. Conventional cross-linked starches were also prepared using the same procedure exactly while, the cross-linking reactions were carried out on a magnetic stirrer (instead of ultrasound bath) with gently stirring the reaction media for 60 min at 45 °C.

2. Materials and methods

2.3. Swelling factor of starch at treatment conditions

2.1. Materials

The aim of this test was measuring the extent to which starch granules swell under different treatment conditions. The swelling factor (SF) of starch samples was evaluated using the method of Builders et al. [23] with some modification. 8% starch suspension was prepared in sodium sulfate solution (10% sdb) and the pH of the suspensions were adjusted to 9, 9.75, 10.5, 11.25 and 12 with 0.5 M NaOH. The prepared suspensions were either sonicated or stirred at 45 °C for 60 min. subsequently, suspensions were transferred to pre-weighed centrifuge tubes and sufficient amount of distilled water (45 °C) was added to get the final concentration of 5%. The tubes were vortexed and centrifuged at 3000g for 20 min. The pellet was precisely weighed and SF was measured using the following equation.

Normal maize starch was a gift from Mahshad Yazd Co. (Tehran, Iran) which contained 25.7% amylose determined by the iodocalorimetry method [21] and 10.9% moisture, 0.43% protein, 0.11% ash and 0.43% fat (determined based on starch dry basis) using the approved methods of American Association of Cereal Chemists [22]. STMP and STPP were supplied by Merck (Darmstadt, Germany). Resistant starch assay kit was obtained from Megazyme International Ireland Ltd. (Bray, Ireland). All the other chemicals used in this research were of analytical grade and obtained from Merck (Darmstadt, Germany). 2.2. Preparation of cross-linked starch samples Based on the method of Woo and Seib [3] with some modifications, 8% starch suspension in sodium sulfate solution 10% (starch dry basis)

SF (g water/g starch) = 111

S1

S2 S2

(1)

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where S1 and S2 represent the weight of wet and dry sediment, respectively.

scanning 0.05°, brag angels (2θ) between 4 and 40°, and step time of 250 s.

2.4. Phosphorus content

2.9. Thermal properties of starch samples

Phosphorus content of the starch samples was determined by the vanadomolybdo phosphoric acid colorimetric method following the procedure described in AOAC 986.24 [24]. Digestion of the starch samples was carried out as follows: 20 mg of starch weighed in a silica crucible and incinerated to white ash at 550 °C for 10 h. The samples cooled down to room temperature and 1.5 mL perchloric acid (60%) plus 3.5 mL HNO3 were added to each container. The blends heated to boil and cooled. Three mL distilled water was added to each mixture and heated. After cooling the solution, mixtures transferred to 10 mL beaker and the volume adjusted to 10 with distilled water. For development of the yellow color, 2 mL of prepared starch solution digest, 3 mL distilled water, 0.5 mL perchloric acid (60%), 3 mL ammonium molybdate (3.5%) and 1.5 mL ammonium vanadate (20 mM) were mixed. The prepared solution was stand for 15 min at room temperature and the absorbance read at 400 nm. Phosphorus standard solutions were prepared by dissolving potassium dihydrogen phosphate in distilled water so that the standard solutions contained 100–700 µg phosphorus/mL.

A TGA/DSC-1 (Mettler-Toledo, Schwerzenbach, Switzerland) instrument was employed to study the thermal properties of native and modified starches. A 1:3 starch to deionized water mixture was prepared at room temperature and stirred well for 1 h in a sealed vessel to equilibrate. Subsequently, 30 mg of the mixture was transferred to a 40 µl aluminum pan which then instantly sealed. Samples were scanned by heating from 25 to 125 °C at a rate of 10 °C/min against an empty sealed crucible as a reference. Thermal transition temperatures i.e. Onset (To), peak (Tp) and conclusion (Tc) temperatures and enthalpy of gelatinization (ΔH) were extracted from DSC thermograms. 2.10. Rapid visco-analyzer (RVA) The pasting characteristics of native and modified starches were examined in a Rapid Visco-Analyzer (RVA) (RVA Starch Master 2, Perten, Australia) through performing the standard 1 profile. Accurately, 28 g of 12.5% starch slurry in distilled water was weighed in a RVA canister. The slurry was manually mixed well with the RVA paddle before the measurement and then the canister inserted into the instrument and a 13 min heating-cooling cycle at a paddle speed of 160 rpm was performed on samples. The starch slurries were heated from 50 to 95 °C at a heating rate of 9 °C/min, held at 95 °C for 2 min, cooled to 50 °C in 4 min and held at this temperature for further 2 min. The pasting parameters including pasting temperature, peak viscosity, hold viscosity, final viscosity, breakdown and set back viscosity were determined from the RVA profile of starch samples.

2.5. Starch digestibility Resistant starch fractions were determined by following the method of Chung et al. [25] using the Megazyme resistant starch assay kit. In brief, during the incubation of starch samples (100 mg) and enzyme mixtures (amyloglucosidase + α amylase) at 37 °C, an aliquot (0.5 mL) were withdrawn from the digest at 20 min and added to 4 mL ethanol (50%) with vigorous stirring followed by centrifugation at 1500g for 15 min. The glucose content of the decanted supernatants was measured using the glucose oxidase/peroxidase (GOPOD) reagent and used to calculate the readily digestible starch (RDS) content through multiplying the measured glucose by 0.9 dividing by 100. A similar procedure was performed to obtain the amount of digested starch after 120 min of digestion process. The slowly digestible starch (SDS) content was defined as the difference of glucose released between 20 and 120 min. The RS fraction was calculated using the following equation.

RS = TS

(RDS + SDS)

2.11. Blood glucose response and glycemic index (GI) Blood glucose response to glucose, native, amorphous and crosslinked starches were determined based on the method described by Van Hung et al. [26]. For this purpose, 25 male mice were housed in separate cages and adapted for 7 days period in a light controlled (12 h dark, 12 h light) laboratory animal facility. Mice were subjected to 500 µl of 7.5% (w/v) suspensions of starch samples or glucose (as the reference) using oral zoned needle. After 0, 30, 60, 90, 150, 180 and 240 min of consumption, blood samples were drawn from the tail vein of mice and blood glucose response curve were plotted against time. The levels of glucose in blood serum were determined with a glucometer (Accu-Chek Aviva plus; Roche Diagnostic Systems, Mannheim, Germany). To calculate the glycemic index (GI) of starches, the incremental area under the curve (iAUC) was measured for each sample and divided by the iAUC determined for the reference (glucose) [27].

(2)

Of which, RS is the resistant starch content (%) and TS is the total starch (%). 2.6. Scanning electron microscopy (SEM) A thin layer of starch granules was spread on a double-sided adhesive tape already attached on an aluminum pin stub. Subsequently, the prepared sample were coated with a thin layer of gold using a sputter coater (Q150T sputter coater, London, England). Morphological properties of samples were investigated by Philips XL30 ESEM FEG (FEI CO., Netherland) operating at an accelerating voltage of 20 kV.

2.12. Statistical analysis A two factor central composite design through response surface methodology of Design Expert software (Stat-Ease, Minneapolis, USA) was selected to design the experiments of the present study in which the resistant starch and phosphorous content were the responses and the concentration of STMP/STPP and pH were the independent variables. The response values were modeled through a second order (quadratic) polynomial equation that analyzed the relationship between dependent and independent variables using a multiple regression equation approach as follow:

2.7. Fourier transform infrared (FT-IR) spectroscopy Native and cross-linked starches were mixed with potassium bromide at a ratio of 1:30 and tableted under pressure. Scans were performed in a FTIR spectrophotometer (Bruker tensor 27) in the wavenumber ranges of 400–4000 cm−1 at a resolution of 4 cm−1. 2.8. X-ray diffraction (XRD)

k

Y=

A Bruker D8 spectrometer (Karlsruhe, Germany) operated at current and voltage of 30 mA and 40 kV, respectively was employed to obtain X-ray diffraction pattern of starch samples. Following settings were adjusted on the instrument: Cu-Kα radiation detector, step size of

0

+ i=1

k iXi

+

ii .Xi i=1

2

+

ij XI Xj i<1

(3)

where Y represents the dependent variable, Xi and Xj denoting the independent variables, β0 is the model intercept, βi, βij and βii are the 112

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linear, interaction and quadratic regression coefficients, respectively. The models capability for fitting the experimental data were evaluated based on the R2 (coefficient of determination) and lack of fit results. Before performing the analysis of variances (ANOVA), the insignificant terms of model were removed through the backward elimination method. All the runs were carried out in triplicate and the average values were reported except for DSC measurements that replicated twice.

the P content of starch. The results of paired t-test analysis (Table 1), showed that at all treatment conditions, samples cross-linked under sonication had a significantly higher P content (P < 0.05). In the case of samples cross-linked at pH values < 10.5, under conventional condition, increasing the cross-linker concentration marginally affected the measured P content, while for sonicated cross-linked counterparts, at these pH ranges increasing the concentration of cross-linker led to a remarkable increase in the P content. These changes in p content were also consistent with the swelling factor observations, of which in conventional treated samples, slight change in swelling factor was obtained at pH values less than 10.5. Through the starch cross-linking using STMP/STPP mixtures, which the main site of chemical reactions are within the granules, two main steps can be enumerated, penetration of cross-linker components into the granules and covalent bonding between ionized hydroxyl groups of anhydroglucose units of starch and phosphate groups of STMP/STPP molecules [2]. In this regard, during sonication, the introduction of cavitation bubbles into the reaction media and their following collapse, resulted in the degradation of amorphous and even crystalline parts of starch granules, together with the creation of cracks and pores on the surface of granules (as further discussed in SEM, DSC and XRD sections). Furthermore, the turbulent flow arising from the microjet streaming of fluid near the collapsing bubbles, increased the mass transfer and led to the penetration of more cross-linkers reactants into the granules through the created channels and pores. Zhang et al. [32] prepared acetylated dioscorea starch under normal and sonication conditions and similarly reported a higher degree of substitution in the samples acetylated under sonication condition. Huang et al. [33] revealed that sonication can effectively increase the reaction efficiency of starch granules through the degradation of granules crystalline structure and creation of cracks and pores. The ANOVA results of second order polynomial model for phosphorous content has been reported in Table 2. The P-values of < 0.0001, the lack of fits of 0.58 and 0.50 and the coefficient of determinations (R2) of 0.983 and 0.985 for models fitted to the starch P content results in conventional and sonication conditions, respectively, showed that the quadratic model can best fit the experimental results of P content. The ANOVA of model parameters showed that the linear terms of pH and cross-linker concentration and the interaction of pH-cross-linker concentration and the quadratic term of pH had significant effect on P variations. A higher value for F and lower value for p represents a more significant influence of model term on the starch P content. From Table 2, it can be seen that pH had the most pronounced impact on the P content variation for both of treatment conditions. pH is a crucial parameter determining the chemical reactivity of starch. Considering the pKa value of 12.5 for hydroxyl groups of starch molecules, increasing the pH, ionize the starch hydroxyl groups which not only loose the starch granular structure by repulsive forces between molecules and facilitate the entry of cross-linker components, but also increases the capacity of starch molecules to react with more negatively charged phosphorous groups [34].

3. Results and discussion 3.1. Swelling factor The inevitability of granular swelling for involvement of starch into chemical reactions has been well documented in numerous studies [28,29]. These researchers have corroborated that some granular swelling is crucial to reach the threshold of chemical reactivity of starch so that in unswollen granules, even the superficial –OH groups were not accessible for chemical reactions. Fig. 1 represents the SF of starches treated under sonication or conventional conditions at different pH values. The SF of the starch samples were remarkably influenced by the treatment condition and pH of the slurry. Comparing to the conventional treated samples, sonication significantly increased the swelling factor at all pH measured. Generally, it’s been reported that high power ultrasound through the severe physical damage, disintegrates the amorphous and even crystalline structures of granule which together with the formation of fissures and channels increases the ability of granules to absorb more water. Similar observation was reported by Falsafi et al. [13] and Sujka et al. [30]. It can also be observed that, increasing the pH, significantly improves the SF of starch which it was more pronounced at pH values higher than 11. Increasing the pH from 9 to 9.75, 10.5, 11.25 and 12 increased the SF from 3.1 to 3.5, 3.9, 5.6 and 7.4 for conventional treated samples and 3.5 to 4.4, 5.1, 7.2 and 10.5 for sonicated samples, respectively. The main phenomenon impacted the starch swelling behavior is the ionization of starch molecule hydroxyl groups under alkaline pH. The repulsive forces among these ionized groups, weaken the starch granule structure and facilitate the entering of water molecules. The Higher swelling factor of starch at alkaline pH were also reported by Builders et al. [23] and Hedayati et al. [31]. 3.2. Phosphorous content The phosphorous (P) content of conventional and sonicated crosslinked starch samples under different treatment conditions are shown in Table 1. The interaction between cross-linker concentration and pH are also shown as surface graphs in Fig. 2. As Fig. 2(a and b) shows, for both conditions, increasing the pH and cross-linker concentration increased

3.3. Starch digestibility Cross-linking diminishes starch digestibility through the introduction of novel covalent bonds into the molecular structure of amylose and amylopectin. However, amongst various products of crosslinking reaction of starches i.e. monostarch mono, di or three phosphates and DSMP, only the latter group contributes to the formation of indigestible starch fractions [34,35]. It was observed that at pH values less than 10.5, variation in pH and cross-linker concentration did not induce any significant changes in RS content of both C-CL and S-CL samples (Fig. 2b and c). At these treatment conditions, sonicated cross-linked samples had a significantly lower RS content (P < 0.05) (Table 1). This could be caused by the alteration of granular structure (because of sonication) as well as the insufficient extent of DSMP (because of the low pH values) that resulted in the eased access of digestive enzymes to starch molecules. At higher

Fig. 1. Swelling factor (g/g) of ultrasound-assisted and conventional treated starch samples at varying pH values. 113

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Fig. 2. Surface graphs of the changes in P content of sonicated cross-linked (a) and conventional cross-linked (b) and RS content of sonicated cross-linked (c) and conventional cross-linked (d) samples.

pH values (pH ≥ 10.5) increasing the concentration of cross-linker and pH, sharply increased the RS content of both S-CL and C-CL samples. However, conversely, sonicated cross-linked samples had remarkably higher RS content than those of conventional cross-linked ones. These observations can be ascribed to the increased amount of ionized hydroxyl groups at higher pH values together with the facilitated and accelerated entry of cross-linker molecules into the granule under sonication condition. The highest RS content (75.9%) was observed in sample prepared at pH = 12 and cross-linker concentration of 15% under sonication condition at which the P content was 0.46. Chen & Kalback [36], outlined that the main reasons of chemical reaction intensification by ultrasound are: the local increase in temperature and

pressure, turbulent flow resulted from elevated mechanical agitation, and sonolysis of –OH groups in the sonication media. The ANOVA of measured RS contents (Table 2) showed that the quadratic model can adequately fit the RS variations in which the Pvalue, lack of fit and R2 were 0.0001, 0.126 and 0.980 for conventional and 0.0001, 0.150 and 0.968 for sonicated cross-linked samples, respectively. From the measured F and P values reported in Table 2, between independent variables, pH was the most important factor in determining the amount of RS. Model parameters showed that pH, cross-linker concentration, interaction of pH- cross-linker concentration and quadratic term of pH were the significant terms in fitted models. As it was found in the results, the highest amount of RS was

Table 2 Regression coefficients of model terms for RS and P content and their significance level. Terms

Conventional conditions P content (%)

Model A – pH B – Cross-linker concentration (%) AB A2 B2

Sonication conditions RS (%)

P content (%)

RS (%)

F-value

P

F-value

P

F-value

P

F-value

P

96.98 385.58 53.58 24.95 20.11 0.18

0.000 0.000 0.000 0.002 0.005 0.674

48.95 151.56 23.47 28.10 39.09 0.03

0.000 0.000 0.001 0.001 0.000 0.868

110.36 422.88 87.37 30.17 10.65 0.00

0.000 0.000 0.000 0.000 0.016 0.845

81.95 271.40 29.12 32.80 69.53 0.06

0.000 0.000 0.001 0.000 0.000 0.808

114

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obtained in the case of sonicated cross-linked samples hence, in further experiments, sonication crosslinking process was optimized to gain the highest amount of RS while the P content is lower than 0.4%.

spectral peaks remained almost identical for all starch samples. This means that the molecular structure of starch stayed intact after sonication and phosphorylation treatments. Nevertheless, some discrepancies were observed in the case of cross-linked samples. For samples crosslinked under conventional condition, the major change was observed in the extent of free, inter and intra molecular O–H linkages (peak at 3433 cm−1) in which the intensity of peak was diminished as compared to the native starch sample. Moreover, a new absorption band was appeared at 1248–1252 cm−1, which is related to the P–O bonds of crosslinked starches [39]. Similar changes but in higher extent were observed for sonicated cross-linked samples, of which the diminution of peak at 3433 cm−1 was larger and the absorption intensity at 1251 cm−1 was clearly sharper. Considering the fact that STMP/STPP molecules react with the O–H groups of starch molecules, a reduction in O–H absorption intensity of starch and the emergence of new P–O band at around 1248–1252 cm−1 showed that the cross-linker groups were well reacted with starch molecules. However, the extent of cross-linking reactions was more pronounced in the case of samples cross-linked under sonication condition which was in accordance with their higher content of RS. During sono-cross-linking reactions, the excessive energy released from the collapsed cavitation bubbles, changes the structure of adjacent granules by creating superficial cracks and fissures, breaking glycosidic bonds and loosening of the granule compact structure, that offer more spaces for percolation of surrounding media into the granule [14]. The elevated specific surface area in sonicated granules caused a remarkable increase in the interaction between ionized hydroxyl groups of glucose molecules and phosphate groups of STMP/STPP which together with the facilitated ingress of cross-linking agent into the granule, enhanced the efficacy of cross-linking reactions that is reflected on the FT-IR absorption spectrum of S-CL starches in form of a sharper peak at 1248–1252 cm−1. Accordingly, Udoetok et al. [18] observed similar increase in cross-linking efficiency of cellulose under ultrasound condition.

3.4. Optimization The numerical optimization in RSM was used to determine the optimum condition of RS fabrication under sonication treatment. The goals set for pH, cross-linker concentration, P content and RS were: in range (9–12), in range (5–15), in range (0–0.4) and maximized, respectively. The optimum condition in which the highest RS content was obtained were as follow: pH = 12 and cross-linker concentration = 12.3%. The RS content of 60.94% and P content of 0.4% were predicted to attain at the optimum condition whose desirability was 0.798. It is noteworthy to mention that higher amount of resistant starch can be obtained at higher cross-linker concentration (as it was shown in Table 1 at pH = 12 and cross-linker concentration of 15%, the RS content of 75.9% was obtained) but at those concentrations, the phosphorous content of cross-linked samples exceed the permissible level reported by Code of Federal Regulations [5]. To confirm the theoretical results of RSM optimization, five samples were prepared under the optimum condition. The average of P and RS content of experimental samples were 59.5 and 0.39%, respectively which was comparable to the results of predicted P and RS by software. At similar pH and cross-linker concentration under conventional condition the amount of RS and P were obtained to be 41.5 and 0.28%. In the rest of paper, different properties of corn starch cross-linked at above mentioned optimal condition under sonication or conventional conditions (S-CL and C-CL, respectively) were investigated. 3.5. SEM results The SEM images of native, sonicated and phosphorylated corn starches are depicted in Fig. 3. Native and treated samples showed polyhedral and sphere shaped morphology. No conspicuous changes were detected between the shape and size of the native and the treated starch granules. Normal corn starches had smoothed surface with no noticeable cracks or fissures (Fig. 3a). However, a remarkable damage to the surface of the granules was detected for sonicated samples, which can be observed as dark pores and elongated fissures (Fig. 3b). Similar cracks and pores were reported on the surface of sonicated oat [13], potato [37] and pinhao [38] starches, and has been ascribed to the cavitation phenomenon that locally induce very high pressures and shear forces leading to the mechanical degradation of the external amorphous and crystalline layers of starch granules. Moreover, such surface disintegrations can happen through the breakage of α-1,6 glycosidic bonds located near the collapsing cavitation bubbles [12]. In samples cross-linked under conventional conditions, some holes appeared sporadically on the surface of the granules (Fig. 3c). While for the sonicated cross-linked samples, deeper notch and grooves scattered uniformly throughout the granules surface together with visible cracks and fissures (Fig. 3d). The emergence of exo-erosions on the surface of starch granules during cross-linking was also reported by Carmona-Garcia et al. [2] which their intensification through sonication might explain the sever cross-linking condition obtained during S-CL preparation resulted from the very high mixing, pressures and shear forces applied during sonication.

3.7. XRD results The XRD measurements were carried out to investigate the variations in type and degree of crystallinity of native, sonicated and phosphorylated samples. The emergence of 5 distinct peaks at brag angels (2θ) of =15.12, 17.05, 18.15, 20.10 and 23.33 is the characteristic of A-type polymorph pattern which is typical of cereal starches. Fig. 5 illustrates that sonication and phosphorylation imparted no significant change in the localization of main X-ray diffraction peaks of samples in contrast to the native starch which indicated both sonication and phosphorylation had no effect on the crystalline pattern of granules. The most conspicuous changes in X-ray diffractograms was the reduction of degree of crystallinity as a result of sonication and phosphorylation. Singh and Nath [40] reported a decrease in relative crystallinity of cross-linked sago starch and ascribed it to the plausible disorders in chains alignment caused by the substitution of hydroxyl groups with phosphates. The reduction in crystallinity as a result of sonication has already been reported by Monroy et al. [41] Zheng et al. [42] and Falsafi et al. [13] for sonicated cassava, sweet potato and oat starches due to the disintegration of weak crystalline structures located mostly at the periphery of the granules during sonication. Hoover and Sosulski [43] reported that cross-linking reactions typically occur at the amorphous fractions of starch granules. Hence, it could be concluded that, sonication would intensify the cross-linking reactions by developing the amorphous regions (reducing the crystallinity) of starch granules. As it can be seen, the samples cross-linked under sonication revealed the least degree of crystallinity which can be the result of severe cross-linking condition together with sonication cavitation leading to the extreme dissociation of crystalline fractions.

3.6. FTIR results The FT-IR analysis was carried out to probe the transformations in molecular structure of different starch samples. The FT-IR spectra of native and modified samples are depicted in Fig. 4. The main characteristic bands were observed at wavenumbers of around 3433, 2927, 1641 and 870–1150 cm−1 which are attributed to the complex stretching vibration of O–H, deformation vibration of C–H, bending/stretching vibration of O–H of the water molecules and stretching of C–O/C–C bonds of anhydroglucose ring, respectively [19]. The shape and position of

3.8. Thermal properties The thermal properties of native and modified starches extracted from their thermograms (Fig. S1 of Supplementary data) are 115

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Fig. 3. SEM micrographs of native (a), sonicated (b), conventional cross-linked (c) and sonicated cross-linked (d) starch samples.

Fig. 4. FT-IR spectra of native (NC), sonicated (SC) and cross-linked (S-CL and C-CL) starch samples.

represented in Table 3. Sonication elevated the phase transition temperatures (To, Tp, Tc) of starch but diminished its gelatinization enthalpy (ΔH). It has been reported that sonication degrades the crystalline fractions of lower integrity within the granules resulting in a decrees in ΔH. While the highly ordered leftovers with elevated melting temperature endure and leading to an increase in the transition temperatures [44,45]. Interestingly, in phosphorylated samples, the introduction of cross-linker ingredients into the starch granules similarly increased their gelatinization temperatures but decreased the enthalpy of gelatinization. These observations reveal that the introduction of covalent bonds into the starch molecules increased their stability and tautened their lattice structure [46]. However, the decrease in ΔH might be due to the dissociation of organized segments of the granules through the sever cross-linking condition. As it can be seen, the most pronounced variations were observed in sonicated cross-linked samples where the ΔH was reduced by 14.4% and the Tp of gelatinization was increased by 8.6%. This was in accordance with XRD and FT-IR results

Fig. 5. X-ray diffraction pattern and relative crystallinity of starch samples.

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Table 3 Thermal properties of native corn (NC), sonicated corn (SC), conventional cross-linked (C-CL) and sonicated cross-linked (S-CL) starches.a, Starch sample

Gelatinization temperatures (°C) To

NC SC C-CL S-CL a b

59.1 60.5 61.0 64.2

Tc − To Tp

± ± ± ±

c

0.21 0.44b 0.17b 0.21a

66.2 68.9 68.3 71.0

ΔH

Tc ± ± ± ±

c

0.11 0.08b 0.34b 0.29a

71.9 73.0 75.7 76.2

± ± ± ±

0.39c 0.26b 0.28a 0.42a

12.8 12.5 14.7 12.0

± ± ± ±

0.17b 0.23bc 0.19a 0.13c

most of bindings are phosphomonoesters. However, in contrast, a remarkable reduction in peak viscosity, indicating the incidence of extensive cross-linking reactions where distarch-monophosphate comprised the main covalent bonds [50]. As it can be observed the sonicated-cross-linked samples showed no detectable peak in RVA viscosity pattern. The excessive crosslinking reactions occurred inside the amorphous and/or crystalline fractions of granules, stiffened the granule structure and induced a diffusional resistance to water percolation inside the granules which suppressed the granular swelling and drastically lowered their occupied volume fraction. However, for samples cross-linked under conventional condition, a late emergence of a small peak was observed at 89 °C which is plausibly the result of partial swelling of less cross-linked granules at high temperature. Similar variation in RVA pattern of cross-linked potato starches was reported by Heo et al. [51].

3.9. RVA results Viscosity development during the heating of a starch suspension is mainly governed by the formation of arrays of deformable swollen granules [47]. From the RVA results (Table 4 and Fig. S2 in Supplementary data) it was observed that through the sole application of sonication, the pasting temperature insignificantly increased from 79.2 to 80.0 °C (P > 0.05). Such change was in accordance with the increment found in the onset transition temperature of gelatinization (DSC results) and could be due to the presence of crystalline remnants of higher integrity remained after sonication that restrains the swelling of starch granules and delays the viscosity development to a higher pasting temperature [49]. However, the damaged granular structure of sonicated samples, diminished their resistance against dissociation by heating and shear, resulted in their lower peak viscosity. Similar observations were reported by Amini et al. [48], Chan et al. [49] and Jambrak et al. [44]. A lower hold viscosity (viscosity determined during the 95 °C holding phase) observed in the case of SC samples, further approved their damaged granular structure leading to their greater fragmentation by shear at constant temperature. The break down values of sonicated starch samples were comparable to that of native counterparts, but a rather higher set back values were obtained for sonicated samples. The setback property has been reported to be related with the reassociation of solubilized starch fractions during the cooling period of RVA measurement [49]. Hence, it could be implied that a higher degree of dissociation was occurred in weakened sonicated starch granules, leading to a greater lixiviation of soluble starch fractions capable of reassociation. Viscosity measurement is reported to be a reliable method for determining the type and extent of crosslinking reactions occurred inside the granules [11]. In this approach, for a cross-linked starch paste, increasing the peak viscosity together with a less pronounced breakdown is an indication of low to mild phosphorylation reactions in which the

3.10. Blood glucose response and GI in mice The postprandial blood glucose level of rats injected with suspensions of glucose, native, amorphous and cross-linked starches are shown in Fig. 6. As it can be seen, the glucose release pattern of samples was differed significantly. After the injection of glucose, amorphous and native starches a sharp increase in blood glucose level was observed after 30 min of consumption which subsequently followed by a rapid reduction to the initial level. The maximum blood glucose levels were 255, 234 and 209 mg/dL for glucose, amorphous and native starches, respectively. The consumption of native starch lowered the blood glucose at 30 and 60 min owing to its less digestible fractions. Both conventional cross-linking and sonication cross-linking treatments decreased the level of blood glucose, in which the S-CL starches had the lowest blood glucose concentrations owing to their highest amount of RS content (vs. other samples). Furthermore, the starches cross-linked under sonication condition revealed a different glucose release pattern in which the peak attained at 60 min and no steep increase or decrease in blood glucose was observed. For each sample, the incremental area under the blood glucose curves were determined and the GI was measured based on the concept described by FAO [27]. The increase in GI values followed the order of glucose > amorphous starch > native starch > C-CL > S-SL with GI values of 100, 92, 77, 53 and 32, respectively. Comparing with the in

Table 4 Pasting properties of native corn (NC), sonicated corn (SC), conventional cross-linked (C-CL) and sonicated cross-linked (S-CL) starches.a, Starch sample

NC SC C-CL S-CL b

11.1 ± 0.07a 10.8 ± 0.16ab 10.2 ± 0.11bc 9.5 ± 0.05c

Results are means of triplicate determinations ± standard deviation (n = 3). Means followed by the same superscript in any column are not significantly different (p > 0.05).

where the lowest degree of crystallinity and the highest extent of chemical cross-linking reactions were observed in sonicated cross-linked samples. In sonicated samples disintegration of crystalline lamellas increased the available sites for chemical reactions which along with the creation of cracks and pores and the turbulent mixing of the reaction media, obtained the highest efficiency of chemical reaction.

a

b

Viscosity (RVU)

b

Pasting temperature (°C)

Peak

Hold

Final

Break down

Set back

5203.4 ± 13.1a 4872.6 ± 8.9b 209.2 ± 3.5c nd

2035.6 ± 9.8a 1618.4 ± 11.2b 191.8 ± 1.6c nd

5437.1 ± 12.2b 5889.7 ± 15.2a 167.3 ± 2.9c nd

3167.8 ± 7.4b 3254.2 ± 4.9a 17.4 ± 0.8c nd

3401.5 ± 11.4b 4271.3 ± 6.3a 24.5 ± 1.1c nd

Results are means of triplicate determinations ± standard deviation (n = 3). Means followed by the same superscript in any column are not significantly different (p > 0.05). 117

79.2 ± 0.3b 80.0 ± 0.6b 87.92 ± 0.1a nd

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Fig. 6. Average concentration of blood glucose in mice after intake of glucose, amorphous, native (NC), sonicated (SC) and cross-linked (S-CL and C-CL) starches.

vitro digestion results, the calculated GI values were negatively correlated with the amount of indigestible starchy fractions (RS) of these samples. The gradual increase in blood glucose after the injection of SCL sample and its lower GI which was corroborate with its high content of RS, showed its capability for incorporation into food products as a good source of dietary fiber. 4. Conclusion The extent of phosphorylation reactions and the resultant resistant starch were remarkably influenced by the cross-linker concentration, pH of the mixture and particularly the presence of sonication. Sonication accelerated the cross-linking reactions by achieving higher phosphorous and RS contents at a specific treatment condition. It was found that at a higher level of phosphorylation obtained by sonication, severe damage occurred to the surface of granules along with the elevation of gelatinization temperature, the reduction of crystallinity and the suppression of viscosity development. It could be concluded that by applying determined optimized condition, cross-linked starch with a high content of resistant starch will be achieved. 5. Declarations of interest None. Acknowledgments The authors wish to profoundly thank Dr. Hadis Rostamabadi and Mohammad Mahdi Rostamabadi for the detailed review of this paper. We also acknowledge the Megazyme Co. and Dr. Barry V. McCleary for providing the resistant starch assay kit. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ultsonch.2018.12.039. References [1] C. Chiu, D. Solarek, Modification of starches, Starch, third ed., Elsevier, 2009, pp. 629–655. [2] R. Carmona-Garcia, M.M. Sanchez-Rivera, G. Méndez-Montealvo, B. GarzaMontoya, L.A. Bello-Pérez, Effect of the cross-linked reagent type on some morphological, physicochemical and functional characteristics of banana starch (Musa paradisiaca), Carbohydr. Polym. 76 (2009) 117–122. [3] K.S. Woo, P.A. Seib, Cross-linked resistant starch: preparation and properties, Cereal Chem. J. 79 (2002) 819–825, https://doi.org/10.1094/CCHEM.2002.79.6.

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