Physicochemical interactions of maize starch with ferulic acid

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Food Chemistry 199 (2016) 372–379

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Physicochemical interactions of maize starch with ferulic acid Rusiru Karunaratne, Fan Zhu ⇑ School of Chemical Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand

a r t i c l e

i n f o

Article history: Received 14 September 2015 Received in revised form 16 November 2015 Accepted 8 December 2015 Available online 8 December 2015 Keywords: Ferulic acid Maize starch Rheology Texture Gelatinization Interaction

a b s t r a c t Ferulic acid is widely present in diverse foods and has great health benefits. Starch is a major food component and can be flexibly employed to formulate various products. In this study, the effect of ferulic acid addition on various physicochemical properties of normal maize starch was explored. The properties including swelling, pasting, steady shear and dynamic oscillation rheology, gelatinization, retrogradation, and gel texture were affected by ferulic acid to various extents, depending on the addition level. Enzyme susceptibility of granular starch to a-amylase was not affected. These influences may be explained by the functions of solubilized as well as insoluble ferulic acid which was in the form of crystals in starch matrix. On the molecular level, V-type amylose–ferulic acid inclusion complex formation was not observed by both co-precipitation and acidification methods. The results of this study may inspire further studies on the interactions of phenolics with other food ingredients and their role in food quality. Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction Ferulic acid [(E)-3-(4-hydroxy-3-methoxyphenyl)-prop-2-enoic acid] (Supplementary Fig. 1) is a type of hydroxycinnamic acid found in many fruits and vegetables. It is sometimes called ‘‘chain breaking” antioxidant due to the radical scavenging properties (Packer, Sies, Eggersdorfer, & Cadenas, 2010). Ferulic acid has demonstrated diverse beneficial effects on human health such as anti-inflammation and free radical scavenging (Mancuso & Santangelo, 2014; Packer et al., 2010). It has been suggested that ferulic acid can treat diverse disorders including Alzheimer’s disease, cancer, cardiovascular diseases, diabetes mellitus, and skin disease (Mancuso & Santangelo, 2014). It is, thus, natural to develop functional foods and nutraceuticals using ferulic acid as the bioactive ingredient. Another scenario is that during food processing and formulation such as tissue disruption, mixing, and cooking, diverse endogenous and exogenous ingredients come into contact and interact with each other. These interactions may impact physicochemical and nutritional properties of food. Ferulic acid in bound and free forms can be found in various types of food items such as cereals (Boz, 2015; Singh, Rehal, Kaur, & Jyot, 2015). Processing of these foods may release ferulic acid from cellular compartments and bound form (Singh et al., 2015), and the released compound may interact with other components such as protein and starch, affecting food quality. Starch is one of the most common food components in human diets. It consists of two major types of macromolecules: the linear ⇑ Corresponding author. E-mail address: [email protected] (F. Zhu). http://dx.doi.org/10.1016/j.foodchem.2015.12.033 0308-8146/Ó 2015 Elsevier Ltd. All rights reserved.

amylose and the branched amylopectin. In nature, starch chains are assembled in the form of semi-crystalline granules. Gelatinization, retrogradation, and interactions of starch can be critical for the quality of many food items rich in starch (e.g., cereal products). The interactions between starch and phenolic compound are gaining research focus during the last few years due to the possible impacts on food properties and nutrition (Zhu, 2015). On the molecular level, the non-covalent interactions between various phenolics and starches can be categorized into V-type amylose inclusion complex formation and non-inclusion complex formation (Zhu, 2015). Amylose undergoes structural changes in the presence of a guest molecule and forms V-type complexes (Ryno, Levine, & Iovine, 2014). Hydrophobic cavities are present within the helices of V-type amylose, entrapping the guest molecules (Lesmes, Cohen, Shener, & Shimoni, 2009). Both amylose and amylopectin interact with starch, but starches with high amylopectin contents (e.g., waxy starch) tend to form fewer or no complexes (Obiro, Ray, & Emmambux, 2012). Non-inclusion complex formation involves the interactions through hydrogen bonds, hydrophobic interaction, and electrostatic and ionic interactions (Bordenave, Hamaker, & Ferruzzi, 2014). On the macroscopic level, phenolics impact various physicochemical properties of starch such as rheology, gelatinization, and retrogradation (Sun-Waterhouse, Zhou, & Wadhwa, 2012; Xiao, Lin, Liu, & Yu, 2012; Zhu, 2010; Zhu & Wang, 2012). For example, with regard to the pasting properties, contradicting results were reported. In one study, tea polyphenols reduced peak viscosity, holding strength, final viscosity and setback viscosity, while increasing the breakdown viscosity (Guo, Tu, Pan, Zhang, & Zhang, 2012). Another study concluded that pasting properties were not influenced by the grain polyphenol content

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(Beta, Corke, Rooney, & Taylor, 2001). This contradiction may be due to the differences in the types of phenolics and starch, and reflects the needs to better understand factors affecting starch– phenolics interactions. Apart from physical properties, several studies have demonstrated the ability of polyphenols in the inhibition of starch enzymatic hydrolysis (Barros, Awika, & Rooney, 2012; Chiang, Li Chen, Jeng, Lin, & Sung, 2014). This suggests the positive role of the interactions on glucose metabolism management for human health. Factors affecting the impact on starch properties include the type of starch and phenolic compound, composition and concentration of the system, and processing conditions (Zhu, 2015; Zhu, Cai, Sun, & Corke, 2009). Another much neglected but important point is that solubility of phenolics tends to play a major role in phenolics–starch interactions. Phenolics tend to have an increasing solubility with the increase of temperature (Cuevas-Valenzuela, González-Rojas, Wisniak, Apelblat, & Pérez-Correa, 2014). Ferulic acid, caffeic acid, and p-coumaric acid have melting points of 170, 196, and 215 °C, respectively (Murga, Sanz, Beltrán, & Cabezas, 2003). Most foods are not processed at such high temperatures, which may cause certain polyphenols to be unevenly dispersed in water. Solubilized phenolics may have different interactions with starch and other molecules present in the system due to the much increased mobility in a liquid medium. This was observed in two studies where one study demonstrated that tea polyphenols, which has a good water solubility, increased the peak temperature (Tp) of starch gelatinization from 71.0 to 74.9 °C (at 15% polyphenol concentration), while another study demonstrated that rutin, which has a rather low solubility, decreased the Tp of rice starch from 67 to 66.5 °C (at 50% concentration) (Xiao et al., 2012; Zhu & Wang, 2012). Phenylpropenoic acids (transcinnamic, caffeic, and ferulic acids) tend to have lower water solubility than hydroxybenzoic acids (gallic and salicylic acids) (Mota, Queimada, Pinho, & Macedo, 2008). The diversity in the solubility of different phenolics contributes to the difficulty in understanding the interactions of starches with various phenolic compounds. This study mainly focused on observing the effect of ferulic acid addition on the swelling, rheological properties, gelatinization, retrogradation, and enzymatic hydrolysis of normal maize starch. Weather V-type amylose inclusion complexes could be formed with ferulic acid was also tested, employing a high amylose maize starch and two preparation methods.

2. Materials and methods 2.1. Materials Normal maize starch (AmiocaTM) (moisture content: 13.32%, apparent amylose content: 24.5%) and high amylose maize starch Gelose 80 (moisture content: 12%, apparent amylose content: 80.4%) were from Ingredion Singapore Pte. Ltd. (Singapore). Gelose 80 was specifically used for the test of amylose inclusion complex formation due to the high amylose content. Normal maize starch was used for the other tests. Apparent amylose contents of starch were measured by iodine-binding based spectrophotometry. Trans-ferulic acid (purity 99%) and a-amylase of Bacillus subtilis were from Sigma–Aldrich (St. Louis, MO, USA). The chemical structure of ferulic acid is illustrated in Supplementary Fig. 1. 2.2. Methods 2.2.1. Particle size determination Mastersizer 2000 (Malvern Instruments, Worcestershire, United Kingdom) was used to measure the particle sizes of normal maize starch and ferulic acid which was dispersed in water (1%, w/w).

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Particles size was measured with the refractive index of 1.5 and absorption index of 0. Sample was dispersed in the dispersion unit using water as dispersant (stirring speed at 2040 rpm), and the obscuration percentage was kept between 10 and 20%. Ultrasound was used for a better dispersion of particles. D[4,3] value and size distribution were monitored. 2.2.2. Swelling power and solubility Starch (150 mg, db, W0) were measured directly into screw capped tubes and 10 mL of water was added and vortexed for 5 s. Ferulic acid was added in proportion (5–20%, w/w). The tubes were incubated in a water bath at 85 °C for 30 min with vortex mixing at 2 min intervals. The tubes were then immediately transferred to an iced water bath for cooling down. The tubes were centrifuged at 2000
g for 35 min. The supernatant was then transferred to aluminum pans. The material that adhered to the tube was considered as the sediment and the weight of the sediment was measured (Ws). The pans containing supernatant were placed in a forced air oven at 100 °C till a constant weight (W1). Water solubility index (WSI) and swelling power were calculated as:

Water solubility index ¼ W1=W0
100%

ð1Þ

Swelling power ¼ Ws=½W0
ð1  WSI=100Þ ðg=gÞ

ð2Þ

2.2.3. Differential scanning calorimetry (DSC) Starch or mixtures (2 mg, db) (ferulic acid was at 5–20%, w/w) was weighed into DSC pans and 4 mL of water was injected through a micropipette. Samples were analyzed by a DSC (Q1000, TA instruments, New Castle, USA) by equilibrating at 30 °C for 2 min before ramping to 135 °C and cooling to 25 °C at a rate of 10 °C/min. After the gelatinisation, the pans were kept in the refrigerator at 4 °C for 21 days. The pans were then re-scanned with the same settings. The onset temperature (To), peak temperature (Tp), conclusion temperature (Tc), and enthalpy change (DH) of gelatinisation were noted. DH was calculated on the basis of starch weight. 2.2.4. Pasting Starch or mixtures (1.75 g, db) (ferulic acid was at 5–20%, w/w) was blended with water to achieve a total weight of 17 g in the canister of a rheometer (Physica MCR 301, Anton Paar, Graz, Austria). Samples were held at 50 °C for 1 min, heated to 95 °C in 7.5 min, held at 95 °C for 5 min before cooling down to 50 °C in 7.5 min and holding at 50 °C for 2 min. The peak time, peak viscosity (PV), hot paste viscosity (HPV), final viscosity (FV), pasting temperature, and peak temperature were measured. Breakdown (BD = PV  HPV) and setback (SB = CPV  HPV) were calculated. 2.2.5. Steady shear analysis Starch suspensions were prepared by mixing total solid weights (19.92 mg, db) with 0.4 mL of water (ferulic acid was at 5–40%, w/ w). The suspensions were then transferred onto the plate of rheometer (Physica MCR 301, Anton Paar, Graz, Austria) using a parallel plate with a diameter of 40 mm and a gap of 1 mm. The edge of the gap was covered with a thin layer of soybean oil to minimize water evaporation. The suspensions were conditioned at 25 °C for 1 min. At a constant shear stress of 5 Pa, temperature was ramped from 25 °C to 95 °C before cooling to 25 °C with a rate of 10 °C/min. Then the samples were sheared from 0.1 s1 to 800 s1 and from 800 s1 to 0.1 s1 at 25 °C. The data was modeled by the power law (3) and Herschel–Bulkley (4) equations.

d ¼ k
cn

ð3Þ

d ¼ do þ k
cn

ð4Þ

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d = shear stress (Pa); k = consistency coefficient (Pa sn); n = flow behavior index; do = yield stress (Pa). 2.2.6. Dynamic oscillatory analysis Starch or mixtures (114 mg, db) (ferulic acid was at 5–40%, w/ w) was mixed with 0.4 mL of water before being loading onto rheometer as described above. Sample was conditioned at 25 °C for 1 min. At the strain of 2% (within the linear viscoelastic range) and frequency of 1 Hz, sample was equilibrated at 25 °C for 1 min and the temperature was ramped from 25 °C to 95 °C and to 25 °C again at a rate of 3 °C/min. The resulting gel was equilibrated at 25 °C for 1 min and then a frequency sweep was conducted from 0.1 Hz to 20 Hz. Storage modulus (G0 ) and loss modulus (G00 ) were recorded. 2.2.7. Gel texture analysis Starch or mixtures (1 g, db) (ferulic acid was at 5–20%, w/w) was mixed with 5 mL of water in screw capped tubes. The tubes were placed in water bath (95 °C) and incubated for 10 min. Then, the tubes were kept in a refrigerator at 4 °C for 24 h before texture profile analysis with a TA.XTPlus Texture Analyzer (Stable Micro Systems, Surrey, UK). Gel was compressed twice to a distance of 10.0 mm. A cylindrical probe with a diameter of 5 mm and a test speed of 0.5 mm/s were used. Hardness, adhesiveness, cohesiveness, and springiness were recorded. 2.2.8. Enzyme hydrolysis Enzyme susceptibility of starch was analyzed by using a-amylase of B. subtilis in 2.9 M sodium chloride solution which contained calcium chloride (3 mM) as described previously (Varatharajan et al., 2011). Substrate solutions were prepared with 180 mg of starch (db), 45 mL of water, and 36 mL of phosphate buffer with 0.0006 M NaCl (pH 6.9). The starch weight was kept constant, therefore, when the ferulic acid was added, the total weight increased (ferulic acid concentrations were 5 and 20%, w/w). Substrate slurry was pre-warmed for 30 min at 37 °C and gently vortexed before adding 9 mL of the enzyme suspension (3 units of enzyme per 1 mg of starch). 1 mL of samples was taken after 1, 3, 6, 10, 24, 33, 50, 56 and 72 h of incubation at 37 °C. The carbohydrate content in the supernatant was analyzed by phenol– sulfuric acid-based method (Dubois, Gilles, Hamilton, Rebers, & Smith, 1956). Briefly, an aliquot of supernatant was mixed with phenol solution (5%) and sulfuric acid. The absorbance of the resulting solution was measured at 490 nm for the calculation of carbohydrate content. 2.2.9. V-type inclusion complex formation? To test if any inclusion complex of Gelose 80 maize starch and ferulic acid might be formed, two methods were used as described previously (Lesmes et al., 2009). Starch (6 g) was dissolved in 600 mL of 0.05 N KOH at 90 °C. Ferulic acid (600 mg) solubilized in methanol (400 mL) was added at 30 °C. The pH was adjusted to 4.7 by adding H3PO4 (2%) and the sample was held for 24 h with gentle stirring for precipitation. Solids were recovered by centrifugation at 20,000
g for 25 min at 4 °C. The resulting samples were washed with methanol (100 mL) 5 times before freeze-drying. For the second method, starch (6 g) in 300 mL of deionized water was heated in a boiling water bath for 30 min with magnetic stirring. Samples were then autoclaved at 135 °C for 20 min. The resulting solution was immediately transferred to a pre-heated water bath at 95 °C with magnetic stirring (350 rpm). Ferulic acid in methanol solution (1.2 g/4.8 mL) was added to the starch system drop-wise. The solution was stirred for 10 min at 95 °C before slowly cooling to room temperature overnight. Precipitate was recovered by centrifugation at 7500
g for 30 min at 4 °C. The precipitate was washed with methanol 5 times before freeze-drying. The resulting

samples were subjected to DSC and wide-angle X-ray diffraction analysis as described previously (Zhu & Wang, 2013). 2.2.10. Data analysis All the tests were in triplicate. Statistical analysis was done by SPSS (version 19) (IBM Corporation, NY, USA). One-way ANOVA determined treatment effects. Duncan’s test was used for the post hoc tests. Statistical significance was based on a confidence limit of 95%. 3. Results and discussion 3.1. Particle size measurement Normal maize starch had a D[4,3] value of 15.2 lm, while that of ferulic acid was 17.7 lm. The similar size of the starch and ferulic acid suggests their mixtures may be well dispersed. However, the size distribution of the ferulic acid displayed a skewed distribution with the 50% median value of 2.9 lm (data not shown). This suggested that ferulic acid tended to aggregate in water, and may be expected to form aggregate in starch systems with changes in the inter-particle pore volume. 3.2. Swelling power and solubility Water solubility index and swelling power of maize starch and mixtures are presented in Table 1. There was a strong relationship between water solubility index of starch and ferulic acid concentration. At 20% ferulic acid concentration, water solubility index increased from 9.4% to 21.0%. Swelling power of starch also increased with increasing ferulic acid concentration. For example, swelling power increased from 13.2 to 16.9 at 20% concentration. The increase in swelling power and water solubility during heating can be attributed to the improved starch–water interactions (Rolée, Chiotelli, & Meste, 2002). The temperature (85 °C) used in the test assisted the interactions between starch and polyphenols (Wu, Lin, Chen, & Xiao, 2011). Furthermore, pH of the system was decreased by the addition of ferulic acid. 20% ferulic acid addition decreased the pH of the system by 2.9. Addition of ferulic acid in wheat starch slurry reduced the pH from 6.8 to 4.3 (Zhu, Cai, Sun, & Corke, 2008). Reducing pH from 7 to 4 increased the solubility of tigernut starch, while little affecting the swelling power (Builders, Mbah, Adama, & Audu, 2014). The influence of pH change as an individual factor on swelling and solubility of maize starch remains to the explored. The interactions between ferulic acid and starch can be hydrophobic, electrostatic, and ionic interactions, and it is also possible for the formation of hydrogen bonds between ferulic acid and starch (Bordenave et al., 2014). Another factor is that the solubilized ferulic acid may be counted in the weight (W1) for the calculation. In order to better understand these factors, the following experiments were conducted.

Table 1 Water solubility index and swelling power of maize starch in the presence of ferulic acid. Sample MS MS + 5% FA MS + 10% FA MS + 15% FA MS + 20% FA

Water solubility index (%) a

9.4 ± 0.5 12.2 ± 0.3b 15.3 ± 0.7c 18.2 ± 0.5d 21.0 ± 0.3e

Swelling power (g/g) 13.2 ± 0.7a 13.7 ± 0.5a 14.3 ± 0.2a 15.1 ± 0.2ab 16.9 ± 0.2b

MS, normal maize starch; FA, ferulic acid; values with the same letters in the same column do not differ significantly (p < 0.05).

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3.3. Gelatinisation Gelatinisation results of starch and mixtures by DSC are in Table 2 and Supplementary Fig. 2. Both To and Tc showed a significant decrease in the presence of ferulic acid, but it was independent of ferulic acid concentration. This suggests that the ferulic acid lowered the thermostability of the starch. The melting temperature of the least stable crystallites is represented by the To value, and the most stable crystallites by the Tc (Zhou, Baik, Wang, & Lim, 2010). Therefore, ferulic acid had an influence over the more stable crystallites as well as the less stable crystallites. Ferulic acid had no effect on the majority of the starch crystallites as the Tp values were unaffected (Zhou et al., 2010). Only 20% ferulic acid concentration (total solid basis) was substantial enough to have an influence on the DH (Table 2). There are three stages of gelatinisation. Firstly, the water gets absorbed and the starch granules get swollen. Then, more water gets absorbed and a rapid loss of birefringence occurs. Lastly, soluble portion of starch gets leached out of the system (French, 1973). As shown in the previous section, ferulic acid increased the swelling power and water solubility of starch. This agreed with the decrease in the gelatinisation temperatures (To and Tc) and DH by the addition of ferulic acid. Pure ferulic acid had a melting peak at around 110 °C in the presence of water (data not shown). The added ferulic acid at the concentrations under the experimental conditions in this study was partially solubilized (Mota et al., 2008). The solubilized ferulic acid (e.g., hydroxyl and carboxyl groups) may interact with starch components and water, decreasing the pH of the system and destabilising the starch granules. The insolubilized crystalline form of ferulic acid probably had little effect on the gelatinization behaviors. A previous study showed that rutin (quercetin-3-O-rutinoside) with low water solubility little affected the gelatinization properties of rice starches (Zhu & Wang, 2012). 3.4. Retrogradation Gelatinized starch and mixtures were stored at 4 °C for 21 days for retrogradation analyzed by DSC (Table 2). Compared with native starch, retrograded starch had lower transition temperature and DH because of the weaker starch crystallinity. Ferulic acid at higher concentrations inhibited the retrogradation of starch, resulting in retrograded starch with lower stability (lower melting temperatures) and less degree of order (lower DH). The sample with 20% ferulic acid did not show any thermal peak, indicating the complete inhibition of retrogradation. The influence of polyphenols on retrogradation depends on the types of the starch and polyphenol as well as their concentrations. Several studies demonstrated that polyphenols inhibited/retarded the retrogradation of starch (Wu, Chen, Li, & Li, 2009; Xiao et al., 2012; Zhu & Wang, 2012). For example, rutin at higher concentrations completely inhibited the retrogradation of rice starches differing in amylose contents (Zhu & Wang, 2012). Another study showed

that black tea extract reduced the retrogradation of rice starches, but had little effect on potato starch (Xiao et al., 2012). The solubilized ferulic acid interacted with starch biopolymer chains through hydrogen bonding, therefore, rendering the starch chains less chance to interact with themselves for re-ordering. Furthermore, the presence of insolubilized ferulic acid diluted the starch matrix, which also decreased the interactions among starch chains. These factors probably resulted in the reduced retrogradation. 3.5. Pasting Pasting profiles of starch and mixtures are in Fig. 1. When the concentration of ferulic acid increased from 0% (control) to 20%, the following changes were observed. The peak time reduced from 12 min to 11.25 min. The peak temperature decreased from 92.2 °C to 87.5 °C. The PV declined from 2.86 Pa s to 1.76 Pa s. There was a substantial decrease in the HPV from 1.50 Pa s to 0.42 Pa s. There was a significant decrease in these parameters with every 5% more of ferulic acid addition (p < 0.05). The FV decreased from 2.93 Pa s to 1.38 Pa s until 10% ferulic acid addition. Further addition of ferulic acid did not alter the FV significantly (p < 0.05). The SB was reduced from 1.42 Pa s to 0.79 Pa s when the ferulic acid concentration was increased to 10%, which indicates the lower rate of starch retrogradation and syneresis (Ragaee & Abdel-Aal, 2006). The pasting temperature did not show a significant change over the concentrations of ferulic acid. The ability of starch to form a viscous paste was reduced with increasing ferulic acid concentration. The solubilized ferulic acid may interact with starch polymer chains, and the solid ferulic acid crystals further diluted the starch matrix, making the starch interactions with each other less frequent. This might decrease the entanglement and formation of amylose double-helix junction zones, which decreased the viscosity of the paste during cooling (Chai, Wang, & Zhang, 2013). A major factor could be the reduced starch content by ferulic acid addition. Furthermore, ferulic acid addition decreased the pH of the system as discussed above. It was found that HPV and FV of wheat starch in the presence of phenolics were positively linked with the initial pH of the system before pasting (Zhu et al., 2008). The increasing temperature during pasting may further solubilize ferulic acid, reducing the pH more. When pH was reduced from 7 to 4, the pasting properties of rice starches (4 genotypes) were slightly altered, and different genotypes showed different susceptibility in pasting to pH alteration (Bao & Corke, 2002). Another study on tigernut starch reported that reducing pH from 7 to 4 little affected the pasting properties (Builders et al., 2014). The pH effect on pasting properties of maize starch remains to be studied. On the other hand, the addition of ferulic acid increased the solid content of the system during the pasting process due to the low solubility of ferulic acid (Mota et al., 2008). This may explain the effect on BD development. BD increased from 1.36 Pa s to 1.55 Pa s with 10% ferulic acid addition. A further increase of ferulic acid concentration reduced BD (p < 0.05).

Table 2 Thermal properties of maize starch in the presence of ferulic acid. Sample

Gelatinization To (°C)

MS MS + 5% FA MS + 10% FA MS + 15% FA MS + 20% FA

Retrogradation Tp (°C)

a

69.6 ± 0.2 68.5 ± 0.5b 68.5 ± 0.4b 68.1 ± 0.2b 68.4 ± 0.2b

DH (J/g)

Tc (°C) a

73.5 ± 0.3 72.8 ± 0.5a 72.4 ± 0.7a 72.1 ± 0.4a 72.2 ± 0.4a

a

78.1 ± 0.3 76.9 ± 0.4ab 76.7 ± 0.8b 76.6 ± 0.4b 76.1 ± 0.7b

To (°C) a

11.9 ± 1.0 10.9 ± 1.0a 10.1 ± 0.3a 10.4 ± 0.3a 8.5 ± 0.3b

Tp (°C) a

56.6 ± 0.2 55.4 ± 0.7ab 54.1 ± 0.4ab 53.4 ± 0.7b

DH (J/g)

Tc (°C) a

58.9 ± 0.7 59.9 ± 0.2a 57.9 ± 0.9a 56.7 ± 0.9a

a

65.6 ± 0.3 63.2 ± 0.3ab 63.2 ± 0.7ab 61.6 ± 0.6b

0.77 ± 0.1a 0.71 ± 0.3a 0.52 ± 0.2b 0.30 ± 0.1c

MS, normal maize starch; FA, ferulic acid; To, onset temperature; Tp, peak temperature; Tc, conclusion temperature; DH, enthalpy change; values with the same letters in the same column do not differ significantly (p < 0.05).

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Fig. 1. Pasting profiles of normal maize starch and ferulic acid mixtures. 0% is the control; 5%, sample containing 5% ferulic acid; 10%, sample containing 10% ferulic acid; 15%, sample containing 15% ferulic acid; 20%, sample containing 20% ferulic acid.

3.6. Steady shear analysis Steady flow characteristics of starch in the presence of ferulic acid at various concentrations are presented (Supplementary Fig. 3). The flow curves of all the samples displayed a pseudoplastic, shear-thinning behavior. The consistency coefficient (k), flow behavior index (n), and yield stress (do), along with the coefficient of determination (R2) for each upward (from low shear rate to high shear rate) or downward (from high shear rate to low shear rate) flow curves for different samples are summarized in the Table 3. Between Herschel–Bulkley and power law models, the former produced a better fit for all the samples with higher R2 (0.999 or higher). The do of the samples showed an increase with the addition of ferulic acid. The downward curve (shear rate decreasing to zero) also had a similar pattern. Higher do of gels with ferulic acid than the control might be attributed to the increased solid component of the sample. The k values increased before decreasing, while the n values decreased before increasing, with increasing ferulic acid addition from 10% to 40%. Both upward and downward curves showed similar patterns. This may suggest that the addition of ferulic acid at 10%

supported the structuring of the starch system. Further addition of ferulic acid may tend to dilute the starch gel matrix, weakening the structure, though more solids were present. The role of ferulic acid in rheological properties of maize starch was further explored by dynamic oscillatory analysis below. 3.7. Dynamic oscillatory analysis Dynamic oscillatory analysis offers information about the elastic and viscous behaviors of starch system (Table 4 and Supplementary Fig. 4). For controlled heating, until the TG0 max was reached, the G0 and G00 moduli increased. This is due to the swelling of the starch granules and the leaching of amylose chains from the granules, forming 3-dimentional gel networks (Correia, Nunes, & Beirao-Da-Costa, 2012; Kong, Kasapis, Bertoft, & Corke, 2010). Ferulic acid not only increased the maximum G0 , but also assisted in reaching it faster as indicated by the decreased TG0 max values. When the starch granule swells, it can form composite networks with ferulic acid. Considering the particle sizes of ferulic acid (Section 3.1) and swollen starch granules (up to several times of the volume of the original granules), the former might support the

Table 3 Power law and Herschel–Bulkley models for steady shear properties of starch and starch–ferulic acid mixtures. Sample

MS MS + FA MS + FA MS + FA MS + FA MS MS + FA MS + FA MS + FA MS + FA

Power law

Herschel–Bulkley

k

n

R2

do (Pa)

k

n

R2

10% 20% 30% 40%

Upward 0.117 ± 0.038a 0.519 ± 0.093b 0.754 ± 0.038c 0.895 ± 0.034c 0.427 ± 0.096b

0.884 ± 0.017a 0.731 ± 0.016b 0.668 ± 0.012c 0.637 ± 0.012c 0.733 ± 0.028b

0.998 0.998 0.998 0.996 0.998

0.155 ± 0.021a 2.476 ± 0.501b 2.896 ± 0.368b 4.619 ± 0.486c 3.008 ± 0.742b

0.111 ± 0.013a 0.347 ± 0.106bc 0.481 ± 0.083d 0.418 ± 0.068cd 0.226 ± 0.046ab

0.890 ± 0.009a 0.789 ± 0.032b 0.731 ± 0.030c 0.742 ± 0.027c 0.820 ± 0.025b

0.998 0.999 1.000 0.999 0.999

10% 20% 30% 40%

Downward 0.107 ± 0.039a 0.427 ± 0.005b 0.321 ± 0.027c 0.236 ± 0.011d 0.171 ± 0.017e

0.897 ± 0.013a 0.758 ± 0.016b 0.794 ± 0.017c 0.834 ± 0.002d 0.866 ± 0.013e

0.998 0.998 0.998 0.998 0.998

0.209 ± 0.021a 3.181 ± 0.344b 3.000 ± 0.176b 2.617 ± 0.416bc 2.271 ± 0.231c

0.100 ± 0.031a 0.240 ± 0.006b 0.175 ± 0.009c 0.133 ± 0.004d 0.095 ± 0.015a

0.906 ± 0.016ab 0.838 ± 0.020c 0.879 ± 0.013a 0.915 ± 0.008b 0.949 ± 0.219d

0.998 0.999 0.999 0.999 0.999

MS, normal maize starch; FA, ferulic acid; data was model with power law and Herschel–Bulkley equations; upward, shear rate from 0.1 s1 to 800 s1; downward, shear rate from 800 s1 to 0.1 s1; k, consistency coefficient (Pa sn); n, flow index; do, yield stress; R2, coefficient of determination; values with the same letters in the same column do not differ significantly (p < 0.05).

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R. Karunaratne, F. Zhu / Food Chemistry 199 (2016) 372–379 Table 4 Dynamic rheological properties of maize starch in the presence of ferulic acid. Sample

Heating

Cooling 0

TG max

G max

0

MS MS + FA MS + FA MS + FA MS + FA

a

10% 20% 30% 40%

78.0 ± 0.0 76.5 ± 0.2b 76.0 ± 0.2c 76.0 ± 0.3c 76.0 ± 0.0c

0

tan dG max

G 95C

0

a

a

3996 ± 38 4693 ± 25b 4997 ± 58c 5769 ± 3d 6123 ± 2e

0.117 ± 0.002 0.127 ± 0.002b 0.139 ± 0.005c 0.148 ± 0.003d 0.153 ± 0.002e

tan d95C a

1320 ± 9 591 ± 20b 405 ± 5c 378 ± 6c 370 ± 3c

Frequency sweep

0

G 25C a

0.098 ± 0.004 0.142 ± 0.003b 0.156 ± 0.003c 0.170 ± 0.002d 0.178 ± 0.001e

tan d25C a

5560 ± 9 7560 ± 4b 6303 ± 2a 5630 ± 47a 4033 ± 42c

a

0.029 ± 0.003 0.091 ± 0.008ab 0.104 ± 0.002b 0.090 ± 0.001ab 0.057 ± 0.001a

G0 20Hz

tan d20Hz

6147 ± 23ab 8390 ± 4c 7267 ± 38bc 6867 ± 5bc 5173 ± 9a

0.067 ± 0.003a 0.153 ± 0.009b 0.167 ± 0.009b 0.155 ± 0.004b 0.125 ± 0.009a

MS, normal maize starch; FA, ferulic acid; units for T and G0 are °C and Pa, respectively; TG0 max, the temperature when storage modulus reaches the maximum during heating; G0 max, maximum storage modulus during heating; tan dG0 max, loss tangent at G0 max during heating; G0 95C, storage modulus at 95 °C during heating; tan d95C, loss tangent at 95 °C during heating; G0 25C, storage modulus at 25 °C (after cooling); tan d25C, loss tangent at 25 °C (after cooling); G0 20Hz, storage modulus at 20 Hz during frequency sweep; tan d20Hz, loss tangent at 20 Hz during frequency sweep; values with the same letters in the same column do not differ significantly (p < 0.05).

the internal bonds are within the gel. Only at 20% ferulic acid addition, the cohesiveness was significantly lower than the control. Gels with higher springiness values promote a ‘‘rubbery” feeling in the mouth and the springiness values decreased with increasing ferulic acid concentration (Everard et al., 2007). Textural properties of starch gels are affected by the volume fraction of the granule, rheological characteristics of the amylose matrix, rigidity of the gelatinized starch, and the interactions between dispersed and continuous phases of the gel (Biliaderis, 1998). After the gel formation, ferulic acid was dispersed in the continuous phase of the gel. The presence of ferulic acid and altered pH of the system reduced the interactions between gelatinized starch chains, especially the formation of the amylose matrix which is most responsible for the initial retrogradation of starch and firming of gel.

partially disintegrated starch granules with some of them filling up the gaps and spaces between the swelling granules. Further heating resulted in extended granule rupture and disintegration of starch, as well as complete melting of the crystallites and weakening of inter-chain interactions (Kong et al., 2010). Addition of ferulic acid decreased the G0 towards 95 °C. Most of the ferulic acids at 95 °C is crystalline, and thus are not involved in matrix formation through hydrogen bonding. Therefore, the ferulic acid may dilute the melted starch matrix and contribute to a faster structural breakdown. G0 of the starch system increased during the controlled cooling. This is due to re-alignment and re-association of starch chains for gelling. Down to 45 °C, addition of ferulic acid most decreased G0 of the gel. At 25 °C, sample with 10% ferulic acid had the highest G0 compared to the rest. Lower concentrations of ferulic acid provided a more elastic gel, compared to the control. Frequency sweep performed from 0.1 Hz to 20 Hz was used to provide further insights on the viscoelastic nature of gels (Kong et al., 2010). At 10% ferulic acid addition, the gel had the highest G0 . G0 decreased with the further addition of ferulic acid. With 40% concentration of ferulic acid, the G0 became lower than that of the control. It was also apparent that gels with ferulic acid were more susceptible to frequency sweep. The presence of ferulic acid solids diluted the starch gel, causing structural defects in the gel. The solubilized ferulic acid may only interact with the amylose and possibly the linear fragment of the amylopectins present in the starch (Chai et al., 2013). The influence of solubilized ferulic acid on starch rheology remains to be separated from that of the solid form.

3.9. Enzymatic hydrolysis Two concentrations (5% and 20%) of ferulic acid were selected to study the impact on the enzymatic hydrolysis of raw maize starch at 37 °C up to 72 h. There was no significant difference between the control and samples containing 5% and 20% ferulic acid at any given time interval (Supplementary Table 1). This may be due to the low solubility of ferulic acid at 37 °C. Nevertheless, it was shown that ferulic acid could efficiently promote insulin secretion, regulating starch metabolism in vivo (Hanhineva et al., 2010; Jung, Kim, Hwang, & Ha, 2007). For example, instead of interacting with starch degradation enzymes, ferulic acid enhanced glucokinase activity and glycogen production in the liver, therefore regulating blood glucose levels in C57BL/KsJ-db/db mice (Jung et al., 2007). This indicates that in vitro studies may not be relevant to in vivo practice. Therefore, it appears rational to use ferulic acid as a functional ingredient to develop nutraceuticals with desired properties of carbohydrate metabolism.

3.8. Gel texture analysis Starch gels were subjected to texture profile analysis after 24 h storage at 4 °C (Table 5). All the values showed a decrease with increasing ferulic acid content, indicating ferulic acid can be used to produce softer starch gels. Adhesiveness is the force required to overcome the attractive forces between the gel surface and the probe surface (Wu, Morris, & Murphy, 2014). The lower adhesiveness achieved with the presence of ferulic acid is beneficial in commercial applications as gels getting adhered to the lips, teeth, or the palate can be undesirable. Cohesiveness denotes how strong

3.10. Inclusion complex formation? The non-covalent interactions between starch and phenolic compound can be either through V-type amylose inclusion complex formation, or through the non-inclusive complex with much weaker binding forces (e.g., hydrogen bonding) (Zhu, 2015). To

Table 5 Gel textural properties of maize starch in the presence of ferulic acid. Sample MS MS + 5% FA MS + 10% FA MS + 15% FA MS + 20% FA

Hardness (g) a

151.4 ± 6.2 87.3 ± 6.7ab 79.5 ± 1.8ab 64.5 ± 4.0ab 40.1 ± 3.0b

Adhesiveness (g s) a

257.3 ± 2.5 224.8 ± 6.3ab 220.1 ± 8.7ab 178.1 ± 8.8ab 87.5 ± 6.4b

Cohesiveness

Springiness a

0.560 ± 0.017 0.468 ± 0.093ab 0.449 ± 0.096ab 0.442 ± 0.079ab 0.407 ± 0.053b

1.018 ± 0.308a 0.980 ± 0.006b 0.972 ± 0.007b 0.967 ± 0.007b 0.962 ± 0.010b

MS, normal maize starch; FA, ferulic acid; gel textural properties were obtained from texture profile analysis (TPA); values with the same letters in the same column do not differ significantly (p < 0.05).

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reveal the nature of the interactions between maize starch and ferulic acid, formation of the inclusion complexes were tested. V-type amylose inclusion complex formation from amylopectin is extremely low due to the limited number of long external branches that can form helices (Conde-Petit, Escher & Nuessli, 2006). Therefore, high amylose maize starch (Gelose 80) was chosen to increase the likelihood of inclusion complex formation. Two types of methods (co-precipitation of over-heated system and acidification of alkaline solution) have been widely used to prepare V-type amylose inclusion complexes with small guest molecules (CondePetit et al., 2006; Zhu, 2015). They were employed to test if inclusion complex could be formed between maize amylose and ferulic acid. The results showed that no inclusion complexes were formed by both methods as measured by DSC (no endo-thermal peaks) and wide-angle X-ray diffraction (Supplementary Fig. 5 shows the samples from the co-precipitation method). The size of the cavity of the helix is limited (Obiro et al., 2012). The aggregate formation of ferulic acid may have reduced the interaction. The low solubility of the ferulic acid may have also played a role in reducing the interaction between starch and ferulic acid. Furthermore, ferulic acid may be not hydrophobic enough to the cavity of amylose helixes. It is likely that molecular interactions between solubilized ferulic acid and starch chains were most of the hydrogen-bondingtype. The complexes might be non-inclusive, as suggested previously for the self-assembled amylose–tea polyphenol complexes (Chai et al., 2013). The nature of the molecular interactions between ferulic acid and starch chains, especially amylose, remains to be better understood. Understanding this type of non-covalent interactions should also be extended to include other types of starches as well as phenolic compounds (Zhu, 2015). 4. Conclusions Addition of ferulic acid significantly affected diverse physicochemical properties of maize starch. The water solubility index of starch appeared to be more dependent on ferulic acid concentration than did swelling power. The To, Tp, Tc, and DH of gelatinization were decreased by the addition of ferulic acid. Ferulic acid decreased the retrogradation of starch by reducing the melting temperatures and DH. PV, HPV, BD, FV, and SB were altered by the presence of ferulic acid, and the pasting temperature was unaffected. Herschel–Bulkley equation well fit the flow curves of starch mixtures, and all the samples displayed a pseudoplastic, shearthinning behavior. The k and do values of both upward and downward curves increased before dropping with the increasing ferulic acid concentration. Dynamic oscillation analysis indicated that increasing ferulic acid content resulted in a structurally unstable gel. The addition of ferulic acid to starch reduced the hardness, adhesiveness, cohesiveness, and springiness of the gel. Ferulic acid had little effect on the enzymatic hydrolysis of starch granules by a-amylase. V-type inclusion complex between maize starch and ferulic acid was not formed by co-precipitation of over-heated system and acidification of alkaline solution methods. Appendix. A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foodchem.2015. 12.033. References Bao, J. S., & Corke, H. (2002). Pasting properties of c-irradiated rice starches as affected by pH. Journal of Agricultural and Food Chemistry, 50, 336–341.

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