Hydrothermal and biocatalytic processes on native cassava flours: behavior of the physicochemical, morphological and pasting properties

Abstract

Dual-modification processing was proposed to alter the structural characteristics and improve the physicochemical and techno-functional properties of native cassava flours. This study aimed to evaluate the effect of hydrothermal and biocatalytic processes on the structural and morphological response of native cassava flour, as well as their effect on the behavior of physicochemical, gelatinization, and pasting characteristics. Native cassava flour was modified by hydrothermal processes of heat-moisture treatment (HMT) or annealing (ANN), or combined treatments of hydrothermal modification followed by a debranching enzyme with pullulanase (ANN-P and HMT-P). The results showed that HMT-P (heat-moisture treatment with pullulanase) and ANN-P (annealing with pullulanase) hydrothermal treatments increased the starch and amylose content in the modified flours. Compared with the ANN treatment, HMT produced changes at the morphological level such as fragmented granules or lacerations on the granular surface and reduced paste viscosity. In turn, both ANN and HMT increased the gelatinization properties, with the peak gelatinization temperature reaching values of 82.04 °C and 84.08 °C, respectively. The decrease in the 1047/1022 cm⁻¹ (OM₁) ratio and the increase in the relative crystallinity (RC) indicated that the hydrothermal and biocatalytic treatments altered the semicrystalline order of the modified cassava flours. Treatments HMT and HMT-P (dual modification with pullulanase) improved hydrophilic properties such as water absorption capacity (WAC) and cold-water solubility (CWS) and reduced setback viscosity; therefore, these processing technologies are feasible in the development of modified flours with better capacity for gel formation and reduction of the retrogradation phenomenon.

Keywords:
Annealing; Debranching; Heat-moisture; Modified flour; Biocatalytic; Pullulanase

HIGHLIGHTS

The heat-moisture treatment (HMT) and annealing (ANN) had a significant effect on the semicrystalline order of the cassava flour

The heat-moisture treatment promoted significant changes in cassava flour pasting properties

The dual modification with pullulanase produced notable changes in the hydrophilic properties of the cassava flour

1 Introduction

Cassava (Manihot esculenta Crantz) is considered a crop of socioeconomic importance in food security policies in Latin America, where around 300 million tons are produced. In Colombia, more than 2.5 million tons are grown, distributed throughout the national territory (Organización de las Naciones Unidas para la Alimentación y la Agricultura, 2022), especially in the Caribbean region where the department of Sucre occupies third place nationwide with a production of 229,399 t for the year 2021(Ministerio de Agricultura y Desarrollo Rural, 2021). It is a staple food crop as a carbohydrate source for more than 500 million people and provides a significant economic livelihood for many farmers, processors, and traders (Chimphepo et al., 2021). The edible part of the tuber contains 32% to 35% carbohydrates, 2% to 3% protein, 0.1% fat, 2.0% fiber, and 0.70% to 2.50% ash (Adesina & Bolaji, 2013; Charoenkul et al., 2011). However, cassava is a highly perishable product due to its high moisture content, which ranges from 75% to 80% w/w. In Colombia, there are few agro-industrialization processes for cassava crops; only 30% is used in the production of native starch and more than 60% is used for human consumption in different presentations (Adesina & Bolaji, 2013). For this reason, there is an urgent need to promote the production of native flours from unconventional sources of high local production and, in turn, promote a reduction in the importation of wheat flour that affects the local economy of a large agri-food sector.

Native cassava flours are composed of starch as the main starchy constituent and non-starch macromolecules for instance fiber, sugars, proteins, lipids, vitamins, and minerals, except for its moisture content (Charoenkul et al., 2011). Native cassava flours have a mild flavor and excellent thickening and gelling attributes; in addition, they have great potential for industrial applications in the preparation of baked and extruded products such as cakes, biscuits, cookies, noodles, macaroni, etc. (Salcedo Mendoza et al., 2017). However, the starch matrix in flour exhibits a weak structure that is unable to effectively trap gas during baking, causing products with structural defects. In turn, native cassava flours exhibit insolubility in cold water, low water retention capacity, and susceptibility to retrogradation, which lead to undesirable changes in the texture of foods (Adesina & Bolaji, 2013; Dudu et al., 2019). In this sense, hydrothermal and biocatalytic modification of the constituent starches of flours has improved their physicochemical and techno-functional potential, increasing their versatility as an ingredient in a wide range of agri-food applications.

Physical and enzymatic modifications, both individually and in combination, can lead to structural and morphological changes in starch that are closely related to the length of the polymeric chains and granular size, which define the behavior of the physicochemical, pasting and gelatinization properties (Pratiwi et al., 2018). Heat and moisture treatment (HMT) is a non-destructive process for the granular structure of starch that is performed above the gelatinization temperature at a restricted moisture content (10% to 30% w/w), but is capable of altering its semicrystalline order, hydrophilic properties, and gelatinization behavior. The production process of starch modified with HMT is easy and can be applied in flours, with a high potential to be carried out on a large scale (Holilah et al., 2021). Several studies have shown the influence of HMT on the physicochemical, structural, and morphological properties of sorghum, wheat, plantain, rice, oat, and yam flours, mainly in the reduction of swelling capacity, solubility and increase in relative crystallinity and gelatinization temperatures (Holilah et al., 2021; Cham & Suwannaporn, 2010; Sun et al., 2014; Bian & Chung, 2016; Xiao et al., 2017; Chávez et al., 2018; Kaur & Singh, 2019; Yu et al., 2021).

Hydrothermal processing of starchy materials by annealing (ANN) is carried out in excess water with a moisture content of 40–60% w/w, under thermal conditions between the glass transition temperature and the gelatinization temperature (Iuga & Mironeasa, 2020). Several studies have confirmed the influence of ANN on various properties of corn, wheat, yam, banana, and rice flours, for example, the fractions of resistant and slowly digestible starch viscosity of the paste, and gelatinization behavior (Yu et al., 2021; Zeng et al., 2015; Cahyana et al., 2019). Similarly, it promotes changes in amylose content, endothermic enthalpy, crystallinity, swelling power, and solubility of the flours (Yu et al., 2021; Iuga & Mironeasa, 2020; Puelles-Román et al., 2021; Vela et al., 2021). Another technological advantage of hydrothermal treatments is that they do not require chemicals, are considered safe, and have gained greater acceptance in food applications.

Debranching is considered a structural modification of starch granules that consists of the breaking of α-(1,6) glycosidic bonds of the branched chains, using enzymatic polypeptides such as pullulanase and isoamylase, altering the molecular order due to redistribution of the polymeric chains in the amylopectin cluster (Li et al., 2017b; Ge et al., 2021). Starches debranched with pullulanase are characterized by having shorter branched chain lengths, altering the semicrystalline order and, therefore, the degree of crystallinity (Li et al., 2017b; Li et al., 2019; Liu et al., 2017). Li et al. (2017b), reported that debranching affects the swelling power of starch granules by altering the behavior of their pasting and gelatinization properties. In addition, the short chains in debranched starchy materials have a higher molecular mobility that, when in contact with water molecules, affects the hydrophilic properties and the retrogradation phenomenon (Liu et al., 2015; Babu & Parimalavalli, 2018). However, there is a lack of information on the determination of the effect of debranching on the structural and physicochemical properties of native tubers.

Concerning dual-modification processing in flour native tubers, there is very limited scientific literature. Some studies have focused on the enzymatic application of pullulanase in gelatinized flours for the production of resistant rice, wheat, and banana flours (Jafari et al., 2017; Chen et al., 2020; Das et al., 2022). However, the scientific gap in the implementation of hydrothermal processes on cassava native flours is notorious. Additionally, insufficient applied research that involves the adaptation of enzymatic processes under sub-gelatinization conditions in granules previously treated by HMT and ANN has been conducted. It is therefore considered that modification by HMT and ANN followed by enzymatic processing with pullulanase on native cassava flours will have an impact on their physicochemical, morphological, structural, and pasting properties. Consequently, the present study aims to evaluate the effect of dual-modification processes combining hydrothermal treatments followed by debranching with pullulanase on the physicochemical, morphological, structural, and pasting properties of native cassava flours.

2. Materials and methods

2.1 Materials

Cassava (Manihot esculenta cv. Venezolana) tubers were supplied by the National Association of Cassava Producers and Processors (ANPPY) located in the municipality of Corozal, Sucre (Colombia). Enzyme polypeptides such as pullulanase from Bacillus licheniformis (Optimax® L-1000, China) and amyloglucosidase from Aspergillus niger (Dextrozyme® GA, Denmark) were donated by Dupont® and Novozymes®, respectively. Potato amylose (A0512, USA) and corn amylopectin (10120, USA) standards were purchased from Sigma-Aldrich®.

2.2 Obtaining native cassava flour

Native cassava flour was obtained following the method proposed by Charles et al. (2007) with some modifications. The tubers were washed, disinfected, peeled, and cut into homogeneous slices between 1 and 2 mm thick. Then, the processed samples were dehydrated in a tray dryer (TD-S/EV, Veneta, Italy) at a temperature of 50 °C and an air speed of 1.8 m/s until reaching a moisture content of 10–11% (w/w). The starchy material obtained was macerated and sieved through a No. 100 mesh (~150 µm). Finally, the native flours were packed in hermetic aluminum bags and stored under refrigeration at 5 °C.

2.3 Proximal analysis of native cassava flour

The following was determined from native cassava flour (HNY) samples: moisture content (AOAC 964.22/90), crude protein by the Kjeldahl method with nitrogen to protein conversion factor of 6,25 (AOAC 955.04/90), ash by the gravimetric method (AOAC 923.03/90), fat by the Soxhlet extraction method (AOAC 920.39/90) and crude fiber (AOAC 985.29/90). Total carbohydrate content was determined by difference (Association of Oficial Analytical Chemists International, 1990).

2.4 Modification of native cassava flour

The native cassava flours were physically modified using HMT, ANN, and dual modification (hydrothermal treatment followed by enzymatic hydrolysis), as described below:

• Heat-moisture treatment (HMT): The native flours were modified by hydrothermal route following the method proposed by Yu et al. (2021) with slight modifications. Initially, 20 g flour samples were hydrated to a moisture content of 25% (w/w), and then stored in airtight containers at a temperature of 6 °C for 24 h for homogenization. Subsequently, the hydrated samples were subjected to hydrothermal treatment at 90 °C for 6 h in a forced convection oven (FD115, BINDER, Germany).

• Annealing (ANN): Native cassava flours were modified by ANN following the methodology proposed by Yue Li et al. (2018) with some modifications. Initially, flour suspensions at 20% w/v were hydrated for 24 h and stored under refrigeration at 6 °C. Then, the suspensions were subjected to a heating process at 60 °C in a thermal bath (MAXIRCUCL-12, Daihan Scientific, Korea) with constant agitation for 6 h. After heating, the suspensions were cooled to room temperature, to then separate the starchy material by centrifugation at 5000 rpm for 5 min.

• Dual modification: Cassava flour hydrothermally treated by HMT and/or ANN was suspended in a 0.1 M sodium citrate buffer solution (pH = 5.0) and hydrolyzed using pullulanase with a biocatalytic activity of 20 U/mg. The enzymatic process was carried out at 60 °C with constant stirring at 450 rpm, for 6 h (Figueroa-Flórez et al., 2019). To remove residual enzyme activity, the hydrolyzed flour suspensions were washed with ethyl alcohol (60% w/v, food grade), followed by water washes. In the end, the starchy material was separated by centrifugation at 5000 rpm for 5 min.

After the modification, the flours were subjected to a drying process in a convective oven at 40 °C (UFB500, Memmert, Germany) until the moisture of 10% to 12% w/w was achieved. Then they were macerated and sieved in a No. 100 mesh (~150 µm). Finally, the modified flours were deposited in hermetic aluminum bags and stored until their subsequent characterization.

2.5 Starch and amylose content

Starch content was determined by the enzymatic method from total amylolysis with suspensions of α-amylase (10 U/mg) and amyloglucosidase (15 U/mg) (Rodríguez-Damian et al., 2013). For the quantification of total glucose, the DNS method (3,5-dinitrosalicylic acid) was used using an Ultraviolet-visible (UV-Vis) spectrophotometer (Pharo300, Merk, Germany) at 540 nm. The amylose content was determined by iodine adsorption spectrophotometry (Figueroa Flórez, 2021) with the following modification: flour samples were dissolved/defatted in a 95% dimethyl sulfoxide (DMSO) solution and subsequently precipitated in 90% methanol. The sample was reacted with I₂/KI solution for 10 min. Then, from a calibration curve of standard solutions of potato amylose and corn amylopectin under concentrations of 0 to 100% w/w, the absorbance value of the amylose/iodine colorimetric reaction at 620 nm was determined.

2.6 Attenuated total reflectance infrared spectroscopy (FTIR-ATR)

Infrared spectra were obtained in the 500 to 4000 cm^-1 region by performing four reading scans at a resolution of 8 cm^-1 using a spectrometer with a single-bounce Attenuated Total Reflectance (ATR) accessory (UATR, PerkinElmer, USA) with a diamond crystal 1.5 mm in diameter. The absorbance ratios in the bands 1047/1022 and 995/1022 cm^-1 were determined to evaluate the degree of molecular order (Bian & Chung, 2016). Data were obtained using PerkinElmer Spectrum 6 software connected to a computer and normalized vectorially by dividing each spectrum by the standard deviation of its absorbance values, for further analysis (Standard Normal Variate (SNV) normalization) based on the methodology proposed by Warren et al. (2016).

2.7 Diffraction patterns and relative crystallinity (RC)

Diffraction patterns of native and modified cassava flours were obtained using a diffractometer (Panalytical, X'Pert MPD, Switzerland) operated at 1.8 kW and 40 mA. The relative crystallinity (RC) was determined as a function of the ratio between the crystalline peaks and the total area, taking as a reference a baseline between the angles 2θ = 5–35◦. The data were processed using Origin Lab software (OriginLab Corp., USA), following the methodology proposed by Figueroa-Flórez et al. (2023).

2.8 Morphological characteristics and birefringence

Initially, 1.0 mg of starch was mixed in 1 mL of distilled water to homogenize the sample. A 10 µL aliquot was poured onto a slide to examine the morphology and birefringence of the granules using a binocular microscope (C-B10, Optika, Italy). Photomicrographs were acquired under clear, polarized light fields at 40× magnification, using a digital camera (OptikamB10, Italy) (Ge et al., 2021).

2.9 Particle size

Particle size was determined by light scattering using a Mastersizer particle analyzer (Model 3000E, Malvern, UK). Measurements were made in triplicate at room temperature, with a refractive index value of 1.52 for flour (Dudu et al., 2019). The size of the particles was expressed as a function of the mean diameter d (0.5), which represents the granular size below 50% of the particle distribution.

2.10 Gelatinization properties

The thermal properties were determined using a rheometer (MCR 302, Anton Paar, Austria), through the geometry of parallel plates with a diameter of 25 mm and gap of 1.0 mm. Once the region of linear viscoelasticity (RVL) was defined, flour suspensions at 30% w/v were subjected to a temperature sweep between 30 and 90 °C keeping constant the frequency of 1.0 Hz and deformation of 0.5% (Pratiwi et al., 2018). During the process, the values of the modulus of elasticity (G′ [Pa]) and viscosity (G″ [Pa]) were obtained by data processing using RheoCompass software (v1.12, Anton Paar, Austria). The parameters recorded included estimated values of the onset temperatures (T_O), peak temperature (T_P), and final gelatinization temperature (T_C).

2.11 Physicochemical properties

Cold-water solubility (CWS) and swelling power (SP) were determined by adapting the method proposed by Chen et al. (2020). For SP, 0.5 g of sample was weighed, and added 12.5 ml of distilled water at 60 °C, the sample was kept in heating at 60°C for 30 min with shaking every 10 min and centrifuged at 3000 RCF for 15 min. The supernatant was dried in an oven at 70°C for 16 h and the final weight of the sample was recorded. For the CWS, flour samples were weighed maintaining a 1% w/v ratio, the sample was shaken for 5 min and centrifuged at 3402 RCF for 15 min, the supernatant was dried in an oven at 110°C for 4 h and the final weight of the sample was recorded. Finally, the water absorption capacity (WAC) was determined by weighing 0.5 g of sample in a tube and adding 5 ml of distilled water. The sample was centrifuged at 3402 RCF for 15 min, the supernatant was removed and the weight of the tube was recorded.

2.12 Pasting properties

A rheometer in rotational mode (MCR 302, Anton Paar, Austria) was used, according to the method described by Li et al. (2018) with slight modifications. Flour suspensions at 4% w/v were subjected to a temperature of 50 °C for 1.0 min, then raised to 95 °C for 7.5 min and maintained at 95 °C for 5 min, cooled to 50 °C in 7.5 min, and finally brought to 50 °C for 2 min. The spindle speed (ST24-2D/2V, Anton Paar, Austria) during the experiment was kept at 960 rpm. The different viscosity parameters were analyzed using RheoCompass software (v1.12, Anton Paar, Austria).

2.13 Experimental design

A categorical unifactorial design was established with four (4) levels corresponding to the type of modification and control treatment, as described in Table 1. The results were expressed as the mean of three replicates ± standard deviation, analyzed by analysis of variance (ANOVA) and Tukey’s test for differentiation of means at a significance level of 5%. Data were processed using Statgraphics statistical software (Centurion XVI, Statgraphics Inc., USA).

Table 1
Experimental design implemented in the modification of cassava flour.

Treatment	Enzyme [concentration, µL]	Nomenclature
Native cassava flour	-	HNY
Heat-moisture treatment (HMT)	-	HMT
Annealing treatment	-	ANN
Dual modification with pullulanase	Pullulanase [40]	HMT-P
Dual modification with pullulanase	Pullulanase [40]	ANN-P

3 Results and discussion

3.1 Proximal analysis of cassava flour

The proximal analysis of native cassava flour (HNY) showed moisture content, ash, crude protein, crude fat, and crude fiber of 10.56% ± 0.37%, 1.14% ± 0.14%, 1.60% ± 0.25%, 0.88% ± 0.14% and 9.41% ± 0.11%, respectively. These differ slightly from those for cassava flours obtained from other cultivars (Alamu et al., 2017; Charles et al., 2007; Afuakwa et al., 2006). These authors explain that these differences are associated with: (1) the variety and quality of native flour; (2) the age of the crop at the time of harvest, type of soil, climatic conditions, vegetative health of the tubers; and (3) the technology implemented in the extraction stage; however, they are within the permissible limits established in the legislation that regulates the production and commercialization of native cassava flour in Latin America (Organización de las Naciones Unidas para la Alimentación y la Agricultura, 2022).

3.2 Starch and amylose content

The starch content (SC) in the modified cassava flours varied with respect to the native flour (Table 2). The results indicated an increase of 2.53% and 6.67% in SC after the HMT and ANN modification processes (p < 0.05), respectively. Similar behavior has been reported by Afolabi et al. (2018) in modified bambara bean (Vigna subterranean (L.) Verdc) flours. In the results obtained the SC continued to increase in the modified cassava flours (between 4.63% and 8.94%) with the inclusion of enzymatic hydrolysis with pullulanase. This behavior can be associated with various phenomena such as (1) the leaching of water-soluble organic materials during the hydration phase of native flours; and (2) the melting of thermolabile non-starch components under the conditions of heating and granular swelling (Cahyana et al., 2019; Afolabi et al., 2018). Dang & Vasanthan, (2019) mentioned that water washing processes of rice bran allow concentration of the fractions of starch and insoluble dietary fiber. From the above, it can be inferred that the hydrothermal and enzymatic treatments – both individual and combined – carried out in an excess of water, favored the separation of water-soluble non-starch materials and the consequent increase in SC. This result is consistent with the increase in the proportion of starch granules and the decrease in non-starch fractions in the modified cassava flours analyzed by bright field microscopy.

Table 2
Amylose content, relative crystallinity, and molecular order.

Treatment	SC (%)	AM (%)	RC (%)	MO1	MO2	d(0.5) (µm)
HNY	76.66 ± 0.57e	17.58 ± 0.43c	44.17 ± 0.43e	0.75 ± 0.00a	1.13 ± 0.00b	16.50 ± 0.00c
HMT	78.65 ± 0.66d	14.32 ± 0.13e	44.67 ± 0.42c	0.73 ± 0.00b	1.18 ± 0.03a	19.80 ± 0.10b
ANN	82.14 ± 0.45b	16.55 ± 0.54d	46.36 ± 0.30a	0.64 ± 0.00c	1.19 ± 0.00a	20.40 ± 0.40a
HMT-P	80.38 ± 0.82c	20.49 ± 0.14b	44.51 ± 0.07d	0.70 ± 0.00d	1.19 ± 0.00a	19.83 ± 0.22a
ANN-P	84.19 ± 0.36a	21.97 ± 0.06a	45.29 ± 0.80b	0.69 ± 0.00e	1.22 ± 0.00a	20.17 ± 0.16a

• HNY: cassava flour; HMT: flour treated by heat and moisture; ANN: flour treated by annealing; HMT-P/ANN-P: dual modification with pullulanase; SC: starch content; AM: amylose content; RC: relative crystallinity; MO₁: molecular order based on the ratio 1047/1022 cm⁻¹; MO₂: molecular order based on the ratio 995/1022 cm⁻¹; d(0.5): average diameter of granules. Values followed by the same superscript letters within a column do not differ statistically (p > 0.05).

From Table 2 it can be observed that amylose content (AM) decreased by between 5.86% and 18.54% with the hydrothermal treatments (p < 0.05). Similar results were reported for both HMT-modified sorghum starches and flours at different moisture contents (Holilah et al., 2021). De La Rosa-Millán et al. (2015) reported similar results in plantain flours after modification by ANN. Changes in the AM of hydrothermally treated native cassava flours may be due to: (1) additional amylose–amylose and/or amylose–amylopectin chain interactions; and (2) an increased amount of complexation between amylose chains and lipid compounds (Holilah et al., 2021; Afolabi et al., 2018; Dang & Vasanthan, 2019). Franco et al. (1995) suggested that the intermolecular bonds between amylose and amylopectin molecules within the granules are stronger at high temperatures; this could explain the difference in AM between HMT and ANN. The enzymatic treatments with pullulanase possibly contributed to greater biocatalysis in the branched areas of the granule where amylopectin is concentrated, causing a significant increase in the AM in the granular structure, results that coincide with those reported in debranched potato starches and potato flours, and rice (Ge et al., 2021; Chen et al., 2020). Experimental tests showed that debranching with pullulanase contributes to the increase in AM, possibly due to the exclusion of short amylopectin chains and the consequent molecular freedom of long amylose chains to complex with iodine (Liu et al., 2017; Chen et al., 2020; Figueroa-Flórez et al., 2019).

3.3 Attenuated total reflectance infrared spectroscopy (FTIR-ATR)

FTIR-ATR spectra are useful for understanding the conformational changes of polymer chains and the semicrystalline order of macromolecules at a short-range level (Bian & Chung, 2016). Values of MO₁ and MO₂ are found in Table 2, and the spectra in the region of 4000 to 500 cm⁻¹ in the native and modified cassava flours are shown in Figure 1. The absorption bands in the range between 3000 and 3600 cm⁻¹ correspond to stretching of OH groups in the starch molecule, and the absorption peaks around 800–1500 cm⁻¹ indicate vibration of the glucose molecule, while the peaks at 862 and 929 cm⁻¹ correspond to vibration of the glucopyranose ring (Yang et al., 2022). The bands at 1083 and 1157 cm⁻¹ represent stretching of the CO bond, while the CC skeletal mode of the α-(1,4) glycosidic bond was characterized by bands at approximately 800–1000 cm⁻¹. In turn, the sharp peak at 1022 cm⁻¹ has been correlated to the stretching of the CO and COC groups in α-(1,6) glycosidic bonds (Figueroa-Flórez, 2021). Likewise, absorption bands were detected at 1640 cm⁻¹ related to α-helix protein structures, while the peak at 1620 cm⁻¹ is associated with β-sheet-type polypeptide conformations (Chávez et al., 2018; Vela et al., 2021). Similar FTIR-ATR spectra have been reported for native yam, rice, and wild potato flours (Bian & Chung, 2016; Yu et al., 2021; Akhila et al., 2022).

Figure 1
FTIR-ATR spectra for native and modified cassava flour. HNY: cassava flour; HMT: flour treated by heat and moisture; ANN: flour treated by annealing; HMT-P/ANN-P: dual modification with pullulanase.

After hydrothermal treatments and enzymatic hydrolysis, the cassava native flour presented a decrease in the peaks located in the absorption bands at 1640 and 1620 cm^-1, while the peaks of the bands at 862 and 929 cm^-1 presented an increase in the modified flours. This could be related to the increase of SC in the modified flours as described in Table 2. On the other hand, the absorption peak at 1047 cm-1 is associated with the crystalline zone, while the band at 1022 cm-1 is linked to the amorphous region (Xu et al., 2018). Therefore, the relationship between the absorption peaks at 1047, and 1022 cm^-1 and the band at 995 cm^-1 was used to estimate Molecular Order 1 and 2 by FTIR-ATR (Warren et al., 2016).

The results in Table 2 reveal that MO₁ decreased (p < 0.05) after the simple and dual-modification processes, a result that could be attributed to the dissociation and unfolding of the double helices that form the crystalline structure (Yang et al., 2022). The difference in molecular order in flours modified by HMT and ANN may be associated with the severity of heat treatment (Pratiwi et al., 2018). Similar results have been described in HMT-modified rice flours and ANN-pretreated corn starch (Bian & Chung, 2016; Chen et al., 2021). This result is also consistent with “Maltese cross” deformation and loss of birefringence analyzed by polarized light microscopy. Meanwhile, the MO₂ values (Table 2) increased in relation to native flour after the hydrothermal and biocatalytic modification processes (p < 0.05); however, there was no significant difference between the modification treatments (p > 0.05). This result could be attributed to conformational changes in the starch structure, possibly due to the breaking of α-(1,6) glycosidic bonds, the effect of the thermal process, and the hydrolytic action of pullulanase, a result similar to that reported in debranched cassava starches (Figueroa-Flórez, 2021).

3.4 Diffraction patterns and relative crystallinity (RC)

The crystallinity patterns of native and modified cassava flours are presented in Figure 2. In HNY samples, a type-A diffraction pattern was identified with four peaks under the angles 2θ = 15, 17, 18, and 23°, typical results of cassava starches acquiring the conformation of a monoclinic polymorphism. Likewise, a weak diffraction peak was observed around 20°, which may be associated with possible interactions of amylose and lipid compounds (Figueroa-Flórez et al., 2023). These crystalline patterns characteristic of native cassava flour were not altered by hydrothermal treatments and subsequent debranching with pullulanase. However, significant variations in the intensity of the peaks were evidenced, suggesting a rearrangement of the amylose-amylopectin and amylose-amylose interactions caused by the modifications, results that may be reflected in a possible increase in the relative crystallinity with respect to the control treatment (HNY), as described in Table 2. (Dudu et al., 2019; Yu et al., 2021; Puelles-Román et al., 2021).

Figure 2
Diffraction patterns of native and modified cassava flours. HNY: Cassava flour; HMT: HMT treated flour; ANN: Annealing treated flour; HMT-P/ANN-P: dual modification with pullulanase.

Hydrothermal treatments by HMT and ANN presented sharper peaks compared to the native counterpart, which suggests an improvement in the semi-crystalline order of the starches, results consistent with those obtained by Yu et al. (2021) and Figueroa-Flórez et al. (2023). Dudu et al. (2019), mentioned that the recrystallization of small crystalline regions and the development of new crystallites in the amorphous region could be related to the displacement of double helix chains during HMT treatment. On the other hand, the increase in the relative crystallinity of ANN-modified cassava flour could be attributed to the realignment of amylose-amylose or amylose-amylopectin linear chains, which affected its semicrystalline order. Similar results have been found in cassava, corn and wheat starch (Figueroa-Flórez et al., 2023; Tukomane et al., 2007; Zhang et al., 2012).

For their part, HMT-P and ANN-P treatments led to a significant increase in the intensities of diffraction peaks under the angles 2θ = 15, 17, 17, 18, 18, 20, and 23°, and relative crystallinity with respect to the native counterpart (See Table 2). These results were in agreement with those obtained on cereal flours and starches after pullulanase debranching (Liu et al., 2017; Li et al., 2019). The increase in crystallinity of the doubly modified flours may be related to the formation of short linear chains caused by the debranching action of pullulanase that could be arranged parallel to each other to form double helices (Li et al., 2017b). In this regard, Li et al. (2019), mentioned that the formation of double helices from short linear chains de-branched by pullulanase contributed to a more ordered crystal structure, which could favor the increase of the relative crystallinity of the doubly modified flours.

3.5 Morphological characteristics and particle size

Microphotographs of native cassava flours show spherical starch granules with the presence of blunt ends and an average granular size of 16.50 μm (Figure 3), results very similar to those reported by Charoenkul et al. (2011). The granules in the native flours presented a clear semicrystalline behavior supported by the formation of the “Maltese cross” form and birefringence capacity under polarized light (Figueroa-Flórez, 2021). In addition, native cassava granules are surrounded by non-starch components, which are mostly constituted of water-soluble, dietary fiber-type water-soluble organic material (Yu et al., 2021; Akhila et al., 2022).

Figure 3
Bright field (A), polarized light (B) and scanning electron (C) microscopy study in native and modified cassava flours. HNY: cassava flour; HMT: flour treated by heat and moisture; ANN: flour treated by annealing; HMT-P/ANN-P: dual modification with pullulanase.

The ANN treatment did not exert an effect on the morphology of the granules with respect to the native counterpart; this observation coincides with microscopic analyses carried out on flours modified by ANN (Cahyana et al., 2019). However, after HMT treatment, slight morphological changes such as fragmented granules or lacerations on the granule surface were observed, results similar to those reported in hydrothermally treated rice flours, associated with granular swelling and slight signs of pre-gelatinization (Xiao et al., 2017). In addition, there was an increase in the granular size (d(0.5)) of the constituent starches of the flours modified by ANN and HMT, which may be due to: (1) predominant granular swelling during the thermal effect of heating; (2) diffusion and adhesion of non-starch components to the surface of the granules; and (3) partial gelatinization and fragmented particle aggregation phenomena during hydrothermal treatments (Dudu et al., 2019; Xiao et al., 2017; Kaur & Singh, 2019; Yu et al., 2021; Iuga & Mironeasa, 2020; Puelles-Román et al., 2021). Additionally, “Maltese cross” deformation and a slight loss of the birefringence capacity of the starch granules were observed in the flours modified by HMT. According to Xiao et al. (2017), these changes can be associated with partial gelatinization of the granules and the consequent change in semicrystalline behavior, results consistent with the variations of molecular order and RC, determined by XRD.

According to the values given in Table 2, the debranching phenomena did not cause changes in the size of the starch granules (d (0.5)) present in the modified cassava flours, after the hydrothermal treatments (p > 0.05). Similar results have been reported in maize granules and cassava tubers hydrolyzed with pullulanase under sub-gelatinization conditions (Figueroa-Flórez, 2021; Li et al., 2017a). However, changes in the birefringence capacity were found under polarized light. The action of pullulanase on starch granules supposes an exogenous action, whose hydrolytic processes are systematic in the branching points of the amylopectin cluster, separating fragments of double helices that constitute the crystalline fraction (Figueroa-Flórez, 2021; Zhang et al., 2022). This result is consistent with the increase in AM in doubly modified flours.

3.6 Gelatinization properties

A dynamic oscillatory test (temperature sweep) was carried out on samples of native and modified cassava flours to understand the intermolecular interactions of the starchy material during the gelatinization phenomenon (Zhang et al., 2022). The results reveal that the elastic modulus (G′) predominated over the viscous modulus (G″), which could suggest that the starch gels in flour show an elastic structure (Figure 4) (Li et al., 2018). In addition, three phases in the viscoelastic behavior of the starch gels in flour were identified: (I) A first phase, in the temperature range of 20–60 °C, where the moduli G′ and G″ did not present an evident change; (II) a second phase of 68–86 °C characterized by a significant increase in viscoelastic moduli possibly associated with structural changes such as irreversible swelling of the granules, melting of crystallites or leaching of starchy components (Cham & Suwannaporn, 2010); and (III) a third phase where viscoelastic stability was exhibited at the end of the heating period. Similar results have been identified in native bean granules and hydrothermally modified rice flours (Cham & Suwannaporn, 2010; Chávez et al., 2018).

Figure 4
Viscoelastic properties of native and modified cassava flours. (A) Behavior of the elastic modulus (G′); (B) behavior of the viscous modulus (G″). HNY: cassava flour; HMT: flour treated by heat and moisture; ANN: flour treated by annealing; HMT-P/ANN-P: dual modification with pullulanase.

Li & Hamaker (2021) stated that the thermal effect of 20 °C to 90 °C treatment is capable of fusing short-range double helices formed between amylopectin/amylopectin or amylopectin/amylose complexes, defining the limits of the swelling and gelatinization processes granular. Based on the above, the onset temperature (T_O), peak temperature (T_P) and final gelatinization temperature (T_C) were estimated, through a rheological test supported by a temperature sweep within the region of viscoelasticity linear. The results reveal that the values of T_P are close and coincide with those estimated in native cassava flours by DSC (Dudu et al., 2019), which allows us to infer that the rheological test could be an effective method in determining gelatinization properties.

The gelatinization properties of the native starches showed significant changes after the modification processes (Table 3). It has been reported that hydrothermal modification by HMT and ANN promotes the stability of double helices through the realignment of linear amylopectin and amylose–amylopectin chains, decreasing the swelling capacity, which affects the glass transition phenomenon (Bian & Chung, 2016; Afolabi et al., 2018; Rocha et al., 2012). This could explain the increase in gelatinization temperatures (T_O, T_P, and T_C), whose results are analogous to those described in modified yam and buckwheat flours (Chávez et al., 2018; Yu et al., 2021). Also, the effect of debranching decreased gelatinization temperatures in cassava flours previously subjected to HMT. This variation is possibly due to the following factors: (1) changes in granular swelling capacity; (2) increased amylose content; (3) loss of birefringence capacity; and (4) decreased relative crystallinity (Li et al., 2019; Das et al., 2022). Some of these factors are consistent with the results found in the present investigation. In addition, among the results obtained the temperature range T_O–T_C was reduced with the implementation of the simple and dual modification, compared to the native HNY counterpart. This behavior could originate from morphological and structural changes exerted during the hydrothermal and enzymatic action on the starch granules, which define both their semicrystalline order and their thermal behavior. Likewise, it has been shown that the increase in gelatinization temperature is more pronounced for T_O (fusion of the weakest crystallites) and less for T_C (fusion of stable and perfect crystals).

Table 3
Gelatinization properties estimated by oscillatory temperature sweeps in modified cassava flours.

Treatment	HNY	HMT	ANN	HMT-P	ANN-P
Gelatinization properties
TO (°C)	68.83 ± 0.03c	80.01 ± 0.121a	79.00 ± 0.01b	78.99 ± 0.01b	78.99 ± 0.30b
TP (°C)	73.91 ± 0.09d	84.08 ± 0.50a	82.04 ± 0.10c	82.05 ± 0.20c	83.06 ± 0.21b
TC (°C)	79.00 ± 0.40c	87.12 ± 0.31a	87.12 ± 0.40a	85.12 ± 0.16b	87.14 ± 0.11a
TC − TO (°C)	10.17 ± 0.22a	7.11 ± 0.10c	8.13 ± 0.20b	7.12 ± 0.23c	8.15 ± 0.41b

• HNY: cassava flour; HMT: flour treated by heat and moisture; ANN: flour treated by annealing; HMT-P/ANN-P: dual modification with pullulanase; T_O: start temperature; T_P: peak gelatinization temperature; T_C: final temperature. Values followed by the same superscript letters in the same row do not differ statistically (p < 0.05).

3.7 Physicochemical and pasting properties

The physicochemical properties of native and modified cassava flours are shown in Table 4. The SP decreased in the modified flours. Zeng et al. (2015) reported a similar decrease in PS in hydrothermally treated waxy rice starch. The flours modified by HMT showed a lower PS than those treated by ANN, which could be due to a greater magnitude of the thermal effect, altering the mobility of the polymeric chains and amylose–amylose and amylose–amylopectin interactions (Yu et al., 2021). The decreased SP may depend on: (1) interactions of amylose and amylopectin; (2) arrangement of starch crystals; and (3) enhancement of protein–starch interaction during modification (Iuga & Mironeasa, 2020; Zeng et al., 2015; Ge et al., 2021; Perraulta-Lavanya et al., 2021). On the other hand, the debranching process increased the SP of the modified flours after the hydrothermal action. A similar result has been reported in sweet potato starches debranched with pullulanase (Ge et al., 2021). Sasaki & Matsuki, (1998) mentioned that the increase in AM is an important factor in SP variation; similar behavior was found in the present study.

Table 4
Physicochemical and pasting properties in native and modified flours.

Treatments	HNY	HMT	ANN	HMT-P	ANN-P
Physicochemical properties
SP (g/g)	2.87 ± 0.01b	2.22 ± 0.06d	2.73 ± 0.07c	2.39 ± 0.02dc	2.90 ± 0.02a
WAC (%)	106.37 ± 0.52e	108.37 ± 0.56d	112.49 ± 0.48c	127.00 ± 0.35a	119.57 ± 0.62b
CWS (%)	7.53 ± 0.18a	5.36 ± 0.27c	4.46 ± 0.03e	7.14 ± 0.25b	4.63 ± 0.10d
Pasting properties
TPT (°C)	71.07 ± 0.31e	82.20 ± 0.20a	81.20 ± 0.20c	80.60 ± 0.35d	81.40 ± 0.17b
VM (mPa.s)	1774.30 ± 0.61a	501.03 ± 0.60e	1715.17 ± 0.76b	1531.33 ± 0.58c	1524.67 ± 0.58d
VR (mPa.s)	950.33 ± 0.61a	354.57 ± 0.51d	151.10 ± 0.36e	615.77 ± 0.64b	613.23 ± 0.21c
VA (mPa.s)	621.30 ± 0.50b	118.67 ± 0.51d	854.93 ± 0.93a	586.27 ± 0.68c	622.23 ± 0.21b

• HNY: cassava flour; HMT: flour treated by heat and moisture; ANN: flour treated by annealing; HMT-P/ANN-P: dual modification with pullulanase; SP: swelling power; WAC: water absorption capacity; CWS: cold-water solubility; T_PT: pasting temperatures; V_M: maximum viscosity; V_R: breakdown; V_A: setback. Values followed by the same superscript letters within a row do not differ statistically (p < 0.05).

The WAC and CWS of the modified flours increased with respect to the native counterpart (HNY). HMT and ANN produced an increase in WAC (p < 0.05), possibly associated with the extension of the amorphous region resulting from the thermal effect during heating, interrupting the hydrogen bonds between amylose/amylopectin that affect the semicrystalline order (Sindhu et al., 2019). Similar results have been reported in sorghum meals treated by HMT Perraulta-Lavanya et al. (2021). In the same way, a significant increase of WAC was evidenced in the cassava flours after the debranching treatment (HMT-P and ANN-P), in comparison with the native flour (HNY). G. Liu et al. (2015) established that an increase in WAC after a debranching process may be due to: (1) decreased amylose content; (2) rearrangement of the semicrystalline order of the starch granule; and (3) greater molecular mobility due to reduced chain lengths. A similar behavior has been reported in debranched sweet potato starches (Babu & Parimalavalli, 2018). Meanwhile, the solubility represents the soluble amylose leached within the starch granule after heating (Chen et al., 2020); this could explain the decrease of CWS percentage in hydrothermally treated modified cassava flours. Similar results have been reported in modified yam and bambara bean (V. subterranean) flours (Yu et al., 2021; Afolabi et al., 2018). However, contradictory behavior occurred in the modified flours after enzymatic hydrolysis, where a significant increase in CWS was determined for the HMT-P and ANN-P treatments. Figueroa-Flórez (2021) explained that the cleavage of glycosidic bonds and subsequent depolymerization of polyglucans increase the proportion of short amylopectin chains, favoring the availability of free hydroxyl groups that have a hydrophilic character. Chen et al. (2022) reported similar results in corn starches treated with pullulanase.

The pasting properties of the native and modified cassava flours are summarized in Table 4. T_PT increased with on implementation of the modification treatments, presenting a similar behavior to the gelatinization peak temperature (T_P) determined with the temperature sweep in the dynamic-oscillatory test. A decrease in the values of maximum viscosity (V_M) was identified in the modified flours after the individual and dual action by hydrothermal and enzymatic pathways. Similar results have been reported in cassava, yam, plantain, and lentil flours subjected to HMT and/or ANN (Dudu et al., 2019; Chávez et al., 2018; Yu et al., 2021; Rodríguez-Damian et al., 2013; Perraulta-Lavanya et al., 2021). About the enzymatic action by debranching, several authors have reported a decrease in the value of maximum viscosity in debranched starches from corn, potato, and sweet potato (Li et al., 2017b; (Ge et al., 2021). The decrease in pasting viscosity in the present study could be associated with: (1) variation in starch and amylose content; (2) decreased PS; (3) changes in semicrystalline order related to birefringence ability; (4) rearrangement of amylose and amylopectin; (5) perfection of crystals that restrain the strength of hydrogen bonding between water molecules and starch molecules; and (6) reduction of branched regions by enzymatic action (Chávez et al., 2018; Yu et al., 2021; Iuga & Mironeasa; 2020; Li et al., 2017b; Ge et al., 2021; Rodríguez-Damian et al., 2013; Perraulta-Lavanya et al., 2021; Chen et al., 2022). These results are consistent with those presented in Tables 2 and 4 for modified cassava flour, being more significant in the hydrothermal treatment by HMT, with a decrease in V_M of approximately 28.24%, compared to the native counterpart.

Breakdown (V_R), established as the difference between the maximum and minimum viscosity during heating at constant temperature, indicates the degree of granular disintegration and molecular decomposition of polymer chains due to shear stress (Kaur et al., 2007). The decrease in V_R in modified cassava flours could be attributed to greater thermal and mechanical stability of the polymer chains caused by better molecular organization during hydrothermal modification (Xu et al., 2018; Li et al., 2020). Similar results have been reported in wheat flours treated by HMT, yam flours modified by ANN, and dually modification of rice flours combining hydrothermal and enzymatic action (Yu et al., 2021; Li et al., 2020; Satmalee & Matsuki, 2011). These same authors point out that a decrease in breakdown can be associated with phenomena such as (1) leaching of free and/or disordered soluble amylose; (2) molecular reorganization; and (3) depolymerization of branch points.

Setback (VA), the difference between the viscosity at the beginning and end of the cooling process, indicates the gelling and retrogradation capacity of starches. Hydrothermal and enzymatic processes, both single and dual, significantly decreased the VA in modified cassava flours, especially in those subjected to HMT and HMT-P with values of 118.67 and 586.27 mPa.s, respectively, compared to the native counterpart (HNY) with a viscosity of 621.30 mPa.s. These results can be attributed to the improvement in the hydrophilic properties of starchy materials such as the increase in WAC, decreased AM, and interaction of starch with other non-starch components in flours (Figueroa-Flórez,2021; Xu et al., 2018; Chen et al., 2022; Fathi et al., 2016). Jafari et al. (2017) argued that WAC expresses the volume occupied by starch granules after swelling in excess water and is an indicator of gelling capacity in aqueous dispersion. In turn, some authors have indicated that a decrease in setback viscosity is the product of better gelling capacity and a reduction of the retrogradation phenomenon, whose physicochemical factors are concomitant in improving the texture properties and extension of the useful life of products such as baked goods formulated from starchy materials (Iuga & Mironeasa; 2020; Li et al., 2020; Fathi et al., 2016).

4 Conclusions

Hydrothermal treatments such as ANN and HMT affected granular size, AM, and semicrystalline order, which delimited the behavior of the physicochemical, gelatinization, and pasting properties of native cassava flours. HMT, with respect to ANN, exhibited a more noticeable impact on the morphological and structural characteristics, promoting significant changes in the pasting profile of the flour. The hydrothermal and biocatalytic treatments increased the SC in the modified flours, impacting the physicochemical and gelatinization properties. In turn, the dual action of ANN-P and HMT-P produced noticeable changes in the hydrophilic properties of the flours, such as CAA and SAF. The HMT and HMT-P treatments emerge as clean and effective technologies for improving hydrophilic properties and reducing setback viscosity – the tendency of a starchy material to retrogradation. Consequently, the application of cassava flours modified by HMT and/or HMT-P in the formulation of baked products could be suggested.

• Cite as:
  Serna-Fadul, T. Y., Figueroa-Flórez, J. A., Ciro-Velásquez, H. J., Salcedo-Mendoza, J. S., & Hernández-Ruydiaz, J. E. (2024). Hydrothermal and biocatalytic processes on native cassava flours: behavior of the physicochemical, morphological and pasting properties. Brazilian Journal of Food Technology, 27, e2024014. https://doi.org/10.1590/1981-6723.01424
• Funding:
  None.

References

• Adesina, B. S., & Bolaji, O. T. (2013). Effect of milling machines and sieve sizes on cooked cassava flour quality. Nigerian Food Journal, 31(1), 115-119. http://doi.org/10.1016/S0189-7241(15)30065-5
  » http://doi.org/10.1016/S0189-7241(15)30065-5
• Afolabi, T. A., Opara, A. O., Kareem, S. O., & Oladoyinbo, F. O. (2018). In vitro digestibility of hydrothermally modified Bambara groundnut (Vigna subterranean L.) starch and flour. Food Science & Nutrition, 6(1), 36-46. PMid:29387359. http://doi.org/10.1002/fsn3.510
  » http://doi.org/10.1002/fsn3.510
• Afuakwa, J. J., Ellis, W. O., Oduro, I., & Aryee, F. N. A. (2006). The physicochemical properties of Xour samples from the roots of 31 varieties of cassava. Food Control
• Akhila, P. P., Sunooj, K. V., Aaliya, B., Navaf, M., Sudheesh, C., Yadav, D. N., Khanc, M. A., Mir, S. A., & George, J. (2022). Morphological, physicochemical, functional, pasting, thermal properties and digestibility of hausa potato (Plectranthus rotundifolius) flour and starch. Appl. Food Res., 2(2), 100193. http://doi.org/10.1016/j.afres.2022.100193
  » http://doi.org/10.1016/j.afres.2022.100193
• Alamu, E. O., Maziya-Dixon, B., & Dixon, A. G. (2017). Evaluation of proximate composition and pasting properties of high quality cassava flour (HQCF) from cassava genotypes (Manihot esculenta Crantz) of β-carotene-enriched roots. Lebensmittel-Wissenschaft + Technologie, 86, 501-506. http://doi.org/10.1016/j.lwt.2017.08.040
  » http://doi.org/10.1016/j.lwt.2017.08.040
• Association of Oficial Analytical Chemists International – AOAC. (1990). Official Methods of Analysis (15th ed). Washington: AOAC.
• Babu, A. S., & Parimalavalli, R. (2018). Effect of pullulanase debranching and storage temperatures on structural characteristics and digestibility of sweet potato starch. Journal of the Saudi Society of Agricultural Sciences, 17(2), 208-216. http://doi.org/10.1016/j.jssas.2016.04.005
  » http://doi.org/10.1016/j.jssas.2016.04.005
• Bian, L., & Chung, H. J. (2016). Molecular structure and physicochemical properties of starch isolated from hydrothermally treated brown rice flour. Food Hydrocolloids, 60, 345-352. http://doi.org/10.1016/j.foodhyd.2016.04.008
  » http://doi.org/10.1016/j.foodhyd.2016.04.008
• Cahyana, Y., Wijaya, E., Halimah, T. S., Marta, H., Suryadi, E., & Kurniati, D. (2019). The effect of different thermal modifications on slowly digestible starch and physicochemical properties of green banana flour (Musa acuminata colla). Food Chemistry, 274, 274-280. PMid:30372939. http://doi.org/10.1016/j.foodchem.2018.09.004
  » http://doi.org/10.1016/j.foodchem.2018.09.004
• Cham, S., & Suwannaporn, P. (2010). Effect of hydrothermal treatment of rice flour on various rice noodles quality. Journal of Cereal Science, 51(3), 284-291. http://doi.org/10.1016/j.jcs.2010.01.002
  » http://doi.org/10.1016/j.jcs.2010.01.002
• Charles, A., Huang, T. C., Lai, P. Y., Chen, C. C., Lee, P. P., & Chang, Y. H. (2007). Study of wheat flour-cassava starch composite mix and the function of cassava mucilage in Chinese noodles. Food Hydrocolloids, 21(3), 368-378. http://doi.org/10.1016/j.foodhyd.2006.04.008
  » http://doi.org/10.1016/j.foodhyd.2006.04.008
• Charoenkul, D., Uttapap, W., Pathipanawat, Y., & Takeda, Y. (2011). Physicochemical characteristics of starches and flours from cassava varieties having different cooked root textures. Lebensmittel-Wissenschaft + Technologie, 44(8), 1774-1781. http://doi.org/10.1016/j.lwt.2011.03.009
  » http://doi.org/10.1016/j.lwt.2011.03.009
• Chávez, C. E., Veyna-Torres, J. I., Cavazos-Tamez, L. M., de la Rosa-Millán, J., & Serna-Saldívar, S. O. (2018). Physicochemical characteristics, ATR-FTIR molecular interactions and in vitro starch and protein digestion of thermally-treated whole pulse flours. Food Research International, 105, 371-383. PMid:29433226. http://doi.org/10.1016/j.foodres.2017.11.029
  » http://doi.org/10.1016/j.foodres.2017.11.029
• Chen, L., McClements, D. J., Yang, T., Ma, Y., Ren, F., Tian, Y., & Jin, Z. (2021). Effect of annealing and heat-moisture pretreatments on the oil absorption of normal maize starch during frying. Food Chemistry, 353, 129468. PMid:33730664. http://doi.org/10.1016/j.foodchem.2021.129468
  » http://doi.org/10.1016/j.foodchem.2021.129468
• Chen, P., Xie, Q. T., Wang, R. M., Wang, S. Y., Cheng, J. S., & Zhang, B. (2022). Effects of pullulanase enzymatic hydrolysis on the textural of acorn vermicelli and its influencing mechanism on the quality. Food Research International, 156, 111294. PMid:35651100. http://doi.org/10.1016/j.foodres.2022.111294
  » http://doi.org/10.1016/j.foodres.2022.111294
• Chen, S. H., Li, X. F., Shih, P. T., & Pai, S. M. (2020). Preparation of thermally stable and digestive enzyme resistant flour directly from Japonica broken rice by combination of steam infusion, enzymatic debranching and heat moisture treatment. Food Hydrocolloids, 108, 106022. http://doi.org/10.1016/j.foodhyd.2020.106022
  » http://doi.org/10.1016/j.foodhyd.2020.106022
• Chimphepo, L., Alamu, E. O., Monjerezi, M., Ntawuruhunga, P., & Saka, J. D. K. (2021). Physicochemical parameters and functional properties of flours from advanced genotypes and improved cassava varieties for industrial applications. Lebensmittel-Wissenschaft + Technologie, 147, 111592. http://doi.org/10.1016/j.lwt.2021.111592
  » http://doi.org/10.1016/j.lwt.2021.111592
• Dang, T. T., & Vasanthan, T. (2019). Modification of rice bran dietary fiber concentrates using enzyme and extrusion cooking. Food Hydrocolloids, 89, 773-782. http://doi.org/10.1016/j.foodhyd.2018.11.024
  » http://doi.org/10.1016/j.foodhyd.2018.11.024
• Das, M., Rajan, N., Biswas, P., & Banerjee, R. (2022). A novel approach for resistant starch production from green banana flour using amylopullulanase. Lebensmittel-Wissenschaft + Technologie, 153, 112391. http://doi.org/10.1016/j.lwt.2021.112391
  » http://doi.org/10.1016/j.lwt.2021.112391
• De La Rosa-Millan, J., Lin, A. H. M., Osorio-Diáz, P., Agama-Acevedo, E., Hamaker, B. R., & Bello-Perez, L. A. (2015). Influence of annealing flours from raw and pre-cooked plantain fruit on cooked starch digestion rates. Stärke, 67(1-2), 139-146. http://doi.org/10.1002/star.201400136
  » http://doi.org/10.1002/star.201400136
• Dudu, O. E., Oyedeji, A. B., Oyeyinka, S. A., & Ma, Y. (2019). Impact of steam-heat-moisture treatment on structural and functional properties of cassava flour and starch. International Journal of Biological Macromolecules, 126, 1056-1064. PMid:30593809. http://doi.org/10.1016/j.ijbiomac.2018.12.210
  » http://doi.org/10.1016/j.ijbiomac.2018.12.210
• Fathi, B., Aalami, M., Kashaninejad, M., & Sadeghi Mahoonak, A. (2016). Utilization of heat-moisture treated proso millet flour in production of gluten-free pound cake. Journal of Food Quality, 39(6), 611-619. http://doi.org/10.1111/jfq.12249
  » http://doi.org/10.1111/jfq.12249
• Figueroa-Flórez, J. A. (2021). Procesos de biocátalisis enzimática en almidones nativos y pre-gelatinizados de yuca: Efectos a nivel morfológico, molecular y de digestibilidad in vitro (Doctoral dissertation). Universidad Nacional de Colombia, Medellín.
• Figueroa-Flórez, J. A., Cadena-Chamorro, E. M., Rodríguez-Sandoval, E., Salcedo-Mendoza, J., & Ciro-Velásquez, H. J. (2019). Cassava starches modified by enzymatic biocatalysis: effect of reaction time and drying method. Dyna, 86(208), 162-170. http://doi.org/10.15446/dyna.v86n208.72976
  » http://doi.org/10.15446/dyna.v86n208.72976
• Figueroa-Flórez, J., Cadena-Chamorro, E., Rodriguez-Sandoval, E., Salcedo-Mendoza, J., & Ciro-Velásquez, H. (2023). Hydrothermal processes and simultaneous enzymatic hydrolysis in the production of modified cassava starches with porous-surfaces. Heliyon, 9(7), e17742. PMid:37539223. http://doi.org/10.1016/j.heliyon.2023.e17742
  » http://doi.org/10.1016/j.heliyon.2023.e17742
• Franco, C. M., Ciacco, C. F., & Tavares, D. Q. (1995). Effect of the heat‐moisture treatment on the enzymatic susceptibility of corn starch granules. Stärke, 47(6), 223-228. http://doi.org/10.1002/star.19950470607
  » http://doi.org/10.1002/star.19950470607
• Ge, X., Shen, H., Su, C., Zhang, B., Zhang, Q., Jiang, H., & Li, W. (2021). Pullulanase modification of granular sweet potato starch: assistant effect of dielectric barrier discharge plasma on multi-scale structure, physicochemical properties. Carbohydrate Polymers, 272, 118481. PMid:34420740. http://doi.org/10.1016/j.carbpol.2021.118481
  » http://doi.org/10.1016/j.carbpol.2021.118481
• Holilah, A., Syarifin, A. N. K., Purnomo, A. S., & Fudholi, A. (2021). The effect of heat moisture treatment on crystallinity and physicochemical-digestibility properties of purple yam flour. Food Hydrocolloids, 20, 106889. http://doi.org/10.1016/j.foodhyd.2021.106889
  » http://doi.org/10.1016/j.foodhyd.2021.106889
• Iuga, M., & Mironeasa, S. (2020).A review of the hydrothermal treatments impact on starch based systems properties. Critical Reviews in Food Science and Nutrition, 60(22), 3890-3915. PMid:31542935. http://doi.org/10.1080/10408398.2019.1664978
  » http://doi.org/10.1080/10408398.2019.1664978
• Jafari, M., Koocheki, A., & Milani, E. (2017). Effect of extrusion cooking on chemical structure, morphology, crystallinity and thermal properties of sorghum flour extrudates. Journal of Cereal Science, 75, 324-331. http://doi.org/10.1016/j.jcs.2017.05.005
  » http://doi.org/10.1016/j.jcs.2017.05.005
• Kaur, A., Singh, N., Ezekiel, R., & Guraya, H. S. (2007). Physicochemical, thermal and pasting properties of starches separated from different potato cultivars grown at different locations. Food Chemistry, 101(2), 643-651. http://doi.org/10.1016/j.foodchem.2006.01.054
  » http://doi.org/10.1016/j.foodchem.2006.01.054
• Kaur, M., & Singh, S. (2019). Influence of heat-moisture treatment (HMT) on physicochemical and functional properties of starches from different Indian oat (Avena sativa L.) cultivars. International Journal of Biological Macromolecules, 122, 312-319. PMid:30385334. http://doi.org/10.1016/j.ijbiomac.2018.10.197
  » http://doi.org/10.1016/j.ijbiomac.2018.10.197
• Li, C., & Hamaker, B. R. (2021). Effects of different storage temperatures on the intra- and intermolecular retrogradation and digestibility of sago starch. International Journal of Biological Macromolecules, 182, 65-71. PMid:33831448. http://doi.org/10.1016/j.ijbiomac.2021.03.195
  » http://doi.org/10.1016/j.ijbiomac.2021.03.195
• Li, H., Li, J., Xiao, Y., Cui, B., Fang, Y., & Guo, L. (2019). In vitro digestibility of rice starch granules modified by β-amylase, transglucosidase and pullulanase. International Journal of Biological Macromolecules, 136, 1228-1236. PMid:31228499. http://doi.org/10.1016/j.ijbiomac.2019.06.111
  » http://doi.org/10.1016/j.ijbiomac.2019.06.111
• Li, M., Liu, C., Zheng, X., Li, L., & Bian, K. (2020). Physicochemical properties of wheat flour modified by heat-moisture treatment and their effects on noodles making quality. Journal of Food Processing and Preservation, 44(9), 1-9. http://doi.org/10.1111/jfpp.14590
  » http://doi.org/10.1111/jfpp.14590
• Li, P., He, X., Dhital, S., Zhang, B., & Huang, Q. (2017a). Structural and physicochemical properties of granular starches after treatment with debranching enzyme. Carbohydrate Polymers, 169, 351-356. PMid:28504155. http://doi.org/10.1016/j.carbpol.2017.04.036
  » http://doi.org/10.1016/j.carbpol.2017.04.036
• Li, Y., Ding, G., Yokoyama, W., & Zhong, F. (2018). Characteristics of annealed glutinous rice flour and its formation of fast-frozen dumplings. Journal of Cereal Science, 79, 106-112. http://doi.org/10.1016/j.jcs.2017.09.016
  » http://doi.org/10.1016/j.jcs.2017.09.016
• Li, Y., Liu, S., Liu, X., Tang, X., & Zhang, J. (2017b). The impact of heat-moisture treatment on physicochemical properties and retrogradation behavior of sweet potato starch. International Journal of Food Engineering, 13(5), 20170001. http://doi.org/10.1515/ijfe-2017-0001
  » http://doi.org/10.1515/ijfe-2017-0001
• Liu, G., Hong, Y., Gu, Z., Li, Z., & Cheng, L. (2015). Pullulanase hydrolysis behaviors and hydrogel properties ofdebranched starches from different sources. Food Hydrocolloids, 45, 351-360. http://doi.org/10.1016/j.foodhyd.2014.12.006
  » http://doi.org/10.1016/j.foodhyd.2014.12.006
• Liu, W., Hong, Y., Gu, Z., Cheng, L., Li, Z., & Li, C. (2017). In structure and in-vitro digestibility of waxy corn starch debranched by pullulanase. Food Hydrocolloids, 67, 104-110. http://doi.org/10.1016/j.foodhyd.2016.12.036
  » http://doi.org/10.1016/j.foodhyd.2016.12.036
• Ministerio de Agricultura y Desarrollo Rural – MADR. (2021). Subsector productivo de la yuca. Retrieved in 2024, February 12, from https://sioc.minagricultura.gov.co/Yuca/Documentos. Cifras Sectoriales 21-06-30.pdf
  » https://sioc.minagricultura.gov.co/Yuca/Documentos.
• Organización de las Naciones Unidas para la Alimentación y la Agricultura – FAO. (2022). Producción mundial de batata. Datos sobre Alimentación y Agricultura Roma, Italia: FAO. Retrieved in 2024, February 12, from http://www.fao.org/faostat/en/#data
  » http://www.fao.org/faostat/en/#data
• Perraulta-Lavanya, J., Gowthamraj, G., & Sangeetha, N. (2021). Effect of heat moisture treatment on the physicochemical, functional, and antioxidant characteristics of white sorghum (Sorghum bicolor (L.) grains and flour. Journal of Food Processing and Preservation, 45(12), 1-13. http://doi.org/10.1111/jfpp.16017
  » http://doi.org/10.1111/jfpp.16017
• Pratiwi, M., Faridah, D. N., & Lioe, H. N. (2018). Structural changes to starch after acid hydrolysis, debranching, autoclaving-cooling cycles, and heat moisture treatment (HMT): a review. Stärke, 70(1–2), 1700028. http://doi.org/10.1002/star.201700028
  » http://doi.org/10.1002/star.201700028
• Puelles-Román, J., Barroso, N. G., Cruz-Tirado, J. P., Tapia-Blácido, D. R., Angelats-Silva, L., Barraza-Jáuregui, G., & Siche, R. (2021). Annealing process improves the physical, functional, thermal, and rheological properties of Andean oca (Oxalis tuberosa) starch. Journal of Food Process Engineering, 44(6), 1-10. http://doi.org/10.1111/jfpe.13702
  » http://doi.org/10.1111/jfpe.13702
• Rocha, T. S., Felizardo, S. G., Jane, J., & Franco, C. M. L. (2012). Effect of annealing on the semicrystalline structure of normal and waxy corn starches. Food Hydrocolloids, 29(1), 93-99. http://doi.org/10.1016/j.foodhyd.2012.02.003
  » http://doi.org/10.1016/j.foodhyd.2012.02.003
• Rodríguez-Damian, A. R., De La Rosa-Millán, J., Agama-Acevedo, E., Osorio-Díaz, P., & Bello-Pérez, L. A. (2013). Effect of different thermal treatments and storage on starch digestibility and physicochemical characteristics of unripe banana flour. Journal of Food Processing and Preservation, 37(5), 987-998. http://doi.org/10.1111/j.1745-4549.2012.00737.x
  » http://doi.org/10.1111/j.1745-4549.2012.00737.x
• Salcedo Mendoza, J. G., Figueroa Flórez, J. A., & Hernández Ramos, E. J. (2017). Agroindustria de productos amiláceos II. Métodos y técnicas de caracterización Retrieved in 2024, February 12, from https://repositorio.unisucre.edu.co/entities/publication/f296800e-e187-461f-9765-fa5bff791589
  » https://repositorio.unisucre.edu.co/entities/publication/f296800e-e187-461f-9765-fa5bff791589
• Sasaki, T., & Matsuki, J. (1998). Effect of wheat starch structure on swelling power. Cereal Chemistry, 75(4), 525-529. http://doi.org/10.1094/CCHEM.1998.75.4.525
  » http://doi.org/10.1094/CCHEM.1998.75.4.525
• Satmalee, P., & Matsuki, J. (2011). Effect of debranching and heat-moisture treatment on the properties of Thai rice flours. International Journal of Food Science & Technology, 46(12), 2628-2633. http://doi.org/10.1111/j.1365-2621.2011.02793.x
  » http://doi.org/10.1111/j.1365-2621.2011.02793.x
• Sindhu, R., Devi, A., & Khatkar, B. S. (2019). Physicochemical, thermal and structural properties of heat moisture treated common buckwheat starches. Journal of Food Science and Technology, 56(5), 2480-2489. PMid:31168130. http://doi.org/10.1007/s13197-019-03725-6
  » http://doi.org/10.1007/s13197-019-03725-6
• Sun, Q., Han, Z., Wang, L., & Xiong, L. (2014). Physicochemical differences between sorghum starch and sorghum flour modified by heat-moisture treatment. Food Chemistry, 145, 756-764. PMid:24128541. http://doi.org/10.1016/j.foodchem.2013.08.129
  » http://doi.org/10.1016/j.foodchem.2013.08.129
• Tukomane, T., Leerapongnun, P., Shobsngob, S., & Varavinit, S. (2007). Preparation and characterization of annealed-enzymatically hydrolyzed tapioca starch and the utilization in tableting. Stärke, 59(1), 33-45. http://doi.org/10.1002/star.200600524
  » http://doi.org/10.1002/star.200600524
• Vela, A. J., Villanueva, M., & Ronda, F. (2021). Low-frequency ultrasonication modulates the impact of annealing on physicochemical and functional properties of rice flour. Food Hydrocolloids, 120, 106933. http://doi.org/10.1016/j.foodhyd.2021.106933
  » http://doi.org/10.1016/j.foodhyd.2021.106933
• Warren, F. J., Gidley, M. J., & Flanagan, B. M. (2016). Infrared spectroscopy as a tool to characterise starch ordered structure: a joint FTIR–ATR, NMR, XRD and DSC study. Carbohydrate Polymers, 139, 35-42. PMid:26794944. http://doi.org/10.1016/j.carbpol.2015.11.066
  » http://doi.org/10.1016/j.carbpol.2015.11.066
• Xiao, Y., Liu, H., Wei, T., Shen, J., & Wang, M. (2017). Differences in physicochemical properties and in vitro digestibility between tartary buckwheat flour and starch modified by heat-moisture treatment. Lebensmittel-Wissenschaft + Technologie, 86, 285-292. http://doi.org/10.1016/j.lwt.2017.08.001
  » http://doi.org/10.1016/j.lwt.2017.08.001
• Xu, M., Saleh, A. S., Gong, B., Li, B., Jing, L., Gou, M., Jiang, H., & Li, W. (2018). The effect of repeated versus continuous annealing on structural, physicochemical, and digestive properties of potato starch. Food Research International, 111, 324-333. PMid:30007693. http://doi.org/10.1016/j.foodres.2018.05.052
  » http://doi.org/10.1016/j.foodres.2018.05.052
• Yang, Z., Zhang, Y., Wu, Y., & Ouyang, J. (2022). The role of drying methods in determining the in vitro digestibility of starch in whole chestnut flour. Lebensmittel-Wissenschaft + Technologie, 153, 112583. http://doi.org/10.1016/j.lwt.2021.112583
  » http://doi.org/10.1016/j.lwt.2021.112583
• Yu, B., Li, J., Tao, H., Zhao, H., Liu, P., & Cui, B. (2021). Physicochemical properties and in vitro digestibility of hydrothermal treated Chinese yam (Dioscorea opposita Thunb.) starch and flour. International Journal of Biological Macromolecules, 176, 177-185. PMid:33581211. http://doi.org/10.1016/j.ijbiomac.2021.02.064
  » http://doi.org/10.1016/j.ijbiomac.2021.02.064
• Zeng, F., Ma, F., Kong, F., Gao, Q., & Yu, S. (2015). Physicochemical properties and digestibility of hydrothermally treated waxy rice starch. Food Chemistry, 172, 92-98. PMid:25442528. http://doi.org/10.1016/j.foodchem.2014.09.020
  » http://doi.org/10.1016/j.foodchem.2014.09.020
• Zhang, B., Cui, D., Liu, M., Gong, H., Huang, Y., & Han, F. (2012). Corn porous starch: Preparation, characterization and adsorption property. International Journal of Biological Macromolecules, 50(1), 250-256. PMid:22100869. http://doi.org/10.1016/j.ijbiomac.2011.11.002
  » http://doi.org/10.1016/j.ijbiomac.2011.11.002
• Zhang, C., Narayanamoorthy, S., Ming, S., Li, K., Cantre, D., Sui, Z., & Corke, H. (2022). Rheological properties, structure and digestibility of starches isolated from common bean (Phaseolus vulgaris L.) varieties from Europe and Asia. Lebensmittel-Wissenschaft + Technologie, 161, 113352. http://doi.org/10.1016/j.lwt.2022.113352
  » http://doi.org/10.1016/j.lwt.2022.113352

Edited by

• Associate Editor:
  Elizabeth Nabeshima.

Publication Dates

• Publication in this collection
  09 Dec 2024
• Date of issue
  2024

History

• Received
  12 Feb 2024
• Accepted
  19 Oct 2024