Intrinsic and extrinsic factors affecting rice starch digestibility

Trends in Food Science & Technology 88 (2019) 10–22

Contents lists available at ScienceDirect

Trends in Food Science & Technology journal homepage: www.elsevier.com/locate/tifs

Review

Intrinsic and extrinsic factors affecting rice starch digestibility a,b

a,b

Michelle R. Toutounji , Asgar Farahnaky , Abishek B. Santhakumar Vito M. Butardo Jr.b,d, Christopher L. Blancharda,b,∗

a,b

T c

, Prakash Oli ,

a

School of Biomedical Sciences, Charles Sturt University (CSU), Wagga Wagga, 2650, NSW, Australia Australian Research Council (ARC) Industrial Transformation Training Centre (ITTC) for Functional Grains, Graham Centre for Agricultural Innovation, CSU, Wagga Wagga, 2650, NSW, Australia c NSW Department of Primary Industries (DPI), Yanco Agricultural Institute, Yanco, 2703, NSW, Australia d Swinburne University of Technology, Faculty of Science, Engineering and Technology, Hawthorn, 3122, VIC, Australia b

A R T I C LE I N FO

A B S T R A C T

Keywords: Starch Digestibility Rice Processing Cooking Retrogradation

Background: The current incidence of obesity and type 2 diabetes is at global epidemic levels. To mitigate their impact, there is a need to develop starch-containing foods that give rise to a low and stable postprandial blood glucose response by increasing the proportion of slowly-digestible and indigestible carbohydrate content. Rice is an ideal target food for such dietary intervention because it is a staple food for over half the world's population. Scope and approach: The starch digestion of cooked white rice grains is usually complete or near complete upon consumption, but the rate of digestion is influenced by intrinsic food properties and extrinsic influences. This review provides an overview of the complex interplay between the starch granule and its interaction with nonstarch components of the rice grain (intrinsic characteristics) as well as the effects of processing (extrinsic factors) on starch digestibility. Key findings and conclusions: The intrinsic properties of white rice grains play a significant role in starch digestibility which can be further enhanced after processing, especially by gelatinisation and retrogradation. Postharvest storage conditions of rice were found to influence starch digestibility but this effect was temperaturedependent. Limited studies investigated starch-lipid and starch-protein interactions in rice, but changes to substrate accessibility have been implicated. Improving our understanding of the effects of processing on starch digestibility can provide an effective tool for food manufacturers to regulate starch digestibility of existing rice varieties.

1. Introduction The incidence of obesity, type 2 diabetes and related chronic diseases is alarmingly high, both in developing and developed countries. Around 1.9 billion adults are either overweight or obese (WHO, 2016b), while 382 million people suffer from type 2 diabetes worldwide (WHO, 2016a). To address these global health concerns, individuals and communities are encouraged to adopt a balanced diet and to increase their physical activity. For diet, the availability of healthy food options is vital and requires a population-based approach involving intervention from both food production (e.g. modification of primary produce) and food processing sectors (e.g. reformulation of food products). The role of dietary components in the prevention of chronic conditions has gained much research attention. Starch is a major component of the human diet and, like other dietary carbohydrates, has been

given an energy value of 17 kJ/g (4 kcal/g). However, it is now well understood that a number of different starch fractions exist which are not digested at an equal rate. These have been classified as rapidly digestible starch (RDS) – digested within 20 min, slowly digestible starch (SDS) – digested between 20 and 120 min, and resistant starch (RS) – digested beyond 120 min (Englyst, Kingman, & Cummings, 1992). Generally, SDS has been shown to elicit a moderate postprandial glycemic and insulinaemic response. This fraction of starch is considered beneficial for the dietary management of individuals with chronic and metabolic conditions, particularly those with type 2 diabetes and hyperlipidaemia (Aller, Abete, Astrup, Martinez, & van Baak, 2011). RS is also considered to be beneficial because it evades digestion in the human gastrointestinal tract and hence food high in this starch fraction has a very low digestibility (Butardo & Sreenivasulu, 2016). In addition, RS performs a physiological function similar to dietary fibre

∗

Corresponding author. School of Biomedical Sciences, Charles Sturt University (CSU), Wagga Wagga, 2650, NSW, Australia. E-mail addresses: [email protected] (M.R. Toutounji), [email protected] (A. Farahnaky), [email protected] (A.B. Santhakumar), [email protected] (P. Oli), [email protected] (V.M. Butardo), [email protected] (C.L. Blanchard). https://doi.org/10.1016/j.tifs.2019.02.012 Received 23 September 2018; Received in revised form 3 December 2018; Accepted 6 February 2019 Available online 13 February 2019 0924-2244/ © 2019 Published by Elsevier Ltd.

Trends in Food Science & Technology 88 (2019) 10–22

M.R. Toutounji, et al.

the starch granule, independent of subsequent hydrolysis. Furthermore, naturally occurring peripheral pores can enhance the effective surface area, increasing the formation of enzyme-substrate complexes. Cereal starches, including rice, have naturally occurring peripheral pores connected to interior channels, resulting in an ‘inside out’ pattern of digestibility, which has a higher hydrolysis rate compared to the ‘outside in’ pattern of potato and high-amylose maize starches (Gallant, Bouchet, & Baldwin, 1997). When comparing sedimentation fractions of rice starch, the presence of surface pores and interior channels had a greater effect on the rate and extent of digestion than the apparent available surface area (as represented by granule size) (Dhital, Butardo, Jobling, & Gidley, 2015). At the molecular level, enzymatic hydrolysis of rice is influenced by the composition of the two different structural types of polysaccharides present in starch: amylose and amylopectin. Amylose is primarily a linear glucan, comprised mostly (> 99%) of α(1–4) bonds with a fewer number of branches connected by α(1–6) bonds. In contrast, amylopectin is a highly branched glucan primarily composed of many short α(1–4) chains, which are interlinked by 4–6% of α(1–6) bonds at the branch points (Buléon, Colonna, Planchot, & Ball, 1998; Tester et al., 2001). Amylose content in rice ranges from 0 to approximately 30% (Butardo et al., 2017), with 1–2% defined as waxy, 2–12% as very low, 12–20% as low, 20–25% as intermediate, and 25% and above as high (Juliano, 2004). Disagreement exists in the literature about the relationship between amylose and starch digestibility of raw rice. Native rice starches with higher amylose levels have been reported to have higher levels of RS (Chung, Liu, Lee, & Wei, 2011; Sagum & Arcot, 2000; Zhu, Liu, Wilson, Gu, & Shi, 2011). Zhu et al. (2011) suggested that amylose molecules in the amorphous regions may initially be hydrolysed by amylase but hydrolysed molecules may then re-associate and become resistant. However, in the same study, there was one exception to the trend whereby the low-amylose rice had a lower RS content than the waxy rice. Similarly, Van Hung, Vien, and Phi (2016) reported that the native waxy rice starch had a significantly higher RS than that of native high-amylose and normal rice starches. In terms of hydrolysis rates, some studies have reported amylose content to be negatively correlated with SDS (Zhu et al., 2011) and digestion rates (Cai et al., 2015; Chung et al., 2011). Cai et al. (2015) suggested that the presence of amylose-lipid complexes prevented hydration and thus amylase penetration of starch granules. However, other studies found that amylose content had no correlation with RDS (Zhou, Ying, Hu, Pang, & Bao, 2018; Zhu et al., 2011) or digestion rate kinetic parameters (Dhital, Dabit, Zhang, Flanagan, & Shrestha, 2015). Establishing a trend between amylose content and enzyme hydrolysis is complicated by the fact that most studies involve a comparison between different rice genotypes. In a more recent study by Lin et al. (2018), rice starches with same genetic background but with different amylose content were used. It was found that starches with different amylose content but the same amylopectin structure had significantly different digestibility. Thus, for different varieties of raw rice, the starch digestion rates is primarily attributed to amylose content, but the amylopectin fine structure can also play a contributory role. This is because it appears that long chain amylopectin which mimics the structure, and therefore the function of amylose, can increase the RS and reduce the digestibility of rice grains (Butardo et al., 2017; Butardo et al., 2011). The supramolecular structural levels of starch also affect the susceptibility of native granules to enzymatic attack. Amylose and amylopectin are arranged in alternating concentric regions of crystalline layers (formed by ordered parallel arrays of double helices of amylopectin) and amorphous layers (mostly containing amylose) (French, 1972; Robin, Mercier, Charbonniere.R, & Guilbot, 1974). Native rice starch, like most other cereal starches, is traditionally classified as an A crystalline type (A polymorph). A-type polymorphs have shorter average chain length and are thermally stable. In contrast, B-type polymorphs have an ordered array of hexagonally packed double helices with greater proportion of helical water (Gidley, 1987). A third

because it provides a substrate for the microbial fermentation of short chain fatty acids (SCFAs) in the human colon (Brouns, Kettlitz, & Arrigoni, 2002). While the nutritional classification of starch fractions is useful, it cannot accurately represent the intricacies of the digestion process. The glycemic index (GI) is a well-established in vivo measure of the postprandial blood glucose raising potential of carbohydrate-containing foods (Jenkins et al., 1981). Regular consumption of high-GI diets has been shown to increase the risk of developing type 2 diabetes (Bhupathiraju et al., 2014). While physiologically informative, there are many practical and logistical limitations to the standard in vivo methods. Thus in vitro digestion models remain a necessary research tool and allow for better control of key factors important to the digestion process (Woolnough, Monro, Brennan, & Bird, 2008). Rice (Oryza sativa L.) is the staple crop for billions of people worldwide, with global consumption estimated at 402 million metric tons (milled rice basis) and a global per capita food use of 54.1 kg per person in 2016/2017 (FAO, 2017). White rice, otherwise known as “milled” or “polished” rice, is the most common form in which rice is consumed. It is produced by physical processing to remove the hull and bran layers to reveal the starchy endosperm, contributing to an overall high proportion of starch of up to 90% (dry weight basis) (Butardo, Sreenivasulu, & Juliano, 2019; Juliano, 2007). The digestion (Juliano, 1985) and intestinal absorption (Strocchi & Levitt, 1991) of cooked white rice is complete or near complete in humans. However the rate of digestion is influenced by several intrinsic (e.g. starch properties, starch-protein interactions and starch-lipid interactions) and extrinsic factors (e.g. hydrothermal treatments and variations of domestic cooking). This review focusses on both in vivo and in vitro studies which examine the role of intrinsic properties of white rice and extrinsic processes that influence starch digestion. 2. The role of intrinsic properties of white rice The digestion of raw starch granules has been described in three phases: enzyme diffusion towards the substrate, enzyme adsorption to the substrate (i.e. formation of the enzyme-substrate complex), and the hydrolytic event (Lehmann & Robin, 2007). In this section (section 2), we focus on the digestibility of raw rice starch and compare it with cooked starch granules whenever possible. Although most rice is consumed as cooked white grains, studies on native starches may enables us to understand the impact of starch structural features that control the rate and extent of amylolysis. Secondary influences by extrinsic processing (including cooking) will be reviewed in section 3. 2.1. The starch granule The digestion of raw starch granules is influenced by many features of the granule including its morphology (e.g. size and shape), surface features (e.g. presence of pores and channels), molecular composition (e.g. size and amount of amylose and amylopectin) and supramolecular structures (e.g. crystallinity, growth rings, packing in cell). Higher order supramolecular organisation is typically denatured during the cooking process but the proportion of amylose and amylopectin, as well as the structural features of starch, continue to play a major role during digestion. Rice has the smallest individual starch granules among the cereal grains, ranging from 3 to 9 μm (Aller et al., 2011). In general, smaller granular size is associated with an increased surface-to-volume ratio, which increases the contact between substrate and enzyme (Blaak et al., 2012) and hence is associated with a proportional increase in digestibility. Initial starch hydrolysis rates, within 10 min (Kong, Kim, Kim, & Kim, 2003) to 12 min (Sheu et al., 2011), were higher in native rice starches when compared to larger starch granules from different botanical origins, including maize, potato, wild pea, and wheat. Wang et al. (2017) observed the same trend and reported that available surface area was a crucial factor in the binding efficiency of the enzyme to 11

Trends in Food Science & Technology 88 (2019) 10–22

M.R. Toutounji, et al.

digestive processes. Aside from looking at rice flours with and without the removal of proteins, Ye, et al. (2018) also investigated the starch digestibility of rice flour with and without the removal of lipids. The starch digestion of cooked rice flour containing endogenous lipids was significantly lower than samples that had lipids removed by petroleum ether extraction. In addition, the starch digestion of rice flour without lipids was slightly lower than the samples without proteins, despite the lipid content being ten times lower than protein content (Ye et al., 2018). Reduced starch digestibility was attributed to endogenous lipids attaching to the starch granular surface, thus reducing accessibility to enzymes. Furthermore, upon gelatinisation of rice flour (discussed in more detail section 3), endogenous lipids were suggested to reduce starch granular swelling, and thus reduce the substrate surface area for enzymatic degradation (Ye et al., 2018). Specific interactions between amylose and lipids appear to be an important factor affecting the digestibility of cereal starches, including rice. A single-helical (V-type) conformation, with six glucosyl residues per turn, is observed when amylose chains bind with small hydrophobic molecules, including lipid molecules (fatty acids, mono- and diglycerides) (Eliasson, 1994). The helix cavity is essentially a hydrophobic tube which, under physiological conditions, easily traps the hydrocarbon chain of the lipid molecule by van der Waals forces, leaving the polar ends of the lipid outside of the helix cavity (Morrison, 1995). The conformational change (random coil to helix) of amylose interferes with the enzyme-starch binding mechanism (Vasanthan & Bhatty, 1996). Starch-lipid complexes have been implicated as a major contributing factor in the lowering the glycemic response of cooked rice with higher amylose levels (Goddard, Young, & Marcus, 1984; Shu, Jia, Ye, Li, & Wu, 2009). Enzymatic resistance of complexes was demonstrated to increase with increasing crystallinity, amylose degree of polymerization, lipid-chain length, and complexation temperature (Eliasson & Krog, 1985; Gelders, Duyck, Goesaert, & Delcour, 2005; Tufvesson, Wahlgren, & Eliasson, 2003). Long-chain saturated monoglycerides were shown to be more resistant to enzymatic hydrolysis compared to short-chain saturated and unsaturated monoglycerides when complexed with cooked rice starch (Guraya, Kadan, & Champagne, 1997). In summary for Section 2, it appears that the most important intrinsic factor influencing rice starch digestibility is the relative proportions and structure of amylose and amylopectin (Butardo et al., 2019). Other components such as storage proteins and lipids play minor contributory roles (Butardo & Sreenivasulu, 2016). It must be noted here, however, that the removal of endogenous proteins and lipids by enzymatic treatment in previous studies could have confounding effects on the digestibility of rice samples. In addition, although not discussed here, the composition and structure of non-starch polysaccharides in influencing digestibility is also beginning to emerge (Butardo et al., 2017; de Guzman et al., 2017).

crystalline polymorph, C-type, is as a combination of A-type and B-type. The polymorph of rice is relevant for its digestibility because Zhang, Ao, and Hamaker (2006) reported that rice starch (A-type) had three times more RDS content than potato starch (B-type). In addition, shifts in rice crystalline polymorph from A to C to B in the same genetic background has been demonstrated to reduce the digestibility of cooked white rice grain in vitro (Butardo et al., 2011). Increased digestion rate of A-type starches was previously thought to be due to a more uneven granular surface resulting in a greater accessible surface area compared to B-type starches (Williamson et al., 1992), however the presence of pores has recently been observed on the surface of raw B-type rice starches (Dhital, Butardo, et al., 2015). The proposed major determinant for reduced enzymatic hydrolysis of B-type rice starch granules was a higher proportion of long chain amylopectin (Butardo et al., 2011; Dhital, Butardo, et al., 2015). This is because elevated proportions of long amylopectin chains have been associated with increased gelatinisation temperature (Butardo et al., 2011), more stable double helices, and stronger crystallites (Wang et al., 2017). 2.2. Proteins White rice contains only around 4–11% proteins (Butardo & Sreenivasulu, 2016). Up to 95% of the endosperm rice protein is in the form of discrete particles called protein bodies (Shih, 2004). Interactions between protein and starch in a food matrix appear to play a role in the rate of starch digestibility of cereals (Jenkins et al., 1987; Rooney & Pflugfelder, 1986; Wong et al., 2009). However, limited studies have investigated the role of starch-protein interactions and their influence on starch digestibility in rice. The scarcity of studies in this space is probably due to the observation that increasing the storage protein content in rice can lead to an increase in hardness, which can in turn negatively affect textural properties and consumer acceptance (Butardo et al., 2019). In one recent study, Ye, et al. (2018) reported a significant increase in starch digestibility after removal of proteins by protease treatment of native long-grain indica rice flour. It was suggested that access to the digestive enzymes was restricted due to attachment of endogenous proteins to the starch granule surfaces as a reduction in granular swelling. Further studies are warranted to explore endogenous protein-starch interactions in rice and its effect on digestibility of starch. For instance, it would be useful to conduct a digestibility experiment using samples with the same genetic background but differing in storage protein contents as the protease treatment methodology described by Ye et al. (2018) might have altered other factors that contribute to rice digestibility. In addition, it would be interesting to identify rice accessions from diverse germplasm collection that have elevated protein content but still retain their soft textural properties as these are preferred by the majority of the Southeast Asian consumers (Butardo et al., 2019). Utilisation of novel processing techniques or other extrinsic factors (section 3) may offer a solution to achieving acceptable sensory properties when protein contents are elevated.

3. The role of extrinsic factors Native starch is often modified to improve specific functional properties. Although, chemical and enzymatic modification of starch is widely implemented, physical modification is preferred in the food industry as it often reduces food safety risks and does not compromise the positive perception of starch as a natural food material (Zavareze, Storck, de Castro, Schirmer, & Dias, 2010). Ageing, hydrothermal processing, parboiling and cooking are all extrinsic factors that affect starch digestibility. Table 1 summarises research that has been conducted to elucidate the impact of these processes on rice digestibility.

2.3. Lipids Lipids in rice are mainly stored in the form of spherosomes, or spherical organelles, which are distributed in the aleurone layer plus the seed coat (56%), in the embryo (22%), and in the endosperm (22%) (Bradbury & Collins, 1982). The majority of lipids in rice, located in the embryo and aleurone layer, are collectively known as non-starch lipids. The lipids that are associated with starch granules (starch lipids) have been found to occur on the surface (surface starch lipids) or inside the granule (true starch lipids). The lipid fractions in rice endosperm mostly consist of lysophospholipids, especially lysophosphatidylcholine (LPC), lysophosphatidylethanolamine (LPE) and lysophosphatidyl-inositol (LPI), and free fatty acids (Morrison, 1988). While the proportion of lipids in white rice is lower than protein and much lower than starch components, they still appear to inhibit

3.1. Storage Limited information is available in the literature on the effects of storage on rice starch digestibility. In an ageing study of Jasmine brown rice at ambient temperature, the storage period of 7 months had no 12

Processing technique

13

Storage

Waxy starch

White grain

White grain

White grains

Waxy starch

White grain

White flour

• %HI starch hydrolysed • EGS • VRDS • RDS • SDS • RS •

of • Degree gelatinisation

hydrolysed • Starch (g/100 g)

Digestibility expressed as

days

of different amorphous matrices in • Formation partially gelatinised and retrograded starch

influences the accessibility of enzymes

ordered crystalline structure in retrograded • Less starch compared to partially gelatinised starch

• Recrystallization of previously gelatinised starch

•

- macropores control starch availability to alphaamylase Differences between lipid and amylose contents between two varieties of rice

volume in grains • Gap - micropores control degree of starch gelatinisation

Proposed mechanism

•

- glucose content ↓ - RDS ↓ - SDS and RS ↑ At 240 min of digestion, microwaved rice stored for 72 h had ↓ reducing sugar content compared to rice cooked in a rice cooker - rice at 4 °C was lowest - rice at −18 °C was highest Extent of hydrolysis ↓ in processed starch compare to native starch At 20 min, 60 min and 90 min, digestibility levels of processed starch were 21%, 42% and 45%

storage time ↑ (regardless of temperature): • As- reducing sugar content ↓

↓)

and intra- units

Borah et al. (2017)

Li et al. (2014)

Chiu and Stewart (2013)

Chung et al. (2010)

Chung et al. (2006)

Hu et al. (2004)

Hibi, Kitamura, and Kuge (1990)

Ito et al. (1988)

References

(continued on next page)

helical reorientation within crystalline • double domains in the development of imperfect crystalline • increase domains and Ap chain entanglement among inter-

nucleus for recrystallization, thus accelerated the rate of crystallisation during storage

gelatinisation by microwave was incomplete • Starch and incompletely gelatinised starch provided a

led to ↑ RDS, ↑ RS, ↓ SDS content • Cooking • amyloseparameters • RSCold storage after cooking led to ↓ RDS, ↑ SDS, ↑ • pasting to starch crystalline structures with • changes processing cooker: RS ↑ after retrogradation (except in variety of intrinsic and extrinsic factors affecting • Rice • Adigestibility the Jasmine variety - no effect). cooker or oven: retrogradation had no • Pressure effect on RS (except in the Jasmine variety which

65 °C) and RE (7 day) treatments

Digestibility of retrograded rice ↓ than cooked • rice Digestibility of retrograded rice ↓ with storage • time rice digestibility ↑ up to 3 h and then ↓ • Non-waxy with storage time rice digestibility was unchanged after 3 h • Waxy and then ↓ with storage time ↓ HI and EGS for all varieties • Retrogradation retrogradation effect among cultivars of • Highest similar amylose contents among waxy cultivars ↓ as the degree of gelatinisation ↑and the • RSdegree of retrogradation ↓ PG starches (7.7–8.6%) was slightly lower • RSthanofnative starch (9.3%) of RE starches (3.0–3.8%) was similar to • RSgelatinised waxy starch (2.9%) ↓ by GW and ↑ by RE • SDS starches had ↓ SDS than PG starches • RE content ↑as a result of gelatinisation • RDS content of GW was the highest (87.9%) • VRDS which was effectively reduced by PG (60 °C,

Effect on digestibility

starch to water, 1:2, w/v and 90 °C for • Gelatinisation: • % starch hydrolysed • 30 min to RT • Equilibration • cycle of crystallisation with: temp cycles of • Repeated 4/45 °C, 24 h time interval of cycles, cycle duration 5

cooked by microwave oven (700 W) and rice sugar • Grains • Reducing cooker (100 °C for 30 min) content (mg/g) content • Cold storage at −18, 4 and 25 °C for 6, 24, 48 or 72 h • Glucose (mg/g) • RDS • SDS • RS

cooked (rice: water, 1:6, w/v) in an electric • Grains • RDS cooker • SDS • Cold storage at 4 °C for 2 and 7 days • RS •RS cooked by rice cooker, conventional oven and • Grains pressure cooker • Cold storage at 4 °C for 3 days

cooked • Grains storage at 5 °C for 1, 3, 5, 24, 48, 144 h • Cold • Made into flour 180 °C for 30 min in excess water • Gelatinisation: • Cold storage at 4 °C for 24 h (GW) • Gelatinised gelatinised (PG): heating at 60 °C, 65 °C, and • Partial 70 °C (RE): cold storage at 4 °C for 2, 4 and 7 • Retrograded days

• •

Gelatinisation/Retrogradation White grain Grains cooked by steaming Cold storage at 5 °C for 1 and 2 days

Samples used in digestion

Table 1 Summary of the effects of processing on the in vitro starch digestion of white rice.

M.R. Toutounji, et al.

Trends in Food Science & Technology 88 (2019) 10–22

14

• • •

HMT: Starches adjusted to 20% MC w.b., Equilibration at RT until needed Heating by microwave oven for 60 min

Waxy and nonwaxy starch

• • •

HMT: Starches adjusted to 20% MC, w.b., Equilibration at RT for 1 h Heating by microwave oven and conventional oven for 30 and 60 min

Waxy and nonwaxy starch

• •

• • • • • •

• RDS • SDS • RSSDI • • % starch hydrolysed

grains soaked in excess water for 8 h at • Paddy ambient temperature (approx. 28 °C) until hull loosened • Boiling • Cooling in sun to 12–13% MC • Drying grains soaked for approx. 16 h • Paddy for 30 min • Steaming to temperature gradients that facilitate • Exposure rapid retrogradation of starch

• • •

After parboiling (compared to native starch): RDS ↑ SDS ↓ RS ↓

•

63.5% compared to 61.0% and 75.7% for native rice, respectively ↓ RS content: 0.23% for native rice and 0.60% for processed rice

Digestibility at 30 min and 120 min time• ↓points: processed samples were 45.0 and

• •

Parboiling (compared to unparboiled samples): SDI ↓ RS ↓

digestion rate ↓ for samples stored at • Overall 37 °C velocity (slope of digestion curve within • ↓firstinitial 20 min) for samples stored at 37 °C extent ↓ samples stored at 37 °C • digestion • rice with ↑ Am content achieved ↑ aging ↑ in quick-cooking and parboiled • digestibility rice and ↓ in parboiled rice • No effect on RS levels

Effect on digestibility

(potentially induced by lipid-amlyose complexes or retrogradation) changes in structure of the rice grain (cohesiveness of the grain or different pore size distribution) making the surface less accessible to enzymatic attack formation of heat resistant amylose-lipid complexes II

gelatinisation and starch molecular • Extensive breakdown

retrogradation

temp shifted towards a higher temp (DSC)

due to: starch retrogradation, increased • Potentially hardness of rice RS due to: Am-lipid complex formation, • Increased carbohydrate-protein interactions, starch

digestibility in processed rice correlated with: • Lower higher insoluble Am, lower pasting profile (RVA), gel

•

•

↑ digestibility, this effect was ↑ for • Waxy: starches heated for 30 min than for 60 min • Non-waxy: No effect

• No effect

maltose per gram of • mg sample

maltose per gram of • mg sample

• • • • •

Anderson and Guraya (2006)

Anderson et al. (2002)

(continued on next page)

- macropores control starch availability to alphaamylase change in orientation of starch polymers in granules degree of starch degradation – starch more accessible to amylase gelatinisation of starch increase in setback viscosity allowing more water penetration and hydration of the granules No change to crystalline structure of starches/gross morphological structure

Ito et al. (1988)

Dutta et al. (2015)

Guha et al. (2011)

Tetens et al. (1997)

Casiraghi et al. (1993)

in hydration-facilitated disruption of • reduction starch granules in aged rice • Am content starch availability to alpha-amylase due to • reduced changes in starch structure after HMT processing

strengthen structure in grain

Zhou et al. (2016)

References

structure changes during storage - ↑ cell wall • grain remnants during ageing which might lead to

Proposed mechanism

of HMT rice ↓ than cooked rice volume in grains • starch hydrolysed (g/100 g) • Digestibility • Gap (control) - micropores control degree of starch gelatinisation

• RDS • SDS • RS

• % starch hydrolysed

release (mg/ • glucose mL)

Digestibility expressed as

and quick-cooking parboiling – • Parboiling conditions not stated

and 37 °C • 46 °Cmonths for digestibility shows up to 12 • months of(data storage)

Processing technique

Dry heat parboiling: paddy grains soaked in approx. 60 °C excess water slow cooked in the water for 18 h Excess water drained Roasting with sand at 140 °C for 11, 13, 15 min and 200 °C for 3, 4 and 5 min Cooling at RT for 6 h Stored at 4 °C Heat Moisture Treatment (HMT) and Annealing (ANN) White grain HMT: Grains adjusted to 20% MC Heating process not described.

Flour

Flour

White grains

Parboiling* White grains

White grains

Samples used in digestion

Table 1 (continued)

M.R. Toutounji, et al.

Trends in Food Science & Technology 88 (2019) 10–22

HMT: Starches (high Am, medium Am, waxy) adjusted to 30% MC Equilibration at RT for 24 h Heating at 110 °C for 8 h

HMT: Paddy grains adjusted to 13%, 16% and 18% MC Autoclaved at 120 °C and 1 kPa pressure for 30 and 60 min Equilibration to 15 °C for 24 h Paddy grains dehulled and milled White grains ground to flour HMT: Grains adjusted to 10, 20 and 30% MC Equilibration at 4 °C for 24 h Heating at 110 °C for 4 h ANN: Starch slurry adjusted to 80% MC Heating at 50 °C for 24 h HMT: Starch adjusted to 25% MC, Equilibrated to 4 °C for 12 h, Oven heating at 110 °C for 8 h ANN-HMT and HMT-ANN: according to Stute (1992) and Chung, Hoover, and Liu (2009)

Starch

Flour

15

Waxy starch

Starch

HMT: Starches adjusted to 15, 20 and 25% MC Equilibration at 4 °C for 4 days Autoclaved at 110 °C for 1 h

Starch

• • • • • • • • • • • • • •

• • •

• • •

Processing technique

Samples used in digestion

Table 1 (continued)

starches had ↓RDS, but ↑ SDS and RS • HMT • ↑SDS and RS ↑ in HMT with higher MC

• RDS • SDS • RS • RDS • SDS • RS • • • •

Compared to native starch: ANN: ↑ RDS levels and ↓ SDS and RS HMT: ↓ RDS and RS but ↑ SDS ANN–HMT: ↑ RDS and SDS but ↓ RS HMT–ANN: ↑ RDS and ↓ SDS and RS levels.

• • •

•

•

•

After HMT (compared to native starch): RDS ↓: - waxy: 77.0 to 57.6% - medium Am: 79.5 to 65.3% - high Am: 90.0 to 73.2% SDS - ↑ waxy: 12.9–24.0% - ↓ medium Am: 14.0 to 10.8% - ↑ high Am: 3.7–4.5% RS ↑ - waxy: 10.2–22.4% - medium Am: 6.5–23.9% - high Am: 6.3–22.4% RDS ↑ samples treated for 30 min and ↓ samples treated for 60 min All samples showed variation in SDS HMT caused ↑ RS

compared to HMT 15% and HMT 20% and their respective native starches

25% had ↑concentration of reducing • HMT sugars at all times during hydrolysis,

Effect on digestibility

• RDS • SDS • RS

• RDS • SDS • RS

• g glucose per 100 g starch

Digestibility expressed as

•

•

•

Zeng et al. (2015)

effect of ANN on digestibility has been attributed • The to:

(continued on next page)

- increases in granule porosity (increases digestibility) - crystalline perfection (decreases digestbility) The effect of HMT on digestibility has been attributed to: - moisture content during HMT - Am-lipid interactions - AmeAm, Am-Ap and/or Ap-Ap interactions Further increases in RDS and SDS and decreases in RS with ANN-HMT are indicative of disruption of crystallites that were perfected upon ANN Decreases in SDS and RS levels and increases in RDS levels in HMT-ANN might result from disrupted crystallites that could not be perfected anymore (consistent with decreased crystallinity and gelatinisation enthalpy)

Wang et al. (2018)

Silva et al. (2017)

Van Hung, Chau, et al. (2016)

Zavareze et al. (2010)

References

apparent amylose content ↑with ↑MC, so HMT could • favour the formation of Am-lipid complexes

which could be converted to RS or RDS after • SDS treatment variety of intrinsic and extrinsic factors affecting • Adigestibility

partly restricting accessibility of starch chains to enzymes

digestbility of processed rice correlated with ↓ • ↑crystallinity digestbility of processed rice may be due to: • ↑accessibility of the amorphous areas by the enzyme • by disruption (especially near the surface of • crystalline the granule) of double helical structures in the • dissociation amorphous regions in thermostable SDS and RS after HMT: interactions • ↑formed during HMT survived after gelatinisation –

Proposed mechanism

M.R. Toutounji, et al.

Trends in Food Science & Technology 88 (2019) 10–22

16

White grains

White flour

White grains

• •

•

o Electric cooker: 25 min o Autoclaving: 45 min o Stone pot: 15 min Cooked grains were frozen at −70 °C, freeze-dried and then ground to flour and passed through 180 μm sieve Pressure cooker: 6–7 min Microwave oven: 13–16 min

maltose per 100 g of • mg sample • % starch hydrolysed

Proposed mechanism

• •

•

compared to boiling (54.3%) - Inga, only slight difference: pressurecooking (67%) compared to boiling (70.2%) - Japonica, only slight difference: pressurecooking (75.1%) compared to boiling (74.6%) RDS was slightly ↓ for pressure-cooked rice compared to boiled for all varieties Compared to raw flour: autoclaving and parboiling had ↑ RDS and ↑ SDS microwaving had no effect on RDS and SDS

% starch hydrolysed starch • Cooking digestibility twofold • Cooking method: no effect

• • • •

- ↑ RAG - ↑ SDI Pressure cooking and steaming had ↑ RS Microwaving ↓ digestibility rate Autoclaving ↑ digestibility Hydrolysis kinetic constants: autoclave (27.9), stone pot (27.2), electric cooker (23.6), microwave oven (22.7)

–

in microstructures, which were caused by the different cooking methods

Khatoon and Prakash (2006)

Lee et al. (2005)

Rashmi and Urooj (2003)

Niba (2003)

Sagum and Arcot (2000)

Dias et al. (2010)

References

(continued on next page)

rate of starch digestibility coincided with degree • The of gelatinisation and were influenced by differences

gelatinisation. Note: maximum gelatinisation was reported in all variations with the exception of one rice variety when pressure cooked.

in amount of water used in the 4 cooking • Variations methods may have influenced the extent of

of the amylose present, especially with • Modification further processing (autoclaving and parboiling)

at 2 h time-point: • Digestibility • none given - Doongara after pressure-cooking (65.2%) ↑

medium- and low- Am starches

↑ the % starch hydrolysed and this effect likely promotes changes in the amorphous • ANN • ANN was more intense as the ANN temperature ↑ areas of granules, making them more susceptible to the action of the enzyme. Evidenced by: and medium-Am starches ANN at 55 °C • highhad ↑ hydrolysis percentage and greater signs lowered crystallinity (HMT55 had the lowest relative • of disintegration than low-Am starch ANN at crystallinity) 55 °C high-Am starch had more pores on granular • ANN surface but ANN only slightly affected morphology of

Effect on digestibility

when compared to other cooking • RDS • Steaming methods: • SDS - ↓ RDS • RSrapidly available glucose - ↓ RAG • (RAG) - ↓ SDI ↑ SDS • starch digestion index (SDI) -Pressure • - ↑ RDS cooking and boiling:

• RDS • SDS

soaked for 1 h (rice: water, 1:5, w/v) before • Grains • % starch hydrolysed cooking methods: • Cooking o Microwave oven (2450 MHz): 9 min 36

• • • • •

o Microwave oven (750 W): 20 min with stirring halfway o Parboiling: 60 °C for 120 min Cooked samples were freeze-dried for 48 h Pressure cooking: 50 g sample in 75–100 mL water for 4–12 min Boiling: 50 g sample in 250–700 mL for 15–35 min Boiling and straining: 50 g sample boiled in 350–600 mL water and remaining water drained Steaming: 50 samples steamed with 75–100 mL water for 20–40 min

added to water (rice: water, 1:5, w/v) • Samples before cooking methods: • Cooking o Autoclaving: 121 °C for 60 min

boiling water for 20 min (rice: water, 1:2, maltose per gram of • Boiling: • mg w/v) sample cooker: 15 psi for 10 min (rice: water, 1:2, • Pressure • %RDSstarch hydrolysed w/v) • SDS • RS •

Cooking White grains

White flour

• •

• % starch hydrolysed

ANN: Starches treated with excess water (1:9 starch/ water, w/w). Incubation in a water bath at 45, 50 and 55 °C for 16 h

Starch

Digestibility expressed as

Processing technique

Samples used in digestion

Table 1 (continued)

M.R. Toutounji, et al.

Trends in Food Science & Technology 88 (2019) 10–22

17

Digestibility expressed as

sugar content • reducing (mg/g) content (mg/g) • glucose • RDS • SDS • RS% starch hydrolysed • hydrolysis index (HI) • estimated glycemic index • (eGI)

• RS

•

•

o Rice cooker: 10 min followed by 10 min on warm setting o Pressure cooker: 70 kPa until cooker could be opened Pre-soaked grains (rice: water, 1:1, 1:1.5, 1:2, w/v) were kept at room temp for 1 h and then cooked as described for non pre-soaked grains Cooked grains were frozen at −80 °C overnight, freeze-dried and then ground to flour and passed through 150 μm sieve

pre-soaked grains (rice: water, 1:1, 1:1.5, 1:2, • Non • % starch hydrolysed w/v)

cooked: 20 min in boiling water • Fully cooked: 10 min in boiling water • Partially • All samples cooled for 30 min at 25 °C

• • • • • •

water, 1:2, w/w) and the mixture was boiled on a stove and placed inan oven at 177 °C until water absorbed. After removing from the oven, the rice was kept at room temperature for 10 min. Rice cooker: 20–30 min (rice: water, 1:1.5, v/v) Conventional oven: 175 °C for 30 min (rice: water, 1:1.5, v/v) Pressure cooker: 6 min (rice: water, 1:4, v/v) then remaining water strained from rice Washing and presoaking of grains in water (1:1, w/ w) at 40 °C for 30 min Rice cooker: 100 °C for 30 min Microwave oven: at 600 W for 15 min, 2 min rest, cooking for an additional 7.5 min

cooker: 20 min cooking followed by 12 min on • Rice • %RDSstarch hydrolysed warm setting (rice: water, 1:2.5 and 1:2, w/w) • SDS rice: rice cooker rice was held at 4 °C for • Stir-fried • RS 24 h and then the rice was stir-fried in a pan (93 °C) • with corn oil (10% d.b.) for 3 min rice: precooking grains with corn oil (10%. • Pilaf d.b.) at 88 °C for 2 min. Water was added (rice:

Processing technique

• no effect

kinetic constant

Fully cooked ↑ HI and eGI compared to • partially cooked cooked vs partially cooked: no effect on • Fully equilibrium starch hydrolysis percentage and

uncooked

cooked ↑ equilibrium starch hydrolysis • %,Fullykinetic constant, HI and eGI compared to

method: no effect on RDS, SDS and • Cooking RS content

oven baking

effect for 3 of the 4 samples • No Pressure cooking ↓ RS content of a jasmine • rice variety compared to the rice cooker and

↑ RS • Stir-frying contents were highest for samples • RDS prepared by rice cooker

prepared in a rice cooker

rice had lowest digestibility, • Stir-fried followed by pilaf rice and then the samples

Effect on digestibility

–

–

–

–

and lipid coating of the starch during stir-frying with corn oil

formation of retrograded starch during cold • The storage, the development of amylose-lipid complex,

Proposed mechanism

Wang et al. (2017)

Tamura et al. (2016)

Li et al. (2014)

Chiu and Stewart (2013)

Reed et al. (2013)

References

AAC, apparent amylose content; Am, amylose; ANN, annealing; Ap, amylopectin; EGI, estimated glycemic index; EGS, estimated glycemic score; GW, gelatinised; HI, hydrolysis index; HMT, heat moisture treatment; MC, moisture content; PG, partially gelatinised; RAG, rapidly available glucose; RDS, rapidly digested starch; RE, retrograded starch; RS, resistant starch; RT, room temperature; SDI, starch digestion index; SDS, slowly digested starch; VRDS, very rapidly digested starch. *parboiling process involving paddy grains.

White flour

White grains

White grains

White grains

White grains and flour

Samples used in digestion

Table 1 (continued)

M.R. Toutounji, et al.

Trends in Food Science & Technology 88 (2019) 10–22

Trends in Food Science & Technology 88 (2019) 10–22

M.R. Toutounji, et al.

and increase the RS content of cooked rice (Chiu & Stewart, 2013). Benmoussa et al. (2007) investigated the digestibility 12 rice flours with a narrow range (15.84–17.18%) of amylose content after cooking and subsequent cooling. Starches from rice cultivars with high levels of long and intermediate/short debranched amylopectin linear chains were positively correlated with SDS and negatively correlated with RDS. Starches with very short amylopectin linear chains had the highest levels of RDS and the lowest levels of SDS. Interestingly, increased RS levels observed in fried-rice samples were driven by retrogradation during the cold storage (prior to stir-frying) and to a lesser extent by amylose-lipid complex formation (Reed, Ai, Leutcher, & Jane, 2013). In addition, partially-gelatinised rice starches, which contain an even higher amount of crystalline ordering, were shown to be more resistant to enzymatic digestion compared to retrograded samples (Chung et al., 2006). From these studies, it seems that the retrogradation process can reduce the starch digestibility of cooked rice, especially those cultivars with high levels of long linear amylopectin chains. In this case, the intrinsic biochemical properties of rice grains (i.e. starch supramolecular structure) had a significant impact on extrinsic processing (i.e. retrogradation), leading to reduced starch digestibility.

effect on starch digestibility of cooked samples (Jaisut, Prachayawarakorn, Varanyanond, Tungtrakul, & Soponronnarit, 2009). In a more recent study, the effects of ageing-induced changes in white rice grains were investigated following storage at 4 °C and 37 °C for 12 months (Zhou, Yang, Su, & Bu, 2016). Samples were cooked as white grains and then freeze-dried prior to digestion. The rice stored at 37 °C exhibited a lower initial velocity (slope of digestion curve within the first 20 min) and a lower overall rate of digestion compared to the rice stored at 4 °C. Reduced digestibility of aged rice stored at 37 °C was attributed to an increase in cell wall strength and a reduction in hydration-facilitated disruption of starch granules (Zhou et al., 2016). Hence, storage could play a role in modulating starch digestibility but this is may only be observed when the ageing process is accelerated (e.g. at a high storage temperature of 37 °C). However, due to limitations in the study design (only 3 varieties and 2 storage temperatures), more research is needed to verify this result. 3.2. Gelatinisation Heating native starch granules in the presence of water causes the granules to swell to several times their original size, leading to disintegration and transformation into a paste or a gel. This process, termed gelatinisation, involves the structural transformation of native starch to reduce or eliminate its semi-crystallinity, birefringence, and higher order supramolecular structure by moist heat denaturation. Chung, Lim, and Lim (2006) evaluated the effect of various gelatinisation processes (complete and partial) by heat treatment at different temperatures (60, 65, or 70 °C for 5 min). The results indicated that the completely gelatinised waxy rice was more susceptible to enzymatic hydrolysis followed by the partially gelatinised and the native starch. Furthermore, it was observed that as the gelatinisation temperature increased, the RDS increased, while the RS and SDS contents decreased. A similar trend was observed in non-waxy samples, whereby an increase in hydrolysis index and estimated GI was observed as the rice cooking degree increased (Tamura, Singh, Kaur, & Ogawa, 2016). Structural changes in starch caused by the gelatinisation process appear to significantly influence the digestibility of cooked rice starch. Several studies have demonstrated a negative correlation between amylose content and starch digestion of cooked rice starches (Kong et al., 2015) and white grains (Brand-Miller, Pang, & Bramall, 1992; Denardin, Walter, da Silva, Souto, & Fagundes, 2007; Tetens et al., 1997). In contrast, rice varieties with similar high-amylose rice that were cooked for their minimum cooking time did not differ in starch digestibility (Panlasigui et al., 1991). Thus, physicochemical properties of rice as influenced by amylose content (Wickramasinghe & Noda, 2008) and amylose leaching during gelatinisation (Lii, Tsai, & Tseng, 1996), may be a greater predictor of starch-digestion rate than amylose content alone (Panlasigui et al., 1991).

3.4. Parboiling Parboiling is a hydrothermal treatment aimed to improve storage life, head rice yield and nutritional properties of rice grains (Bhattacharya, 2011). Conventional parboiling involves processing paddy rice grains by soaking and subsequent draining of excess water, cooking (usually with steam) to gelatinise the starch, followed by drying prior to being milled (Bhattacharya, 2011). Less common parboiling methods have slightly altered treatments after the soaking step, for example low moisture parboiling (high-pressure steaming) and dryheat parboiling (combined conduction heating/drying step) (RochaVillarreal, Serna-Saldivar, & Garcia-Lara, 2018). Conventional parboiling has generally been observed to lower the digestibility of rice both in vivo (Wolever et al., 1986) and in vitro (Bhattacharya, 2011; Casiraghi, Brighenti, Pellegrini, Leopardi, & Testolin, 1993; Guha, Umesh, Reddy, & Malleshi, 2011; Juliano, 2004; Tetens et al., 1997; Wolever et al., 1986). Pressure parboiling was shown to be especially effective for rice, lowering the GI (in vivo) by 30% compared to non-parboiled rice (Larsen et al., 2000). It was presumed that the high amylose content of the rice variety used in this study along with the extent of the parboiling method allowed for the formation of higher amounts of type II amylose-lipid complexes (consists of well-defined crystallites with a melting temperature above 100 °C). However, there is some evidence that parboiling treatments do not always lower rice digestibility. There was no difference between the GI of conventionally parboiled and non-parboiled rice (Larsen et al., 1996). However, it must be noted that in the same study, the GI of parboiled rice with high amylose content was lower than that of parboiled rice with a low amylose content. Another study demonstrated that dry heat parboiling increased RDS and lowered RS leading to increased starch digestibility (Dutta, Mahanta, & Singh, 2015). Reduced starch digestibility of parboiled rice has been attributed to retrogradation of gelatinised starch after the parboiling process, increased lipid-amylose complexation, increased hardness of the rice and changes to granular surface morphology (Casiraghi et al., 1993; Guha et al., 2011). Thus, studies that have reported an increased starch digestibility after parboiling treatment may be due to insufficient time for retrogradation of starch to occur between the gelatinisation and drying steps.

3.3. Retrogradation Retrogradation is the recrystallization of amylose (short-term) and amylopectin (long-term). The process is characterized by a series of physical changes including increased viscosity and turbidity of pastes, gel formation, exudation of water and increased degree of crystallinity (Hoover, Hughes, Chung, & Liu, 2010). The highest crystallisation rates (nucleation) for rice were observed at 4 °C (Baik, Kim, Cheon, Ha, & Kim, 1997). Enzymatic susceptibility to retrograded rice starch seems to be determined by the extent of structural disruption of the starch during gelatinisation and the subsequent reordering of the molecules during the process of retrogradation (Wang, Li, Copeland, Niu, & Wang, 2015). Retrogradation by cold storage, and subsequent reordering of the starch molecules, has been demonstrated to lower the starch digestibility rate (Benmoussa, Moldenhauer, & Hamaker, 2007; Borah, Deka, & Duary, 2017; Chung et al., 2006; Chung, Liu, Wang, Yin, & Li, 2010; Hu, Zhao, Duan, Zhang, & Wu, 2004; Li, Han, Xu, Xiong, & Zhao, 2014)

3.5. Heat-moisture treatment and annealing Heat moisture treatment (HMT) and annealing (ANN) are processes aimed to alter the properties of starch by the manipulation of temperature and moisture levels. Both hydrothermal treatments involve 18

Trends in Food Science & Technology 88 (2019) 10–22

M.R. Toutounji, et al.

et al., 2015). The effect of combined modifications by HMT and ANN on rice starch digestibility has also been investigated. One study observed that treatment by ANN-HMT increased RDS and SDS content and lowered RS content in waxy rice starch, which was likely the result of crystalline disruption by HMT (Zeng et al., 2015). Other studies noted an increase in RS content for ANN on acid treated rice starch (Van Hung, Chau, et al., 2016) and ANN-cross-linked starch (Song, Park, & Shin, 2011). While HMT and ANN treatments do not reach gelatinisation temperature, partial gelatinisation could be an important driver of digestibility in these hydrothermal treatments.

incubation at temperatures above the glass transition temperature but below the gelatinisation temperature. HMT is defined as heat incubation of starch at low moisture levels (< 35%, w/w) whereas ANN is heat incubation of starch in excess water (> 60%, w/w) or at intermediate water (40–55%, w/w) (Jacobs & Delcour, 1998). The effect of HMT on the rice starch digestibility was found to be inconsistent in the literature (higher, lower or no effect on digestibility). A higher rate of digestibility was demonstrated in waxy starches heated in either a conventional or microwave oven when compared to non-heated samples (Anderson, Guraya, James, & Salvaggio, 2002). Similarly, HMT rice starches produced by autoclaving had higher digestibility compared to their respective native starches (Zavareze et al., 2010). In contrast, decreased RDS and increased SDS and RS levels were observed in HMT rice starches (Van Hung, Chau, & Phi, 2016; Wang et al., 2018) and HMT rice flours heated for 60 min (Silva et al., 2017). In addition, when more realistic forms of rice was used (rice grains), the starch digestibility rates of HMT rice were lower when compared with steamed rice (Ito, Yoshida, Okazaki, & Kobayashi, 1988). One study observed no effect after HMT of waxy and non-waxy rice starches (Anderson et al., 2002). Inconsistencies in the effect of HMT on the starch digestibility of rice may be attributed to differences in the processing treatment used in terms of moisture content, temperature and time. For HMT samples adjusted to similar moisture levels and heated with similar temperatures, heating time was shown to influence digestibility. Longer heating time (60 min compared to 30 min) during HMT was shown to increase digestibility (Anderson et al., 2002; Silva et al., 2017) due to RS formation in these samples (Silva et al., 2017). However, an extended heating time of 8 h was shown to lower RS content in waxy rice starch as compared with native starch (Zeng, Ma, Kong, Gao, & Yu, 2015). Furthermore, the trend of decreasing RDS with increasing RS has been demonstrated in HMT starches with high, medium and low amylose content and is thought to occur (along with heat-stable SDS) due to amylose-amylopectin interactions formed during HMT which persisted after heat treatment (Van Hung, Chau, et al., 2016). However, this explanation contradicts another study which reported HMT waxy starches with reduced RDS to also have reduced RS levels (Zeng et al., 2015). This is probably because waxy starches have no amylose and lower proportion of long chain amylopectin (Butardo et al., 2017). Moisture content also influenced the extent to which HMT changed digestibility. HMT starches prepared by autoclaving at 15, 20 and 25% moisture were more susceptible to alpha-amylase, and this effect increased with increasing moisture content (Zavareze et al., 2010). In the same study, increased digestibility also correlated with decreased crystallinity whereby HMT starches were more vulnerable to crystalline disruption, especially near the granular surface, improving accessibility by hydrolytic enzymes. Conversely, starch digestibility was shown to decrease with increasing moisture content in samples adjusted to 10, 20 and 30% moisture (Wang et al., 2018). This was attributed to the disorganisation of original structure of starch followed by the rearrangement of starch molecules to allow for the formation of agglomerated starch granules and producing starch molecules with a higher degree of ordering (Wang et al., 2018). The major difference in HMT processing between the two contradictory studies was the use of high pressure during heating (Zavareze et al., 2010), which may have led to complete gelatinisation of the sample. It is possible that the introduction of high pressure during HMT enhanced partial gelatinisation and disruption of higher molecular order, exposing the long glucan chains to increased susceptibility to enzymatic digestion. ANN treatment and combined ANN-HMT treatments have an influence on rice starch digestibility. Rice starches treated by ANN have shown increased digestibility by alpha-amylase (Dias, Zavareze, Spier, de Castro, & Gutkoski, 2010), as well as increased RDS levels and decreased SDS and RS levels (Zeng et al., 2015). This trend has been attributed to an increase in granular porosity and a decrease in crystallinity which both facilitate enzyme access to the starch substrate (Zeng

3.6. Cooking methodology As mentioned previously, rice is unique among other grains in that it is mainly consumed in the white grain form (Butardo & Sreenivasulu, 2016). As a wholegrain, plain rice is cooked in water until it is soft and suitable for consumption, with cooked rice texture preference varying greatly between cultures (Butardo et al., 2019). The majority of rice cooking worldwide involves the use of an open or closed vessel over an open flame (or other source of heat) with either excess water (rapid/ gentle boil method) or where an exact amount of water is completely absorbed (absorption method) (Bhattacharya, 2011; Li et al., 2014). Less common cooking methods involve the use of a pressure cooker, a double boiler (steaming) or a microwave oven. The extent of cooking can be conveniently assessed by squashing white rice grains in between two glass slides. Absence of white core indicates complete cooking. During the cooking process, starch granules are gelatinised which greatly increases susceptibility to enzymatic degradation. Cooked, white rice samples were shown to have a significantly higher starch digestibility compared to uncooked samples in a number of in vitro (Khatoon & Prakash, 2006; Sagum & Arcot, 2000; Tamura et al., 2016) and in vivo studies (Jung et al., 2009; Wolever et al., 1986). Reduced starch hydrolysis in high amylose starches has been attributed to incomplete gelatinisation of amylose after normal cooking conditions (Bjorck, 1996). Tamura et al. (2016) investigated the impact of cooking degree on digestibility by cooking white nonwaxy rice grains in boiling water for 10 min (partially cooked) and 20 min (fully cooked). The fully cooked samples had an increased hydrolysis index and estimated GI than the partially cooked samples but had no significant difference was observed for the kinetics or equilibrium starch hydrolysis percentage. A similar result was reported by Chung et al. (2006) for partially gelatinised waxy rice starches. Rice cooking methodology can significantly influence starch digestibility. Hence, care must be taken in optimising the amount of water and length of time for cooking to ensure replicability and reliability of the digestibility assay. Rashmi and Urooj (2003) investigated the nutritionally important starch fractions of digested rice grains that were prepared by pressure cooking, boiling, boiling and straining and steaming. Among the cooking methods, steaming produce the lowest RDS and the highest SDS among all varieties. Lee, Lee, Han, Lee, and Rhee (2005) also reported the significant differences in rice starch digestibility as influenced by cooking methodology. In descending order, autoclaving had the highest digestibility, followed by cooking in a stone pot, electric cooker and a microwave oven. However, Li, et al. (2014) found that freshly cooked rice prepared in a rice cooker was found to have a lower digestibility than samples cooked in the microwave. Reed et al. (2013) investigated the effects of common rice cooking methods including preparation by rice cooker, stir-frying and pilaf (in a seasoned broth) on starch digestibility. Stir-fried rice had the lowest starch hydrolysis rate and highest RS content. Chiu and Stewart (2013) reported that the type of cooking equipment (rice cooker, conventional oven, pressure cooker) made no difference to the RS content of freshly cooked rice, with the exception of pressure-cooked Jasmine rice which had lower RS content. Similarly, Khatoon and Prakash (2006) found that there was no difference in the starch digestibility between samples prepared in the microwave and pressure cooker. From the above 19

Trends in Food Science & Technology 88 (2019) 10–22

M.R. Toutounji, et al.

studies, it appears that a higher rate of starch digestibility was associated with the cooking methods that coincided with degree of gelatinisation, regardless of cooking equipment. However, a more systematic study comparing different cooking methods using optimised cooking time and amount of water is needed to establish an accurate trend. In summary for Section 3, it appears that the most significant extrinsic factor influencing the rice grain digestibility are the primary processes of gelatinisation and retrogradation. This suggest that modifications to the methodology of secondary extrinsic factors such as parboiling and cooking could be a useful means to manipulate the digestibility of rice-based food.

Impact of postprandial glycaemia on health and prevention of disease. Obesity Reviews, 13, 923–984. Borah, P. K., Deka, S. C., & Duary, R. K. (2017). Effect of repeated cycled crystallization on digestibility and molecular structure of glutinous Bora rice starch. Food Chemistry, 223, 31–39. Bradbury, J. H., & Collins, J. G. (1982). Lipids of the major histological components of rice studied by C-13 nuclear magnetic-resonance spectroscopy. Cereal Chemistry, 59, 159–162. Brand-Miller, J., Pang, E., & Bramall, L. (1992). Rice: A high or low glycemic index food? American Journal of Clinical Nutrition, 56, 1034. Brouns, F., Kettlitz, B., & Arrigoni, E. (2002). Resistant starch and "the butyrate revolution". Trends in Food Science & Technology, 13, 251–261. Buléon, A., Colonna, P., Planchot, V., & Ball, S. (1998). Starch granules: Structure and biosynthesis. International Journal of Biological Macromolecules, 23, 85–112. Butardo, V. M., Anacleto, R., Parween, S., Samson, I., de Guzman, K., Alhambra, C. M., et al. (2017). Systems genetics identifies a novel regulatory domain of amylose synthesis. Plant Physiology, 173, 887–906. Butardo, V. M., Fitzgerald, M. A., Bird, A. R., Gidley, M. J., Flanagan, B. M., Larroque, O., et al. (2011). Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediated RNA silencing. Journal of Experimental Botany, 62, 4927–4941. Butardo, V. M., & Sreenivasulu, N. (2016). Chapter two - tailoring grain storage reserves for a healthier rice diet and its comparative status with other cereals. In W. J. Kwang (Vol. Ed.), International review of cell and molecular biology: Vol. 323, (pp. 31–70). Academic Press. Butardo, V. M., Sreenivasulu, N., & Juliano, B. O. (2019). Rice grain quality: State of the art and future prospects. In N. Sreenivasulu (Ed.). Rice grain quality: Methods and protocols. Humana Press. Cai, J. W., Man, J. M., Huang, J., Liu, Q. Q., Wei, W. X., & Wei, C. X. (2015). Relationship between structure and functional properties of normal rice starches with different amylose contents. Carbohydrate Polymers, 125, 35–44. Casiraghi, M. C., Brighenti, F., Pellegrini, N., Leopardi, E., & Testolin, G. (1993). Effect of processing on rice starch digestibility evaluated by in vivo and in vitro methods. Journal of Cereal Science, 17, 147–156. Chiu, Y. T., & Stewart, M. L. (2013). Effect of variety and cooking method on resistant starch content of white rice and subsequent postprandial glucose response and appetite in humans. Asia Pacific Journal of Clinical Nutrition, 22, 372–379. Chung, H. J., Lim, H. S., & Lim, S. T. (2006). Effect of partial gelatinization and retrogradation on the enzymatic digestion of waxy rice starch. Journal of Cereal Science, 43, 353–359. Chung, H. J., Liu, Q. A., Lee, L., & Wei, D. Z. (2011). Relationship between the structure, physicochemical properties and in vitro digestibility of rice starches with different amylose contents. Food Hydrocolloids, 25, 968–975. Chung, H. J., Hoover, R., & Liu, Q. (2009). The impact of single and dual hydrothermal modifications on the molecular structure and physicochemical properties of normal corn starch. International Journal of Biological Macromolecules, 44, 203–210. Chung, H. J., Liu, Q. A., Wang, R. L., Yin, Y. L., & Li, A. K. (2010). Physicochemical properties and in vitro starch digestibility of cooked rice from commercially available cultivars in Canada. Cereal Chemistry, 87, 297–304. Denardin, C. C., Walter, M., da Silva, L. P., Souto, G. D., & Fagundes, C. A. A. (2007). Effect of amylose content of rice varieties on glycemic metabolism and biological responses in rats. Food Chemistry, 105, 1474–1479. Dhital, S., Butardo, V. M., Jobling, S. A., & Gidley, M. J. (2015). Rice starch granule amylolysis Differentiating effects of particle size, morphology, thermal properties and crystalline polymorph. Carbohydrate Polymers, 115, 305–316. Dhital, S., Dabit, L., Zhang, B., Flanagan, B., & Shrestha, A. K. (2015). In vitro digestibility and physicochemical properties of milled rice. Food Chemistry, 172, 757–765. Dias, A. R. G., Zavareze, E. D., Spier, F., de Castro, L. A. S., & Gutkoski, L. C. (2010). Effects of annealing on the physicochemical properties and enzymatic susceptibility of rice starches with different amylose contents. Food Chemistry, 123, 711–719. Dutta, H., Mahanta, C. L., & Singh, V. (2015). Changes in the properties of rice varieties with different amylose content on dry heat parboiling. Journal of Cereal Science, 65, 227–235. Eliasson, A. C. (1994). Interactions between starch and lipids studied by dsc. Thermochimica Acta, 246, 343–356. Eliasson, A. C., & Krog, N. (1985). Physical-properties of amylose monoglyceride complexes. Journal of Cereal Science, 3, 239–248. Englyst, H. N., Kingman, S. M., & Cummings, J. H. (1992). Classification and measurement of nutritionally important starch fractions. European Journal of Clinical Nutrition, 46, S33–S50. FAO F. a. A. O. o. t. U. N.. (2017). Rice market monitor, Vol. 20 (Rome, Italy). French, D. (1972). Fine structure of starch and its relationship to the organization of starch granules. Journal of the Japanese Society of Starch Science, 19, 8–25. Gallant, D. J., Bouchet, B., & Baldwin, P. M. (1997). Microscopy of starch: Evidence of a new level of granule organization. Carbohydrate Polymers, 32, 177–191. Gelders, G. G., Duyck, J. P., Goesaert, H., & Delcour, J. A. (2005). Enzyme and acid resistance of amylose-lipid complexes differing in amylose chain length, lipid and complexation temperature. Carbohydrate Polymers, 60, 379–389. Gidley, M. J. (1987). Factors affecting the crystalline type (ac) of native starches and model compounds - a rationalization of observed effects in terms of polymorphic structures. Carbohydrate Research, 161, 301–304. Goddard, M. S., Young, G., & Marcus, R. (1984). The effect of amylose content on insulin and glucose responses to ingested rice. American Journal of Clinical Nutrition, 39, 388–392. Guha, M., Umesh, S. S., Reddy, S. Y., & Malleshi, N. G. (2011). Functional properties of slow carbohydrate digestible rice produced adapting hydrothermal treatment.

4. Conclusion Rice is arguably the most important source of dietary carbohydrate in the world and thus its use as a nutritional intervention tool in the management and prevention of diet-related chronic disease has been implicated. However, the digestibility of starch in polished rice is complex, influenced by an interplay between intrinsic food characteristics and extrinsic food processing factors. Intrinsic factors, such as the nature of the starch structure as well as starch-lipid and starch-protein interactions, play a fundamental role in digestibility. Although the impact of rice starch structure on digestibility needs further investigation, digestion rates tend to decrease as the length of glucan chains increase. There are limited studies on how lipids and proteins impact on starch digestibility. It appears that enhancing starch-protein and starchlipid interactions confer a reduction in digestibility by reducing substrate accessibility, however, further studies are need to substantiate this hypothesis. Furthermore, as rice is consumed and digested in the cooked form, understanding the interactions between intrinsic and extrinsic factors is required to fully understand its digestibility. Improving our knowledge on the intrinsic and extrinsic factors affecting starch digestion will assist in developing new rice varieties with altered digestibility properties. Enhancing our understanding of how processing impacts of starch digestibility may provide an effective tool for food manufacturers to modulate starch digestibility of existing rice varieties and deliver rice-based foods with lower digestibility and acceptable sensory properties. Acknowledgements M.R. Toutounji was supported by a scholarship from the Australian Research Council Industrial Transformation Training Centre for Functional Grains [Identifier Number: IC140100027] and a top-up scholarship from Agrifutures Australia. The authors declare no conflict of interest. References Aller, E., Abete, I., Astrup, A., Martinez, J. A., & van Baak, M. A. (2011). Starches, sugars and obesity. Nutrients, 3, 341–369. Anderson, A. K., & Guraya, H. S. (2006). Effects of microwave heat-moisture treatment on properties of waxy and non-waxy rice starches. Food Chemistry, 97, 318–323. Anderson, A. K., Guraya, H. S., James, C., & Salvaggio, L. (2002). Digestibility and pasting properties of rice starch heat-moisture treated at the meltin temperature (T-m). Starch Staerke, 54, 401–409. Baik, M. Y., Kim, K. J., Cheon, K. C., Ha, Y. C., & Kim, W. S. (1997). Recrystallization kinetics and glass transition of rice starch gel system. Journal of Agricultural and Food Chemistry, 45, 4242–4248. Benmoussa, M., Moldenhauer, K. A. K., & Hamaker, B. R. (2007). Rice amylopectin fine structure variability affects starch digestion properties. Journal of Agricultural and Food Chemistry, 55, 1475–1479. Bhattacharya, K. R. (2011). Rice quality: A guide to rice properties and analysis (1st ed. ed.). . Bhupathiraju, S. N., Tobias, D. K., Malik, V. S., Pan, A., Hruby, A., Manson, J. E., et al. (2014). Glycemic index, glycemic load, and risk of type 2 diabetes: Results from 3 large US cohorts and an updated meta-analysis. American Journal of Clinical Nutrition, 100, 218–232. Bjorck (1996). Starch: Nutritional aspects. In A. C. Eliasson (Ed.). Carbohydrates in foods (pp. 505–553). (Sweden). Blaak, E. E., Antoine, J. M., Benton, D., Bjorck, I., Bozzetto, L., Brouns, F., et al. (2012).

20

Trends in Food Science & Technology 88 (2019) 10–22

M.R. Toutounji, et al.

treatment of potato starch. Cereal Chemistry, 51, 389–406. Rocha-Villarreal, V., Serna-Saldivar, S. O., & Garcia-Lara, S. (2018). Effects of parboiling and other hydrothermal treatments on the physical, functional, and nutritional properties of rice and other cereals. Cereal Chemistry, 95, 79–91. Rooney, L. W., & Pflugfelder, R. L. (1986). Factors affecting starch digestibility with special emphasis on sorghum and corn. Journal of Animal Science, 63, 1607–1623. Sagum, R., & Arcot, J. (2000). Effect of domestic processing methods on the starch, nonstarch polysaccharides and in vitro starch and protein digestibility of three varieties of rice with varying levels of amylose. Food Chemistry, 70, 107–111. Sheu, W. H. H., Rosman, A., Mithal, A., Chung, N., Lim, Y. T., Deerochanawong, C., et al. (2011). Addressing the burden of type 2 diabetes and cardiovascular disease through the management of postprandial hyperglycaemia: An Asian-Pacific perspective and expert recommendations. Diabetes Research and Clinical Practice, 92, 312–321. Shih, F. F. (2004). Chapter 6: Rice proteins. RICE: Chemistry and technology (pp. 143–162). American Association of Cereal Chemists, Inc. Shu, X. L., Jia, L. M., Ye, H. X., Li, C. D., & Wu, D. X. (2009). Slow digestion properties of rice different in resistant starch. Journal of Agricultural and Food Chemistry, 57, 7552–7559. Silva, W. M. F., Biduski, B., Lima, K. O., Pinto, V. Z., Hoffmann, J. F., Vanier, N. L., et al. (2017). Starch digestibility and molecular weight distribution of proteins in rice grains subjected to heat-moisture treatment. Food Chemistry, 219, 260–267. Song, J. Y., Park, J. H., & Shin, M. (2011). The effects of annealing and acid hydrolysis on resistant starch level and the properties of cross-linked RS4 rice starch. Starch Staerke, 63, 147–153. Strocchi, A., & Levitt, M. D. (1991). Measurement of starch absorption in humans. Canadian Journal of Physiology and Pharmacology, 69, 108–110. Stute, R. (1992). Hydrothermal modification of starches - The difference between annealing and heat moisture-treatment. Starch-Starke, 44, 205–214. Tamura, M., Singh, J., Kaur, L., & Ogawa, Y. (2016). Impact of the degree of cooking on starch digestibility of rice - an in vitro study. Food Chemistry, 191, 98–104. Tester, R. F., Debon, S. J. J., Qi, X., Sommerville, M. D., Yousuf, R., & Yusuph, M. (2001). Amylopectin crystallisation in starch. In T. L. Barsby, A. Donald, & P. Frazier (Eds.). Starch: Advances in structure and function. Cambridge, UK: The Royal Society of Chemistry. Tetens, I., Biswas, S. K., Glitso, L. V., Kabir, K. A., Thilsted, S. H., & Choudhury, N. H. (1997). Physico-chemical characteristics as indicators of starch availability from milled rice. Journal of Cereal Science, 26, 355–361. Tufvesson, F., Wahlgren, M., & Eliasson, A. C. (2003). Formation of amylose-lipid complexes and effects of temperature treatment. Part 1. Monoglycerides. Starch Staerke, 55, 61–71. Van Hung, P., Chau, H. T., & Phi, N. T. L. (2016). In vitro digestibility and in vivo glucose response of native and physically modified rice starches varying amylose contents. Food Chemistry, 191, 74–80. Van Hung, P., Vien, N. L., & Phi, N. T. L. (2016). Resistant starch improvement of rice starches under a combination of acid and heat-moisture treatments. Food Chemistry, 191, 67–73. Vasanthan, T., & Bhatty, R. S. (1996). Physicochemical properties of small- and largegranule starches of waxy, regular, and high-amylose barleys. Cereal Chemistry, 73, 199–207. Wang, S. J., Li, C. L., Copeland, L., Niu, Q., & Wang, S. (2015). Starch retrogradation: A comprehensive review. Comprehensive Reviews in Food Science and Food Safety, 14, 568–585. Wang, H. W., Liu, Y. F., Chen, L., Li, X. X., Wang, J., & Xie, F. W. (2018). Insights into the multi-scale structure and digestibility of heat-moisture treated rice starch. Food Chemistry, 242, 323–329. Wang, S., Li, P., Zhang, T., Yu, J., Wang, S., & Copeland, L. (2017). In vitro starch digestibility of rice flour is not affected by method of cooking. LWT, 84, 536–543. WHO, W. H. O. (2016a). Global report on diabetes. In. Geneva, Switzerland. WHO, W. H. O. (2016b). Obesity and overweight. Wickramasinghe, H. A. M., & Noda, T. (2008). Physicochemical properties of starches from Sri Lankan rice varieties. Food Science and Technology Research, 14, 49–54. Williamson, G., Belshaw, N. J., Self, D. J., Noel, T. R., Ring, S. G., Cairns, P., et al. (1992). Hydrolysis of A- and B-type crystalline polymorphs of starch by α-amylase, β-amylase and glucoamylase. Carbohydrate Polymers, 18, 179–187. Wolever, T. M. S., Jenkins, D. J. A., Kalmusky, J., Jenkins, A., Giordano, C., Giudici, S., et al. (1986). Comparison of regular and parboiled rices - explanation of discrepancies between reported glycemic responses to rice. Nutrition Research, 6, 349–357. Wong, J. H., Lau, T., Cai, N., Singh, J., Pedersen, J. F., Vensel, W. H., et al. (2009). Digestibility of protein and starch from sorghum (Sorghum bicolor) is linked to biochemical and structural features of grain endosperm. Journal of Cereal Science, 49, 73–82. Woolnough, J. W., Monro, J. A., Brennan, C. S., & Bird, A. R. (2008). Simulating human carbohydrate digestion in vitro: A review of methods and the need for standardisation. International Journal of Food Science and Technology, 43, 2245–2256. Ye, J. P., Hu, X. T., Luo, S. J., McClements, D. J., Liang, L., & Liu, C. M. (2018). Effect of endogenous proteins and lipids on starch digestibility in rice flour. Food Research International, 106, 404–409. Zavareze, E. D., Storck, C. R., de Castro, L. A. S., Schirmer, M. A., & Dias, A. R. G. (2010). Effect of heat-moisture treatment on rice starch of varying amylose content. Food Chemistry, 121, 358–365. Zeng, F., Ma, F., Kong, F. S., Gao, Q. Y., & Yu, S. J. (2015). Physicochemical properties and digestibility of hydrothermally treated waxy rice starch. Food Chemistry, 172, 92–98. Zhang, G., Ao, Z., & Hamaker, B. (2006). Slow digestion property of native cereal starches. Biomacromolecules, 7, 3252–3258.

International Journal of Food Properties, 14, 1305–1317. Guraya, H. S., Kadan, R. S., & Champagne, E. T. (1997). Effect of rice starch-lipid complexes on in vitro digestibility, complexing index, and viscosity. Cereal Chemistry, 74, 561–565. de Guzman, M. K., Parween, S., Butardo, V. M., Alhambra, C. M., Anacleto, R., Seiler, C., et al. (2017). Investigating glycemic potential of rice by unraveling compositional variations in mature grain and starch mobilization patterns during seed germination. Scientific Reports, 7. Hibi, Y., Kitamura, S., & Kuge, T. (1990). Effect of lipids on the retrogradation of cooked rice. Cereal Chemistry, 67, 7–10. Hoover, R., Hughes, T., Chung, H. J., & Liu, Q. (2010). Composition, molecular structure, properties, and modification of pulse starches: A review. Food Research International, 43, 399–413. Hu, P. S., Zhao, H. J., Duan, Z. Y., Zhang, L. L., & Wu, D. X. (2004). Starch digestibility and the estimated glycemic score of different types of rice differing in amylose contents. Journal of Cereal Science, 40, 231–237. Ito, K., Yoshida, K., Okazaki, N., & Kobayashi, S. (1988). Effect of processing on the poresize distribution and digestibility of rice grain. Agricultural & Biological Chemistry, 52, 3001–3007. Jacobs, H., & Delcour, J. A. (1998). Hydrothermal modifications of granular starch, with retention of the granular structure: A review. Journal of Agricultural and Food Chemistry, 46, 2895–2905. Jaisut, D., Prachayawarakorn, S., Varanyanond, W., Tungtrakul, P., & Soponronnarit, S. (2009). Accelerated aging of jasmine brown rice by high-temperature fluidization technique. Food Research International, 42, 674–681. Jenkins, D. J., Thorne, M. J., Wolever, T. M., Jenkins, A. L., Rao, A. V., & Thompson, L. U. (1987). The effect of starch-protein interaction in wheat on the glycemic response and rate of in vitro digestion. American Journal of Clinical Nutrition, 45, 946–951. Jenkins, D. J. A., Wolever, T. M. S., Taylor, R. H., Barker, H., Fielden, H., Baldwin, J. M., et al. (1981). Glycemic index of foods - a physiological-basis for carbohydrate exchange. American Journal of Clinical Nutrition, 34, 362–366. Juliano, B. O. (1985). Rice: Chemistry and technology (pp. 774). (2nd ed.). St Paul MN, USA: American Association of Cereal Chemists. Juliano, B. O. (2004). Rice: Overview. In C. Wrigley (Ed.). Encyclopedia of grain science (pp. 41–48). Oxford: Elsevier. Juliano, B. O. (2007). Rice chemistry & quality. [Science city of muñoz. Nueva Ecija]: Philippine Rice Research Institute. Jung, E. Y., Suh, H. J., Hong, W. S., Kim, D. G., Hong, Y. H., Hong, I. S., et al. (2009). Uncooked rice of relatively low gelatinization degree resulted in lower metabolic glucose and insulin responses compared with cooked nice in female college students. Nutrition Research, 29, 457–461. Khatoon, N., & Prakash, J. (2006). Nutritional quality of microwave and pressure cooked rice (Oryza sativa) varieties. Food Science and Technology International, 12, 297–305. Kong, X. L., Chen, Y. L., Zhu, P., Sui, Z. Q., Corke, H., & Bao, J. S. (2015). Relationships among genetic, structural, and functional properties of rice starch. Journal of Agricultural and Food Chemistry, 63, 6241–6248. Kong, B., Kim, J., Kim, M., & Kim, J. (2003). Porcine pancreatic α-amylase hydrolysis of native starch granules as a function of granule surface area. Biotechnology Progress, 19, 1162–1166. Larsen, H. N., Christensen, C., Rasmussen, O. W., Tetens, I. H., Choudhury, N. H., Thilsted, S. H., et al. (1996). Influence of parboiling and physico-chemical characteristics of rice on the glycaemic index in non-insulin-dependent diabetic subjects. European Journal of Clinical Nutrition, 50, 22–27. Larsen, H. N., Rasmussen, O. W., Rasmussen, P. H., Alstrup, K. K., Biswas, S. K., Tetens, I., et al. (2000). Glycaemic index of parboiled rice depends on the severity of processing: Study in type 2 diabetic subjects. European Journal of Clinical Nutrition, 54, 380–385. Lee, S. W., Lee, J. H., Han, S. H., Lee, J. W., & Rhee, C. (2005). Effect of various processing methods on the physical properties of cooked rice and on in vitro starch hydrolysis and blood glucose response in rats. Starch Staerke, 57, 531–539. Lehmann, U., & Robin, F. (2007). Slowly digestible starch – its structure and health implications: A review. Trends in Food Science & Technology, 18, 346–355. Li, J. T., Han, W. F., Xu, J. D., Xiong, S. B., & Zhao, S. M. (2014). Comparison of morphological changes and in vitro starch digestibility of rice cooked by microwave and conductive heating. Starch Staerke, 66, 549–557. Lii, C. Y., Tsai, M. L., & Tseng, K. H. (1996). Effect of amylose content on the rheological property of rice starch. Cereal Chemistry, 73, 415–420. Lin, L. S., Zhang, L., Cai, X. L., Liu, Q. Q., Zhang, C. Q., & Wei, C. X. (2018). The relationship between enzyme hydrolysis and the components of rice starches with the same genetic background and amylopectin structure but different amylose contents. Food Hydrocolloids, 84, 406–413. Morrison, W. R. (1988). Lipids in cereal starches - a review. Journal of Cereal Science, 8, 1–15. Morrison, W. R. (1995). Starch lipids and how they relate to starch granule structure and functionality. Cereal Foods World, 40, 437. Niba, L. L. (2003). Processing effects on susceptibility of starch to digestion in some dietary starch sources. International Journal of Food Sciences & Nutrition, 54, 97–109. Panlasigui, L. N., Thompson, L. U., Juliano, B. O., Perez, C. M., Yiu, S. H., & Greenberg, G. R. (1991). Rice varieties with similar amylose content differ in starch digestibility and glycemic response in humans. American Journal of Clinical Nutrition, 54, 871–877. Rashmi, S., & Urooj, A. (2003). Effect of processing on nutritionally important starch fractions in rice varieties. International Journal of Food Sciences & Nutrition, 54, 27–36. Reed, M. O., Ai, Y. F., Leutcher, J. L., & Jane, J. L. (2013). Effects of cooking methods and starch structures on starch hydrolysis rates of rice. Journal of Food Science, 78, H1076–H1081. Robin, J. P., Mercier, C., Charbonniere, R., & Guilbot, A. (1974). Lintnerized starches. Gel-filtration and enzymatic studies of insoluble residues from prolonged acid

21

Trends in Food Science & Technology 88 (2019) 10–22

M.R. Toutounji, et al.

Carbohydrate Polymers, 195, 1–8. Zhu, L. J., Liu, Q. Q., Wilson, J. D., Gu, M. H., & Shi, Y. C. (2011). Digestibility and physicochemical properties of rice (Oryza sativa L.) flours and starches differing in amylose content. Carbohydrate Polymers, 86, 1751–1759.

Zhou, Z. K., Yang, X., Su, Z., & Bu, D. D. (2016). Effect of ageing-induced changes in rice physicochemical properties on digestion behaviour following storage. Journal of Stored Products Research, 67, 13–18. Zhou, X., Ying, Y. N., Hu, B. L., Pang, Y. H., & Bao, J. S. (2018). Physicochemical properties and digestibility of endosperm starches in four indica rice mutants.

22