Food Research International xxx (xxxx) xxx

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Food Research International

journal homepage: www.elsevier.com/locate/foodres

Black rice (Oryza sativa L.) processing: Evaluation of physicochemical

properties, in vitro starch digestibility, and phenolic functions linked to type
2 diabetes
Halah Aalim a, Di Wang a, Zisheng Luo a, b, c, *
a
Zhejiang University, College of Biosystems Engineering and Food Science, Key Laboratory of Agro-Products Postharvest Handling of Ministry of Agriculture and Rural
Affairs, Zhejiang Key Laboratory for Agri-Food Processing, National-Local Joint Engineering Laboratory of Intelligent Food Technology and Equipment, Hangzhou,
310058, People’s Republic of China
b
Ningbo Research Institute, Zhejiang University, Ningbo, 315100, People’s Republic of China
c
Fuli Institute of Food Science, Zhejiang University, Hangzhou 310058, People’s Republic of China

A R T I C L E I N F O A B S T R A C T

Keywords: Black rice is recognized for managing diabetes in Chinese folk medicine. Therefore, the present study investigates
Black rice the effect of thermal treatments and the succeeding cooking on black rice physicochemical properties, phenolic
Phenolic compounds composition, total antioxidant activity (TAA), enzymes and glycation inhibition in addition to starch di­
Starch digestion
gestibility. Thermal decomposition of anthocyanin and cyanidin-3-glucoside was evident across all processing
Cooking
methods and reflected in increasing levels of protocatechuic acid, while proanthocyanidins (TPAC) were sus­
Roasting
Frying ceptible to cooking. Roasting of grains sustained total phenolics (TPC), flavonoids (TFC), TPAC, and antilipase
Enzyme inhibition activity. Additionally, the combined effect of frying and cooking diminished TFC, TPAC, and α-glucosidase in­
Amylose contents hibition. The thermally treated grains showed pronounced activity against α-amylase, α-glucosidase, and gly­
cation, whereas their cooked counterparts reduced the estimated glycemic index (eGI), and enhanced resistant
starch (RS). Processed grains chrominance, TAA, and apparent amylose content (AAC) showed a significant
correlation with phenolics. These findings are demonstrating that black rice processing is favorable for the di­
etary management of metabolic disorders such as diabetes and hyperlipidemia.

1. Introduction
Rice (Oryza sativa L.) is a fundamental source of calorie intake and
energy hemostasis. Black rice is a whole grains type that is not only a
source of carbohydrate and fibers but also characterized by substantial
contents of diverse classes of bioactive metabolites include phenolic
acids, flavonoids, anthocyanins, proanthocyanidins, and tocotrienols
(Melini, Panfili, Fratianni, & Acquistucci, 2019; Zaupa, Calani, Del Rio,
Brighenti, & Pellegrini, 2015). Accumulating epidemiological studies
advocate for the numerous health-promoting qualities of black rice
phenolics, including ameliorating oxidative stress and chronic diseases
such as cancer, cardiovascular diseases, and progressive metabolic dis­
orders such as type 2 diabetes and obesity (Deng et al., 2013). Studies
have reported the antidiabetic effect of dietary phenolic extracts of
peaches (Nowicka, Wojdyło, & Laskowski, 2018), blueberry (Spínola,
Llorent-Martínez, & Castilho, 2019), rice bran (Aalim, Belwal, Jiang,
et al., 2019; Aalim, Belwal, Wang, et al., 2019), green tea and grape
seeds (Sergent, Vanderstraeten, Winand, Beguin, & Schneider, 2012).
Therefore, dietary phenolic compounds offer a complementary nutri­
tional approach for diabetes management.
Although rice is considered a major glycemic load contributor in
rice-consuming communities, black rice grain has been recommended
for diabetes remediation in Chinese folk medicine (Deng et al., 2013).
Rice domestic cooking methods are usually relating to the cultural
background and personal preference of the consumers. Hence starch
gelatinization through cooking is required to attain desirable palat­
ability, flavor, texture, and enhance digestibility (Zaupa et al., 2015).
Accordingly, factors control phenolic predestination in processed rice
includes: (i) interactions with starch that limit their solubility (Zheng
et al., 2021), (ii) decomposition of ester linkage (Hou, Qin, Zhang, Cui,

Abbreviations: BR, raw; RC, raw cooked; Ro, roasted; Ro.C, roasted cooked; F, fried; F.C, fried cooked grains of black rice.
* Corresponding author at: College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, People’s Republic of China.
E-mail address: luozisheng@zju.edu.cn (Z. Luo).

https://doi.org/10.1016/j.foodres.2020.109898
Received 16 May 2020; Received in revised form 4 November 2020; Accepted 5 November 2020
Available online 10 November 2020
0963-9969/© 2020 Elsevier Ltd. All rights reserved.

Please cite this article as: Halah Aalim, Food Research International, https://doi.org/10.1016/j.foodres.2020.109898
H. Aalim et al.
& Ren, 2013), (iii) variations in rice varieties (Melini et al., 2019), and
(iv) leaching from the food matrix into processing medium (Zaupa et al.,
2015). As a result, various processing methods could tip substantially
different consequences regarding phenolic compounds (Melini et al.,
2019; Surh & Koh, 2014; Zaupa et al., 2015).
This work builds upon previous literature, suggesting that desirable
changes in rice starch properties and phenolic stability can occur during
processing (Limwachiranon, Jiang, Huang, Sun, & Luo, 2019; Qi et al.,
2019). The present research focused on one or a combination of two
traditional domestic processing techniques, thermal treatments (i.e.,
roasting and frying), and the subsequent cooking. Nevertheless, to our
knowledge, there are no reports regarding the impact of processing on
the rice phenolics inhibition of digestive enzymes linked to type 2 dia­
betes (α-glucosidase, α-amylase, and lipase) and glycation of bovine
serum albumin. Therefore, the purpose of this study was to examine the
fate of individual phenolic compounds in black rice after processing and
their associated biological activities. Besides, investigate the effect of
processing on the starch digestibility and the grains physiochemical
qualities that provide an accurate, and realistic estimation for the
health-promoting qualities of black rice in its daily consumable forms.
2. Materials and methods
2.1. Chemicals and reagents
2,2-Diphenyl-1-picrylhydrazyl (DPPH), 2,2-azinobis-3-ethylbenzo­
thiazoline-6-sulphonic acid (ABTS), 4,6-tripryridyls-triazine (TPTZ),
ρ-nitrophenyl-α-d-glucopyranoside (α-ρNPG), nitrophenyl acetate
(pNPA), potato starch, aminoguanidine hydrochloride, acarbose, orli­
stat, phenolic acids were obtained from Aladdin Industrial Co.
(Shanghai, China). α-Glucosidase from Saccharomyces cerevisiae,
α-amylase (type VI-B; from porcine pancreas), lipase (type II; from
porcine pancreas), potato amylose, corn amylopectin and trolox were
obtained from Sigma Chemical Co. (St. Louis, MO, USA). Bovine serum
albumin (BSA, ≥98%) was obtained from Amresco Co. (Ohio, USA). All
chemicals were analytical grade, and chromatographic chemicals were
of HPLC grade.
2.2. Sample preparation
Black unpolished rice was cultivated in Shenyang, Liaoning prov­
ince, People’s Republic of China, and acquired commercially from the
local market. Two different thermal treatments traditionally used in
domestic cooking were applied; roasting and oil frying. Rice grains (100
g) were spread to one layer depth in an ovenware tray and roasted for 20
min at 180 ◦ C in an oven to grantee color and aroma development
producing roasted rice (Ro). For oil frying (F), 100 g of grains were
stirred fried with 50 mL of maize oil in a stainless steel pan at 140 ◦ C for
5 min. Raw black rice (BR) was used as control.
The initial volume of cooking water was determined before the
experiment to ensure complete absorption of water and full starch
gelatinization at the end of the cooking. Briefly, raw or thermally treated
grains were fully cooked using a commercial automatic rice cooker (MB-
FS3073, Midea Co, China) using a consistent ratio of 1:1.8 (w/v) of rice
to purified water. The same cooking program was used for all samples,
as recommended by the manufacturer, to provide a similar cooking
degree and texture. Raw cooked (R.C), roasted cooked (Ro.C), and fried
cooked (F.C) grains were allowed to cool down for 10 min after the
cooking completed. All processing experiments were replicated twice.
All rice samples were freeze-dried, then grounded under liquid nitrogen
using IKA laboratory mill M20 (Janke & Kunkel Co., Staufen, Germany),
and finally stored frozen at − 20 ◦ C in the dark until further analysis.
2.3. Extraction of phenolic compounds
Each sample (1.0 g) was extracted with 20 mL of 70% ethanol (v/v)
2
Food Research International xxx (xxxx) xxx
under sonication (450 W, 40 kHz) at 60 ◦ C for 80 min using an ultrasonic
bath (DS-7510DT, Sonxi Ultrasonic Instrument Co., Shanghai, China).
The supernatants were collected by centrifugation at 11,000g for 15 min
at 4 ◦ C and stored at 4 ◦ C until further analysis. An equivalent of 10 g
extract was filtered through a 0.45 µm membrane for purification.
Ethanol was evaporated under vacuum and lyophilized. The dry extract
was reconstituted in water or ethanol at a suitable concentration for
antidiabetic and antiglycation assays.
2.4. Determination of phenolic contents
Total phenolic content (TPC), total flavonoid content (TFC), and
phenolic composition were determined as described in our previous
work (Aalim, Belwal, Wang, et al., 2019). TPC results were expressed as
mg gallic acid equivalent per 100 g (mg GAE/100 g), and TFC results
were expressed as mg catechin equivalent (CE) per 100 g (mg CE/100 g).
The identification and quantification of each phenolic compound were
respectively based on matching the retention time and the calibration
curve of known standards using the HPLC system (Waters Alliance 2695)
coupled with photodiode array detector (PDA, Waters 2998) using a C18
column (5 µm, 250 × 4.6 mm, Walch). Total proanthocyanidin content
(TPAC) was quantified by a butanol-HCl assay (Porter, Hrstich, & Chan,
1985). The results were expressed as mg proanthocyanidins equivalent
(PE) per 100 g (mg PE/100 g). Total anthocyanin content (TAC) was
determined by the spectrophotometric pH differential method (Lee,
Durst, & Wrolstad, 2005), and the results were expressed as mg
cyanidin-3-glucoside equivalent (CGE) per 100 g (mg CGE/100 g).
2.5. Determination of total antioxidant activity (TAA)
TAA was determined using DPPH, ABTS scavenging activity and
ferric reducing activity power (FRAP), and the assays were adopted from
our previous report (Aalim, Belwal, Wang, et al., 2019). The results were
expressed as mM trolox equivalent/g (mM TE/g).
2.6. Determination of in vitro antidiabetic and antiglycation activity
Pancreatic α-amylase, yeast α-glucosidase, pancreatic lipase, and
BSA/fructose glycation inhibition assays were adopted from our previ­
ous report (Aalim, Belwal, Wang, et al., 2019). The results were
expressed as the concentration required to obtain a 50% inhibition effect
IC50 values (mg/mL), acarbose, orlistat, and aminoguanidine were used
as a respective positive control.
2.7. Determination of changes in color parameters
Color parameters of raw and processed samples were measured with
a color difference meter (CR-400, Konica Minolta, Tokyo, Japan). Before
color measurements, the instrument was calibrated with white calibra­
tion tile. Color parameters were expressed in the CIE L*a*b* color space:
L* indicates lightness (100 = white, 0 = black); a* indicates redness-
greenness (positive = red); b* indicates yellowness-blueness (positive
= yellow). Besides, the color intensity or saturation indicated by chroma
(C), the hue angle (H◦ ) and total color difference (ΔE) were calculated
by applying the following formulas:
( )1/2
C = a*2 + b*2 (1)
(2)
◦
H = tan− 1 (b*/a*)
[ ]1/2
ΔE = (L*r − L*P )2 + (a*r − a*P )2 + (b*r − b*P )2 (3)
where the subscripts r and p indicate raw and processed rice,
respectively.
H. Aalim et al.
Fig. 1. Total phenolic, flavonoids, proanthocyanidins, and anthocyanin contents of raw, and processed black rice grains. Values are means ± standard deviations (n
= 6). Mean values with different letters are statistically different (p < 0.05).
2.8. Apparent amylose content (AAC)
Apparent amylose content (AAC) was determined using the iodine
adsorption method as described by Limwachiranon et al. (2019). Potato
amylose and corn amylopectin were used as the standard, and AAC was
calculated as (%) of amylose in proportion to total sample weight (dry
basis).
2.9. In vitro starch digestibility
Starch digestion kinetics was determined according to the procedure
described by Warren, Zhang, Waltzer, Gidley, & Dhital, (2015) with
some modifications. Cooked rice samples (100 mg, dry weight basis) was
suspended in 9 mL of acetate buffer (0.2 M, pH 6, containing 200 mM
CaCl2 and 0.5 mM MgCl2). The samples were equilibrated in a 37 ◦ C.
Next, I mL of mixed enzyme solution had an activity of 10 U/mL
α-amylase, and 18 U/mL of amyloglucosidase was added. Aliquots (100
μL) of enzymatic hydrolysate were withdrawn at 0, 10, 20, 30, 60, 120,
150, 180 min, and combined with 100 μL of 95% ethanol (v/v) to
inactivate the enzymes. The unreacted starch residue was separated
after centrifugation at 2000g for 5 min, and glucose concentration was
measured with the GOPOD assay. Furthermore, the percentages of the
starch fractions of rapidly digestible starch (RDS) (hydrolyzed portion
within 0–20 min), slowly digestible starch (SDS) (hydrolyzed portion
within 20–120 min) and resistant starch (RS) (the undigested portion
after 120 min) were calculated based on the following equations (Eng­
lyst, Kingman, & Cummings, 1992):
(
0.9
) standard deviation.
RDS (%) = (G20 − G0 )× × 100 (4)
TS
( )
0.9
SDS (%) = (G120 − G20 ) × × 100
TS
RS (%) = [100 − RDS − SDS]
where G is glucose concentration (g/100 g dry weight), and TS is total
starch contents (g/100 g dry weight). TS was measured with a total
starch kit (K-TSTA-100A, Megazyme International, Wicklow, Ireland).
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2.10. Kinetics of starch hydrolysis
The kinetics of the starch digestion data was estimated by a first-
order equation introduced by Guggenheim to determine the rate con­
stant of first-order reactions (Butterworth, Warren, Grassby, Patel, &
Ellis, 2012):
Ci+1 − Ci = C∞ e− kt (1 − e− kΔ
) (7)
where C∞ corresponding to the concentration of digested starch at the
endpoint of the reaction is unknown, C was measured at times that are
separated by a constant time increment Δt (i.e., the intervals between,
t1, t2, t3, etc., are all Δt), and k is a pseudo-first-order rate constant.
Hydrolysis indices (HI) of the samples equivalent to the area under
digestibility curves (AUC) during simulated small intestinal digestion
and the estimated glycemic index (eGI) is calculated by the following
equation (Goñi, Garcia-Alonso, & Saura-Calixto, 1997):
eGI = 39.71 + 0.549HI (8)
2.11. Statistical analysis
Analysis of variance (ANOVA) was performed employing Duncan’s
Multiple Range Test, and the statistical significance was defined at a
level of P < 0.05. The correlation analysis was performed with Pearson’s
correlation test. Data analysis was carried using SPSS version 20.0 (SPSS
Inc., Chicago, Illinois, USA) software. All determinations were con­
ducted in triplicate, and the data were presented as mean values ±
3. Results and discussion
(5) 3.1. Effect of processing on phenolic contents
(6) TPC, TFC, TPAC, and TAC of raw and processed black rice were
shown in Fig. 1. Raw grains had considerably higher levels of phenolic
contents when compared with processed grains. Generally, roasting did
not cause any loss of TPC, TFC, and TPAC. In the case of cooking, there
was an apparent but nun-significant loss of TPC and TFC, excluding TFC
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Table 1 genetics, preprocessing, storage period, and handling conditions (Goufo

Phenolic compounds (mg/100 g) of raw and processed black rice grains. & Trindade, 2017). Noteworthy, the grains investigated in the current
Sample BR R.C Ro Ro.C F F.C study were obtained commercially, as they were packed and stored after
been subjected to various processing such as parboiling and drying.
Aldehyde derivatives
SYAD 6.76 ± 5.94 ± 22.23 ± 7.31 ± 6.85 ± 5.92 ± Phenolic profiles of raw and processed grains were evaluated to
0.79b 1.81b 0.12a 2.25b 0.36b 2.01b establish the effect of thermal processing on the stability of individual
phenolic compounds, as presented in Table 1 and Fig. S1. As can be seen,
Hydroxybenzoic acids
GA 0.93 ± 3.24 ± 4.30 ± 1.16 ± 2.60 ± 0.89 ± 18 phenolic compounds and 1 anthocyanin compound were identified
0.10c 0.07b 0.36a 0.03c 0.32b 0.00c and quantified in raw and processed grains. Quantitative results indi­
PCA 143.23 359.88 247.85 219.30 156.08 199.42 cated that hydroxybenzoic acids were the most abundant phenolic
± 35.02b ± 5.89a ± 3.37ab ± 9.42ab ± 11.73b ± 8.18b
compounds in BR and accounts for 42.17% of TPC followed by flavo­
HBA 15.38 ± 27.37 ± 31.80 ± 15.78 ± 12.74 ± 7.78 ±
0.03abc 1.56ab 0.63a 0.70abc 1.70bc 0.20c noids 33.43% of TPC and hydroxycinnamic acids 13.64% of TPC. Other
VA 43.80 ± 22.29 ± 27.75 ± 21.86 ± 18.67 ± 33.83 ± relevant families were aldehyde derivatives as syringaldehyde 1.31% of
5.24a 0.54b 8.81b 0.55b 1.35b 1.18ab TPC.
SYA 14.18 ± 1.59 ± 24.23 ± 0.71 ± 12.80 ± 8.83 ± Furthermore, cyanidin-3-glucoside was the most predominant
1.10ab 0.85b 1.09a 0.09b 1.61ab 1.76ab
phenolic compound (30.39% of TPC) and constituting the majority of
Hydroxycinnamic acids total anthocyanins in BR (62.63% of TAC). Previously, cyanidin-3-
CHA 11.26 ± 21.91 ± 9.56 ± 8.55 ± 11.99 ± 6.99 ±
glucoside was identified as the predominant anthocyanin in black rice
2.05bc 0.40a 0.04bc 1.40bc 1.39b 1.52c
CA 1.85 ± 4.11 ± 5.77 ± 5.60 ± 4.55 ± 5.92 ±
(Hiemori, Koh, & Mitchell, 2009; Hou et al., 2013; Surh & Koh, 2014).
0.48b 3.43ab 0.32a 1.53a 0.44ab 0.75a Likewise, hydroxybenzoic acids level mainly corresponded to the
COA 6.42 ± 6.16 ± 23.66 ± 4.89 ± 5.75 ± 5.14 ± amount of protocatechuic acid, accounting for the second dominant
0.02b 2.04b 0.30a 1.10b 1.28b 1.13b phenolic compound and comprised of 27.76% of TPC. Moreover, the
SIN 27.22 ± 10.66 ± 4.96 ± 1.39 ± 6.95 ± 4.98 ±
third abundant phenolic compounds in black rice were vanillic acid and
4.47a 2.16b 2.23b 1.39b 0.00b 1.57b
FA 8.37 ± 5.65 ± 3.04 ± 2.00 ± 4.93 ± 3.22 ± sinapic acid, followed by p-hydroxybenzoic acid, syringic acid, isoferulic
0.71a 0.00ab 0.56ab 0.05b 0.84ab 0.17ab acid, and chlorogenic acid. In addition, the studied variety was char­
iFA 12.19 ± 7.67 ± 11.07 ± 12.73 ± 8.26 ± 10.42 ± acterized by minute amounts of gallic acid, caffeic acid, and quercetin
0.31ab 0.57b 0.40ab 2.42a 1.53ab 2.11ab (in total ≤1% of TPC). Considering the effect of processing on phenolic
CIN 3.06 ± 1.01 ± 1.22 ± 10.42 ± 5.41 ± 11.80 ±
0.01ab 0.28b 0.02b 0.69a 0.34b 0.73a
compounds, the increase of hydroxybenzoates (90.5–15.3%) was asso­
ciated with 6.7% decrease due to F, and the increase of aldehyde de­
Flavonoids
rivatives (189.2–7.0%) accompanied with 4% decrease during R.C.
C3G 156.76 116.18 135.15 36.72 ± 24.09 ± 21.64 ±
± 30.53a ± 6.74a ± 27.43a 1.09b 2.7b 8.84b While, a decrease of flavonoids (66.6–12.81%) was associated with
ECAT 6.35 ± 2.02 ± 8.57 ± 16.76 ± 19.42 ± 21.34 ± 1.2% increase due to Ro, followed by the reduction of hydrox­
2.48b 0.29c 0.79b 2.81a 1.02a 1.18a ycinnamates (33.3–15.8%).
RU 4.32 ± 3.97 ± 0.75 ± 4.05 ± 7.43 ± 2.09 ± The thermal stability of cyanidin-3-glucoside was a function of the
1.25ab 3.46ab 0.05b 0.89ab 0.12a 0.96ab
QU 1.31 ± 0.24 ± 0.33 ± 2.43 ± 5.37 ± 5.72 ±
processing method with the highest loss found in grains treated using
0.95b 0.12b 0.12b 0.07ab 1.31a 0.84a Ro.C, F, and F.C (~84–86%). In general, cyanidin-3-glucoside decom­
KF 1.23 ± 2.87 ± 2.57 ± 1.73 ± 2.31 ± 2.28 ± posed to protocatechuic acid and negligible amounts of phlor­
0.06b 0.55a 0.27a 0.44ab 1.07ab 0.44ab oglucinaldehyde (Hiemori et al., 2009). The higher activation energy of
iRH 2.51 ± 3.56 ± 3.01 ± 5.58 ± 4.74 ± 4.52 ±
anthocyanins is indicative of their vulnerability to elevate temperature
0.41e 0.26 cd 0.27de 0.06a 0.04ab 0.44bc
and pH during processing (Hou et al., 2013). Moreover, peonidin-3-
Values are expressed as mean ± standard deviation (n = 6). Mean values with glucoside was considered as the second-leading anthocyanin in black
different letters within the same row are statistically different (p < 0.05). rice, and more thermally stable than cyanidin-3-glucoside (Hiemori
Abbreviations: BR; raw, R.C; raw cooked, Ro; roasted, Ro.C; roasted cooked, F;
et al., 2009; Hou et al., 2013), hence contribute to the TAC values
fried. F.C; fried cooked: SYAD, syringaldehyde; GA, gallic acid; PCA, proto­
observed in this study. Likewise, vanillic acid and sinapic acid were
catechuic acid; HBA, p-hydroxybenzoic acid; VA, vanillic acid; SYR, syringic
significantly affected by all thermal processing, with the highest loss
acid; CHA, chlorogenic acid; CA, caffeic acid; COA, p-coumaric acid; SIN, sinapic
acid; FA, ferulic acid; iFA, isoferulic acid; CIN, cinnamic acid; C3G, cyanidin-3- found in F and Ro.C grains, respectively. While p-hydroxybenzoic acid,
glucoside; ECAT, (− )-epicatechin; RU, rutin; QU, quercetin; KF, kaempferol; syringic acid, (− )-epicatechin, isoferulic acid, cinnamic acid, and iso­
iRH, isorhamnetin. rhamnetin, which were found to be more thermally stable. Furthermore,
the concentration of chlorogenic acid, protocatechuic acid, and
value for F.C grains. However, all processing methods except for roast­ kaempferol significantly increased during R.C, whereas gallic acid,
ing resulted in a significant decrease in TPAC. Nevertheless, a constant caffeic acid, syringaldehyde, p-coumaric acid, and kaempferol concen­
significant loss of TAC was noted, regardless of the type of thermal tration significantly increased during Ro. Additionally, rutin and quer­
treatment used. Moreover, despite the best effort to remove the pro­ cetin levels highly increased during F.
cessing oil during the extraction via centrifugation, the polar extract of Pearson correlation coefficient between phenolic constituents
maize oil showed TPC, and TFC values of 36.5 ± 3.8 mg GAE/100g rice, (Table S1) revealed that TFC was the major contributor to TPC and TPAC
and 140.2 ± 0.0 mg CE/100g rice, respectively, with no detectable (r ≥ 0.888). Also, TPAC was relevant to TPC and TAC (r ≥ 0.690), which
TPAC. These values could partially contribute to the overall phenolic point out the integrative effect of the thermal degradation products
stability of F. and F.C samples. between these phenolic groups. Moreover, syringaldehyde and p-cou­
The values of phenolic contents obtained in this study were appre­ maric acid showed moderate correlations with TPC, TFC, and TPAC (r ≥
ciably different from those reported in the literature (Melini et al., 2019; 0.590). Besides, gallic acid correlated with TPC (r = 0.614), while TPAC
Rao et al., 2018; Shao et al., 2018; Ziegler et al., 2018). Conversely, lack was influenced by cyanidin-3-glucoside (r = 0.762). A strong correlation
of proanthocyanidins was evident in Chinese and Brazilian black rice is observed between TAC and cyanidin-3-glucoside (r = 0.911) as a key
varieties (Shao et al., 2018; Ziegler et al., 2018). These prominent dis­ contributor, while sinapic acid and ferulic acid showed moderate cor­
crepancies in findings could be attributed to variances in black rice relations with TAC (r ≥ 0.607). On the other hand, negative correlations
varieties, extraction techniques, crop origin, cultivation conditions, were observed for all phenolic groups in association with cinnamic acid,
quercetin, and isorhamnetin (r ≥ 0.579). Interestingly, the B-ring

4
H. Aalim et al.
Fig. 2. (a) Total antioxidant capacity and (b) Antidiabetic and antiglycation activities of black rice grains and the respective control drug (C). Values are means ±
standard deviations (n = 6). Mean values with different letters with the same test are statistically different (p < 0.05).
substitution and glycosylation pattern of quercetin, and isorhamnetin
are directly associated with the cyanidin and peonidin with glucose and
rutinose as sugar moieties, respectively (Bordiga et al., 2014). This shed
light on the negative correlation amongst these flavonols and TAC as a
result of thermal processing.
3.2. Effect of processing on antioxidant activity
TAA of raw and processed grains was evaluated employing ABTS,
DPPH, and FRAP assay (Fig. 2a). For raw grains, TAA was 5.80, 14.20,
and 13.62 mM TE/g for DPPH, ABTS, and FRAP assay, respectively.
Different processing methods of black rice grains were characterized by
comparable levels of TAA (p > 0.05); however, roasting enhanced TAA
significantly when determined as ABTS. Similarly, the decline in DPPH
scavenging activity of buckwheat after roasting was associated with the
Maillard reaction product formation (Bhinder et al., 2019). Consistently,
an increase of 16% of the FRAP had previously been reported for risotto
cooking of black rice (Zaupa et al., 2015).
Furthermore, the phenolic contents are significant contributors to
TAA in processed grains, as TPC, TFC, and TPAC showed a strong pos­
itive correlation with ABTS and FRAP (r ≥ 0.626) while showing
negative correlations with DPPH (r ≥ − 0.968). The same trend was
observed among various rice genotypes (Bordiga et al., 2014; Rao et al.,
2018). More specifically, Rao et al. (2018) found that cyanidin-3-
glucoside and peonidin-3-glucoside were accountable for over 90% of
black rice ABTS scavenging activity. In contrast, DPPH scavenging ac­
tivity was negatively influenced by phenolic contents, implying that
processing has led to the loss of the readily degradable DPPH scavengers.
Besides, gallic acid, p-hydroxybenzoic acid, syringaldehyde, and p-
coumaric acid showed moderate correlations with ABTS (r ≥ 0.640).
Quercetin and sinapic acid correlated with ABTS and FRAP (r ≥
− 0.582), also DPPH correlated with p-coumaric acid (r ≥ − 0.638). As
well, the strong association among TAA (r ≥ 0.693) was evident.
3.3. Effect of processing on antidiabetic and antiglycation activity
The inhibitory effects of raw and processed black rice on α-amylase,
α- glucosidase, lipase, and BSA/fructose glycation were expressed as
IC50 values (mg/mL), as an adverse indicator is presented in Fig (2b).
Raw black rice IC50 values were (8.36, 19.37, 36.02, and 4.48 mg/mL for
α-amylase, α- glucosidase, lipase, and glycation inhibition, respectively).
As anticipated, the respective positive control acarbose, orlistat, and
aminoguanidine showed the highest inhibitory effects with IC50 values
of 0.07, 2.29, 0.016, and 1.00 mg/mL, for α-amylase, α- glucosidase,
5
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lipase, and glycation inhibition respectively.
All cooking treatments seem to improve lipase inhibitory activity.
Whereas, the thermal treatments of roasting and frying decrease
α-amylase and lipase inhibitory activity significantly. Nevertheless, α-
glucosidase and glycation inhibitory activity significantly improved
after thermal treatments and cooking, until F.C. treatment had led to the
loss of both activities. Black rice showed higher antiglycation activity,
and processing further enhanced the activity.
Likewise, α-amylase activity positively influenced by protocatechuic
acid and chlorogenic acid (r ≥ 0.608), and negatively with vanillic acid
(r = -0.625). Further, α- glucosidase activity was subjective to gallic acid
and p-hydroxybenzoic acid (r ≥ 0.618). Notably, α-amylase inhibition
has been promoted mainly by anthocyanins, while phenolic acids and
polymeric procyanidins showed strong α-glucosidase inhibition (Kato-
Schwartz et al., 2020; Nowicka et al., 2018). Likewise, cyanidin-3-
glucoside was the leading anti-hyperglycemic agent of M. faya berry
phenolic extracts (Spínola et al., 2019). Further, p-coumaric acid was a
much potent α-glucosidase inhibitor than the standard drug acarbose
(Aalim, Belwal, Jiang, et al., 2019). Our findings suggest that the anti-
hyperglycemic effect the processed grains were mainly driven by the
synergistic effect of the phenolic compounds rather than the changes in
phenolic levels. Similarly, in silico studies indicated that the inhibition
kinetic of plant extracts followed an intricate binding pattern with
digestive enzymes (Kato-Schwartz et al., 2020). Our results of
carbohydrate-hydrolyzing enzymes inhibition support the view that
black rice consumption could regulate the postprandial glucose blunt.
Pancreatic lipase is a key enzyme in dietary triglycerides digestion
and absorption. Phenolic compounds at concentrations easily attainable
during food intestinal digestion are effective pancreatic lipase inhibitors
(Sergent et al., 2012). Our results emphasize the role of TFC, TPAC, and
syringic acid (r ≥ 0.631) as important lipase inhibitors in processed
grains. Also, phenolic compounds associated with rice such as (− )-epi­
catechin, gallic acid, ferulic acid, p-coumaric acid, kaempferol, and
quercetin were the leading hypolipidaemic compounds (Aalim, Belwal,
Jiang, et al., 2019; Sergent et al., 2012).
Processed black rice exhibited good antiglycation activity, which is
negatively correlated with isorhamnetin (r = 0.693) and positively with
vanillic acid (r = 0.861). Previously, quercetin and cyanidin-3-glucoside
standards showed potent AGEs inhibitory activity than the experimental
antidiabetic drug aminoguanidine (Spínola et al., 2019). Most impor­
tantly, glycation inhibitory activity was found to be a function of
phenolic compounds profile and concentration (Aalim, Belwal, Wang,
et al., 2019). Correspondingly, α- glucosidase inhibitory activity posi­
tively correlated with ABTS and FARP (r ≥ 0.621), while antiglycation
H. Aalim et al. Food Research International xxx (xxxx) xxx

Table 2 parameters were largely dependant on the phenolic composition, which

Effect of processing on the chrominance of black rice grains. was in accordance with Shao et al. (2018). The values of L* parameter
L* a* b* C H◦ ΔE were largely influenced by TPC, TFC, TPAC, and p-hydroxybenzoic acid
(r ≥ 0.581), while negatively influenced by cinnamic acid, (− )-epi­
BR 51.68 ± 3.85 ± 0.72 ± 3.92 ± 0.18 ± 0
0.27 a 0.05 d 0.08 e 0.06f 0.02f catechin and quercetin (r ≥ − 0.791). Whereas, a* values negatively
R.C 48.23 ± 10.52 ± 2.53 ± 10.82 ± 0.24 ± 7.74 ± influenced by TFC, TPAC, and syringic acid (r ≥ − 0.665), whereas b*
0.66b 0.05 a 0.08 d 0.03 a 0.01 e 0.29c and H◦ showed moderate correlations with TAC (r ≥ − 0.813). Likewise,
Ro 52.25 ± 2.52 ± 4.83 ± 5.44 ± 0.96 ± 4.42 ± C values were positively correlated with protocatechuic acid (r = 0.594)
0.46 a 0.02f 0.10 a 0.10 d 0.00 a 0.05 e
Ro. 47.19 ± 6.56 ± 3.37 ± 7.37 ± 0.47 ± 5.92 ±
and negatively with TPAC (r = -0.611). Similarly, ΔE positively corre­
C 1.18b 0.07c 0.08c 0.10c 0.01 d 0.76 d lated with (− )-epicatechin (r = 0.754) and negatively with TPAC and
F 27.44 ± 3.06 ± 3.97 ± 5.01 ± 0.86 ± 24.47 ± TAC (r ≥ − 0.682). Interestingly, color parameters also influenced by the
0.24c 0.02 e 0.04b 0.02 e 0.00b 0.52b phenolics that derived the antioxidants and antidiabetic activities.
F.C 23.29 ± 6.77 ± 4.69 ± 8.23 ± 0.60 ± 28.81 ±
Worth mentioning, the liberation of reducing sugars, and amino acids
0.02 d 0.02b 0.02 a 0.02b 0.00c 0.31 a
form the rice matrix during processing, and the consequent formation of
Values are expressed as mean ± standard deviation (n = 6). Mean values with Maillard reactions products during processing also influence grain’s
different superscripts in the same column are statistically different (p < 0.05). chrominance (Qi et al., 2019).

activity positively correlated with α-amylase and adversely with
α-glucosidase inhibitory activity (r ≥ 0.583), indicating that these ac­
tivities are driven by the same molecules from the extract. There is
limited information available on the biological abilities of processed
black rice extracts to compare their role in controlling diabetes. How­
ever, cooked black rice using rice cooker exhibited similar inhibitory
potencies on inflammatory activities compared to raw grains, whereas
neither cyanidin-3-glucoside nor protocatechuic acid showed anti-
inflammatory activity (Bhawamai, Lin, Hou, & Chen, 2016).
3.4. Effect of processing on grains chrominance
As shown in Table 2, while Ro maintained the values of L*, F.C
caused a significant (p < 0.05) reduction compared to BR. R.C showed a
significant (p < 0.05) increase in a* value, and Ro reduced the redness
compared to BR. Ro and F.C significantly (p < 0.05) enhanced b* values
compared to BR. All processing methods significantly (p < 0.05)
enhanced C and H◦ of BR with R.C, and Ro caused the most significant
increase, respectively. Interestingly, processing produced minimal color
variance (ΔE) except for F and F.C, which caused a pronounced reduc­
tion (p < 0.05) in the grain’s color.
With regards to Pearson correlation coefficient, variations in color
3.5. Effect of processing on apparent amylose content
Amylose is considered to be a substantially linear polymer of α-1,4-
linked glucose molecules, although some branching occurs on the
amylose chains (Amagliani, O’Regan, Kelly, & O’Mahony, 2016). Based
on AAC, rice varieties were categorized into waxy (0–2%), very low
(3–9%), low (10–19), intermediate (20–25%), and high (>25%)
amylose (Gani et al., 2017). Therefore, the studied variety was consid­
ered as a very low amylose variety. Processing led to a significant
variation in the AAC of black rice (Fig. 3a). Interestingly, frying caused
the most significant increase in AAC, while Ro caused a nonsignificant
reduction. Further, the three cooking processes resulted in a significant
(p < 0.05) enhancement in AAC. Moreover, AAC is negatively influ­
enced by TPAC, vanillic acid, and syringic acid (r ≥ − 0.712). Interest­
ingly, the formation of amylopectin-phenolic complexation led to the
formation of amylose-like structures in pure amylopectin (Li, Pernell, &
Ferruzzi, 2018). Therefore, the increase in measurable AAC after cook­
ing and frying is caused by the interaction between the grain’s phenolic
compounds and amylopectin.

Fig. 3. (a) Apparent amylose content (AAC) and (b) the dynamic curves of in vitro enzymatic digestion of cooked grains. Values are means ± standard deviations (n
= 6). Mean values with different letters with the same test are statistically different (p < 0.05).

6
H. Aalim et al.
Table 3
Effect of processing on the starch nutritional fractions, digestion kinetics, and estimated glycemic index.
Starch (%)
RDS SDS RS
R.C 16.94 ± 1.80 a 40.99 ± 5.70 a 42.07 ± 4.29b
Ro.C 14.17 ± 0.48b 23.99 ± 2.61b 61.84 ± 2.44 a
F.C 13.11 ± 0.62b 21.88 ± 2.40b 65.01 ± 2.10 a
Values are expressed as mean ± standard deviation (n = 6). Mean values for each variety with different superscripts in the same column are statistically different (p <
0.05) (n = 6).
Abbreviations: K, first-order rate coefficients; C∞, equilibrium starch hydrolysis concentration; HI, hydrolysis index; eGI, estimated glycemic index; RDS, rapidly
digestible starch; SDS, slowly digestible starch; RS, resistant starch.
3.6. Effect of processing on the starch digestibility
Further comparison was made on starch digestibility. Cooked rice
grains were subjected to in vitro enzyme hydrolysis due to the poor di­
gestibility of raw, ungelatinized rice starch (Tamura, Singh, Kaur, &
Ogawa, 2016). The dynamic curves of in vitro digestion at varying time
points are shown in Fig. 3b. The hydrolysis ratio of grains gradually
increased over time with thermal treatments resulted in a consistent
reduction. The effect of thermal treatments on starch nutritional frac­
tions and first-order kinetic of Guggenheim equation were shown in
Table 3. The grains were characterized by significantly higher RS
compared to the other fractions, with F.C had the highest (p < 0.05) RS.
Accordingly, thermal treatments led to a significant decline of RDS, and
SDS, respectively. Previously, ghee frying of red and white rice signifi­
cantly lower the digestion rate and enhanced RS (Kaur, Ranawana, Teh,
& Henry, 2015). Further, the cooking method largely influences the
starch specific structure and digestibility (Li et al., 2020).
The endpoint hydrolysis concentration (C∞) was higher in R.C,
whereas the first-order rate coefficient (K) was lower in R.C compared
with processed grains; moreover, processing rice grains decreased HI
and eGI. Additionally, RS was found to be influenced by the differences
in starch structure, physicochemical properties, and texture character­
istics of the grains (Zhu, Fang, Qian, Guo, & Huo, 2021). The formation
of SDS and RS, in addition to the amylose–lipid complex, limit the starch
granule exposure to the digestive enzymes, thus reducing the glycemic
load of the meals, which would play a role of importance in diabetes
management.
Many factors have been identified to influence starch hydrolysis and
kinetic parameters. Previous reports indicate that rice grains contain
considerable amounts of phytate, which interacts with proteins and
starch in the rice matrix and decreases their digestibilities (Qi et al.,
2019). Recent studies have demonstrated that phenolic compounds such
as anthocyanins and proanthocyanidins induced spatial arrangement
disorder in rice starch structure, increase RS, and limit starch di­
gestibility (Dhital, Brennan, & Gidley, 2019; Zheng et al., 2021).
Further, inconsistencies might occur among different in vitro digestion
techniques (Hasjim, Lavau, Gidley, & Gilbert, 2010), as the values of k
and RS were found to be dependant on the sample homogenization, rice
cooking, oral digestion step, the concentration and the combined action
of amyloglucosidase and α-amylase enzymes (Tamura et al., 2016;
Warren et al., 2015).
4. Conclusion
The current study provides important insights into the health-
promoting properties of domestic processed black rice associated with
phenolic compounds and starch. It has been shown that the common
feature for the processed grains is to maintain their TPC, TAA, and
inhibitory potential against lipase and glycation. In addition, the ob­
tained results showed that the interaction between phenolics and
amylopectin during cooking led to a significant increase in amylose.
Roasting improved the phenolic contents and α-glucosidase inhibition
activity, while adversely affect AAC. Besides, the significant increase of
Food Research International xxx (xxxx) xxx
Guggenheim HI (%) eGI
− 1 2
K (min ) C∞ (%) R
0.008 ± 0.000c 89.88 ± 0.35 a 0.966 52.62 ± 0.68 a 68.60 ± 0.37 a
0.012 ± 0.001b 44.18 ± 2.10b 0.981 29.87 ± 1.61b 56.11 ± 0.88b
0.019 ± 0.002 a 36.59 ± 0.78c 0.964 27.28 ± 1.48b 54.68 ± 0.79b
K values by thermal treatments could be nutritionally unfavorable as
low k values reflect diffusion of pancreatic α-amylase into the starch
granule as digestion proceeds, which could be encountered by the suf­
ficient inhibitory action of phenolics on digestive enzymes. These results
are demonstrating that black rice is a remarkable raw material for
functional properties to the food products.
CRediT authorship contribution statement
Halah Aalim: Conceptualization, Formal analysis, Methodology,
Investigation, Writing - original draft. Di Wang: Resources. Zisheng
Luo: Funding acquisition, Resources, Writing - review & editing,
Supervision.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments
This work was supported by the Key Research and Development
Program of Zhejiang Province [2018C02049].
Appendix A. Supplementary material
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.foodres.2020.109898.
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