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Eur Food Res Technol (2017) 243:2115–2126

DOI 10.1007/s00217-017-2912-4

ORIGINAL PAPER

Use of almond shell as food ingredient


Imen Kacem1 · Nuria Martinez‑Saez2 · Fatma Kallel1 · Khawla Ben Jeddou1 ·
Claire Boisset Helbert3 · Semia Ellouze Chaabouni1,4 · Maria Dolores del Castillo2 

Received: 27 February 2017 / Revised: 28 April 2017 / Accepted: 13 May 2017 / Published online: 27 May 2017
© Springer-Verlag Berlin Heidelberg 2017

Abstract Almond shell is a major waste from the almond inhibitory activity of a lignin-carbohydrate complex is
processing industry. Its feasibility as natural source of health- reported. Biscuits containing non-caloric sweetener soluble
promoting components was examined. The by-product was (2.5%) and insoluble (5.6%) dietary fiber, natural antioxi-
fractionated under basic conditions following an easy scale- dants (1.34 mg of gallic acid equivalents/g) and α-glucosidase
up process. The chemical composition of the recovered frac- inhibitors (1 g of biscuit–1 mg of acarbose) achieved a high
tion and its antioxidant and antidiabetic properties were eval- sensorial score (7.2 out of 9) when almond shell was incor-
uated. Novel information regarding the chemical composition porated to them. The application of a fraction from almond
of the polysaccharides was also obtained. Almond shell is shell containing lignin-polysaccharides complexes as food
formed by lignin-carbohydrate complexes possessing antioxi- ingredient in biscuit formulations for people with particular
dant properties and capacity to inhibit α-glucosidase. Accord- nutritional requirements is feasible and new.
ing to our knowledge, this is the first time α-glucosidase
Keywords  Almond shell · Antidiabetic effect · Antioxidant
properties · Dietary fiber · Novel ingredient · Novel food
The original version of this article was revised: The given name
and family name of fourth, fifth and sixth authors were swapped
inadvertently. The author names are corrected now. Introduction
Electronic supplementary material  The online version of this
article (doi:10.1007/s00217-017-2912-4) contains supplementary Increased oxidative stress and inflammation processes play
material, which is available to authorized users. a major role in causing chronic diseases such as diabetes
[1]. Diabetes mellitus is characterized by high blood glu-
* Maria Dolores del Castillo
cose levels, resulting from insulin deficiency or functional
mdolores.delcastillo@csic.es
http://www.cial.uam-csic.es disturbance of the receptors, with alterations in the metabo-
lization of carbohydrates, proteins and lipids [2].
Nuria Martinez‑Saez
http://www.cial.uam-csic.es Inhibition of α-glucosidase significantly decreases post-
prandial hyperglycemia after the intake of a diet rich in gly-
1
Enzymes and Bioconversion Unit, National Engineering cemic carbohydrates, which is a key strategy in the control
School, Sfax University, P.O. Box 1173‑3038, Sfax, Tunisia
of diabetes [3]. Acarbose, a potent α-glucosidase inhibitor,
2
Institute of Food Science Research (CIAL, UAM‑CSIC), represents a new concept in the treatment of metabolic dis-
C/Nicolás Cabrera, 9. Campus de Cantoblanco. Universidad
orders, particularly type 2 diabetes, and in some countries,
Autónoma de Madrid, 28049 Madrid, Spain
3
prediabetes. It reduces the absorption of dietary carbohy-
Service de Chromatographie Purification et analyse de
drates by reversible competitive inhibition of α-glucosidase
polysaccharides CERMAV-CNRS, 601 rue de la Chimie,
38041 Grenoble Cedex 9, France activity, reducing post-prandial blood glucose increment
4 and insulin response. Acarbose is considered an efficient
Common Service Unit of Bioreactor Coupled with an
Ultrafilter, National Engineering School, Sfax University, oral antidiabetic drug even though it produces side effects
P.O. Box 1173‑3038, Sfax, Tunisia such as diarrhea and flatulence [4].Therefore, it would be

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2116 Eur Food Res Technol (2017) 243:2115–2126

meaningful to search for new glucosidase inhibitors from Apparatus


natural products without such side effects.
Agro-industrial by-products are considered promising A microplate spectrophotometer BioTekpowerWaveTM
opportunities, offering new biologically active and func- XS (BioTek Instruments, United States), a texture analyzer
tional components for application in food and pharma- (LLOYD instruments, England), an activity water system
ceutical industries [5]. Almond shell is a major waste of (Aw Sprint TH-500, Novasina, Switzerland) and Agilent
the almond processing industry. This by-product has been GC 6850A instrument equipped with HP-5MS capillary
used in the production of bioethanol [6]. However, to the column were used for the analyses.
best of our knowledge its application in foods as a healthy
ingredient has not been previously reported. Almond shell Food ingredients
is a thick woody endocarp, mainly composed of cellu-
lose, hemicelluloses and lignin [7]. Some polysaccharides The basic ingredients used to elaborate the biscuits(i.e.,
in the cell walls of lignified plants can link to lignin to wheat flour, sucrose, sunflower oil, baking powder, salt,
form lignin–carbohydrate complexes (LCCs). These com- stevia powder containing 3% steviol glycosides) were pur-
plexes are known by their excellent anti-HIV, antiviral chased at specialized and certified food local markets. Food
and pro- or anti-inflammatory activities [8]. As far as we grade soy lecithin was provided by Manuel Riesgo SA
know, there are no reports dealing with the α-glucosidase (Spain).
inhibitory activity of LCCs. Moreover, data on the chemi- Almond shell was collected in the city of Sfax (Tuni-
cal composition of extracts enriched in polysaccharides sia), ground and sieved to small particles between 0.2 and
from almond shell suggest they could potentially be used 0.5 mm. Data on physico-chemical characterization of
as functional food ingredients with antioxidant properties almond shell is provided in Online Resource 1.
[7]. The development of new functional ingredients has
the advantage that food manufacturers can add extra value Sample preparation
to products the consumer is already familiar with. Biscuits
could represent a potential candidate for the addition of Almond shell as novel food ingredient
functional ingredients, but their nutritional profile has to
be improved in view of formulating functional products, Extraction was performed following the procedure
reduced in sugars and caloric content. Therefore, this described by Ebringerová et al. [7] with minor modifica-
study aims to evaluate the effect of almond shell fractions tions to obtain fractions with antioxidant capacity and high
enriched in polysaccharides and lignin on antioxidant and polysaccharide content. Ground almond shell was treated
α-glucosidase activities; as well as their usefulness as with 5% NaOH (1:10 w/v) at 60 °C for 1 h, vacuum fil-
natural food ingredients to reduce the risk or treat type 2 tered in a büshi funnel using cellulose filter paper, added
diabetes. Healthier biscuits have been prepared using the with three volumes of isopropanol and incubated overnight
novel food ingredient and stevia as a natural non-caloric at 4 °C. Finally, the fraction was isolated by decreasing the
sweetener. pH to 7 by adding concentrated acetic acid and centrifuging
at 4500 rpm for 15 min at 20 °C. The isolate fraction was
exhaustively dialyzed against distilled water under mag-
Materials and methods netic stirring for three days at 4 °C and then freeze-dried.
The powder was stored in sealed plastic bags at 4 °C until
Reagents use.
The obtained alkali-extracted almond shell fraction
Fiber kit and d-glucose, mannose and fructose kit were (AEASF) was dissolved in water (1:10 w/v) and centri-
supplied by Megazyme International Ireland Ltd. Sul- fuged at 4000 rpm for 10 min at 20 °C. The supernatant
furic acid (93–98%) and ethanol (96%) were purchased (water soluble fraction, WSF) and precipitate (water insolu-
from Panreac SA (Spain). Phenol (5%, w/v), 2,2-azino-bis ble fraction, WIF), were recovered. WIF was washed with
[3-ethylbenzothiazoline-6-sulphonic acid (ABTS)], potas- water (1:10 w/v) and centrifuged. Water soluble fractions
sium persulphate, Folin–Ciocalteu reagent and 6-hydroxy- were then mixed. WSF and WIF were frozen at −20 °C,
2,5,7,8-tetramethylchromane-2-carboxylic acid (trolox), freeze-dried and stored until analysis. WSF in a concen-
α-glucosidase from rat intestine and 4-methylumbellif- tration of 1 mg/ml was further fractionated by ultrafiltra-
eryl α-d-glucopyranoside (4-MUG) were purchased from tion using filter devices with a molecular weight cut-off of
Sigma Chemical Co (St. Louis, MO, USA). Water was 3 kDa (millipore), following the instructions of the manu-
purified using Milli-Q system. All other chemicals and rea- facturer. Fractions containing water soluble compounds
gents were of analytical grade. with higher (HMW) and lower (LMW) molecular weight

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Eur Food Res Technol (2017) 243:2115–2126 2117

than 3 kDa were frozen at −20 °C and freeze-dried. Pow- (d-mannose-d-fructose-d-glucose assay procedure, Mega-
dered samples (AEASF, WIF, WSF, HMW and LMW) zyme International Ireland, Ireland). The method was
were stored under dry conditions until analysis. Sam- adapted to a micromethod format. Results were expressed
ples preparations were performed in triplicate. Yields are as %. The analysis was performed in triplicate.
expressed as percentage (%).
Total carbohydrates
Food preparation
Carbohydrate content was determined in WSF and its cor-
Biscuits with AEASF as food ingredient (B, C, E and F)
responding HMW and LMW fractions using the phenol–
and those without AEASF (controls, A and D) were for-
sulfuric acid method described by Musako et al. [9]. The
mulated as indicated in Table 1. The dough was prepared
color reaction was initiated by mixing 100 µl of samples
by mixing salt, baking powder and sugar or stevia. Mineral
with 300 µl of concentrated sulfuric acid (93–98%) and
water at room temperature was added to the dry mixture
followed with the addition of 90 µl of phenol (5%, w/v) in
and thoroughly blended to obtain a homogeneous mix-
a glass flask. The reaction mixture was kept at 90 °C for
ture. Lecithin and oil were mixed in a separate bowl and
5 min. After cooling the samples to room temperature, the
then added to the mixture. Finally, flour was added gradu-
absorbance was measured at 490 nm. A calibration curve
ally to the mixture, and the dough was kneaded to obtain
was constructed using glucose (0.1–0.4 mg/ml). Reagent
homogeneous, elastic and slightly sticky dough. The dough
and sample blanks were also prepared and analyzed in each
was allowed to rest for 30 min and shaped into discs with
set of samples. All measurements were performed in tripli-
a 4-cm diameter and 0.8-cm thickness. The surface of each
cate and results were expressed as %.
biscuit was punctured several times using a fork to prevent
puffing. In the formulations with AEASF, it was combined
with the flour and added as described above. The biscuits Dietary fiber
were baked at 190 °C for 20 min in the oven. Two sets of
four biscuits were baked in duplicate (n = 8). The biscuits Dietary fiber (DF) content [insoluble (IDF), soluble (SDF)
were placed in the center of the tray forming a square, to and total (TDF)] was determined in AEASF and its soluble
reduce variability during baking. The biscuits were cooled (WSF) and insoluble (WIF) fractions using the total dietary
to room temperature prior to analysis (18–20 °C). fiber assay kit (Megazyme International Ireland, Ireland) as
indicated in the manufacturer’s instructions, and based on
Physico‑chemical and nutritional characterization an enzymatic–gravimetric method. Results were expressed
of the novel ingredient (AEASF) and food formulations as %. The analysis was performed in triplicate.

Free mannose, fructose and glucose Monosaccharide composition of polysaccharides extracted


from almond shell
Mannose, fructose and glucose contents were deter-
mined in WSF, HMW and LMW fractions using an The elemental monosaccharide composition of the polysac-
enzymatic kit following the manufacturer’s instructions charide extracted from WSF, LMW and HMW fractions

Table 1  Food formulations: Ingredients (g) Biscuit formulations


A, control biscuit using sucrose
as sweetener; B and C, sucrose A B C D E F
biscuits containing alkali-
extracted almond shell (AEASF, Wheat flour 56.00 52.13 40.70 65.85 62.84 51.09
3.9 and 15.3%, respectively) Water 20.00 20.00 20.00 23.50 23.51 23.51
as source of dietary fiber; D,
Sunflower oil 7.75 7.75 7.75 9.11 9.11 9.11
control biscuit using stevia
as sweetener; E and F, stevia Baking powder 0.55 0.55 0.55 0.65 0.65 0.65
biscuits containing AEASF (3 Salt 0.37 0.37 0.37 0.43 0.43 0.43
and 14.7%, respectively) Lecithin 0.33 0.33 0.33 0.39 0.39 0.39
Sucrose 15.00 15.00 15.00 – – –
Stevia – – – 0.07 0.07 0.07
AEASF – 3.87 15.30 – 3 14.75
Total 100 100 100 100 100 100

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was analyzed by gas chromatography–flame ionization formulations (A, B, C, D, E and F) was determined by
detector (GC–FID) as described by Ben Jeddou et al. [10]. ABTS radical scavenging activity measured as described
by Oki et al. [12]. Previously, biscuits were dissolved in
Lignin content water (100 mg/ml) and centrifuged. Then, supernatants
were diluted with PBS (5 mM, pH7.4).
The content in lignin was measured on WIF, WSF, HMW Two and a half mL of 7 mM ­ABTS·+ aqueous solution was
and LMW fractions from the AEASF. On the basis of the mixed with 44 µl of 140 mM potassium persulfate. The mix-
standard T222 om-11, 1 g (m0) of oven-dry-matter was ture was then allowed to stand in the dark for 16 h at room
placed in a 1 l flask with 15.0 ml of 72% sulphuric acid temperature. The working solution of the radical ­ABTS·+ was
and kept at 20 °C for 1 h in a thermostatic water-bath. After prepared by diluting the stock solution 1:75 (v/v) in 5 mmol/l
this, 575 ml of distilled water were added and the mixture of sodium phosphate buffer pH 7.4 to yield an absorbance
was brought to boiling for 4 h under reflux. The insoluble value of 0.7 ± 0.02 at 734 nm. The working solution of
fraction was recovered in a tarred fritted glass filter (m1) ­ABTS·+ (270 µl) was added to 30 µl of sample solution in
of porosity no. 3 and washed with hot water until neutral a microplate. Absorbance was then measured at 734 nm for
pH. The set filter-lignin was oven-dried at 105 °C for 24 h, 10 min at 30 °C with measurements every 2 min. After 5 min,
cooled in a desiccator and finally weighed (m2), determin- the reaction was complete. Trolox (0.15–2 µmol/l) was used
ing the acid insoluble lignin content (% in dry basis) as: as standard and results were expressed as the % of inhibition,
m2 − m1 IC50 and µmol trolox equivalents (eq.)/g sample. All meas-
Acid insoluble lignin (%) = × 100. urements were performed in triplicate.
m0
The original QUENCHER assay (direct ABTS) was also
The filtrate obtained from the crucible was kept for solu- performed on the insoluble fraction of the AEASF (WIF)
ble lignin estimation, which was measured spectrophoto- by measuring the quenching activity of the ­ABTS·+ rea-
metrically at 280 nm. Acid-soluble lignin was determined gent as detailed by Açar et al. [13] for insoluble fractions.
according to TAPPI UM 250 standards. It can be estimated WIF was first diluted tenfolds in cellulose and then 10 mg
through the following expression: of this mixture were weighed. The reaction was started by
adding 10 ml of ­ABTS·+. The mixture was vortexed for
Acid soluble lignin (%) 1 min and placed on a rotator in the dark. After mixing for
= {(Absorbance at 280nm × dilution factor/20) × 100}/ 30 min at 37 °C, the sample was centrifuged at 5000 rpm
(1000 × m0 ). for 2 min. The absorbance of clear supernatant was meas-
ured at 734 nm. The decrease in color was correlated to
Total phenolic content the antioxidant concentration. Trolox (0.2–2 mmol/l) was
used to calculate overall antioxidant capacity. Results were
Folin–Ciocalteu adapted to a micromethod format [11] expressed as mmol trolox eq./g WIF. All measurements
was selected to determine the total phenolic content (TPC) were performed in triplicate.
in the WSF, HMW and LMW fractions. The reaction was
initiated by mixing 10 µl of sample with 150 µl of freshly Alpha‑glucosidase inhibitory activity assay
prepared Folin–Ciocalteu solution. The mixture was equili-
brated for 3 min at room temperature and then 50 µl of This assay was performed on the soluble fractions of the
sodium bicarbonate solution were added. The reaction was AEASF (WSF, LMW and HMW) and the biscuits formu-
followed for 120 min at 37 °C by measuring absorbance at lations (A–F). Alpha-glucosidase enzyme was previously
735 nm. Sample blank and reagent blank were also ana- extracted to the assay. Briefly, 100 mg of rat intestine pow-
lyzed in each set of samples. A gallic acid calibration curve der were dissolved in 3 ml of NaCl (0.9%), sonicated in
was used for quantification (0.1–1 mg/ml). Results were an ice bath for 6 min and then centrifuged at 10,000g for
expressed as mg gallic acid equivalents (GAE)/g sample. 30 min. The supernatant containing the enzyme was stored
All measurements were performed in triplicate. in the freezer. In a 96-well microplate, 100 μl of sample
dissolved in PBS 100 mM (pH 6.9) were mixed with 100 μl
Biological activities of the novel ingredient (AEASF) of α-glucosidase (diluted 1/10) and 100 μl of 4-MUG
and food formulations (2 mM). Fluorescence was then monitored at an excita-
tion wavelength of 360 nm and an emission wavelength of
Total antioxidant capacity 460 nm for 30 min at 37 °C. Blank of sample and nega-
tive control (buffer, enzyme and 4-MUG) were included.
Antioxidant capacity of the soluble fractions from the Acarbose was used as a positive control. The percentage of
AEASF (WSF, LMW and HMW) and the biscuits α-glucosidase inhibition was calculated using the equation

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Eur Food Res Technol (2017) 243:2115–2126 2119

Fnc − Fs significance tests using the software SPSS Version 13.0


α − Glucosidase inhibition(%) = × 100,
Fnc ­(IBM® ­SPSS® Statistics, USA).

where Fnc and Fs are the fluorescence of the negative


control and sample, respectively. All measurements were Results and discussion
performed in triplicate.
Ingredient characterization
Quality attributes of the biscuits
Chemical composition of AEASF
Water activity and pH
The extraction yield of the AEASF was 9.6 ± 1.5%. This
The water activity (Aw) of biscuits (A–F) was measured yield was lower than that obtained by Ebringerová et al.
by a water activity meter. The ground biscuit was placed [7] and it may be related to the botanical origin of almond
in the specimen holder of the device to record its water tree. An economical extraction and purification of process
activity. The analysis was performed in duplicate and the has been used. However, the extraction yield was achieved.
mean value was reported. The combined use of low intensity heat (60 °C) with other
For the pH, 1 g of ground biscuit was mixed with unconventional technologies such as ultrasound and micro-
50 ml of deionized water and vortexed for 5 min. The wave-assisted extraction, high pressure combined with
mixture was held at room temperature for 1 h to sepa- thermal processing, supercritical carbon dioxide (SC-CO2),
rate solid and liquid phases. After carefully removing the pulsed electric fields assisted processing to improve extrac-
supernatant layer, pH was measured using a pH meter. tion yield of AEASF or subcritical water extraction may
The analysis was carried out in duplicate. be investigated in the future. These approaches have been
proposed as promising technologies that can be useful for
Color and texture analyses extraction of glucosinolates and isothiocyanates from natu-
ral sources. They are difficult to isolate because their high
Color parameters were expressed according to CIE reactivity. In addition, their hydrolysates are believed to be
L*a*b* scale [14]. Measurements were made using the toxic and anti-nutritional for animals. Non-conventional
Hunter Lab system with a colorimeter (Minolta CR-300, techniques seem to ensure high extraction yields and low
Japan). Four independent measurements of a* (redness), degradation of them [15].
b* (yellowness) and L* (lightness) parameters were car- Table  2a shows DF values corresponding to AEASF,
ried out on the top and bottom areas of the biscuits (A–F). WSF and WIF. AEASF under the conditions hereby
The hardness of the biscuits (A–F) was measured described showed a quantity of TDF of 43.2% (w/w).
using a texture analyzer. Results were expressed as new- The SDF content (25%) was greater than the IDF content
ton (N). The analysis was carried out in duplicate. (18.28%), with an IDF/SDF ratio of 1:1.4 DF was also
found in the two fractions isolated from AEASF. WSF con-
Sensorial analysis of the biscuits tained  ≈40% TDF and SDF was three times higher than
IDF. WIF, accounting for 22.1 ± 1.4% of the AEASF, was
Sensory evaluations of the biscuits (A–F) were carried mainly composed of IDF (81 ± 0.2). Almond shell can be
out. Ten pre-trained panelists participated in the sensory considered a natural abundant source of both SDF and IDF.
tests. Biscuits with 6-digit number codes were randomly SDFs have been linked to reduced cholesterol in the blood
presented to panelists. A 9-point hedonic scale (1 = dis- and decreased intestinal absorption of glucose, whereas
like extremely, 5 = neither like nor dislike, 9 = liked IDFs are associated with water absorption and intestinal
extremely) was used to evaluate the biscuits for color, regulation [16]. These physiological effects of SDFs and
flavor, crispness, hardness, mouthfeel and overall accept- IDFs depend on their structural and physical properties,
ability. Panelists were asked to swallow samples and to which can result in behavior such as hydration, swelling
rinse their mouths with water between samples. Five and and enzymatic attack [16].
higher scores of overall acceptability were considered as Total carbohydrate content, free glycemic sugars and
acceptable in this study. TPC of WSF and the corresponding HMW and LMW
fractions were also evaluated. WSF was rich in carbohy-
Statistical analysis drates (44.5 ± 5%). HMW (44.5% of the WSF) presented
19.5  ± 3.2% carbohydrates and LMW fraction (55.5% of
Data were expressed as mean ± standard deviation (SD). the WSF) 25 ± 2.6% carbohydrates. No free simple sug-
The data were then analyzed using Duncan’s method for ars (fructose, glucose and mannose) were found in the

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2120 Eur Food Res Technol (2017) 243:2115–2126

Table 2  a Content of total (TDF), insoluble (IDF) and soluble (SDF) arabinose (3.5%). Glucose, rhamnose and galacturonic
dietary fiber of the alkali-extracted almond shell (AEASF) and its acid were significantly lower (p < 0.05). On the basis of
soluble (WSF) and insoluble (WIF) fractions, and b monosaccharide
composition of the water soluble fraction (WSF) and its correspond- the results, it can be concluded that xylose was present in
ing high (HMW) and low (LMW) molecular weight fractions the backbone and some residues of galactose, arabinose,
glucose, rhamnose and galacturonic acid might be linked
TDF (%) IDF (%) SDF (%)
in the position of branched structure in the HMW fraction.
a As shown in Table 2b, the LMW fraction is mainly com-
 AEASF 43.24 ± 0.76b 18.28 ± 0.49b 24.96 ± 1.91b posed of glucose (13.5%), followed by significantly smaller
 WSF 39.88 ± 0.26a 9.73 ± 0.81a 30.16 ± 0.48c amounts (p < 0.05) of xylose and arabinose. Galacturonic
 WIF 87.55 ± 0.40c 80.95 ± 0.21c 6.60 ± 0.58a acid, galactose and rhamnose (p > 0.05) were present in the
Monosaccharide (%) WSF HMW LMW lowest quantities. All these results demonstrate the hetero-
geneity of these polysaccharides.
b
Regarding the lignin composition, results showed values
 Arabinose 7.13 ± 0.49B 3.45 ± 0.62B 3.68 ± 0.18B
of 2.5 ± 0.1%, 8.7 ± 0.8%, 11.4 ± 0.5% and 0.4 ± 0.04%
 Galactose 5.88 ± 1.57B 4.72 ± 0.73C 1.16 ± 1.18A
for the WIF, WSF, HMW and LMW fractions, respectively.
 Glucose 14.69 ± 1.44C 1.15 ± 0.15A 13.54 ± 1.82C Lignin is considered as non-carbohydrate DF and a com-
 Xylose 13.92 ± 1.24C 9.07 ± 1.41D 4.85 ± 0.24B plex chemical compound usually derived from wood and
 Rhamnose 0.91 ± 0.08A 0.68 ± 0.13A 0.23 ± 0.07A some algae as well as an integral part of the secondary
 Galacturonic acid 1.94 ± 0.14A 0.46 ± 0.09A 1.48 ± 0.07A cell walls of plants [19]. All these results implied that the
Results were expressed as % obtained ingredient is a lignin–carbohydrates complex in
Data are presented as mean  ±  SD. Different letters in lowercase which the relative high contents of carbohydrate constitu-
indicate significant differences (p < 0.05) between the samples of the ents make hydrophobic lignin highly water soluble [20].
same column
Different letters in uppercase indicate significant differences Biological activity of the novel ingredient
(p < 0.05) between the monosaccharides of the same sample
Total antioxidant capacity  Figure  1a shows the antioxi-
dant capacity of almond shell fractions (WSF, HMW and
isolated fractions (WSF, HMW and LMW), indicating that LMW fractions). All samples presented antioxidant char-
ingredients with a low glycemic index were obtained. TPC acter. The IC50 values for WSF, HMW and LMW frac-
of the WSF, HMW and LMW fractions were 47.6 ± 1.8, tions were 0.21, 0.22 and 0.86 mg/ml, respectively, cor-
31.7 ± 0.4 and 21.8 ± 0.6 mg GAE/g, respectively. These responding to 786.8, 768 and 192.9 µmol of trolox eq./g,
values were in the range reported by Sfahlan et al. [17], respectively. All the results described above indicated that
who obtained TPC values in almond shell ranging from the active substances (WSF, HMW and LMW fractions)
18.4 to 62.7 mg GAE/g. Moreover, these values obtained comprised lignin as well as carbohydrate, had antioxidant
in this study were higher than those quantified in hazel- capacity. Previous reports showed that lignins are hindered
nuts kernel which varied from 491.2 to 1700.4 mg GAE/ phenolic polymers which have strong antioxidant properties
kg depending on the cultivar and environmental conditions [21]. Carbohydrates were also proved to exhibit free radical
[18]. scavenging activities [10]. Therefore, the potential antioxi-
The monosaccharide composition of the WSF, HMW dant capacity of these fractions may be due to the supply of
and LMW fractions was that illustrated in Table 2b. The hydrogen by the carbohydrate or lignin constituents, which
monosaccharide composition showed that the WSF is combine with radicals and forms a stable radical to termi-
mainly composed of glucose (14.7%) and xylose (13.9%) nate the radical chain reaction. Basing on our results, the
(p > 0.05), followed by arabinose and galactose (p > 0.05), antioxidant power of WSF should be attributed to its HMW
and finally, by galacturonic acid and rhamnoses (p > 0.05). fraction, which contained high lignin content. Lignin seems
These results are in agreement with others studies which to be major contributor to the overall antioxidant character
reported that the water soluble fraction of almond shell found for WSF. The total antioxidant capacity of WSF was
treated with 5% NaOH during 60 min is composed of xylan higher than that previously reported for hazelnut kernels
and pectin polymers. It was also reported that the water (1682.5 µmol of trolox eq./kg) [18].
insoluble fraction is composed of xylan with low pectin WIF showed an overall antioxidant capacity of
contamination [7]. 1530 mmol of trolox eq./g. Results indicate that almond
The monosaccharide composition of the HMW frac- shell is a good source of insoluble antioxidant DF. The
tion showed that xylose (9.1%) was the significantly high- antioxidant character of this polymer may be closely asso-
est sugar (p < 0.05), followed by galactose (4.7%) and ciated to the high amount of xylanin its structure [7]. The

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Eur Food Res Technol (2017) 243:2115–2126 2121

Fig. 1  Concentration-response (a)
curves of total antioxidant HMW fracon LMW fracon WSF
capacity as the percentage 100
(%) inhibition of the radical 90

Inhibition of ABTS.+ (%)


­ABTS·+ of the a fractions 80
recovered from almond shell
70
(WSF water soluble fraction,
60
HMW water soluble compounds
with molecular weight higher 50
than 3 kDa, LMW water soluble 40
compounds with molecular 30
weight lower than 3 kDa); b 20
biscuits containing sucrose (A 10
control) and AEASF fiber (B 0
and C “high fiber content”), 0 2 4 6 8 10 12 14 16 18 20
and c biscuits containing stevia
as sweetener (D control) and mg/ml
AEASF fiber (E and F “high (b)
fiber content”). Data are pre- [A] [B] [C]
sented as mean  ±  SD 100
90
Inhibition of ABTS•+ (%)

80
70
60
50
40
30
20
10
0
0 5 10 15 20 25 30 35 40
mg/ml

(c)
[D] [E] [F]
100
90
Inhibition of ABTS•+ (%)

80
70
60
50
40
30
20
10
0
0 5 10 15 20 25 30 35 40
mg/ml

WIF antioxidant property may also be ascribed to lignin diseases associated with oxidative stress and inflammation.
[20] which is present in 2.5%. On the other hand, phenolic The presence of DF and polyphenols has also been reported
compounds may be bound to the structure of polysaccha- to decrease the glycemic index [24].
rides and lignin enhancing the antioxidant properties of the
complex [22]. Inhibition of intestinal α‑glucosidase activity in vitro  The
The transportation of dietary antioxidants through effect of the novel ingredient (AEASF) on α-glucosidase
the gastrointestinal tract has been described as an essen- activity is shown in Fig. 2a. The three samples (WSF, HMW
tial function of DF [23]. Polyphenols linked to DF may and LMW fractions) inhibited the activity of this enzyme.
be released in the colon by the action of bacterial micro- IC50 values were of 1.5, 1.2 and 7.9 mg/ml, correspond-
biota, producing bioactive metabolites and an antioxidant ing to 23.2, 30.3 and 4.5 mg of acarbose eq./g for the WSF,
environment, thereby reducing the risk of gastrointestinal HMW and LMW fractions, respectively. Results indicated

13

2122 Eur Food Res Technol (2017) 243:2115–2126

that the HMW fraction is composed of more efficient inhib- (≈45 g) of “high fiber content” biscuits supplemented with
itors of the enzyme than the LMW fraction. This activity AEASF (B, C, E and F biscuits) can provide 2.8, 6.9, 3.6
may be ascribed to both lignin–carbohydrate complex and and 7.9 g of TDF and 0.86, 1.2, 1.1 and 1.53 g of SDF,
phenols. Polyphenols possess the ability to bind to the active respectively. Therefore, a moderate consumption (5 units/
protein pocket of the α-glucosidase enzyme [25]. Several day) of the novel “high fiber content” biscuit formulations
studies suggest that plant polyphenols act as inhibitors of (F) made with stevia and AEASF fiber provides 23% of the
carbohydrate hydrolyzing enzymes [26]. Carbohydrates daily average amount of TDF recommended by the WHO
were also proved to possess α-glucosidase inhibitory activ- and 24% of the SDF recommended by the ADA.
ity [27]. Therefore, the strong potential α-glucosidase inhib- Addition of AEASF significantly increased (p < 0.05)
itory activity may be due to both effect of carbohydrates the TPC of the biscuits (Table 3), achieving the highest val-
and lignin containing polyphenols. As far as we know, there ues the C and F biscuits. No significant differences in TPC
is no report to date, describing the α-glucosidase inhibitory were found between control biscuits (A and D) (p > 0.05)
activity of a lignin-carbohydrate polymer. and among the biscuits supplemented with the same per-
The capacity of the HMW fraction to inhibit the activ- centage of fiber [B and E (p > 0.05); C and F (p > 0.05)].
ity of α-glucosidase (90%) was higher than that reported Thus, supplementation of novel biscuits with AEASF fiber
for wheat, buckwheat, corn and oats (18–31%) [28], and not only improves the balance of DF of the food formula-
was comparable to that found for sorghum (95%). Results tions but also their phenolic content.
also indicated that almond shell is source of α-glucosidase Antioxidants and α-glucosidase inhibitors may be
inhibitors. Therefore, it can be incorporated into food as a degraded during the baking process. No data on the ther-
potential antidiabetic agent. To the best of our knowledge, mal stability of biocompounds present in AEASF have
this is the first time that this property is associated with been previously reported. Biscuit formulations containing
fractions recovered from this agronomical by-product. this novel ingredient (B, C, E and F) showed significantly
higher (p < 0.05) antioxidant capacity than control biscuits
Characterization of biscuits (A and D) (Fig. 1b, c). The antioxidant capacity values of
the biscuits containing equal amounts of AEASF (B and E;
DF composition and bioactivity properties C and F) were of the same order of magnitude (p > 0.05).
Biscuits with the highest DF content (C and F) presented
The DF content of the different biscuits (A–F) is shown in the greatest antioxidant capacity. These results fit with the
Table  3. The highest values were found for C and F bis- TPC above described and support the stability of antioxi-
cuit formulations (15.4 and 17.7% TDF) containing stevia dant compounds to the thermal treatment.
and sucrose, respectively, and both, AEASF as ingredient As can be observed in Fig. 2b, c, the α-glucosidase
source of DF (43%). As expected, the lowest amounts of inhibitors in the novel biscuits resisted the baking process.
fiber were reported by A (sucrose) and D (stevia) control The “high fiber content” biscuits (C, 15.4% and F, 17.6%)
biscuits (4.0 and 4.1%). According to the nutritional claims corresponding to the highest concentration of AEASF
approved by the European Commission Regulation (EU) showed the highest inhibitory potential against the activity
No 1924/2006 [29] relative to fiber content, new biscuit of α-glucosidase. According to our calculations, the intake
formulations containing AEASF fiber (B, C, E and F) could of 1 g of biscuit may correspond to 1 mg of acarbose and
be classified within “high fiber content” nutritional claim moderate consumption of these novel biscuits (5 units/day)
(≥6 g of fiber per 100 g).The incorporation of the novel may exert an antidiabetic effect similar to that of 50 mg of
ingredient (AEASF) to the biscuit formulation significantly acarbose. Novel biscuits made using ingredients recovered
(p < 0.05) increased the amount of TDF above 6% and from almond shell (AEASF) present a great potential as
the proportion of IDF. The SDF/IDF ratios were of 1:1.7 functional and/or medical food since they may be useful in
and 1:1.5, for sucrose (A) and stevia (B) control biscuits, reducing the risk and treating chronic metabolic disorders
1:2.2 for B and E biscuits, and 1:4.6 and 1:4.1 for C and related to the metabolism of carbohydrates and oxidative
F, respectively. The soluble/insoluble fiber ratio has been stress such as type 2 diabetes.
established at 1:3 [30], which in concordance with our find-
ings. Recommendations with regard to DF consumption Quality parameters
differ depending on the regulatory body. For instance, the
World Health Organization (WHO) suggests a daily con- The measurement of Aw is crucial considering the develop-
sumption of 27–40 g of TDF. However, the American Die- ment of a food product. It can be used for the determination
tetic Association (ADA) recommends an intake between of shelf-life and it is an analysis of quality control [31]. As
20 and 30 g of fiber/day, of which 3–10 g should be SDF shown in Table 3, sucrose replacement by stevia increased
(15–30% soluble fiber).The consumption of a portion Aw. These results agree with others previously reported

13
Eur Food Res Technol (2017) 243:2115–2126 2123

Fig. 2  Inhibitory effect on (a)


alpha-glucosidase activity of
the a fractions recovered from LMW fracon WSF acarbose HMW fracon

Inhibition of α-glucosidase (%)


almond shell (WSF water solu- 100
ble fraction, HMW water solu- 90
ble compounds with molecular 80
weight higher than 3 kDa, LMW
70
water soluble compounds with
molecular weight lower than 60
3 kDa); b biscuits containing 50
sucrose (A control) and AEASF 40
fiber (B and C “high fiber con- 30
tent”), and c biscuits containing 20
stevia as sweetener (D control)
10
and AEASF fiber (E and F
“high fiber content”). Data are 0
presented as mean  ±  SD 0 5 10 15 20 25
mg /ml
(b)
[A] [B] [C]
80
Inhibition of α-glucosidase (%)

70
60
50
40
30
20
10
0
0 10 20 30 40 50 60
mg/ml

(c)
[D] [E] [F]
70
Inhibition of α-glucosidase (%)

60

50

40

30

20

10

0
0 10 20 30 40 50 60
mg/ml

[32, 33]. However, the increase of almond shell DF in the Aw decrease may be attributed to the greater ability to
formulation of biscuits slightly decreased their Aw, which strongly bind water of the soluble and insoluble fibers pre-
is in concordance with those results described by Garcia- sent in almond shell compared to wheat flour and there-
Serna et al. [33] who observed less moisture content when fore lower water availability in the biscuits. Addition of
coffee silverskin was incorporated as DF in biscuits. This AEASF may enhance the quality of dietary biscuits made

13

2124 Eur Food Res Technol (2017) 243:2115–2126

with stevia. Similar results reported by Prokopov et al.


Table 3  Total (TDF), soluble (SDF) and insoluble (IDF) dietary fiber, total phenolic content (TPC) and quality attributes (pH, Aw, hardness and color) of the proposed biscuits: A, control
sucrose biscuit; B and C, sucrose biscuits containing alkali-extracted almond shell (AEASF, 3.9% and 15.3%, respectively) as source of dietary fiber; D, control stevia biscuit; and E and F, ste-

27.56 ± 2.05e 40.27 ± 9.42a, b
12.15 ± 0.90c 58.37 ± 10.97b
−2.20 ± 0.22a 158.54 ± 24.01d
27.79 ± 2.10e 19.03 ± 1.69a
16.37 ± 0.75d 24.69 ± 1.78a
92.98 ± 2.75c
Hardness (†N)
[34] showed that adding 10 and 20% cabbage leaf power
rich of dietary fiber to sponge cake, increased water bind-
ing and thereby water retention power. Aw below 0.5 limits
the growth of all microorganisms and chemical degrada-
tive reactions in food are widely decreased [35]. Then, all

1.36 ± 0.51b
the tested biscuits containing sucrose or stevia and with or
without almond shell DF, can be considered microbiologi-
cal safe. Previous studies recognize the use of dietary fiber
b*

as an aid in delaying the aging of bakery products [34].


The demand for health-oriented products that contain-
b

7.74 ± 0.24d
12.78 ± 0.54e
5.00 ± 0.26c
0.56 ± 0.85a
12.20 ± 0.54e
1.57 ± 0.10

ing high fiber, natural antioxidants, and low calorie content,


such as those proposed in the present article is increasing
because of their beneficial health effects [34]. The replace-
a*

ment of sugar by stevia scarcely decreased pH values of the


d

56.74 ± 0.85b
47.06 ± 1.09a
103.41 ± 0.39e
65.82 ± 1.64c
46.61 ± 1.37a

biscuit formulations (Table 3) unlike those recent results


100.57 ± 0.45

found by other authors [32], who associate steviosides with


increase of pH in biscuits. In contrast, supplementation with
Color

AEASF fiber significantly (p < 0.05) increased the pH (≥7).


L*

Our results are in accordance with those pH values observed


b

7.04 ± 0.19b

for biscuits, which have been described to range from 7.0 to


7.5 ± 0.08c
7.79 ± 0.14c
6.49 ± 0.37a

7.51 ± 0.09c
6.98 ± 0.12

Data are presented as mean  ±  SD. Different letters indicate significant differences (p < 0.05) between samples (A–F)

7.3 [36]. These values are suitable for stability or keeping


qualities due to the fats being more readily attacked and bro-
PH

ken down in an acid medium than in alkaline medium [37].


Quality attributes

Sugar replacement significantly increased (p < 0.05) L*


0.35 ± 0.018c
0.32 ± 0.013c
0.25 ± 0.04b
c

0.21 ± 0.02a

0.32 ± 0.02c

and increased a*, color parameters (Table 3). The addition


0.31 ± 0.01

of AEASF to the biscuit formulation significantly affected


their color profile (online resource 2). L* and b* parameters
Aw

significantly (p < 0.05) decreased in a dose-dependent man-


ner, while a* increased with the addition of DF (Table 3).
TPC ­(mgφGAE/g)

These results are in line with those previously reported by


1.42 ± 0.14b

1.34 ± 0.17b
a

3.02 ± 0.07c
0.87 ± 0.18a

2.79 ± 0.07c
0.91 ± 0.13

Garcia-Serna et al. [33]. These findings support the poten-


tial of almond shell components as natural coloring.
Texture analysis of biscuits is shown in Table 3. Sucrose
biscuits were harder than those made with stevia [32, 33,
38]. Addition of AEASF significantly increased (p < 0.05)
a, b

69.16 ± 3.80b

69.08 ± 4.66b
82.16 ± 2.74c
59.71 ± 2.01a

80.52 ± 5.16c
63.48 ± 1.20

the hardness of biscuits in a dose-dependent manner. These


via biscuits containing AEASF (3% and 14.7%, respectively)

mechanical changes are related to an increase in fibers and


IDF (%)

carbohydrates and to reduced gluten development capacity.


Dietary fiber and antioxidant compounds

Popov-Raljic et al. [39] previously reported that the nature of


DF used in biscuits affects their rheological properties, water
b, c

30.84 ± 3.81b

30.92 ± 4.66b
17.84 ± 2.74a
40.29 ± 2.02c

19.48 ± 5.15a
36.53 ± 1.19

activity, viscosity and sensorial characteristics such as color.


According to our results, almond shell incorporated as
SDF (%)

DF in combination with stevia produces dietary biscuits


with acceptable quality properties.
  GAE Gallic acid equivalents
6.26 ± 0.14a,b

8.12 ± 1.11b
15.40 ± 2.17c

17.66 ± 3.35c
a

4.10 ± 0.33a
3.95 ± 0.45

Sensorial analysis
TDF (%)

All biscuits prepared hereby were evaluated for their color,


flavor, crispness, hardness, mouthfeel and overall accept-
  N Newton

ability using 9-point hedonic scale (Table 4). According to


Biscuits

the data, both the sweetener and the DF content have influ-
ence on the sensorial analysis of the biscuits. Regarding
A

D
B
C

E
F

13
Eur Food Res Technol (2017) 243:2115–2126 2125

Table 4  Sensory evaluation scores (1–9 scale) of biscuits: A, con- (“high fiber content”, 6.3 and 15.4%, respectively); D, control stevia
trol sucrose biscuit; B and C sucrose biscuits B and C, sucrose bis- biscuit, and E and F, stevia biscuits containing AEASF dietary fiber
cuits containing alkali-extracted almond shell (AEASF) dietary fiber (“high fiber content”, 8.12 and 17.7%, respectively)

Biscuits Color Flavor Crispness Hardness Mouthfeel Overall acceptability

A 6.8 ± 1.75a 5.8 ± 1.54a 6.5 ± 0.52b 6.1 ± 0.83a, b 6.5 ± 0.52b 7 ± 0.81a, b


B 7.2 ± 1.22a 5.7 ± 1.41a 6.8 ± 0.78b 6.1 ± 1.51a, b 7.8 ± 0.91a 7.6 ± 0.51a
C 5 ± 1.24c 5.7 ± 1.63a 6.9 ± 0.87b 5.4 ± 1.62b, c 6.5 ± 1.50b 7.1 ± 0.99a, b
D 6.3 ± 1.15a, b 6.4 ± 1.17a 5.7 ± 0.82c 5.6 ± 0.48b, c 6.1 ± 0.73b 6.4 ± 0.84b, c
E 6.2 ± 0.78a, b 6.6 ± 1.57a 7.6 ± 0.51a 6.7 ± 0.45a 6.6 ± 1.17b 7.2 ± 0.78a, b
F 5.4 ± 1.07b, c 5.7 ± 1.33a 7 ± 0.66a, b 4.7 ± 0.9c 5 ± 0.94c 6.1 ± 1.19c

Data are expressed as mean ± standard deviation (n = 10). In each column, values with different superscript letters are significantly different
(p < 0.05)

the use of stevia as sweetener, can be observed crispness Conclusion


was significantly (p < 0.05) scored lower (D, 5.7) than the
biscuit containing sucrose (A, 6.5) and overall acceptability Fractions recovered from almond shell following the pro-
decreased (F, 6.1) when compared to the respective biscuit cedures hereby described have a great added value due
made with sucrose (C, 7.1). The other attributes were not to their potential to prevent and/or treat diabetes as a diet-
affected by the replacement of sucrose by stevia. As pre- related chronic disease. Biscuits made with the almond shell
viously reported, fructooligosaccharides (FOS) presents contain SDF and IDF, natural antioxidants and inhibitors of
slight sweetness and could enhance taste of the biscuits α-glucosidase enzyme, and in addition, they present accepta-
by masking negative off-flavors from stevia, and therefore, ble sensorial properties according to consumers’ preferences.
to improve the overall acceptance [40]. As far as AEASF
fiber addition is concerned, biscuits were less appreciated Acknowledgements  The present research was funded by AGL2014-
for the color, hardness and mouthfeel attributes when high 57239-R project and The Ministry of Higher Education And Scientific
Research, Tunisia. Martinez-Saez, N. thanks the Autonomous Univer-
amount of AEASF was added (C and F biscuits) but more sity of Madrid (U.A.M) for her FPI-predoc fellowship.
appreciated for the crispness. Similar results demonstrated
by Prokopov et al. [34] showed that the addition of 10 and Compliance with ethical standards 
20% cabbage leaf powder changed the sensory cakes char-
acteristics, which became less appreciated for the sensation Conflict of interest  The authors declare that they have no conflicts
of interest.
for sweetness and the color.
Moreover, there were no significant differences in the
Compliance with ethical requirements  This article does not contain
flavor for all biscuits, contrary to what was reported by
any studies with animals or intervention human trials.
Prokopov et al. [34], who showed that the sponge cake made
with cabbage leaf powder has a strongly expressed odor spe-
cific towards the sample odor. Moreover, those “high fiber
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