Assessment of Chemical Composition and Antioxidant Properties of Defatted Flours Obtained From Several Edible Insects

Download as pdf or txt
Download as pdf or txt
You are on page 1of 9

Article

Assessment of chemical composition and antioxidant


properties of defatted flours obtained from several
edible insects

Carmen Botella-Martı́nez, Raquel Lucas-González,


José A Pérez-Álvarez, Juana Fernández-López and
Manuel Viuda-Martos

Abstract
The aims of this study were determined the chemical composition and the antioxidant properties of defatted
flours obtained from several commercially available edible insects such as Acheta dosmesticus, Tenebrio
molitor, Zophobas morio, and Rhynchophorus ferrugineus to establish their utilization as ingredient in the
development of new food products. The proximate composition of flour was determined using AOAC meth-
ods while for antioxidant capacity, four different methodologies were employed (DPPH, ABTS, FIC, and
FRAP). The total phenolic content and the tannin content were also determined. All flours analyzed had a
high protein content with values ranging between 64.17 and 72.55 g/100 g flour. With regard to the antioxidant
activity, R. ferrugineus showed the highest values for DPPH, ABTS, and FRAP assays with values of 2.03, 4.93,
and 8.46 mg Trolox equivalent/g flour, respectively. For FIC assay, A. dosmesticus and T. molitor had the
highest values 0.47 and 0.48 mg EDTA equivalent/g flour. Defatted flours obtained from edible insects ana-
lyzed could have several applications as ingredients to the development new foods due to its good nutrient
content and as a functional food for the prevention of oxidation.

Keywords
Edible insects, flours, antioxidant, bioactive compounds, defatted
Date received: 5 June 2020; accepted: 24 August 2020

INTRODUCTION
the world habitants are calculated roughly in more than
Worldwide, there are a large number of researches 9000 million of people, which represents an additional
focused on the search for various nonconventional 50% more of food. Edible insects are an alternative
sources of proteins, which could help to improve the source of protein compared to domestic animals-
nutritional value of several food products at low price. based foods, and they show additional benefits that
In this way, the demand for relatively inexpensive include the use of less rearing land, a high rate of repro-
sources of proteins, which could be incorporated in to duction, and high feed conversion efficiency (Klunder
value-added food products is increasing. Edible insects et al., 2012). Additionally, edible insects can avoid
are attracting growing interest in the food industry due deforestation for pasture use, present a high efficiency
to their potential to serve as an alternative protein on water and soil use and edible mass compared to
source (Zielińska et al., 2018). The reason to introduce
this kind of food in western countries is that in 2050, IPOA Research Group, Agro-Food Technology Department,
Escuela Politécnica Superior de Orihuela, Miguel Hernández
Food Science and Technology International 0(0) 1–9
University, Alicante, Spain
! The Author(s) 2020 Article reuse guidelines: Corresponding author:
sagepub.com/journals-permissions Manuel Viuda-Martos, IPOA Research Group, Agro-Food
DOI: 10.1177/1082013220958854 Technology Department, Miguel Hernández University, Orihuela,
journals.sagepub.com/home/fst Alicante, Spain.
Email: [email protected]
Food Science and Technology International 0(0)

conventional livestock and they are responsible for a MATERIAL AND METHODS
relatively low emission of greenhouse gases and ammo-
Material and sample preparation
nia (Poma et al., 2017). Nevertheless, it should be noted
that, in most western countries, the use of insects as a House crickets (Acheta dosmesticus), mealworms
food product is usually considered as a primitive prac- (Tenebrio molitor), and superworms (Zophobas morio)
tice causing disgust depending on the anatomical part were acquired from ‘‘la grilleria’’ (Valencia, Spain); red
of the insect ingested (Jensen and Lieberoth, 2019). palm weevil (Rhynchophorus ferrugineus) was obtained
Nonetheless, consumers would be more receptive to from ‘‘Fundacion Palmeral de Elche’’ (Elche, Spain).
the consumption of these products as long as they After reception, the samples (1000 live crickets, 1000
cannot distinguish anatomical parts. The addition of mealworms, 1000 superworms, and 500 red palm
edible insects in everyday consumer products such as weevil) were placed in a freezer at 30  C for 24 h.
cookies, pasta, or bakery products where they are not Then, the samples were freeze dried for 24 h. After
perceptible, instead of incorporating them in to the diet, this, a grinder mill and sieves were employed to achieve
and linking them with well-known flavors are some different edible insect flours.
strategies to confront with neophobia or the poor sen- To remove oils, the flours were mixed with hexane in
sory characteristics of these products (Megido et al., the ratio of 1:5 (w/v) and then they were left in an
2016). ultrasound bath without temperature control for 1 h.
One way to start eating edible insects in the diet or Then, the samples were centrifuged at 6500  g for
using them in the development of novel foods is obtain- 15 min at 10  C and the supernatants were collected in
ing flour from them. These flours could be used as a flasks. The flour fraction that remains in the tube was
product for food fortification for numerous reasons. mixed with hexane (1:5 w/v) and shaken actively for
First of all, these flours have a high content in protein, 2 min and then they were left for 1 h in an ultrasound
which show a great biological value with a high-quality bath. For a second time, the samples were centrifuged
amino acid profile and a high level of digestibility. at 6500  g for 15 min at 10  C. Residual hexane was
Furthermore, edible insects are a great source of a removed from the flours by evaporation at 45  C
diversity of minerals such as: copper, iron, magnesium, overnight. The four flours obtained (Figure 1) were
manganese, phosphorous, selenium, and zinc and vita- A. dosmesticus flour (ADF), T. molitor flour (TMF),
mins like riboflavin, pantothenic acid, biotin, or folic Z. morio flour (ZMF), and R. ferrugineus flour (RFF).
acid (Ramos-Elorduy et al., 2012; Rumpold and
Schlüter, 2013). However, in order to avoid possible
Chemical composition
lipid oxidation processes of these flours, which are
rich in polyunsaturated fatty acids, it is necessary to The chemical composition (fat, ash, protein, and mois-
carry out a previous defatted process to increase the ture content) of edible insect flours was analyzed using
chemical stability and increase their shelf life. On the the pertinent AOAC methodologies (AOAC, 2016).
other hand, the flours obtained from commercially
available edible insects and invertebrates represent a
Edible insect extracts
potential source of antioxidant ingredients. These anti-
oxidant properties are related, as mentioned by Extracts from edible insects flours were prepared
Di Mattia et al. (2019), with several factors such as according to the method described by Lucas-Gonzalez
their taxonomy, eating habits, the life cycle (e.g. egg, et al. (2018) with some modifications. Therefore, 1 g of
larva, pupa, or adult), insect pre-processing before to edible insect flour was mixed with 10 mL of methanol–
study (e.g. use of the entire edible insect vs. several water (80:20, v/v) in a homogenizer Ultra-Turrax at
parts are removed), or the way in which the insects 12,000 r/min for 4 min. Later, the mixture was centri-
were treated (heat and mechanical managements). The fuged at 5000  g for 8 min at 5  C and the supernatants
negative part of consuming insects is the possibility of were collected in flasks. The pellet was homogenized
allergies. Actually, the prevalence of insect food allergy with 10 mL of acetone–water (70:30, v/v) in a homogen-
in Europe is not known. However, there are some izer UltraTurrax at 12,000 r/min for 4 min. Again, the
reports on food allergy to insects in Asia (Broekman samples were centrifuged at 5000  g for 8 min at 5  C.
et al., 2017). The supernatants of the two phases were mixed in a
Thus, the aims of this study were to determine the round-bottomed flask and evaporated until dryness
chemical composition and antioxidant properties of using a rotary evaporator R-205 (Büchi, Flawil,
defatted flours obtained from several commercially Switzerland) under reduced pressure (<0.1 bar) at
available edible insects to establish their applications 40  C. The solids were re-suspended in 7 mL of metha-
as potential ingredient in the development of new nol. Then, these extracts were filtered through a
food products. 0.45 mm filter and kept at 30  C until analysis.

2
Botella-Martı́nez et al.

Cricket Superworms Mealworms Red palm weevil


(Acheta domesticus) (Zophobas morio) (Tenebrio molitor) (Rhynchophorus ferrugineus)

Acheta domesticus flour Zophobas morio flour Tenebrio molitor flour Rhynchophorus
ADF ZMF TMF ferrugineus flour
RFF

Figure 1. The flours obtained from edible insects such as Acheta dosmesticus, Tenebrio molitor, Zophobas morio, and
Rhynchophorus ferrugineus.

reported by Mahdavi et al. (2017). The results were


Total phenol, total flavonoid, and tannin content
expressed as mg EDTA equivalent/g sample.
The total phenolic content (TPC) of edible insect flours
was determined using the Folin–Ciocalteu’s reagent ABTS assay. The radical cation (ABTSþ) scavenging
(Singleton and Rossi, 1965). The results were expressed activity was determined using the methodology
as g Gallic Acid equivalent (GAE)/100 g dry sample. described by Gullón et al. (2015). The results were
The tannin content (TC) was estimated using the van- expressed as mg Trolox equivalent/g sample.
illin–HCl in methanol assay (Price et al., 1978). The
results were expressed as mg Catechin equivalent
Statistical analysis
(CE)/100 g dry sample.
All experiments were carried out in triplicate and data
were reported as mean  standard deviation. The data
Antioxidant activity
collected for chemical composition, TPC, TC, and anti-
DPPH assay. The DPPH free radical scavenging cap- oxidant capacity were analyzed by one-way analysis of
acity was determined by the method described by variance. To discover whether there were significant
Brand-Williams et al. (1995) using the stable radical differences (p < 0.05) between the levels of the main
DPPH. Results were expressed as mg Trolox equivalent factor, contrasts between means were made using the
(TE)/g sample. Tukey’s test. The statistical analyses were made using
Statgraphics 5.1 for Windows (Statistical Graphics
Ferric-reducing antioxidant power. Ferric-reducing Corp., Rockville, MD).
antioxidant power (FRAP) was determined following The protein content, TPC, and TC were compared
the recommendations of Oyaizu (1986). The results with the values obtained for antioxidant capacity
were expressed as mg Trolox equivalent/ g sample. through Pearson’s correlation test. For that, a low cor-
relation was considered for r-values comprising
Ferrous ion chelating capacity. Ferrous ion chelating between 0.1 and 0.3; a moderate correlation was
assay (FIC) was measured by inhibiting the formation achieved with r-values ranging between 0.3 and
of Fe2þ–ferrozine complex following the methodology 0.7. Finally, a strong correlation was considered for

3
Food Science and Technology International 0(0)

r-values higher than 0.7. The variables were con- the type of insect analyzed and the life cycle in which
sidered not correlated for values of r lower than 0.1 it is found. However, it should be borne in mind that
(Pellegrini et al., 2018). data on the amount of protein in flours that can be
extracted from insects previously dried, milled,
RESULTS AND DISCUSSION defatted, and suspended in aqueous solutions had a
great variability. Several factors such as the solid/
Chemical composition
water ratio, pH, and temperature play an important
The proximal composition of defatted flours obtained role (Zhao et al., 2016).
from several edible insects is presented in Table 1. With Nonetheless, the protein content of the defatted
reference to the protein content, the flour obtained flours from edible insects obtained in this work indi-
from ADF showed the highest (p < 0.05) values fol- cates that these flours could be used in the food indus-
lowed by the flours obtained from RFF and ZMF try as a potential source of protein in the development
with no statistically significant differences (p > 0.05) of novel foods. Therefore, there are recent studies
between samples. Finally, TMF showed the lowest pro- where the flours obtained from several insects are uti-
tein values (p < 0.05). Similarly, for fat content, ZMF lized as ingredients to improve the protein content
had the highest (p < 0.05) values followed by the flours of the food products. Thus, González et al. (2019)
obtained from TMF and ADF with no statistically sig- used insects’ flour obtained from Hermetia illucens,
nificant differences (p > 0.05) between samples. The A. domesticus, and T. molitor as protein-rich ingredient
flour obtained from RFF had the lowest (p < 0.05) fat for bakery products. These authors reported that the
content. With reference to moisture, all samples showed protein content in bread increased between 9.66% and
a low moisture content with no statistical differences 28.55%. Azzollini et al. (2018) used flour obtained
(p > 0.05) between ADF and RFF and between TMF from T. molitor at two concentrations, 10% and
and ZMF. However, TMF and ZMF showed higher 20%, for elaborated cereal snacks and assessed the
moisture content (p < 0.05) than ADF and RFF. The nutritional properties as a function of the different
ash content had values ranging between 2.66 and processing techniques used during fabrication. These
4.77 g/100 g flour with statistically significant differ- authors reported that the addition of T. molitor flour
ences (p < 0.05) between all defatted flour analyzed. increased the protein content and improved the snack
The main component of the defatted flours obtained digestibility. The second largest component of insect
from edible insects is proteins. In general, the protein nutrient composition is fat. This fat has a high content
values obtained in this study were in agreement with of polyunsaturated fatty acids, like linoleic acid,
those reported by van Huis (2016) who mentioned that a-linolenic acid, or several o-3. The fact is that, in
the protein content varies between 7% and 91% dry general, the oils obtained from insects are liquid at
weight depending on the insect species, with most room temperature. This property makes them an
insects containing around 60%. Similarly, Xiaoming ideal candidate to be used as ingredients in several
et al. (2010) analyzed the protein content present in food products such as emulsions, frying oils,
several edible insect species. These authors informed food lubricants, etc. (da Silva Lucas et al., 2020). In
that the protein content was in the range of 13–77% this work, although part of the fat content has been
by dry matter, reflecting the large variability of tested eliminated, a small part remains. This low fat content
species. Zielińska et al. (2015) informed that edible can provide these polyunsaturated fatty acids to foods
insects have a high protein content, which varies in this type of flour and it may be used as an
between 20% and 76% of dry weight, depending on ingredient.

Table 1. Chemical composition of defatted flours obtained from some edible insects.

Sample Proteins Fat Ash Moisture

ADF 72.55  0.21a 4.49  0.16b 4.77  0.04a 4.95  0.19b


RFF 68.18  1.56b 2.42  0.05c 2.66  0.04d 4.99  0.02b
TMF 64.17  0.31c 4.67  0.07b 3.04  0.24c 6.29  0.71a
ZMF 67.56  0.70b 5.29  0.19a 3.55  0.03b 6.58  0.11a
Values expressed as g/100 g dry matter (mean values).
Values followed by the same letter within the same column are not significantly different (p > 0.05) according to Tukey’s multiple range
test.
ADF: Acheta dosmesticus flour; TMF: Tenebrio molitor flour; ZMF: Zhophobas morio flour; RFF: Rhynchophorus ferrugineus flour.

4
Botella-Martı́nez et al.

Total phenol and tannin content


reported values of 7.77 and 9.77 g GAE/100 g sample
The TPC and TC of different extract solutions of for M. facilger and H. whellani, respectively. This great
defatted flours obtained from some edible insects are variability depends on several factors and thus Di
presented in Table 2. The TPC varied from 1.09 to Mattia et al. (2019) informed that insects characterized
3.83 g GAE/100 g sample. The flour obtained from by vegetarian dietary habit showed a high content of
RFF showed the highest (p < 0.05) TPC followed by phenolic compounds than those characterized by a car-
the flour obtained from TMF. The flours obtained nivorous habit.
from ADF and ZMF had the lowest values (p < 0.05) Tannins have a biological and pharmacological
with no statistically significant differences (p > 0.05) activity, which includes antioxidative, antibacterial,
between them. With regard to the TC, again the flour antiviral, cardioprotective, antitumor, anti-inflamma-
obtained from RFF showed the highest (p < 0.05) tory, and immune-modulatory (Kumari and Jain,
values followed by the flour obtained from TMF. 2012). With regard to the phenolic content, tannins
ZMF had the lowest TC (p < 0.05). The TPC could also have been detected in edible insects. Thus, the
be used as an important indicator of antioxidant cap- results achieved in this study were higher than those
acity of a foodstuff and they may be utilized as an ini- described by Omotoso and Adesola (2018) who ana-
tial screen for several products when proposed as a lyzed the TC of four edible insects namely, Cirina
natural source of antioxidants in the development of forda, Periplanata americana, Rhynchophorus phoenicis,
new foods (Viuda-Martos et al., 2011). Nevertheless, and Zonocerus variegatus. These authors reported that
it should be noted that the TPC depends on several the TC values were 0.61, 0.54, 0.72, and 1.13 mg/100g
factors such as the part of the product used to obtain for R. phoenicis, C. forda, Z. variegatus, and P. amer-
the extract, the method used to obtain the flours, and icana, respectively. On the other hand, Chakravorty
the solvents or the methodology employed to measure. et al. (2016) mentioned that the TC of Oecophylla smar-
Several previous studies have described the presence of agdina and Odontotermes sp., two common species of
phenolic compounds in edible insects and in extracts edible insects used as food in India were 496.67 and
obtained from them. Nevertheless, the accessible data 615.0 mg/100 g, respectively. These values were higher
for the phenolic content of defatted flours obtained than those obtained in this study.
from edible insects analyzed in this work are scarce.
Several authors found polyphenolic compounds in
Antioxidant activity
flours or extracts obtained from numerous insects.
Thus, Navarro del Hierro et al. (2020) reported that The results of antioxidant capacity using DPPH,
the phenolic content of lyophilized flours obtained FRAP, FIC, and ABTS assays are summarized in
from A. domesticus and T. molitor using different Table 3. In DPPH assay, the antioxidant capacities of
extraction methods and solvents ranged between 0.3 defatted flours obtained from several edible insects
and 5 g GAE/100 g for A. domesticus and 0.8 and tested varied from 0.24 to 2.03 mg Trolox equivalent/
3.8 g GAE/100 g for T. molitor. These values were, in g flour. The flour obtained from RFF showed the high-
general, higher than those values obtained in this work. est (p < 0.05) values followed by the flour obtained
Similarly, Di Mattia et al. (2019) studied the TPC of from TMF. No statistically significant differences
defatted flours obtained from edible insects and inver- (p > 0.05) were found ADF and ZMF, which had the
tebrates. These authors informed that the TPC varied lowest antioxidant activity values measure with this
between 0.125 and 0.496 g GAE/100 g sample. In method.
another study, Kunatsa et al. (2020) analyzed the In FRAP assay, again the flour obtained from RFF
TPC of edible insects (Macrotermes facilger and had the highest (p < 0.05) values (8.46 mg Trolox
Henicus whellani) from Zimbabwe. These authors equivalent/g flour). ADF and TMF had the lowest

Table 2. Total phenolic and tannin content of defatted flours obtained from some edible insects.

Sample ADF RFF TMF ZMF


a
TPC 1.09  0.12c 3.83  0.08a 1.95  0.09b 1.15  0.19c
TCb 4.21  0.09c 9.45  0.10a 5.89  0.07b 3.92  0.07d
Values followed by the same letter within the same row are not significantly different (p > 0.05) according to Tukey’s multiple range test.
a
Values expressed as g Gallic Acid equivalent (GAE)/100 g dry matter (mean values).
b
Values expressed as mg Catechin equivalents/100 g dry matter.
ADF: Acheta dosmesticus flour; TMF: Tenebrio molitor flour; ZMF: Zhophobas morio flour; RFF: Rhynchophorus ferrugineus flour.

5
Food Science and Technology International 0(0)

Table 3. Antioxidant activity of defatted flours obtained from several edible insects measured with four
different methodologies: DPPH, ABTS, FRAP, and FIC.

Sample DPPH FRAP FIC ABTS

ADF 0.24  0.02c 2.82  0.18c 0.47  0.04a 1.26  0.12c


RFF 2.03  0.01a 8.46  0.13a 0.39  0.03b 4.93  0.38a
TMF 0.76  0.14b 3.08  0.18c 0.48  0.01a 3.12  0.25b
ZMF 0.27  0.03c 3.67  0.02b 0.32  0.06b 1.43  0.08c
For DPPH, FRAP, and ABTS assays values expressed as mg Trolox equivalent/g flour. For FIC assay values
expressed as mg EDTA equivalent/g flour.
Values followed by the same letter (a–b) within the same column are not significantly different (p > 0.05) according to
Tukey’s multiple range test.
ADF: Acheta dosmesticus flour; TMF: Tenebrio molitor flour; ZMF: Zhophobas morio flour; RFF: Rhynchophorus
ferrugineus flour; FRAP: ferric-reducing antioxidant power; FIC: ferrous ion chelating capacity.

Table 4. Pearson’s correlation coefficients between the different antioxidant assays (DPPH, ABTS, FRAP, and FIC) and
the protein, total phenolic, and tannin content.

Pearson’s correlation coefficients

Proteins TPC TC DPPH FRAP FIC ABTS

Proteins 1 0.862 0.632 0.525 0.651 0.234 0.637


TPC 1 0.857 0.906 0.959 0.231 0.924
TC 1 0.873 0.909 0.409 0.934
DPPH 1 0.965 0.688 0.925
FRAP 1 0.556 0.835
FIC 1 0.841
ABTS 1
TPC: total phenolic content; TC: tannin content; FRAP: ferric-reducing antioxidant power; FIC: ferrous ion chelating capacity.

antioxidant activity values measure with FRAP method high correlations were found between TPC–DPPH,
with no statistical differences (p > 0.05) between them. TPC–FRAP, and TPC–ABTS with r-values of 0.906,
For FIC assay, ADF and TMF had the highest ferrous 0.959, and 0.924; however, a low correlation was
chelating capacity with no statistical (p > 0.05) differ- obtained between TPC and FIC (r ¼ 0.231). Similarly,
ences between them. Likewise, no statistically signifi- the correlations between TC–DPPH, TC–FRAP, and
cant differences (p > 0.05) were obtained between TC–ABTS were higher with r-values ranging between
RFF and ZMF samples, which presented the lowest 0.873 and 0.934. When the correlation between assays
values. Finally, in ABTS assay, the flour obtained was analyzed, a positive correlation was found.
from RFF had the highest (p < 0.05) values followed Particularly, DPPH–ABTS, DPPH–FRAP, and
by the flour obtained from TMF. No statistically sig- FRAP–ABTS showed a strong correlation with
nificant differences (p > 0.05) were obtained between r-values higher than 0.7, whilst between DPPH and
ADF and ZMF, which had the lowest antioxidant FIC, ABTS and FIC, and FRAP and FIC there was
activity values measure in this method. a correlation moderate with r values comprising
Table 4 shows the correlation coefficients (r) between between 0.3 and 0.7. These results showed that flours
the antioxidant properties assessment with DPPH, obtained from edible insects had comparable activity in
ABTS, FRAP and FIC assays, TPC, TC, and protein all determinations.
content of flours obtained from edible insects. Thus, Lipid oxidation is the major concern of the food
the correlations Proteins–DPPH, Proteins–FRAP, and industry since this process causes severe changes in
Proteins–ABTS showed a moderate correlation (r lower products such as: the appearance of unpleasant odors
than 0.7 and higher than 0.3) with r values of 0.525, and flavors, decrease in the product shelf-life, signifi-
0.651, and 0.637 respectively, whilst the correlations cant changes in texture and color and, therefore, a
Protein–FIC assay had a low correlation (r lower decrease in the nutritional value of food (Alamed
than 0.3) with a r-value of 0.234. In the same way, et al., 2009). If oxidation is analyzed from a point of

6
Botella-Martı́nez et al.

view of human health, reactive oxygen species (ROS) found that extracts of grasshoppers, silkworm, and
like superoxide anion (O2), hydrogen peroxide (H2O2), crickets with values of 2.55, 2.48, and 2.37 mmol TE/
and hydroxyl radical (OH), are constantly created in 100 g, respectively showed the highest values of antioxi-
cellular metabolism, which could be particularly harm- dant capacity, measured with ABTS assay. On the
ful to cell components at elevated concentrations other hand, the extracts obtained from grasshoppers,
(Najafian and Babji, 2012). Oxidative stress is asso- African caterpillars, and cricket with values of 2.12,
ciated with cellular toxic processes that could provoke 1.88, and 1.81 mmol Fe2þ/100 g, respectively display
several pathologies such as carcinogenesis, cardiovascu- the highest FRAP values.
lar diseases, stroke, arthritis, and aging (Rahal et al., The antioxidant mechanisms through which proteins
2014). Antioxidants are a group of compounds that exercise this activity are not completely understood;
have the function of inhibiting and/or reducing effects nevertheless, it is known that the amino acid content
caused by the deleterious action of free radicals and as well as the sequence of the resulting peptides have a
nonradical reactive species (Barbosa et al., 2010). significant role in their antioxidant activity (Sarmadi
However, it should be borne in mind that it is very and Ismail, 2010). In this regard, Serpen et al. (2012)
difficult to measure the antioxidant capacity of a com- informed that moderate heat treatments may raise the
pound using one single methodology due to the anti- antioxidant capacity of several proteins as a result of
oxidant mechanism, in biological matrices, being so changes in their tertiary and quaternary structures. In
complex and numerous different factors playing a role scientific literature, there are several works that inform
in these mechanisms (Huang et al., 2005). For that that hydrophobic and aromatic amino acids, as well as
reason, in this work four different methodologies with histidine, methionine, tyrosine, lysine, and cysteine,
different antioxidant mechanisms were used. improve the force of antioxidant peptides through
Actually, the scientific attention has been focused on proton-donation capacity, electron-donation capacity,
the use of natural products with antioxidant properties or by radical scavenging capacity (Da Rocha et al.,
to protect tissues and food products from damage by 2018; Najafian and Babji, 2012). With respect to this,
free radicals. Thus, edible insect flours with a high con- Liu et al. (2016) reported that peptides with a low
tent of proteins, have received particular attention molecular weight such as methionine and lysine
because of studies that have reported that these flours showed more amino acids exposed to interact with
are highly efficient antioxidants and they show free rad- free radicals and this increases their antioxidant effect.
ical scavenging capacity for decreasing the toxic effects With regard to proteins, the action mechanism set in
of chemical agents. In this way, Zielińska et al. (2017a) motion by the antioxidant activity of phenolic and tan-
analyzed the antioxidant potential of some edible nins is still not clearly understood. Tannins have the
insects using free radical-scavenging capacity, ion che- ability to act as both primary antioxidants (e.g.
lating capacity, and reducing power assays. These donate hydrogen atom or electrons) and secondary
authors reported that the highest anti-radical capacity antioxidants. Additionally, these compounds showed
against 2,2-diphenyl-1-picrylhydrazyl radical was the capacity to chelate metal ions like Feþ2, which
achieved for baked cricket (Gryllodes sigillatus) hydrol- interfere with the Fenton reaction and in that way,
ysate with an IC50 value of 10.90 mg/mL and that delay the oxidation process (Karamac et al., 2006).
against ABTS radical was the highest for raw T. molitor The inhibition of lipid peroxidation by tannin constitu-
hydrolysate with an IC50 value of 5.3 mg/mL. Locust ents can act via the inhibition of cyclooxygenase
(Schistocerca gregaria) hydrolysate had the highest (Zhang et al., 2004). In the case of phenolic com-
Fe2þ chelation capacity with a IC50 value of pounds, several mechanisms have been proposed such
2.57 mg/mL. Similarly, Zielińska et al. (2017b) assessed as a direct hydrogen atom transfer, a single electron
the antioxidant capacity of extracts obtained of edible transfer, a sequential proton loss-electron transfer, or
insects Amphiacusta annulipes, Z. morio, Agnetina annu- metal chelating activity (Klein and Lukeš, 2007; Mayer
lipes, and Locusta migratoria after in vitro gastrointes- and Rhile, 2004; Rojano et al., 2008).
tinal digestion using DPPH, ABTSþ, FIC, and FRAP
assays. Insects that demonstrated the highest
antioxidant activities in each antioxidant assay were
CONCLUSIONS
A. annulipes in DPPH assay with values of Defatted flours obtained from A. dosmesticus, T. moli-
19.1 mg/mL; Z. morio in ABTS assay with values of, tor, Z. morio, and R. ferrugineus could have several
4.6 mg/mL; and A. annulipes in FIC and FRAP assays applications as ingredients in the development new
with values of 58.82% and 0.652 mg/mL, respectively. foods due to its good nutrient content and as a func-
Di Mattia et al. (2019) analyzed the capacity of several tional food for the prevention of oxidation. However,
extracts, obtained by 12 commercially edible insects, to in order for the consumption of insects and products
show an antioxidant effect in vitro. These authors derived from them to be generalized worldwide, three

7
Food Science and Technology International 0(0)

major hurdles must be overcome. First of all, it must be Da Rocha M, Alemán A, Baccan GC, et al. (2018). Anti-
ensured that the consumption of insects is safe through inflammatory, antioxidant, and antimicrobial effects of
the use of insect farms where the feeding, growth, underutilized fish protein hydrolysate. Journal of Aquatic
control of diseases of insects is assured. Secondly, the Food Product Technology 27: 592–608.
neophobic problems against entomophagy must be da Silva Lucas AJ, Menegon de Oliveira L, da Rocha M and
Prentice C. (2020). Edible insects: An alternative of nutri-
overcome in those countries where insect consumption
tional, functional and bioactive compounds. Food
is not widespread. Finally, analyze and determine the
Chemistry 311: 126022.
possible allergy problems that could be generated by Di Mattia C, Battista N, Sacchetti GP and Serafini M. (2019).
the consumption of insects. Antioxidant activities in vitro of water and liposoluble
extracts obtained by different species of edible insects
DECLARATION OF CONFLICTING INTERESTS and invertebrates. Frontiers in Nutrition 6: 106.
The authors declared no potential conflicts of interest with González CM, Garzón R and Rosell CM. (2019). Insects as
respect to the research, authorship, and/or publication of this ingredients for bakery goods. A comparison study of
article. H. illucens, A. domestica and T. molitor flours. Innovative
Food Science and Emerging Technology 51: 205–210.
Gullón B, Pintado ME, Fernández-López J, Pérez-Álvarez JA
FUNDING and Viuda-Martos M. (2015). In vitro gastrointestinal
The authors received no financial support for the research, digestion of pomegranate peel (Punica granatum) flour
authorship, and/or publication of this article. obtained from co-products: Changes in the antioxidant
potential and bioactive compounds stability. Journal of
Functional Foods 19: 617–628.
ORCID iDs
Huang DJ, Ou BX and Prior RL. (2005). The chemistry
Juana Fernández-López https://orcid.org/0000-0002-4771- behind antioxidant capacity assays. Journal of
8437 Agricultural and Food Chemistry 53: 1841–1856.
Manuel Viuda-Martos https://orcid.org/0000-0001-9801- Jensen NH and Lieberoth A. (2019). We will eat disgusting
3819 foods together – evidence of the normative basis of
Western entomophagy-disgust from an insect tasting.
REFERENCES Food Quality and Preference 72: 109–115.
Alamed J, Chaiyasit W, McClements JD and Decker EA. Karamac M, Kosinska A and Amarowicz R. (2006).
(2009). Relationships between free radical scavenging Chelating of Fe(II), Zn(II) and Cu(II) by tannin fractions
and antioxidant activity in foods. Journal of Agricultural separated from hazelnuts, walnuts and almonds.
and Food Chemistry 57: 2969–2976. Bromatologia i Chemia Toksykologiczna 39: 257–260.
Association of Official Analytical Chemists [AOAC] (2016). Klein E and Lukeš V. (2007). DFT/B3LYP study of the sub-
Official Methods of Analysis Chemists, 20th ed. stituent effect on the reaction enthalpies of the individual
Washington, DC: AOAC International. steps of sequential proton loss electron transfer mechan-
Azzollini D, Derossi A, Fogliano V, Lakemond CMM and ism of phenols antioxidant action: Correlation with phen-
Severini C. (2018). Effects of formulation and process con- olic C-O bond length. Journal of Molecular Structure 805:
ditions on microstructure, texture and digestibility of 153–160.
extruded insect-riched snacks. Innovative Food Science Klunder HC, Wolkers-Rooijackers J and Korpela JM. (2012).
and Emerging Technology 45: 344–353. Microbiological aspects of processing and storage of
Barbosa KBF, Costa NMB, Alfenas RCG, De Paula SO, edible insects. Food Control 26: 628–631.
Minim VPR and Bressan J. (2010). Estresse oxidativo: Kumari M and Jain S. (2012). Tannins: An antinutrient with
Conceito, implicações e fatores modulatórios. Revista de positive effect to manage diabetes. Research Journal of
Nutrição 23: 629–643. Recent Sciences 1: 1–8.
Brand-Williams W, Cuvelier ME and Berset C. (1995). Use of Kunatsa Y, Chidewe C and Zvidzai CJ. (2020).
a free radical method to evaluate antioxidant activity. Phytochemical and anti-nutrient composite from selected
LWT-Food Science and Technology 28: 25–30. marginalized Zimbabwean edible insects and vegetables.
Broekman HCHP, Knulst AC, Jong G, Gaspari M, Jager Journal of Agricultural and Food Research 2: 100027.
CFH, Houben GF, et al. (2017). Is mealworm or shrimp Liu Y, Wan S, Liu J, Zou Y and Liao S. (2016). Antioxidant
allergy indicative for food allergy to insects? Molecular activity and stability study of peptides from enzymatically
Nutrition & Food Research 61: 1601061. hydrolyzed male silkmoth. Journal of Food Processing and
Chakravorty J, Ghosh S, Megu K, Jung C and Meyer- Preservation 41: 13081.
Rochow VB. (2016). Nutritional and anti-nutritional com- Lucas-González R, Fernández-López J, Pérez-Álvarez JA
position of Oecophylla smaragdina (Hymenoptera: and Viuda-Martos M. (2018). Effect of particle size on
Formicidae) and Odontotermes sp. (Isoptera: phytochemical composition and antioxidant properties of
Termitidae): Two preferred edible insects of Arunachal two persimmon flours from Diospyros kaki Thunb. vars.
Pradesh, India. Journal of Asia-Pacific Entomololgy 19: ‘‘Rojo Brillante’’ and ‘‘Triumph’’ co-products. Journal of
711–720. the Science and Food and Agricultural 98: 504–510.

8
Botella-Martı́nez et al.

Mahdavi B, Yaacob WA and Din LB. (2017). Chemical com- Rumpold BA and Schlüter OK. (2013). Nutritional compos-
position, antioxidant, and antibacterial activity of essential ition and safety aspects of edible insects. Molecular
oils from Etlingera sayapensis A.D. Poulsen & Ibrahim. Nutrition & Food Research 57: 802–823.
Asian Pacific Journal of Tropical Medicine 10: 819–826. Sarmadi BH and Ismail A. (2010). Antioxidative peptides
Mayer JM and Rhile IJ. (2004). Thermodynamics and kin- from food proteins: A review. Peptides 31: 1949–1956.
etics of proton-coupled electron transfer: Stepwise vs. con- Serpen A, Gökmen V and Fogliano V. (2012). Total antioxi-
certed pathways. Biochimica et Biophysica Acta 1655: dant capacities of raw and cooked meats. Meat Science 90:
51–58. 60–65.
Megido RC, Gierts C, Blecker C, et al. (2016). Consumer Singleton VL and Rossi JA. (1965). Colorimetry of total
acceptance of insect-based alternative meat products in phenolics with phosphomolybdic phosphotungstic acid
Western countries. Food Quality and Preference 52: reagents. American Journal of Enology and Viticulture 16:
237–243. 144–158.
Najafian L and Babji AS. (2012). A review of fish-derived van Huis A. (2016). Edible insects are the future? Proceedings
antioxidant and antimicrobial peptides: Their production, of the Nutrition Society 75: 294–305.
assessment, and applications. Peptides 33: 178–185. Viuda-Martos M, Ruiz-Navajas Y, Fernández-López J,
Navarro del Hierro J, Gutierrez-Docio A, Otero P, Reglero G Sendra E, Sayas-Barberá E and Pérez-Álvarez JA.
and Martin D. (2020). Characterization, antioxidant activ- (2011). Antioxidant properties of pomegranate (Punica
ity and inhibitory effect on pancreatic lipase of extracts granatum L.) bagasses obtained as co-product in the
from the edible insects Acheta domesticus and Tenebrio juice extraction. Food Research International 44:
molitor. Food Chemistry 309: 125742. 1217–1223.
Omotoso OT and Adesola AA. (2018). Comparative studies Xiaoming C, Ying F and Hong Z. (2010). Review of the
of the nutritional composition of some insect orders. nutritive value of edible insects. Edible insects and other
International Journal of Entomology and Nematology invertebrates in Australia: Future prospects. In:
Research 2: 1–9. Proceedings of a workshop on Asia-Pacific resources and
Oyaizu M. (1986). Studies on products of browning reaction: their potential for development, Bangkok, 19–21 February
Antioxidative activity of products of browning reaction 2008, pp. 85–92.
prepared from glucosamine. Japan Journal of Nutrition Zhang YJ, DeWitt DL, Murugesan S and Nair MG. (2004).
44: 307–315. Novel lipid-peroxidation and cyclooxygenase inhibitory
Pellegrini M, Lucas-González R, Riccoi A, et al. (2018). tannins from Picrorhiza kurrora seeds. Chemistry &
Chemical, fatty acid, polyphenolic profile, techno-func- Biodiversity 1: 426–441.
tional and antioxidant properties of flours obtained from Zhao X, Vázquez-Gutiérrez JL, Johansson DP, Landberg R
quinoa (Chenopodium quinoa Willd) seeds. Industrial Crops and Langton M. (2016). Yellow mealworm protein for
and Products 111: 28–46. food purposes – Extraction and functional properties.
Poma G, Cuykx M, Amato E, Calaprice C, Focant JF and PLoS ONE 11: e0147791.
Covaci A. (2017). Evaluation of hazardous chemicals in Zielińska E, Baraniak B, Karaś M, Rybczyńska K and
edible insects and insect-based food intended for human Jakubczyk A. (2015). Selected species of edible insects as
consumption. Food and Chemical Toxicology 100: 70–79. a source of nutrient composition. Food Research
Price ML, Vansoyoc S and Butler LG. (1978). A critical International 77: 460–466.
evaluation of the vanillin reaction – An assay for tannins Zielińska E, Baraniak B and Karaś M. (2017a). Antioxidant
and sorghum grain. Journal of Agricultural and Food and anti-inflammatory activities of hydrolysates and pep-
Chemistry 26: 1214–1218. tide fractions obtained by enzymatic hydrolysis of selected
Rahal A, Kumar A, Singh V, et al. (2014). Oxidative stress, heat-treated edible insects. Nutrients 9: 970.
prooxidants, and antioxidants: The interplay. BioMedical Zielińska E, Kara M and Jakubczyk A. (2017b). Antioxidant
Research International 2014: 761264. activity of predigested protein obtained from a range of
Ramos-Elorduy J, Moreno JMP and Camacho VHM. (2012). farmed edible insects. International Journal of Food Science
Could grasshoppers be a nutritive meal. Food and and Technology 52: 306–312.
Nutrition Science 3: 164–175. Zielińska E, Karaś M, Jakubczyk A, Zieliński D, Baraniak B.
Rojano B, Sáez J, Schinella G, et al. (2008). Experimental and (2018). Edible insects as source of proteins. In: Mérillon
theoretical determination of the antioxidant properties of JM and Ramawat K (eds) Bioactive Molecules in Food.
isoespintanol (2-isopropyl-3,6-dimethoxy-5-methylphe- Reference Series in Phytochemistry. Cham: Springer, pp.
nol). Journal of Molecular Structure 877: 1–6. 1–53.

You might also like