Proteines Des Criquets
Proteines Des Criquets
Proteines Des Criquets
LWT
journal homepage: www.elsevier.com/locate/lwt
A R T I C L E I N F O A B S T R A C T
Keywords: House cricket (Acheta domesticus; AD) and yellow mealworm (Tenebrio molitor; TM) are two promising insect
Insect powder species for possible novel food applications. In this research the insect protein fractions were extracted, char
Protein extraction acterised, and used in the manufacturing of pasta by replacing semolina with 14% of powdered proteins. Pasta
Novel food
samples were then analysed to evaluate technological quality aspects. Results showed that insect protein in
Pasta fortification
Technological properties
clusion resulted in a darker (L* value: 76.7, 53.4, 59.9 for control, AD and TM, respectively) and firmer (12.4,
13.7, 13.8 N: control, AD and TM, respectively) AD and TM pasta, and a higher water absorption index for AD
(148, 178, 150%: control, AD and TM, respectively). In conclusion, both extracts offer interesting opportunity for
pasta formulations, possibly leading to an improved protein content and quality. From an industrial perspective,
the present study demonstrated that the tested edible insects can provide protein extracts for the possible
fortification of pasta with high-quality protein and technological traits, thus representing an ingredient with
interesting potential for several food applications.
1. Introduction Oonincx, 2017), and generate fewer emission of greenhouse gases than
cattle or pigs (Oonincx et al., 2010). The potential sustainability of insect
For centuries, edible insects have been an important source of nu farming makes them one of the alternative protein sources to face the
trients for humans worldwide; in fact, a wide variety of species are increase in global protein demand (Berggren, Jansson, & Low, 2019).
commonly consumed in many countries such as Asia, Africa, Latin The manufacturing and marketing of insect-based food products has
America, and they ensure a valuable supply of nutrients (Belluco et al., become interesting also in Western Countries, where insects can be
2013). Despite the nutritional composition of insects can display sig exploited to enhance the nutritional value of food products. In the EU,
nificant variations according to species, development stage, environ the Novel Foods Regulation (Regulation (EU) 2015/2283) has entered
mental conditions, and substrate on which they feed themselves into force in 2018 and it explicitly considers whole insects. Furthermore,
(Kouřimská & Adámková, 2016), they can generally be considered a following the 2021’s positive scientific opinions of the European Food
significant source of high-quality protein, with an interesting amino acid Safety Authority about Locusta migratoria, Acheta domesticus and Tene
profile, essential fatty acids, microelements and other bioactive com brio molitor, the European Union (EU) Member States authorities have
pounds (Elhassan, Wendin, Olsson, & Langton, 2019). The growing recently approved the drafts implementing regulation aiming to
scientific and commercial interest regarding the use of insects as food, as authorise the commercialisation of Locusta migratoria on the EU market
well as feed (Dalle Zotte, 2021), is mainly linked to the fact that they can (https://ipiff.org/insects-novel-food-eu-legislation), while dried Tene
represent a valuable mean to ensure food security in areas subjected to brio molitor and Acheta domesticus have already been approved with the
significant demographic growth and resources scarcity, but also to Regulation (EU) 2021/882 and Regulation (EU) 2022/188 respectively.
improve the sustainability of feed/food production. In fact, it has been In these Countries, however, insect consumption is still very limited,
documented that farming insects allows a significant reduction in land mainly attributable to cultural habits and bias (Mancini, Moruzzo, Ric
and direct water use compared to conventional crops (Van Huis & cioli, & Paci, 2019). From this viewpoint, promoting a positive attitude
* Corresponding author.
E-mail addresses: gabriella.pasini@unipd.it (G. Pasini), marco.cullere@unipd.it (M. Cullere), mara.vegro@unipd.it (M. Vegro), barbara.simonato@univr.it
(B. Simonato), antonella.dallezotte@unipd.it (A. Dalle Zotte).
https://doi.org/10.1016/j.lwt.2022.113638
Received 29 April 2022; Received in revised form 30 May 2022; Accepted 4 June 2022
Available online 7 June 2022
0023-6438/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
G. Pasini et al. LWT 164 (2022) 113638
toward entomophagy could be a goal in stimulating consumers to eat 2.3. Protein recovery from insect powder and amino acid composition
and cook insects (Megido et al., 2016). Up to now, the most promising
strategy to increase insect acceptability, and thus the market potential of Insect powder samples from adult house cricket and yellow meal
insects in Western diets, seems to be their processing into powder form worm larva were defatted using n-hexane (ratio 1:10 – sample:solvent).
to be used as an ingredient for different food products, thus avoiding Samples were processed twice in 48 h at room temperature by stirring at
visual recognition of insects (Balzan, Fasolato, Maniero, & Novelli, 70 RPM/min (M201-OR shaker, MPM Instruments, Milan, Italy), after
2016). ward, they were centrifuged (Beckman Coulter, Brea California, USA) at
In the recent past, there has been growing research into the possible 20,000 g for 30 min. Pellets were recovered and dried under a nitrogen
application of flour, paste, and protein extracts obtained from different stream at 20 ◦ C to obtain a defatted powder.
insect species into several food products including bakery goods (da The protein from the defatted powder was extracted in PBS buffer
Rosa Machado & Thys, 2019; González, Garzón, & Rosell, 2019), brown (0.01 mol L− 1 Na2HPO4/NaH2PO4, 0.015 mol L− 1 NaCl, pH 7.4), ratio of
rice flour and cake (Indriani, Ab Karim, Nalinanon, & Karnjanapratum, 1:10 w/v, by continuous stirring at room temperature for 48 h. Samples
2020), cereal bars (Ribeiro et al., 2019) and other snacks (Azzollini, were then centrifuged at 20,000 g for 30 min, the supernatants were
Derossi, Fogliano, Lakemond, & Severini, 2018). Among the possible collected by vacuum filtration (GF/A – 90 mm, Whatman; Cytiva,
food applications of insects there is pasta, a well-known traditional Marlborough, MA), and then freeze-dried (Edwards Italy, Milan, Italy)
cereal-based food, characterised by a high palatability, an interesting to recover a fine powder. The protein content of the two extracts was
nutritional profile, and also by a moderate glycaemic index (Bustos, calculated using 6.25 as nitrogen-to-protein conversion factor.
Perez, & Leon, 2015). Being a staple food, pasta could represent an
excellent carrier of nutrients and bioactive compounds, and the novel The extraction yield (%) was calculated and expressed on starting weight basis
ingredient should be easily incorporated into the pasta microstructure by the following equation: extraction yield % = [weight of extract (g) / weight
and ensure its technological quality, including colour, cooking time and of sample (g)] * 100
loss, water absorption, swelling index, and texture profile (De Marco, Extraction efficiency was calculated on starting protein basis by the following
Steffolani, Martínez, & León, 2014). Despite the popularity and com equation: extraction efficiency % = [total extracted protein (g) / total protein
mercial relevance of this food product, published research about its content (g)] * 100
possible fortification with insects is still limited. A recent study has
successfully fortified durum wheat pasta with house cricket powder up The amino acid composition of the two protein extracts was deter
to an inclusion level of 15% (Duda, Adamczak, Chełminska, Juszkie mined after acid hydrolysis and pre-column derivatisation with 6-ami
wicz, & Kowalczewski, 2019), while incorporating grasshopper (Locusta noquinolyl-N-hydroxysuccinimidyl carbamate (AQC), separated by RP-
migratoria) or yellow mealworm into egg pasta with a 15% inclusion HPLC and analysed by UV detection (Agilent 1260 Infinity, Agilent
level revealed an improvement in the nutritional profile (protein and Technologies, Santa Clara, CA, USA) following a method adapted from
fat), but it harmed cooking performance and overall sensory accept European Pharmacopoeia (Council of Europe, 2005). Briefly, for Ala,
ability, the latter likely attributable to the lipid fraction (Çabuk & Yil Arg, Asp, Glu, Gly, His, Ile, Leu, Lys, Met, Phe, Pro, Ser, Thr, Tyr, and Val
maz, 2020). Based on above mentioned, isolating and extracting insect determination, protein of the sample was hydrolysed with hydrochlo
proteins seems theoretically desirable to increase the protein content of ride acid (6 M) at 105 ◦ C for 24h. Cys was determined as the sum of
pasta. However, the possible impact of extracted insect proteins on the cysteine and cystine, after reaction with dithiodipropionic acid, pro
technological traits of pasta is still unknown, yet needs to be studied. ducing a mixed disulphide, which then underwent acid hydrolysis
Therefore, the present research aimed to i) evaluate a laboratory- accordingly. After hydrolysis, the samples were neutralized with sodium
scale manufacturing protocol of a powder enriched with proteins from hydroxide (8 M), adjusted to volume, and filtered at 0.45 μm. Then, the
Acheta domesticus and Tenebrio molitor; ii) characterise the proteins of derivatisation step was conducted according to the manufacturer’s in
insect protein-rich powders; iii) evaluate the impact of the incorporation structions (AccQTag Ultra Derivatisation Kit; Waters, Milford, MA).
of 14% of insect protein powders on selected technological quality traits
of dry pasta. 2.4. Sodium dodecyl sulphate-polyacrylamide gel electrophoresis (SDS-
PAGE)
2. Material and methods
The molecular weight distribution of the protein fraction obtained
2.1. Raw materials from insects was visualised with SDS-PAGE using 8–16% TGX Stain-Free
Gel (Bio Rad, Hercules, CA). The samples were dissolved in 0.5 M
Commercial wheat semolina (Triticum durum), the raw material for Tris–HCl Laemmli buffer (Sigma Aldrich, St. Louis, MO) pH 6.8, con
pasta production, was bought in a local supermarket and its composi taining 15% (w/v) glycerol, 1.5% (w/v) SDS and 8% 2-mercaptoetha
tion, as reported on the label, was: 70.8 g/100 g of total carbohydrates, nol, in ratio 1:3 (w/v), heated at 100 ◦ C in a water bath for 5 min and
12.5 g/100 g of proteins, 1.8 g/100 g of total fat and 2.6 g/100 g of total centrifuged for 3 min at 10.000 g. Afterward, 30 μL of the solution was
dietary fibre. applied to the gel and the electrophoresis was conducted at a constant
Dried larvae of yellow mealworm (Tenebrio molitor) and adult house current of 48 mA. The molecular weight standard proteins were the Pre-
cricket (Acheta domesticus) were provided by INEF (Insect Novel Stained Broad Range Molecular Weight Markers (Bio-Rad). Finally, gels
Ecologic Food, Piombino Dese, Italy). The dried insect samples were were stained with 0.05% (w/v) Coomassie Brilliant Blue R-250 (Bio
ground with liquid nitrogen to obtain a fine powder. Rad), 5% (w/v) TCA, 17% (v/v) methanol, and 6% (v/v) acetic acid, and
de-stained in 7% (v/v) acetic acid.
2.2. Proximate composition of insect powder 2.5. Preparation of pasta samples enriched with insect protein fraction
Analysis of the insect powder was carried out in triplicate following The pasta was made using a professional Lillodue pasta-making
the AOAC - Association of Official Analytical Chemists (2000) proced machine (Bottene, Schio, Italy). The samples were prepared with total
ures to determine the dry matter (DM; method no. 934.01), crude pro wheat semolina (Control sample), and by replacing semolina with 14%
tein (CP; method no. 2001.11), crude fibre (method no. 978.10), and ash of insect powdered proteins to reach the claim "high protein" pasta,
(method no. 967.05) contents. The ether extract was determined after according to the Regulation (EC) No 1924/2006, at least 20% of the
acid hydrolysis (European Community, 1998 19). energy value of the food must be provided by protein. Total semolina
2
G. Pasini et al. LWT 164 (2022) 113638
and the blend semolina/insect powdered proteins were added with 35% (Acheta domesticus) were defatted. After defatting, the insects powder
tap water at 40 ◦ C, kneaded for 10 min and extruded into a “tagliatelle” contained high amount of protein (64.9 and 57.9% DM for AD and TM,
shape, 5.0 cm long and 3 mm thick. Finally, the freshly extruded pasta respectively) with a residual amount of lipids (6.7 and 10.9% DM,
samples were air-dried at 50 ◦ C in a Jouan® dryer (Thermo Fisher Sci respectively; Table 1). The hexane defatting allowed to increase the
entific, Waltham, Massachusetts, USA) for about 12 h to reach a final protein yield of about 8% in both samples compared to the initial values
moisture content of 12.5% (w/w), as required by Italian law (DPM which is a result that could be further improved optimizing the defatting
February 9, 2001, n.187). For each sample, n = 3 pasta batches were process. In fact, another study considering ethanol-defatted mealworms
obtained 1) CP: wheat control pasta, 2) AD: pasta formulated with adult achieved an efficiency of about 30% (Zhao, Vázquez-Gutiérrez,
house cricket (Acheta domesticus) protein extract, and 3) TM: pasta Johansson, Landberg, & Langton, 2016).
formulated with yellow mealworm (Tenebrio molitor) larvae protein
extract. 3.2. Protein-enriched fraction, electrophoretic profile and amino acid
composition
2.6. Standard parameters of pasta quality
The yield and extraction efficiency of PBS-soluble proteins from
Colour. The colour of the raw pasta was analysed according to the defatted insect powders are shown in Table 2. The extraction yield of AD
CIELAB system (CIE, 1976) using a CR-300 colorimeter (Konica Minolta, was 1.5-fold higher than that of TM (64.3% vs 41.2%). The proteins were
Tokyo, Japan), taking L* value (lightness), a* value (redness), and b* simply extracted in PBS buffer and the difference between samples was
value (yellowness) at three different points on the sample surface. Each probably due to the different protein solubility caused by heat treatment
colour value represents the mean of five different measurements. during the insect drying process, and/or interaction between protein
Moreover, to assess colour changes in AD and TM samples compared to and residual fat, as the latter was greater in TM than in AD. Despite the
the control sample (CP), the following equation was applied: hexane is reported to be the best solvent (L’hocine, Boye, & Arcand,
√̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅ 2006), given the high fat content in edible insects, the defatting step can
ΔE = (ΔL*)2 + (Δa*)2 + (Δb*)2 be difficult and incomplete. Moreover, extraction yields obtained from
aqueous, or salt extraction are usually lower than those obtained by
where: ΔE = Total colour difference. alkaline solubilisation (Gravel & Doyen, 2020). In any case, our results
revealed an extraction efficiency higher than that obtained by Chatsu
ΔL* = L* control− L* treatment wan, Nalinanon, Puechkamut, Lamsal, and Pinsirodom (2018) in protein
Δa* = a* control− a* treatment isolates of two types of grasshoppers. In addition, although the extrac
Δb* = b* control− b* treatment tion yield was not greater, the extraction efficiency was high (75.2% and
88.7% in AD and TM, respectively) and similar to that obtained by
Pasta cooking quality. Ten grams of pasta were cooked in 100 mL Azagoh et al. (2016). Despite it is difficult to compare samples analysed
boiling water. The pasta optimum cooking time (OCT), and cooking loss in different studies, these results show that salt-water solubilisation can
(CL) were determined accordingly the AACC - American Association of be used for proteins separation.
Cereal Chemists (2000) methods 44-15A and 66–50, respectively. Water The electrophoretic profiles and molecular weight distribution of
absorption index was expressed as % increase of pasta weight after insect protein fractions from insect samples are shown in Fig. 1. The gels
cooking. revealed different proteins mobility, in any case, less than 75 kDa for all
Texture Analyses. Firmness and adhesiveness in cooked pasta, after samples. Based on the intensity, bands ≤20 kDa were abundant for TM
removing water excess, were analysed using a TA.XTplus Texture Ana sample. In particular, bands ranging from 12 to 15 kDa are strongly
lyser (Stable Micro System, Ltd., Godalming, UK) equipped with a 50 kg visible and also reported by other authors (Azagoh et al., 2016; Janssen,
load cell. Five pasta stripes of 5 cm length were positioned parallel next Vincken, Arts, Fogliano, & Lakemond, 2019; Yi et al., 2013) which could
to each other on the texture analyser platform. A rectangular probe (35 correspond to haemolymph proteins at ~ 12 kDa (Yi et al., 2013), and
mm × 50 mm) was used. The test parameters were: pre-test speed (2 cockroach allergen-like protein ~15 kDa (Nebbia et al., 2019). Next,
mm/s), test speed (1 mm/s), post-test speed (3 mm/s), percentage bands ranging from 15 to 30 kDa, also reported by Yi et al. (2013), were
deformation (90%). Firmness was calculated as the maximum force peak hypothesized to be larval cuticle proteins that make up the exoskeleton
required to compress the pasta sample. Stickiness was calculated as the of insects (Andersen, Hojrup, & Roepstorff, 1995), e.g.
maximum peak force to separate the probe from the sample’s surface. chymotrypsin-like protein (24 kDa) (Elpidina et al., 2005). Other bands
The results were reported as the mean value of 6 replicates. observed at around 60 kDa could belong to β-glycosidase (59 kDa),
trypsin-like proteinases (59 kDa), and melanisation-engaging types of
2.7. Statistical analysis protein (65 kDa) (Yi et al., 2013). These bands found in TM sample were
also prevalent in the AD sample. Similar findings were noted by Bubler
One-way analysis of variance (ANOVA) was carried out indepen et al. (2016) and Brogan (2018).
dently for each dependent variable. A post-hoc Tukey’s HSD multiple
comparison test was used to identify statistically homogeneous subsets
α = 0.05. Statistical analysis was performed with CoStat Software 6.45
(Minitab Inc., State College, Pennsylvania, USA).
3
G. Pasini et al. LWT 164 (2022) 113638
Table 2 Table 3
Yield and extraction efficiency of PBS-soluble proteins from defatted adult Amino acid composition (mg/100 g sample) of PBS-soluble proteins from
Acheta domesticus (AD) and Tenebrio molitor (TM) larvae (mean ± S.D.). defatted adult Acheta domesticus (AD) and Tenebrio molitor (TM) larvae (mean ±
Insect species AD TM
S.D.).
Insect species AD TM
Extraction yield, % 64.3 ± 5.4 41.2 ± 4.7
Total protein in PBS powder extract, % 48.8 ± 1.7 51.4 ± 1.9 Essential amino acids:
Extraction efficiency, % 75.2 ± 5.2 88.7 ± 5.9 Histidine 606 ± 41.1 258 ± 13.9
Isoleucine 2290 ± 155 977 ± 44.8
Leucine 1079 ± 75.4 490 ± 63.3
Lysine 4040 ± 297 6963 ± 221
Methionine 511 ± 38.8 181 ± 19.4
Phenylalanine 1038 ± 65.5 439 ± 34.2
Threonine 924 ± 83.0 683 ± 84.5
Valine 1793 ± 122 1157 ± 84.8
Tryptophan 97.8 ± 8.22 54.5 ± 9.50
Conditionally essential:
Arginine 1248 ± 98.6 524 ± 34.7
Cysteine 245 ± 33.6 252 ± 15.8
Glycine 2109 ± 123 967 ± 73.5
Proline 2131 ± 120 787 ± 57.1
Tyrosine 987 ± 87.4 849 ± 80.2
Nonessential amino acids:
Alanine 4035 ± 198 3797 ± 139
Aspartic acid 2867 ± 281 2621 ± 102
Glutamic acid 8020 ± 579 11908 ± 673
Serine 1275 ± 106 746 ± 97.5
4
G. Pasini et al. LWT 164 (2022) 113638
Fig. 2. From left to right: visual appearance of the control pasta (CP), pasta with Acheta domesticus (AD), and pasta with Tenebrio molitor (TM) protein extracts.
5
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