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Nutritional composition of five commercial edible insects in South Korea

Article  in  Journal of Asia-Pacific Entomology · April 2017


DOI: 10.1016/j.aspen.2017.04.003

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Journal of Asia-Pacific Entomology 20 (2017) 686–694

Contents lists available at ScienceDirect

Journal of Asia-Pacific Entomology


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

Nutritional composition of five commercial edible insects in South Korea MARK


a b b,⁎ c,d
Sampat Ghosh , So-Min Lee , Chuleui Jung , V.B. Meyer-Rochow
a
Agriculture Science and Technology Research Institute, Andong National University, 760-749, Republic of Korea
b
Department of Plant medicine, Andong National University, 760-749, Republic of Korea
c
Research Institute of Luminous organisms, Hachijo-jima, Tokyo 100-1623, Japan
d
Department of Genetics and Physiology, Oulu University, 90140, Finland

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

Keywords: The nutritional potential of five preferred insect species used as food and feed in Korea, Allomyrina dichotoma
Sustainability (Coleoptera: Dynastidae), Protaetia brevitarsis (Coleoptera: Cetoniidae), Tenebrio molitor (Coleoptera:
Climate change Tenebrionidae), Teleogryllus emma (Orthoptera: Gryllidae), and Gryllus bimaculatus (Ortoptera: Gryllidae), was
Micro-livestock accessed. Most of these species contained high protein contents with low variation (53.2 to 58.3%) except for P.
Amino acid
brevitarsis, whose protein tally amounted to 44.2%. Fat contents of the insects varied widely (11.9 to 34.5%). G.
Animal oil
bimaculatus was found to contain the least amount of fat, but highest amount of protein including essential amino
acids. T. molitor contained the highest amount of fat (34.5%), suggesting a possible future role as a commercial
source of oil. A total of 17 amino acids (8 essential, 1 conditional essential and 8 non-essential) as well as 26 fatty
acids (12 SFA, 6 MUFA and 8 PUFA) were determined. Except for methionine all other essential amino acids
satisfied the protein level recommended by FAO/WHO/UNU (2007). The MUFA proportion was highest in the
beetle larvae, but PUFA contents were maximal in the cricket adults. Compared with conventional animal meats
and chicken eggs, especially the crickets that we examined seem superior from a nutritional perspective as they
contain higher amounts of protein, iron, zinc and magnesium and possess fats with fewer SFAs but more PUFAs
(with the exception of A. dichotoma). Systematic farming of these insects could be one sustainable alternative to
vertebrate animal food with less environmental pressures.

Introduction with the increasing scientific encouragement that insects receive as a


promising aid to achieve sustainable levels of nutrition, the regulatory
Worldwide the number of edible insects species is considered to be institutions of many countries are in the process of framing legislative
about 2000 (Jongema, 2015) and the number of people regarding structures related to the use of insects for human consumption
insects as food is at least 2 billion, i.e., approximately 30% of the global (Halloran, 2014). As a consequence, existing insect-based bio-industries
population (VanHuis et al., 2013). Despite an early interest in insects as have been augmented with edible insect segments although the process
food (Holt, 1885; Bequaert, 1921; Bergier, 1941; Bodenheimer, 1951) it is in its infancy and scope exists to improve the situation.
was not until 1975 when it was suggested that insects could have a role In the context of Korea the use of arthropods including insects in the
to play in safeguarding global future food security (Meyer-Rochow, traditional Korean medicine is an age old practice (Okamoto and
1975). Interest in insects as a food source has risen since then and has Muramatsu, 1922; Meyer-Rochow, 2013) and certain species like
received attention primarily in connection with the two issues (a) of silkworms (Bombyx mori) and grasshoppers (Oxyoa sinuosa and Acrida
having a sustainable food source for future food demands (VanHuis lata: Nonaka, 1991; Pemberton, 1999) have been accepted as part of the
et al., 2013) and (b) of tackling undernutrition particularly in the regular food system. Prompted by new Korean legislation regarding
developing world (Nadeau et al., 2014). insect industries in 2010, edible insect farming on a commercial scale
A number of initiatives have been taken by a variety of organiza- has become a new challenge. Anticipating the appreciable growth rate
tions foremost and for all the FAO in promoting scientific facts about of an insect based industry in the near future the Ministry of
the utilization of insects as food and feed. However, unclear regulation Agriculture, Food and Rural Affairs of the Republic of Korea aims to
and legislation toward farming and selling insects for human consump- increase the nation's insect market from 265 million USD in 2015 to 436
tion and animal feed are obstacles that still need to be overcome. Thus million USD in 2020 (MAFRA, 2016).


Corresponding author.
E-mail address: cjung@andong.ac.kr (C. Jung).

http://dx.doi.org/10.1016/j.aspen.2017.04.003
Received 13 February 2017; Received in revised form 11 April 2017; Accepted 13 April 2017
Available online 13 April 2017
1226-8615/ © 2017 Published by Elsevier B.V. on behalf of Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society.
S. Ghosh et al. Journal of Asia-Pacific Entomology 20 (2017) 686–694

Table 1
Inventory of preferred insects used as food and feed in Korea.

Scientific names Korean name Taxonomic position Life cycle (in days) Life stage of Primary Feed Retail price (Won
commercial interest purpose per 100 g Dry
Order Family Immature Adult weight)

Allomyrina Jang su pung Coleoptera Dynastidae 38a 20b 75 Larvae Medicinal Fermented saw dust 80,000
dichotoma dengi
a b
Protaetia brevitarsis Huin jeom Coleoptera Cetoniidae 55 30 45 Larvae Medicinal Fermented saw dust 80,000
baki kkot muji
a b
Tenebrio molitor Gal saek geo Coleoptera Tenebrionidae 210 7 120 Larvae Food Wheat bran and 8000
jeo ri Chinese cabbage
Teleogryllus emma Wang gwi ttu Orthoptera Gryllidae 77c 56 Late nymph Feed Wheat bran and 40,000
ra mi anchovies
Gryllus bimaculatus SSang byeol Orthoptera Gryllidae 45c 20 Late nymph Feed Wheat bran and 26,000
gwi ttu ra mi anchovies

a
Larvae.
b
Pupae.
c
Nymph.

From the commercial point of view, five insect species (Table 1), i.e. anchovies resemble those used in Thailand (Hanboonsong et al., 2013).
3 beetles of Allomyrina dichotoma (Coleoptera: Dynastidae), Protaetia The samples were brought to the laboratory, degutted, then freeze-
brevitarsis (Coleoptera: Cetoniidae), Tenebrio molitor (Coleoptera: Te- dried, ground to a powder and prepared as dry matter (DM) for further
nebrionidae), and 2 crickets of Teleogryllus emma (Orthoptera: Grylli- analysis. All the solvents and chemicals used in the study were of
dae) and Gryllus bimaculatus (Ortoptera: Gryllidae) are given priority in analytical grade.
Korea (Kim and Jung, 2013). Larvae of the beetles are generally used in
traditional medicines and as food, while adult crickets find mainly use
as animal feed (Sah and Jung, 2012; Park and Jung, 2013). One of the Proximate analyses
challenges besides developing specific rearing technologies and diets is
the need to maintain the quality of the products in terms of the Proximate compositions, i.e. crude protein, crude fat, crude fibre,
nutrition, hygiene and sanitation. ash and nitrogen free extract (NFE) were estimated following standard
The nutritional values of insects vary even within species depending methods recommended by the Association of Official Analytical
on season, life stages, diet and on how the insects are prepared prior to Chemists (AOAC, 1990). Moisture percentage was calculated by drying
consumption (Ramos-Elorduy et al., 2002; Yhoung-Aree, 2010; Jensen the sample in an oven at 100 °C for 2 h. The dried sample was put into a
et al., 2011; Ghosh et al., 2016). Thus, to the industry it must be of the desiccator, allowed to cool and the reweighed. The process was
utmost importance to follow an established rearing protocol to main- repeated until constant weight was obtained. Crude protein was
tain nutritional contents constant in different batches of production. determined by the Kjeldahl method and total protein content was
Until now insect farming systems in the country are restricted to small calculated as the amount of total N determined multiplied by nitrogen-
sized entrepreneurships and there are no reports containing life cycle to-protein conversion factor of 6.25. Fat percentage was calculated by
analyses conducted with different combinations of inputs for farming in drying fats after extraction in a Soxhlet using Diethyl ether. Ash
mind. To maintain quality consistency and help understand the percentage was calculated by combusting the samples in silica crucible
potential of insects as food, it seems important and timely to put on placed in a muffle furnace. The percentage of carbohydrate was
record information on the nutritional contents of prospective commer- determined by subtracting all of the components (crude protein, crude
cial insect species. The present study has been carried out to examine lipid and ash) from 100. All of the analyses were performed in triplicate
the selected insects species under current rearing practice could provide and expressed as mean ± standard deviation. Differences were tested
nutrients i.e., protein, amino acids, fat and minerals for human with one-way analysis of variance (ANOVA) followed by Tukey test
nutrition satisfactorily. using SAS 9.4.

Materials and methods Amino acid analysis

Insect rearing, sample collection and preparation Amino acid composition was determined by Sykam Amino Acid
analyzer S433 (Sykam GmbH, Germany) following the standard method
Specimens of the last instar larvae of 3 beetle species Allomyrina of AOAC (1990). The ground samples were hydrolyzed in 6 N HCl for
dichotoma (Coleoptera: Dynastidae), Protaetia brevitarsis (Coleoptera: 24 h at 110 °C under nitrogen atmosphere and then concentrated with
Cetoniidae), Tenebrio molitor (Coleoptera: Tenebrionidae) and mixtures rota-evaporator. The concentrated samples were reconstituted with
of late nymphs and adults of the cricket species Teleogryllus emma sample dilution buffer supplied by the manufacturer (0.12 N, pH 2.20).
(Orthoptera: Gryllidae) and Gryllus bimaculatus were obtained from The hydrolyzed samples were analyzed for amino acid composition.
commercial insect farms in Korea during May 2016. Mealworms are The operating condition of the amino acid analyzer was as the
grown in well ventilated wooden containers, generally 20–25 cm deep following:
with large surface area and smooth sides to prevent the insects from Instrument: Amino acid analyzer (Sykam GmbH, Germany)
escaping. Mealworms are usually raised on wheat bran with few leaves Column: LCA K07/Li (PEEK – column 4.6 × 150 mm)
of Chinese cabbage as a source for water uptake and being nocturnal are Application: Physiological
kept in a dark environment. Grubs of the beetles A. dichotoma and P. Detector: Photometer (570 nm, 440 nm)
brevitarsis are grown in cemented tanks or spacious plastic containers. Detection principle: Ninhydrin reaction
The insects are generally raised on fermented saw dust. Cricket farming Inert gas: N2
in Korea is a comparatively new activity (Jang and Jung, 2013) and The amino acid score was calculated based on FAO/WHO/UNU
farming methods with crickets being raised on wheat bran and dried (2007).

687
S. Ghosh et al. Journal of Asia-Pacific Entomology 20 (2017) 686–694

Fatty acid analysis relationship between the insects' protein pattern and the ideal protein
pattern recommended by FAO/WHO/UNU (2007) joint consultation.
Fatty acid composition was analyzed by gas chromatography flame Fatty acid compositions characterize the fat quality. In total 26 fatty
ionization detection (GC-14B, Shimadzu, Tokyo, Japan), following the acids belonging to three different categories, i.e., saturated, mono-
standard method of the Korean Food Standard Codex (2010). The unsaturated and poly-unsaturated were identified (Table 4). As an
samples were derivatised into fatty methyl esters (FAMEs) following the overall trend the proportion of mono-unsaturated fatty acids (MUFAs)
method described by of Lepage and Roy (1986). Identification and was highest in the beetle larvae whereas poly-unsaturated fatty acids
quantification of FAMEs were accomplished by comparing the retention (PUFAs) were more common in the crickets. In case of beetle larvae
times of peaks with those of pure standards purchased from Sigma and oleic acid predominated with varied proportion (46.6 to 60.8%)
analyzed under the same conditions. The results were expressed as a whereas linoleic acid (an essential fatty acid) was found predominant
percentage of individual fatty acids in the lipid fraction. The operating in crickets' oil. Palmitic acid was the second most abundant fatty acid
condition of GC for fatty acid analysis was as the following: followed by palmitoleic acid in the fat fractions of A. dichotoma and P.
Instrument: Gas Chromatography (GC-14B, Shimazdu) brevitarsis larvae, whereas linoleic acid was the second most common
Column: SP-2560 followed by palmitic acid in T. molitor larvae and crickets. The n-6
Detector: Flame Ionization detector (FID) PUFA was significantly more abundant than the n-3 PUFA. Compared
with those known from animal meats and chicken eggs the PUFA
Minerals analyses proportions of the crickets in the present study were significantly higher
and, except for A. dichotoma larvae, the SFA proportions of all other
Minerals were analyzed following the standard method of the tested insects were found to be smaller (Fig. 4).
Korean Food Standard Codex (2010). The dried powder samples were Among 5 macro and 4 micro minerals, phosphorus was most
digested with nitric and hydrochloric acid (1:3) at 200 °C for 30 min. abundant except for A. dichotoma and P. brevitarsis larvae, in which
Each sample was filtered using Whatman filter paper (0.45 μm) and potassium was dominant (Table 5). All the beetle larvae were found to
stored in washed glass vials before analysis. Minerals were analyzed by have high K/Na ratio (P. brevitarsis larvae = 9.5; A. dichotoma lar-
inductively-coupled plasma-optical emission spectrophotometer (ICP- vae = 8.4; T. molitor larvae = 6.8). One of the important micronutri-
OES 720 series Agilent). ents, iron content was found to be highest in P. brevitarsis followed by A.
dichotoma larvae. In Fig. 5 mineral contents between insect and
Results conventional foods of animal origin are compared. Iron and zinc
contents of our insects were higher than what had been reported for
Proximate nutritional composition of five insect studied is repre- conventional animal meats and chicken eggs.
sented in Table 2. Most species contained high amount of protein with
low variation (54–58%), but P. brevitarsis contained the least (44.2%). Discussion
The fat contents were highly variable (11.9 to 34.5%) with T. molitor
possessing the highest amount (34.5%). Unlike conventional animal Insects as an alternative source of food
meats, insects contained higher fibre material ranging from 4 to 11%.
Significant differences have been found in the nutrients composition According to the current report on the state of food (in)security of
among 5 studied insects. G. bimaculatus was found to contain the the world, the number of undernourished people, defined as unable to
highest amount of protein and the least amount of fat of the five species. acquire enough food to meet the daily minimum dietary energy
The ash contents of the crickets were higher than those of the beetle requirements over a period of one year, has arrived at 793 million
larvae. Fig. 1 represents comparisons of protein and fat content (FAO, 2015). Africa continues to lag behind the global and regional
between the different insect species and conventional food sources of declining trend of undernutrition. The number of under or malnour-
animal origin, allowing us to appreciate the nutritional profile of insects ished people has increased to 217.8 million in 2014–16 from 175.7
as possible contributors to a wholesome diet for humans. Protein million in 1990–92. The major cause of this is diet deficient in
contents of the insects were found to be much higher than those macronutrients (protein, carbohydrate and fat) leading to protein-
reported for beef and pork, the two most accepted animal meats around energy malnutrition (PEM) and in micronutrients (electrolytes, miner-
the world. However, the reverse held true for fat. als, vitamins) leading to specific micronutrient deficiencies (Table 5).
Amino acid compositions, characterizing protein quality of the The overall nutrient profiles of the studied insect species surpass
studied insect are represented in Table 3. Glutamic acid, non-essential those of conventional livestock in that they contain comparable, if not
amino acid, predominated among the 17 amino acids identified in the higher protein but lower fat content (Fig. 1). The world population is
insects, including 8 essential and one conditionally essential acid. anticipated to reach 9 billion by 2050 and the challenge to feed the
Among the essential amino acids, leucine was dominating followed increasing population is huge, given the limited agricultural resources
by valine in all the insects studied with the exception of P. brevitarsis in of land and water in climate-change era (FAO, 2009). Thus, safe-
which the reverse was true. Comparisons in relation to individual guarding sustainability has become the most pertinent challenge of
amino acid contents between the examined insects and conventional today. In this context, insect must be viewed as an alternative source of
foods of animal origin are shown in Fig. 2 (a–g). Fig. 3 represents the animal protein in terms of micro-livestock.

Table 2
Proximate nutrients compositions (% DM) of selected insects used as food and feed in Korea.

Components Allomyrina dichotoma Protaetia brevitarsis Tenebrio molitor Teleogryllus emma Gryllus bimaculatus Pr > F
larvae larvae larvae adult adult

Protein⁎ 54.18 ± 1.50 44.23 ± 0.25 53.22 ± 0.32 55.65 ± 0.28 58.32 ± 0.33 < 0.0001
Fat 20.24 ± 0.25 15.36 ± 0.40 34.54 ± 0.87 25.14 ± 0.11 11.88 ± 0.21 < 0.0001
Fibre 4.03 ± 0.30 11.06 ± 0.35 6.26 ± 0.03 10.37 ± 0.19 9.53 ± 0.46 < 0.0001
Ash 3.88 ± 0.19 6.90 ± 0.07 4.04 ± 0.13 8.17 ± 0.03 9.69 ± 0.06 < 0.0001
Nitrogen free extract (NFE) 17.67 ± 1.25 22.45 ± 0.27 1.94 ± 1.08 0.67 ± 0.33 10.59 ± 0.35 < 0.0001


All tests of ANOVA with dF 4,10.

688
S. Ghosh et al. Journal of Asia-Pacific Entomology 20 (2017) 686–694

Fig. 1. Comparison of protein and fat content (% dry matter, DM basis) of studied insects with conventional food sources of animal origin (data other than insects were obtained from
USDA database (2015) and calculated on the basis of dry weight).

Nutritional potential of insects 1984).


Protein levels of the studied edible insects satisfied the level of all
Protein the recommended essential amino acids by FAO/WHO/UNU (2007)
The protein content of our beetle larvae was higher than that (Fig. 3). The quality of the protein as related to human nutrition largely
available in published reports on several other beetle larvae like those depends on the amino acid composition. Essential amino acid contents
of passalid beetles of Oileus rimator, Passalus punctiger, longhorn beetle of insects were comparable to resource-intensive animal protein sources
of Aplagiognathus spinosus, or scarabeid beetle of Phyllophaga sp. (Finke, (Fig. 2 a–g). An effective utilization of dietary proteins requires an
2004; deConconi et al., 1984), Palm weevils of Rhynchophorus palmar- appropriate balance between essential and non-essential amino acid
um or R. phoenicis, Rhino beetle of Oryctes boas, and longhorn beetle of and other nitrogen containing compounds. Of the non-essential amino
Analeptes trifasciata (Cerda et al., 2001; Banjo et al., 2006; Ekpo and acids glutamic acid, in agreement with other scientific reports, was
Onigbinde, 2005), but lower than that of cactus weevil, Metamasius found to be dominating (Rumpold and Schluter, 2013; Chakravorty
spinolae (deConconi et al., 1984). The protein content (53.2%) of our T. et al., 2016; Ghosh et al., 2016). Most attention has been given to the
molitor larvae was somewhat higher than that reported for the same essential amino acid lysine as it has been found to be limited in the
species by Finke (2004) (49.1%) and Ravzanaadi et al. (2012) (46.4%). staple cereals like rice, wheat, cassava and maize (Macrae et al., 1993).
The protein content of our crickets was slightly lower than that reported The lysine content of P. brevitarsis and G.bimaculatus was marginal, but
for other orthopteran species like Chondacris rosea and Brachytrupes arginine was found in moderate amounts in all of the insects analyzed.
orientalis (Chakravorty et al., 2014), Sphenarium, Romalea, Trimerotro- Arginine is an essential amino acid especially for children as it is
pis, Acheta spp. and a few others (Blásquez et al., 2012), but it was required for growth but they cannot synthesize it.
comparable to Plectrottetra nobilis, and Melanoplus sp. (deConconi et al.,

Table 3
Amino acid composition (g/100 g dries materials) of selected insects used as food and feed in Korea.

Amino acid Allomyrina dichotoma Protaetia brevitarsis Tenebrio molitor Teleogryllus emma Gryllus bimaculatus
larvae larvae larvae adult adult

Valinea 2.72 ± 0.007 2.49 ± 0.014 2.94 ± 0.003 2.92 ± 0.035 3.20 ± 0.028
Isoleucinea 2.12 ± 0.000 1.62 ± 0.007 1.98 ± 0.000 2.15 ± 0.057 2.16 ± 0.035
Leucinea 3.12 ± 0.000 2.31 ± 0.035 3.37 ± 0.007 3.96 ± 0.134 3.97 ± 0.049
Lysinea 2.42 ± 0.014 1.75 ± 0.014 2.01 ± 0.014 2.61 ± 0.021 2.42 ± 0.007
Threoninea 1.87 ± 0.021 1.55 ± 0.007 1.83 ± 0.000 1.92 ± 0.035 2.00 ± 0.035
Phenylalaninea 1.75 ± 0.007 1.62 ± 0.007 1.76 ± 0.021 1.79 ± 0.049 1.83 ± 0.014
Methioninea ND 0.31 ± 0.007 ND ND 0.27 ± 0.007
Histidinea 2.35 ± 0.007 1.82 ± 0.057 2.80 ± 0.014 2.41 ± 0.014 2.50 ± 0.078
Tyrosineb 3.77 ± 0.014 3.30 ± 0.035 3.45 ± 0.005 2.61 ± 0.049 2.73 ± 0.021
Arginine 2.58 ± 0.042 2.09 ± 0.042 2.23 ± 0.000 3.71 ± 0.643 3.60 ± 0.035
Aspartic acid 2.66 ± 0.035 2.26 ± 0.021 2.76 ± 0.070 3.85 ± 0.085 3.60 ± 0.035
Glutamic acid 8.69 ± 0.049 5.54 ± 0.134 5.78 ± 0.028 6.51 ± 0.085 6.39 ± 0.071
Serine 2.90 ± 0.042 2.55 ± 0.035 2.20 ± 0.065 2.95 ± 0.078 2.73 ± 0.007
Glycine 2.78 ± 0.042 2.24 ± 0.417 2.61 ± 0.120 2.54 ± 0.064 3.32 ± 0.007
Alanine 2.20 ± 0.021 2.44 ± 0.035 3.96 ± 0.007 4.59 ± 0.071 5.64 ± 0.014
Cystine 4.35 ± 0.170 2.63 ± 0.035 3.16 ± 0.000 3.81 ± 0.078 5.10 ± 0.000
Proline 2.46 ± 0.057 2.63 ± 0.064 1.66 ± 0.007 1.62 ± 0.007 1.99 ± 0.014
EAA 20.12 16.78 20.14 20.37 21.08
NEAA 28.62 22.38 24.36 29.58 32.75
Total 48.74 39.16 44.50 49.95 53.83

a
Indicates essential amino acids for adult human.
b
Indicate conditional essential amino acid for adult human.

689
S. Ghosh et al. Journal of Asia-Pacific Entomology 20 (2017) 686–694

Fig. 2. Comparison of selected essential amino acids distribution in the protein fraction (% of total amino acids) of studied insects with conventional foods of animal origin (data other
than insects were obtained from USDA database (2015).) (a–g.)

Fat shown to decrease plasma cholesterol concentrations. Both species of


The amounts of fat in the beetle larvae were found to be higher than crickets contained higher amounts of PUFA than MUFA, which agrees
the reported from diverse scarab beetles; Onthophagus seniculus (14%), with the fatty acid composition of Chondacris rosea (Acrididae), but not
O. mouhoti (12.1%), Onitis sp. (16.6%), Copris nevinsoni (12.7%), with another cricket Brachytrupes orientalis (Gryllidae) (Chakravorty
Liatongus rhadamitus (12.2%), Helicopris bucephalus (13.5%) (Bophimai et al., 2014). On the other hand, in case of the beetles, MUFAs were
and Siri, 2010). Fat content of T. molitor larvae (34.5%) was almost in most abundant and this finding is in full agreement with the report by
agreement with the value 32.7% which was reported by Ravzanaadii Bophimai and Siri (2010). However, the feeding guild, not taxonomic
et al. (2012) for the same species. The fat content of both cricket species proximity, often determines body composition (Fontaneto et al., 2011).
was within the range reported for orthopteran species (Blásquez et al., PUFA/SFA ratios of grain-fed (wheat bran based diet) T. molitor
2012).The assessment of the quality of the fat is a complex issue. SFAs larvae = 1.12; T. emma = 2.81 and G. bimaculatus = 1.33 were higher
are a dietary factor having their greatest negative effect on LDL than the recommended value of 0.4 (FAO/WHO, 2003), but this did not
cholesterol. In contrast MUFA and PUFA of the n-6 family have been apply to the xylophagous grubs of P. brevitarsis (0.44) or A. dichotoma

690
S. Ghosh et al. Journal of Asia-Pacific Entomology 20 (2017) 686–694

Fig. 3. Comparison of selected essential amino acids distribution in the protein fraction (% of total amino acids) of studied insects with recommended protein pattern (individual amino
acid in g/100 g protein i.e. %) based on FAO/WHO/UNU (2007) consultation [⁎indicates essential amino acid and ⁎⁎indicates conditional essential amino acid].

Table 4
Fatty acid composition (g/100 g DM) of selected insects used as food and feed in Korea.

Fatty acid Allomyrina dichotoma Protaetia brevitarsis Tenebrio molitor Teleogryllus emma adult Gryllus bimaculatus adult
larvae larvae larvae

C12:0 Lauric acid 0.02 0 0.11 0.02 0.04


C13:0 Tridecanoic acid 0 0 0.15 0 0
C14:0 Myristic acid 0.12 0.07 1.63 0.18 0.05
C15:0 Pentadecanoic acid 0.01 0.02 0.02 0.02 0.01
C16:0 Palmitic acid 6.42 1.81 4.71 3.06 2.16
C17:0 Heptadecanoic acid 0.01 0.02 0.02 0.04 0.03
C18:0 Stearic acid 0.28 0.30 0.08 0.07 0.76
C20:0 Arachidic acid 0.03 0.09 0.04 0.09 0.12
C21:0 Heneicosanoic acid 0.01 0 0.01 0.04 0.04
C22:0 Behenic acid 0.01 0.01 0.01 0.01 0.03
C23:0 Tricosanoic acid 0.02 0.03 0.15 0.07 0
C24:0 Lignoceric acid 0 0.01 0.01 0.01 0.01
C14:1 Myristoleic acid 0 0.03 0.07 0.02 0
C16:1 Palmitoleic acid 1.32 1.61 0.89 0.91 0.17
C17:1 cis-10-Heptadecenoic acid 0.01 0.004 0.03 0.03 0.01
C18:1n-9, cis Oleic acid 7.94 7.85 15.56 6.98 2.91
C20:1 cis-11-Eicosenoic acid 0.02 0.02 0.02 0.04 0.03
C22:1n-9 Erucic acid 0.01 0.01 0.01 0.04 0.01
C18:2n-6, cis Linoleic acid 0.69 0.91 7.57 9.61 4.15
C20:2 cis-11,14-Eicosadienoic acid 0 0 0.04 0.02 0.04
C22:2 cis-13,16-Docosadienoic acid 0 0.01 0.04 0.01 0.02
C18:3n-6g-Linolenic acid 0.01 0.01 0.01 0 0.01
C18:3n-3Linolenic acid 0.01 0.04 0.11 0.22 0.08
C20:3n-6 cis-8,11,14,17-Eicosatrienoic acid 0.01 0 0.01 0.01 0.02
C20:4n-6 Arachidonic acid 0.08 0.07 0 0.27 0.01
C20:5n-3 cis-5,8,11,14,17-Eicosapentaenoic 0.01 0 0 0.01 0
acid
SFA 6.93 2.36 6.94 3.61 3.25
MUFA 9.30 9.52 16.58 8.02 3.13
PUFA 0.81 1.04 7.78 10.15 4.33
Total 17.04 12.92 31.30 21.78 10.71
n-3 0.02 0.04 0.11 0.23 0.08
n-6 0.79 1.00 7.67 9.92 4.25

(0.12). PUFAs of the n-3 family have multiple beneficial effects these insects into functional food (Aluko, 2012). Compared with
reducing the risk of coronary heart disease (CHD), primarily modulat- conventional foods of animal origin the insect fat was clearly superior
ing the VLDL metabolism and reducing plasma triglycerides (TGs) (Fig. 4). Although scope exists to improve or manipulate the higher
(Nordøv et al., 2001; Demaison and Moreau, 2002). The share of the n- palmitic acid (a SFA) content of A. dichotoma larvae and the smaller
6 family was much higher than the n-3 in the PUFA fractions of all of amount of linoleic acid (a PUFA) in A. dichotoma and P. brevitarsis.
the studied insects, which could be fortified with n-3 PUFAs to turn Although insects are being seen mostly as a source of protein, many

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S. Ghosh et al. Journal of Asia-Pacific Entomology 20 (2017) 686–694

Fig. 4. Comparison of different fatty acids categories of selected insects with conventional food of animal origin (data other than insects were obtained from USDA database (2015).)

Table 5 and several other chronic diseases including hypertension and colon
Mineral content (mg/100 g of dried material) of selected insects used as food and feed in cancer (NAMS, 2001). The high K/Na ratio (P. brevitarsis larvae = 9.5;
Korea. A. dichotoma larvae = 8.4; T. molitor larvae = 6.8) makes these beetle
Minerals Allomyrina Protaetia Tenebrio Teleogryllus Gryllus
larvae potentially valuable in comparison with conventional animal
dichotoma brevitarsis molitor emma bimaculatus meats (Pork = 6; beef = 4.5; veal = 3.8 and chicken = 2.7). Low
larvae larvae larvae adult adult potassium levels in humans have been linked to a variety of physiolo-
gical disorders including respiratory and renal ones and hypertension
Calcium 123.40 258.56 78.42 193.54 240.17
Magnesium 283.56 327.60 315.23 152.48 143.65
(Cohn et al., 2000). Magnesium is required for various enzymatic
Potassium 1249.1 2001.4 737.00 895.50 1079.9 reactions in the body. Unlike plant-based phosphorus, the phosphorus
Sodium 148.38 211.60 108.82 278.23 452.99 in insects is readily available (Capinera, 2008).
Phosphorus 860.69 1140.4 1039.2 1085.4 1169.6 Iron deficiency is of widespread concern in developing countries
Iron 14.26 16.20 10.02 10.75 9.66
and infants in the weaning stage, young children, women of child
Zinc 10.26 11.89 11.74 18.47 22.43
Copper 1.43 1.82 2.00 2.19 4.55 bearing age and sickly adults often receive insufficient amounts of iron
Manganese 8.64 5.89 1.50 5.86 10.36 from their diet. Zinc is an important micro mineral and component of a
large number (> 300) of enzymes. It is an essential participant in the
metabolism of carbohydrates, proteins, fats and nucleic acids and
species are rich in valuable oils that can be used directly or indirectly in furthermore it has a crucial role to play in polynucleotide transcription
improving texture, flavour and digestibility of a food. Low amounts of and thus in the process of genetic expression. Copper plays an
PUFAs such as linoleic and linolenic acid in the A. dichotoma and P. important role in cellular respiration, peptide amidation, neurotrans-
brevitarsis larval oil can provide high oxidative stability to food mitter biosynthesis, pigment formation and connective tissue strength,
(Mariod, 2013). Blending with conventional oil sources these insects but it is toxic in excess. Iron, zinc and copper contents of the studied
oils could be expected to improve oxidative stability of the oil by insects were found to be higher, but not dangerously so, than those of
increasing MUFA concentrations (especially oleic acid) and decreasing conventional foods of animal origin (Fig. 5). Assuming good bioavail-
PUFAs (especially linoleic acid). Insect fat could possibly also be used to ability of the mineral contents, the studied insects could be regarded as
keep parity with the increasing demand of animal fat. useful in attempts to mitigate the risk of undernutrition of micronu-
trient deficiencies.

Minerals
Calcium is an essential mineral, playing vital roles by virtue of its Insect food and economy
phosphate salts in neuromuscular function, in many enzyme-mediated
processes like blood clotting, bone and tooth formation. Compared with The underlying cause of undernutrition is poverty. The increasing
other minerals of nutritional importance calcium uptake by the body is cost of livestock products like meat, milk etc. makes these food items
relatively inefficient with only 25–30% becoming absorbed and sodium inaccessible to a large section of people particularly in the developing
administration actually raising calcium excretion, presumably because and underdeveloped world. In industrialized countries per capita
sodium competes with calcium for re-absorption in the renal tubule. consumption of meat and milk has been projected almost 3 times
Calcium content of all of the studied insects was much higher than that higher than in developing countries; South Asia and Sub-Saharan Africa
of conventional foods of animal origin except chicken eggs (Fig. 5). are far below that level (http://www.who.int/nutrition/topics/3_
Apart from the nutritional point of view, calcium has also received foodconsumption/en/index4.html). Insects could offer economical
substantial interest in the medical sciences for its role in osteoporosis and sustainable animal protein. The high feed conversion efficacy,

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S. Ghosh et al. Journal of Asia-Pacific Entomology 20 (2017) 686–694

Fig. 5. Comparison of minerals content (mg/100 g DM) of selected insects with conventional foods of animal origin (data other than insects were obtained from USDA database (2015).)

much less requirement of water and land, and fewer diseases and higher current legislation within the European Union (EU) places insects under
portion of utilizable parts (lack of bones) make insects a suitable source the category of ‘novel food’ (EC 258/1997), although insect-containing
(Jung, 2016). However, reality shows that there are obstacles which “maggot cheese” in Sardinia, “Milbenkäse” in Germany and “palm
cause even poor people to refrain from turning to insects: not only in weevil dishes” in Reunion Island have a long history. The Agence
industrialized countries like Japan and Korea, but also developing féderale pour la Sécurité de la Chaîne alimentaire of the AFSCA of
countries like, for example, Nagaland in North-East India and Thailand, Belgium published a list that contains 10 species of insects, namely
the retail price of insects is often higher than that of conventional house cricket (Acheta domestica), African migratory locust (Locusta
animal meats. Retail costs in South Korea of 100 g dried G. bimaculatus migratoria migratorioides), super mealworm (Zophobas atratus morio),
larvae, T. molitor larvae and P. brevitarsis larvae are 26,000 won mealworm (Tenebrio molitor), lesser mealworm (Alphitobius diaperinus),
(26USD), 8000 won (8 USD) and 80,000 won (80 USD), respectively, greater wax moth (Galleria mellonella), American desert locust
which is much higher than the cost of pork in Korea and other (Schistocerca americana gregaria), banded cricket (Gryllodes sigillatus),
developed countries (AHDB, 2014). In Thailand retail cost of 1 kg of lesser wax moth (Achoria grisella) and silkworm (Bombyx mori) as fit for
cricket is almost 6 USD (200 Thai Baht) while lean pork costs 4.5 USD human consumption.
(155 Thai Baht). Costs of insets are high, because in developing In contrast, the Food Standards of Australia and New Zealand
countries an initiative to develop insect farms is often lacking and (FSANZ) consider super mealworm (Z. morio), house cricket (A.
harvesting edible species from the wild is then the only mechanism to domestica), and mealworm (T. molitor) as non-traditional, but not novel
procure insects for consumption. The cost of labour determines more food. As far as Korea is concerned in 2010 the government announced
than anything else the retail price. legislation of a special law aiming to promote insects industry. Korean
Ministry of Food and Drug Safety (MFDS) had authorized two insect
Future outlook in industrial perspective species; Gryllus bimaculatus and T. molitor as legitimate food ingredients
after grasshopper and silkworm pupae in 2015, and subsequently, two
Another obstacle in regard to edible insect farming is lack of more species, Protaetia brevitarsis and Allomyrina dichotoma were newly
legislation. However, regulatory authorities of some countries have added to the list (MFDS, 2016). The Ministry of Agriculture, Food and
taken position in making competent legislation in order to identify introduced a five year road map in order to advance research and
insect species as most promising candidates based on regional tradition, development of edible insects with an aim to support farms that raise
availability of data on nutrition, toxicity and ease with which such industrially eligible insects (MAFRA, 2016).
insects can be bred in captivity and processed for marketing. The With their higher protein, iron, zinc, and magnesium content, the

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S. Ghosh et al. Journal of Asia-Pacific Entomology 20 (2017) 686–694

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Acknowledgement Kim, H.-S., Jung, C., 2013. Nutritional characteristics of edible insects as potential food
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Korean Food Standard Codex, 2010. Ministry of Food and Drug Safety (Republic of
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Korea) .
Gyeongbuk FTA grant (2016) to CJ. Thanks are extended to Andong Lepage, G., Roy, C.C., 1986. Direct transesterification of classes lipids in a one-step
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