Soybean hawkmoth (Clanis bilineata tsingtauica) as food ingredients: a review

ABSTRACT

The soybean hawkmoth, known as Clanis bilineata tsingtauica (CBT), is a traditional edible insect of East Asia. CBT larvae are an ideal nutrient source containing 18 amino acids and 19 fatty acids. The total essential amino acid contents could meet the requirement of preschool children and adults. Long chain fatty acid content, especially linolenic acid is quite high than egg or soybean. Various active components, such as oil, polysaccharide, chitosan, can change the anti-oxidative, anti-aging, anti-fatigue, hypolipidemic and anti-bacterial properties. CBT larvae are of high protein, low fat, and easily absorbed by the human body. Thus, CBT larvae could be used as an alternative food ingredient, such as whole food and individual active component resource. Edible CBT foods could meet the emerging global demand for animal protein and resolve the food security issues. This review will provide an insight into CBT nutrient composition and their potential application in functional foods.

RESUMEN

La polilla conocida como Clanis bilineata tsingtauica (CBT) es un insecto comestible, tradicional de Asia oriental. Las larvas de CBT son una fuente ideal de nutrientes y contienen 18 aminoácidos y 19 ácidos grasos. El contenido total de aminoácidos esenciales puede satisfacer las necesidades tanto de niños en edad preescolar, como de adultos. El contenido de ácidos grasos de cadena larga, especialmente de ácido linolénico, es bastante más elevado que el del huevo o la soya. Varios componentes activos, entre ellos, el aceite, el polisacárido y el quitosano, pueden modificar las propiedades antioxidantes, antienvejecimiento, antifatiga, hipolipidémicas y antibacterianas. Las larvas de CBT poseen un alto contenido de proteínas y un bajo contenido de grasas, y son fácilmente absorbidas por el cuerpo humano. Ello significa que podrían utilizarse como ingrediente alimentario alternativo, como alimento completo y como recurso individual de componentes activos. Los alimentos comestibles a base de CBT podrían satisfacer la emergente demanda mundial de proteínas animales y resolver los problemas de seguridad alimentaria. Esta revisión proporciona una perspectiva de la composición de nutrientes de las CBT y su potencial aplicación en alimentos funcionales.

GRAPHICAL ABSTRACT

KEYWORDS:

• Clanis bilineata tsingtauica
• edible insect
• food ingredient
• health function
• functional food

PALABRAS CLAVE:

• Clanis bilineata tsingtauica
• insecto comestible
• ingrediente alimentario
• función sanitaria
• alimento funcional

1. Introduction

Insects can be a potential sustainable food source for humans owing to enormous biodiversity and high nutritional, environmental, and economic value (K. Kim et al., 2019b; Ramos-Elorduy, 2010). Around 2 billion people consume insects as a food source worldwide (Nowakowskia et al., 2021). Edible insects are gaining interest as alternative food sources for the increasing world population (Antonietta, 2020; Otero et al., 2020). The Food and Agriculture Organization of the United Nations (FAO) recognized that edible insects could play an important role in improving global food and nutrition security (Mutungi et al., 2017). In addition, FAO recommended that people can supplement their daily diet with edible insects, since they are consumed in some stage of their life cycle as food resources (van Huis et al., 2013). Currently, over one thousand identified species have historically been recorded and consumed by one third of the world’s population, mostly in Asia, Latin America, and Africa, for more than two thousand years (Jiménez et al., 2020; Raheem et al., 2018). Asian people started cultivating silkworms (Bombyx mori) artificially 5200 years ago (Ghosh et al., 2017; Yi et al., 2010). Until now, 324 species of insects from 11 orders have been documented that are either edible or associated with ‘Entomophagy’ (Feng, Chen, et al., 2018). The most commonly consumed insects in China and other East Asian countries include caterpillars, beetles, bees, wasps, crickets, ants, termites, and flies (X. Chen et al., 2009). Although the usual approach of insect collection is from the wild or cultivated field, edible insects often fail to meet the increasing consumption demand affected by seasons and market variations. There is a growing interest in rearing insects for commercial purposes, and an industrial scale production will be required to ensure a steady supply (Raheem et al., 2018; Kim et al., 2019a). At present, Bombyx mori pupae are the only insect legally documented in the food catalogue in China (Feng, Zhao, et al., 2020; Gao et al., 2018). In addition, other insects and their by-products, including almost all edible insect species are consumed only as folk food and traded in local markets, of which soybean hawkmoth is one of them (Figure 1). Soybean hawkmoth, Clanis bilineata tsingtauica, (CBT) belonging to the Lepidoptera, Sphingidae is an important economic insect widely distributed in East and South Asia (Sun, 2018; Wu, 2012). The CBT larvae (CBTL) are commonly called ‘Doudan’ and ‘Bean ginseng’. Moreover, its edible stage includes the whole larval stage from the first to the fifth instar (X. Chen et al., 2009). In this review, we provide an overview of the nutrition, functional evaluation, and safety of CBTL.

Figure 1. Different developmental stage and common foods of Clanis bilineata tsingtauica.

Figura 1. Diferentes estados de desarrollo y alimentos comunes de Clanis bilineata tsingtauica.

2. Eating culture of soybean hawkmoth

CBT is an agricultural pest, mainly feeding on leguminous crops. While controlling the CBT outbreak, people innovatively converted it to a novel protein resource with great edibility (X. Chen et al., 2009; Feng, Zhao, et al., 2020). CBTL consumption has long been a traditional folkways culture, but it is difficult to find out the exact origin of this diet custom. The earliest document appeared in the book On Farming and Sericulture (C.N. Li, 1982). The cooking and oil extraction method was recorded by Song-ling Pu (1640–1715), a famous litterateur of the Qing Dynasty, in detail. In another book, The Addition to Compendium of Materia Medica, written by Xue-min Zhao (1719–1805), reported that CBTL were edible (Zhao, 2007). Until now, CBTL has always been favored and has become a local traditional specialty insect food in Beijing city, Jiangsu, Anhui, Henan, Shandong Province, and their surrounding regions (Sun et al., 2018; Wu, Meng, et al., 2000). Compared to Bombyx mori and other insects, CBTL has also been highly accepted in these areas (A.J. Liu et al., 2019). CBTL provides significant economic benefits as it can be utilized continuously (Feng, Zhao, et al., 2020). China holds the largest consumer of CBTL, with a consumption rate of approximately 100, 000 tons/year (Pan et al., 2018; Yan et al., 2020). At present, the most common processing method includes cooking the fresh larvae into delicious food using traditional Chinese cooking techniques, including stir frying, deep frying, stewing, roasting, and pan frying (Figure 1). Besides direct consumption after cooking, CBTL can be processed into different types of common food. For instance, freeze-dried, fried, fresh meat, and canned fresh meat CBTL food are quite common. It is worth mentioning that the canned CBTL meat was developed for industrial food application (H.B. Wang et al., 2013; Wu, Lu, et al., 2017).

3. Nutrition and functional evaluation

CBTL is rich in nutrition, especially protein, edible oil, and other functional components showing various activities (Table 1).

Table 1. Nutritional contents of some edible insects in 100 g dry weight.

Tabla 1. Contenido nutricional de algunos insectos comestibles en 100 g de peso seco

Published data of nutritional value	Common edible insects
	Soybean hawkmoth (Clanis bilineata tsingtauica)	Silkworm (Bombyx mori)	Oak silkmoth (Antherea pernyi)	Rice grasshopper (Oxya chinensis)	The Central American locust (Schistocerca piceifrons piceifrons)	The cricket (Gryllus bimaculatus)	Yellow mealworm (Tenebrio molitor)	Sweet potato hawkmoth (Herse convolvuli)
Stage	Larvae	Chrysalides	Chrysalides	Adults/Nymph	Adults/Nymph	Adults/Nymph	Larvae	Larvae
Protein, %	65.5	60.03	55.01	20.80	80.26	58.32	38.30	53.7
Lipid, %	23.68	29.47	26.63	2.20	6.21	11.88	26.72	16.3
Carbohydrate, %	NR	0.92	NR	NR	NR	NR	26.25	NR
Ash, %	2.17	5.79	4.03	1.20	3.35	9.69	4.10	NR
Fiber, %	3.77	NR	NR	1.20	12.56	9.53	NR	NR
Chitin, %	NR	NR	NR	NR	11.88	NR	NR	NR
Reference	Wu et al. (2000)	Adalina and Maharani (2018)	Feng et al. (2020)	Zhao et al. (2002)	Pérez-Ramírez et al. (2019)	Ghosh et al. (2017)	Adalina and Maharani (2018)	Chen (1997)

NR, non-reported.

NR, no reportado.

3.1. Basal components

CBTL contains 75.4%−75.6% moisture, 15.41% protein, 5.0% oil, 3.77% dietary fiber, 2.17% ash and various vitamins in fresh weight. In dry weight, protein content is 63.7%−65.5% (w/w) and oil content is 21.5%−23.68% (w/w) (Table 2) (Sun, 2018; Tian & Zhang, 2012a; Wu, Meng, et al., 2000).

Table 2. Proximate chemical composition of Clanis bilineata tsingtauica larvae.

Tabla 2. Composición química aproximada de las larvas de Clanis bilineata tsingtauica.

Chemical composition		Component (%)
Moisture		75.46^a	75.6^b
Ash in fresh Clanis bilineata tsingtauica larvae		NR	2.17^b
Protein in fresh Clanis bilineata tsingtauica larvae		NR	15.41^b
Oil in fresh Clanis bilineata tsingtauica larvae		NR	5.0^b
Dietary fiber in fresh Clanis bilineata tsingtauica larvae		NR	3.77^b
Vitamin in fresh Clanis bilineata tsingtauica larvae	Vitamin B1	NR	4.9 × 10^−5c
	Vitamin B2	NR	5.2 × 10^−4c
	Vitamin B12	NR	1.412 × 10^−3c
	Vitamin C	NR	9.8 × 10^−4c
	Vitamin E	NR	3.065 × 10^−3c
Lipid in dry Clanis bilineata tsingtauica larvae		21.5^a	23.68^c
Unsaturated fatty acid in dry Clanis bilineata tsingtauica larvae (%)	Linoleic acid C18:2	1.71^a	1.49^c
	Linolenic acid C18:3	7.33^a	8.65^c
	Oleic acid C18:1	4.23^a	5.06^c
	Total	13.27^a	15.20^c
Saturated fatty acid in dry Clanis bilineata tsingtauica larvae(%)	Stearic acid C18:0	0.84^a	0.75^c
	Palmitoleie acid C16:0	6.79^a	7.59^c
	Other	0.60^a	0.14^c
	Total	8.23^a	8.48^c
Protein in dry Clanis bilineata tsingtauica larvae		63.7^a	65.5^c
Essential amino acid in dry Clanis bilineata tsingtauica larvae (%)	Histidine	0.986^a	1.95^c
	Isoleucine	3.068^a	1.92^c
	Leucine	3.618^a	2.44^c
	Lysine	4.025^a	2.30^c
	Methionine	2.087^a	2.39^c
	Cysteine	3.572^a	1.79^c
	Phenylalanine	2.331^a	2.38^c
	Threonine	1.474^a	1.54^c
	Tyrosine	2.312^a	2.35^c
	Valine	2.587^a	2.75^c
	Tryptophane	0.903^a	0.660^c
	Total	26.96	22.47
Nonessential amino acid in dry Clanis bilineata tsingtauica larvae (%)	Alanine	4.265^a	2.73^c
	Argnine	1.971^a	2.09^c
	Aspartic acid	2.864^a	2.23^c
	Glutamic acid	4.154^a	5.64^c
	Glycine	2.230^a	2.11^c
	Proline	4.817^a	2.14^c
	Serine	1.442^a	2.12^c
	Total	21.74	19.06
Total amino acid		48.706^a	41.53^c

^aWere cited from Tian and Zhang (2012a). ^bWere cited form Sun (2018). ^cWere cited form Wu et al. (2000). NR, non-reported.

^aFueron citados en Tian and Zhang (2012a). ^bFueron citados en Sun (2018). ^cFueron citados en Wu et al. (2000). NR, no reportado.

3.1.1. Protein and amino acids

The protein content in CBTL dry matter is around 63.7%−65.50% (w/w) which is much higher than soybean (40%) or eggs (13%) (Tian & Zhang, 2012a; Xia, Wu, et al., 2012). The crude fat content is 23.68% (w/w) in CBTL (Wu, Meng, et al., 2000). The ratio of protein to crude fat (P/G) in CBTL is 2.96; thus, CBTL is considered as a high-protein insect instead of a high-fat insect. CBTL contains 18 kinds of amino acids, excluding two nonessential amino acids, asparagine, and glutamine. Of them, eight are essential amino acids (lysine, threonine, methionine, valine, tryptophan, phenylalanine, leucine, and isoleucine) with a dry weight of 224.73 g·kg⁻¹ (Xia, Wu, et al., 2012). According to the amino acid scoring (AAS) pattern recommended by FAO/WHO/UNU in 1985, lysine is the first limiting amino acid of CBTL, having an AAS of 53.27. Threonine is the second limiting amino acid with an AAS of 54.71 (Table 3). Total essential amino acids (including histidine) in CBTL is 343.11 mg/g protein, which is close to the total essential amino acid content 460 (408–558) mg/g recommended by FAO/WHO/UNU for baby, more than the total amino acids content 339 mg/g for preschool children (2–5 years old), 241 mg/g for preschool children (10–12 years old), and 127 mg/g for adults (Food and Agricultural Organization, World Health Organization, United Nations University [FAO/WHO/UNU], 1985).

Table 3. Amino acid score of essential amino acid in Clanis bilineata tsingtauica larvae.

Tabla 3. Puntuación de aminoácidos esenciales en las larvas de Clanis bilineata tsingtauica.

Essential amino acid	Amino acid scoring pattern recommended by FAO/WHO/UNU in 1981				Content in Clanis bilineata tsingtauica larvae (mg/g protein)	AAS
	Baby	Preschool children (2–5)	Preschool children (10–12)	Adult
Histidine	26 (18–36)	(19)	(19)	16	29.77	114.50
Isoleucine	46 (41–53)	28	28	13	29.31	63.72
Leucine	94 (83–107)	66	44	19	37.24	40.04
Lysine	66 (53–76)	58	44	16	35.16	53.27
Methionine+Cysteine	42 (29–60)	25	33	17	63.79	151.87
Phenylalanine+Tyrosine	72 (68–118)	63	33	19	72.21	100.30
Threonine	43 (40–45)	34	38	9	23.53	54.71
Tryptophane	17 (16–17)	11	(9)	5	10.08	59.27
Valine	55 (44–77)	35	25	13	42.03	76.42
Total (beside Histidine)	434 (390–552)	320	222	111	313.34	−
Total (include Histidine)	460 (408–588)	339.00	241.00	127.00	343.11

In animal experiments, Xia, Wu, et al. (2012) fed three groups of rats with casein, CBTL protein, and no protein diet for 10 days, respectively. The nutritional parameters measured for the group fed with the CBTL protein diet showed a positive nitrogen balance of 1.37, net protein retention of 2.9, and true digestibility of 95.8%, which were comparable to those measured for the group fed with the casein diet. The results suggested that CBTL protein may be a suitable alternative dietary protein source for humans.

3.1.2. Oil

It was reported that CBTL contained 19 kinds of fatty acids (8 saturated fatty acids, 3 monounsaturated fatty acids, 5 polyunsaturated fatty acids, and 3 odd chain fatty acids) (Sun, 2018). The oil proportion in fresh and dried CBTL is 5% and 23.68% (w/w), respectively. Moreover, the content of unsaturated fatty acids was higher than saturated fatty acids. C₁₆ ~ C₁₈ fatty acids share more than 97% fatty acids. Short chain contents, medium chain, and super long chain fatty acids are less than long chain fatty acids (Table 4). The essential unsaturated fatty acid content accounts for 64.17% of the total fatty acid (Wu, Meng, et al., 2000). More importantly, CBTL contained linoleic acid and α-linolenic acid, which are essential fatty acids that cannot be synthesized in the human body and can only be provided through food. The content of linoleic acid (C_18:2) was 6.29 g/100 g fatty acid. Linolenic acid (C_18:3) was found to be with the highest content among essential unsaturated fatty acids (36.53–46.91 g/100 g fatty acid). Total essential fatty acid and linolenic acid (C_18:3) contents is much higher than that in egg or soybean, while other fatty acids contents are less advantageous compared with egg or soybean (Sun et al., 2018; Tian & Zhang, 2012b; Wu, Meng, et al., 2000; Yang, 2018). Briefly, long chain fatty acids content, especially linolenic acid (C_18:3) in CBTL oil, is quite high. CBTL oil is a potential alternative to edible oil.

Table 4. Composition and content of fatty acids in Clanis bilineata tsingtauica larvae, egg and soybean.

Tabla 4. Composición y contenido de ácidos grasos en las larvas de Clanis bilineata tsingtauica, el huevo y la soya

Fatty acid	Contant in Clanis bilineata tsingtauica larvae^a (g/100 g fatty acid)		Contant in egg (g/100 g fatty acid)	Contant in soybean (g/100 g fatty acid)
Linoleic acid C18:2	6.29^a	9.24^b	14.20^c	53.90^c
Linolenic acid C18:3	36.53^a	46.91^b	0.10^c	8.20^c
Stearic acid C18:0	3.15^a	2.55^b	8.00^c	3.40^c
Palmitoleie acid C16:0	32.05^a	23.84^b	26.40^c	10.80^c
Oleic acid C18:1	21.35^a	14.65^b	41.70^c	23.20^c

^aWere cited from Wu et al. (2000). ^bWere cited from Sun (2018). ^cWere cited from Yang (2018).

^aFueron citados en Wu et al. (2000). ^bFueron citados en Sun (2018). ^cFueron citados en Yang (2018).

3.2. Functional components

The functional food research directs towards ingredients, their functions and underlying mechanisms (Im et al., 2019). Active components, such as oil, polysaccharide, and chitosan could exhibit anti-oxidative, anti-aging, anti-fatigue, hypolipidemic, and anti-bacterial properties. The structure of some active components has been identified (Tian, 2016; Wu, Lu, et al., 2017), and their mechanism of action has been tested in vivo or in vitro (Sun et al., 2018; Tian & Zhang, 2012c). The active components in CBTL and their function are summarized here (Figure 2).

Figure 2. Functional components in Clanis bilineata tsingtauica larvae.

Figura 2. Componentes funcionales de las larvas de Clanis bilineata tsingtauica.

3.2.1. Anti-oxidation active components

CBTL contains unsaturated fatty acids, polysaccharides, and other compounds. These active components exhibited good antioxidant properties. Oil extracted from CBTL showed strong antioxidant activities in vitro (Sun et al., 2018; Wade & Hoelle, 2020). In scavenging 2, 2-diphenyl-1-picrylhydrazyl (DPPH) radicals test, lipid peroxidation inhibitory activity IC₅₀ was 76.23 μg/mL through soxhlet extraction and 80.47 μg/mL through ultrasound-assisted aqueous extraction. However, in β-carotene bleaching test, IC₅₀ was 1.56 mg/mL through soxhlet extraction and 2.67 mg/mL through ultrasound-assisted aqueous extraction. Further, ultrasound extraction could obtain more biologically active ingredients than soxhlet extraction, which suggests that optimization of the extraction method could obtain more active components. Since the extraction method is one of the factors affecting antioxidant activity, more potential extraction methods need to be evaluated further. In addition, CBTL oil also exhibited antioxidant activity against PC12 cells injured by H₂O₂ because of 14 fatty acids, lecithin (200 mg/g), cephalin (100 mg/g), and high protein contents in the extractions (Sun et al., 2018). Similarly, Musca domestica, Bombyx mori, Acheta domesticus, and Tenebrio molitor displayed high antioxidant capacities (Ai et al., 2012; Joaquin et al., 2020; Mattia et al., 2019). In mealworm oil, abundant glucosamine derivatives and functional peptides led to a high antioxidant capacity (Son et al., 2020).

Polysaccharide CBP₃, isolated by alcohol precipitation, has a strong antioxidant ability that could inhibit free radicals in vitro (Tian & Zhang, 2012c). The reductive activity of CBP₃ exhibited a significant positive relationship with its concentration and the scavenging ratio of O^2- and OH radical (·OH). The scavenging ratio of ·OH (IC₅₀ = 591 μg/mL) and O₂⁻ (IC₅₀ = 536 μg/mL) may be related to structure characterizations (Tian, 2016).

When the individual active components of CBTL are separated and tested for their anti-oxidation effects independently, Sun (2018) found that CBTL extract exhibited better effect presumably due to the synergistic effects of various active components in the CBTL extract. In contrast, the protein extract of Tenebrio molitor, Ulomoides dermestoides, and Bombyx mori exhibited high antioxidant activities in some edible insects (Baek et al., 2020; Flores et al., 2020). CBTL also contains high protein content, suggesting the peptides or amino acids to be antioxidant. However, little is known about the anti-oxidation activities of protein. Thus, CBTL is a good source of functional food ingredients.

3.2.2. Anti-aging active components

In vivo and in intro research showed that CBTL exhibited anti-aging function, which may be related to chitosan components. Chitosan, a polymer composed primarily of β-(1 → 4)-2-amino-2-deoxy-D-glucose (D-glucosamine) monomers, is derived by deacetylation of naturally occurring biopolymer. Water-soluble chitosan of CBTL skin showed favourable anti-ageing activities on superoxide anion, showing considerable scavenging activities and hydroxyl radicals and reducing capacity, with scavenging activities increased to 87.04% (hydroxyl radical scavenging activity) and 79.81% (2,2-Diphenyl-β-picrylhydrazyl radical scavenging activity) at a concentration of 120 mg/mL (Wu, Lu, et al., 2017). Using the model of subacute aging mice induced by subcutaneous injection of D-galactose, it was found that both water extraction and 75% ethanol extraction significantly prolonged the time of loaded-swimming, enhanced the viscera index and the activity of total superoxide dismutase and glutathione peroxidase, and decreased malondialdehyde contents. CBTL exhibited anti-aging effect by improving immune and antioxidant capacity. Moreover, intragastric water-soluble chitosan of CBTL skin administration significantly increased the activities of superoxide dismutase and glutathione peroxidase and inhibited the formation of malondialdehyde in brains and sera of mice in a dose-dependent manner in D-galactose-induced-aged mouse model in vivo study (Wu, Lu, et al., 2017). Thus, anti-aging effect of CBTL results from its anti-oxidation activity. Interestingly, the anti-aging effect of an edible grasshopper (Oxya chinensis sinuosa) results from downregulated production of inflammatory cytokines (Im et al., 2019). Thus, the anti-aging mechanism of CBTL needs to be investigated at cellular and molecular levels.

3.2.3. Anti-fatigue active components

The anti-fatigue properties of CBTL were also studied with water and alcohol extraction (X.W. Liu et al., 2014; Xu et al., 2014). At a high CBTL dose, the swimming and climbing time of the mice was significantly prolonged, with improved moving endurance. In addition, the contents of blood urea nitrogen and blood lactic acid decreased, and the contents of hepatic glycogen increased after exercise. It was concluded that CBTL exhibited anti-fatigue functions by alleviating physical fatigue in the mouse model. This is similar to a stinkbug Aspongopus chinensis (S. Li et al., 2020).

3.2.4. Hypolipidemic active components

Chitooligosaccharide was capable of inhibiting the increase in body weight by decreasing plasma total cholesterol, triacylglycerol, and low-density lipoprotein cholesterol levels to 1.88 ± 0.46 mmol/L, 1.37 ± 0.05 mmol/L, 0.61 ± 0.02 mmol/L, respectively, and increasing high-density lipoprotein cholesterol (HDL-C) level to 0.82 ± 0.11 mmol/L in the mouse fed with high fat diets (Xia, Chen, et al., 2013). A similar phenomenon was observed in a Hercules beetle Allomyrina dichotoma (K. Kim et al., 2019b).

3.2.5. Anti-bacterial active components

Many insects and their products, such as Musca domestica and Dinoponera quadriceps exhibited anti-bactericidal effects (Rocha et al., 2021; Z.T. Wang et al., 2017). In CBTL, both chitooligosaccharides and original chitosan showed significant inhibitory activities against Bacillus subtilis (Bacillales: Bacillaceae). With the addition of the chitooligosaccharides, the number of colonies at 0 h was slightly lower than that at 48 h. These findings suggested that the chitooligosaccharides from CBTL skin were highly effective at inhibiting the growth of B. subtilis (Wu, 2012).

In brief, CBT, unlike other common edible insects, has high protein content. CBTL contains 18 amino acids and 19 fatty acids. The total essential amino acid content can meet the demand of preschool children and adults. Compared to egg and soybean, the long chain fatty acid content of CBTL, especially linolenic acid (C_18:3) is quite high. Both oil and polysaccharide have excellent biological activity, and protein may also be a potential antioxidant component. It possesses different anti-aging mechanisms than edible locusts. Moreover, complex mixtures showed higher efficacy than their individual components due to synergistic effects (Im et al., 2019; Sun et al., 2018). Thus, CBTL could be used as an alternative food ingredient, such as whole food and individual active component resource.

4. Potential hazards and risks

Although the presence of toxic and allergic substances is important, a limited number of studies exist on the possible toxicity of edible insects (Mishynaa & Glumacb, 2021). However, all the studied edible insects in China are non-toxic (Gao et al., 2018). A previous study reported that two entomogenous fungus, ‘Jiuzhou’ caterpillar fungus (Cordyceps kyushuensis) and ‘Taishan’ caterpillar fungus (Cordyceps taishanensis) grown in CBTL are non-toxic (C. Chen et al., 2005; Guo & Li, 2000; B. Liu et al., 1984). Nonetheless, the toxicological assessment of CBTL has not been reported yet. The toxicological evaluation should be implemented according to the current version of the standard in effect, such as Regulation (EU) 2015/2283 of the European Parliament and Council on novel foods (Turck et al., 2021), ‘Procedures for toxicological assessment of food’ (NHCPRC, 2014) (GB 15193.1–2014) and ‘Regulations on Application and Acceptance of Raw Materials for New Food’ (NHCPRC, 2014). The toxicological assessment is a judgment process based on the data/results obtained from standard testing procedures. Specifically, suppose the relevant literature and component analysis did not find toxic effects of the food and had long-term consumption history without any harmful effects in substances (or raw materials for new food). In that case, it can be evaluated by acute toxicity test, genotoxicity tests, ninety days oral toxicity test, and teratogenic test (NHCPRC, 2020). According to the test results, assessors determine whether to conduct a toxicokinetics test, a reproductive toxicity test, a chronic toxicity test, and a carcinogenicity test (NHCPRC, 2014). Ji et al. (2009) reported that 18% of the reported cases of fatal anaphylaxis and anaphylactic shock to food in China were due to the ingestion of insects. However, CBTL caused only one reported case of anaphylaxis for such a long time (Steffie & Kitty, 2018). The case was about a 36 year old male who consumed CBTL and drank beer, resulting in an allergic reaction (Zhang, 2007). According to the diagnosis, it might have been related to the heterotypic protein in CBTL. This case of anaphylaxis occurred rapidly, belonging to type I allergy. In addition, attention must be paid to harmful microorganisms, parasites, toxins, heavy metals, veterinary drugs, hormones, and pesticide residues in the context of food safety (Antonietta, 2020; Mutungi et al., 2017; Schröge & Wätjen, 2019).

5. Prospect

The present study sought to review the research progress on nutrition, functional evaluation, and safety of a traditional edible insect CBTL. Previous studies on CBTL mainly focused on three aspects: bio-ecological characteristics related to rearing techniques and nutrition evaluation and its utilization as an edible insect. CBTL is a rich source of novel proteins, fatty acids, and active components. CBTL are excellent alternative to foods that can be used as essential supplement of protein, edible oil, and functional food ingredients. However, exploration of their characteristics and the development of more active components is still needed. Overall, CBTL consumer market still needs to be expanded, which is influenced by season and region. The total amount of CBTL resources is small, the development of cooking methods and specialty dishes is relatively slow, the processing capacity is limited, and the development degree of nutrition and health care products is not significant. Recent research focuses on the use of edible insects as food ingredients to fortify more traditional forms of food such as bread, tortilla, cookies. This trend might open up alternative ways to include them in our daily diet (Melgar-Lalanne & Alvarez, 2019). CBTL is generally considered to be safe with a long history of consumption in China. Toxicological assessment, allergens, and pollutants should be considered for the evaluation process. In addition, the effects of insect farming on the ecological environment should be evaluated. Insect farming and integrated utilization can result in great economic benefits and significant commercial development value in developing countries. Besides evaluation, process development, and utilization, there will also be a need for new regulations and legislation about the use of insects in food production in order to ensure consumer safety. Certainly, edible insect production has great potential with respect to sustainable food production for the growing population (S.K. Kim et al., 2017; van Huis & Oonincx, 2017). Edible CBT foods could meet the emerging global demand for animal protein and resolve the food security issues (Nowak et al., 2016). The insect industry is rapidly developing but still faces many challenges, which can only be encountered with the cooperation of all stakeholders (van Huis, 2020).

Acknowledgments

This work was supported by the Chinese Modern Agricultural Industry Technology System (Grant number CARS-04); National Key R&D Program of China (Grant number 2018YFD0201004); and China Postdoctoral Science Foundation (Grant number 2018M631876).

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by the China Postdoctoral Science Foundation [2018M631876]; Chinese Modern Agricultural Industry Technology System [CARS-04]; National Key R&D Program of China [2018YFD0201004].