Abstract
Edible insects are a food source that has high nutritional value. Domestic silkworm pupae are an important by‐product of sericulture and have a long history as food and feed ingredients in East Asia. Silkworm pupae are a good source of protein, lipids, minerals, and vitamins and are considered a good source of nutrients for humans. Silkworm pupae are a valuable insect source of substances used in healthcare products, medicines, food additives, and animal feed. Because silkworm pupae are being increasingly used in the human diet, potential allergic reactions to the substances they contain must be elucidated. Here, we present an overview of the benefits of silkworm pupae. First, we describe their nutritional value. Second, we report their functional properties and applications, focusing on their potential use in the food and pharmaceutical industries. Finally, we consider the current state of research regarding silkworm pupae‐induced allergies.
Keywords: allergen, allergy, food safety, function, insect protein, nutrition, silkworm pupae
Short abstract
Silkworm pupae have high nutritional value and varied biological activities. Silkworm pupae are a valuable insect source for healthcare products, medicine, food additives, and feed. Allergic reactions induced by silkworm pupae need attention and further research.
1. INTRODUCTION
Demand for sustainable sources of nutrition is increasing. Thus, edible insects, which have long formed part of the human diet in Asia, Africa, and Latin America (de Castro et al., 2018), have become a primary focus of scientific research in recent years. However, the allergic risks of consuming insects must be evaluated. Allergic reactions associated with eating edible insects range from a mild localized reaction to a more severe systemic clinical response. The main clinical symptoms include respiratory (e.g., dyspnea, asthma), gastrointestinal (e.g., nausea, vomiting, diarrhea), and skin (e.g., flushing, urticaria, rash, pruritus,) reactions (de Gier & Verhoeckx, 2018).
The silkworm (Bombyx mori) is a cultivated insect that is reared at large scales. Silkworm and its metabolites have high nutritional, medicinal, and economic value (Ratcliffe et al., 2011; Yang et al., 2009). The silkworm lifecycle encompasses four distinct developmental stages: ova, larva, pupa, and imago. Silk is obtained from the cocoon when silkworms transform from larvae to pupae.
The pupae of the two silk‐producing moths are edible. Silkworm pupae are frequently used as food in Asian countries, including Japan, Korea, India, and, especially, China (Zhou & Han, 2006). In China, silkworm pupae are eaten as food and are also an important component of traditional Chinese medicines used to treat hypertension and fatty liver (Zhang & Zhang, 2001). With increasing demand for sustainable animal‐derived dietary protein, edible insects are of interest as a source of protein (FAO, 2013). Silkworm pupae are considered a premium source of animal protein. They represent the only insect food in the List of Novel Food Resources published by the Ministry of Health of China and are widely used in dietary supplements, medicines, and animal feed in China and Korea (Kim et al., 2008; Zhu, 2004). In China, more than 100,000 tons of fresh silkworm pupae are produced annually (Dong & Wu, 2010). In recent years, silkworm pupae are used as raw materials in the food industry because of their high nutritional value and varied biological activities.
A major concern regarding novel sources of protein, including silkworm pupae, is their potential to cause food allergy (Pali‐Schöll et al., 2019). In recent years, large numbers of cases of allergic reactions to silkworm pupae have been reported (Ji et al., 2008), including serious allergies, and, even anaphylactic shock (van der Poel & Chen, 2009; Araujo et al., 2014). Thus, allergies to silkworm pupae are now the subject of extensive research worldwide.
This review describes the nutritional value of silkworm pupae, their functional properties, and potential applications. Within this framework, allergies to silkworm pupae are evaluated.
2. NUTRITIONAL VALUE OF SILKWORM PUPAE
Extensive data show that silkworm pupae have a well‐balanced nutrient profile, making them suitable as human food. Essentially, silkworm pupae are a good source of protein, fat, minerals, and vitamins. Compared to conventional food, they have higher content of three calorigenic nutrients (protein, fat, and carbohydrates), providing up to 230 kcal per 100 g. The values of key nutrients in silkworm pupae compared with other common foods are listed in Table 1.
TABLE 1.
Name | Edible part (%) |
Energy (kcal) |
Water (g) |
Protein (g) |
Fat (g) |
Carbohydrate (g) |
VA (μg) |
B1 (mg) |
B2 (mg) |
B3 (mg) |
VE (mg) |
Na (mg) |
Ca (mg) |
Fe (mg) |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Silkworm pupae | 100 | 230 | 57.5 | 21.5 | 13 | 6.70 | 0 | 0.07 | 2.23 | 2.2 | 9.89 | 140.2 | 81 | 2.6 |
Egg (white part) | 87 | 138 | 75.8 | 12.7 | 9 | 1.50 | 310 | 0.09 | 0.31 | 0.2 | 1.23 | 94.7 | 48 | 2 |
Milk | 100 | 54 | 89.8 | 3 | 3.2 | 3.40 | 24 | 0.03 | 0.14 | 0.1 | 0.21 | 37.2 | 104 | 0.3 |
Chicken | 66 | 167 | 69 | 19.3 | 9.4 | 1.30 | 48 | 0.05 | 0.09 | 5.6 | 0.67 | 63.3 | 9 | 1.4 |
Pork (lean meat) | 100 | 143 | 71 | 20.3 | 6.2 | 1.50 | 44 | 0.54 | 0.1 | 5.3 | 0.34 | 57.5 | 6 | 3 |
Sea shrimp | 51 | 79 | 79.3 | 16.8 | 0.6 | 1.50 | 0 | 0.01 | 0.05 | 1.9 | 2.79 | 302.2 | 146 | 3 |
Tilapia | 55 | 98 | 76 | 18.4 | 1.5 | 2.80 | 0 | 0.11 | 0.17 | 3.3 | 1.91 | 19.8 | 12 | 0.9 |
Date sources: Food Ingredients Table of China (2017).
Abbreviations: B1, Thiamin; B2, Riboflavin; B3, Niacin; Ca, calcium; Fe, Iron; Na, Sodium; VA, Retinol; VE, Tocopherol.
The protein content of silkworm pupae is about 21.5%, which is higher than that of other typical animal products. On a dry‐weight basis, the protein content of silkworm pupae has been reported to be as high as 49%–54% (Longvah et al., 2011; Nowak et al., 2016). The proteins of silkworm pupae are considered complete proteins because of their high content of essential amino acids. In fact, silkworm contains all the amino acids required by the human body and in the appropriate proportions based on the recommendations of the FAO/World Health Organization (WHO) (Köhler et al., 2019; Ni et al., 2003; Wang et al., 2009; Yang et al., 2009; Zhou & Han, 2006). In general, insect proteins are highly digestible (Capinera and Finke, 2008). The amino acid score and protein digestibility‐corrected amino acid score of silkworm pupae are 100 and 86, respectively (Longvah et al., 2011). Furthermore, the amino acid score of proteins in silkworm pupae protein was 100 with respect to the amino acid profile of a 2–5‐year‐old child (FAO/WHO, 1985) (Longvah et al., 2011). Therefore, silkworm is a good source of protein that could be used as an alternative dietary source of protein for human nutrition.
Edible insects also have high fat content. In particular, dry silkworm pupae have a fat content of 25%–30% (Kouřimská and Adámková, 2016; Longvah et al., 2011). Silkworm pupae have high monounsaturated and polyunsaturated fatty acid contents and low saturated fat content (Payne et al., 2016). About 70%–80% of the fatty acid content of silkworm pupae is unsaturated, while about 1% is unsaponifiable matter in oil, including campesterol, β‐sitosterol, and cholesterol. In particular, silkworm pupae have almost 71% α‐linolenic acid content (Pereira et al., 2003; Rao, 1994; Zhao, Li, et al., 2015; Zhao, Wang, et al., 2015). Silkworm pupae are a good source of functional fatty acids. Furthermore, the oxidative stability of their total lipid content is very high, as the synergistic effect between tocopherol and phospholipids prevents the oxidation of lipids (Kotake‐Nara et al., 2002).
Some insect species, including weevil larvae and termites, have high quantities of saturated fat, however silkworm pupae do not (Payne et al., 2016). Based on WHO guidelines, limiting the dietary intake of saturated fat minimizes the risk of cardiovascular disease (World Health Organization (WHO), 2015). Silkworm pupae contain edible lipids of high quality that are used as raw materials in medicine (Shanker et al., 2006; Wang et al., 2013). For instance, after eating silkworm pupae oil for 18 weeks, rats showed a notable increase in high‐density lipoprotein cholesterol levels, with significantly reduced triglyceride and total cholesterol levels (Longvah et al., 2012). Silkworm pupae oil also regulates plasma lipid and lipoprotein levels in the serum of rats by activating apoproteins and lipid‐metabolizing enzymes. Thus, it could be used to treat hyperlipidemia (Hu & Chen, 2011). Therefore, silkworm pupae represent a good source of fats for human consumption.
Edible insects are also rich in minerals, including phosphorus, calcium, potassium, sodium, iron, zinc, magnesium, copper, and manganese (Kouřimská & Adámková, 2016). Silkworm pupae are a good source of calcium and iron (Table 1) and have high potassium content (34.0 mg/g), with a low Na/K ratio (0.08), and high zinc content (36 μg/g) (Zhou & Han, 2006), all of which are important for human health and nutrition. In addition, the heavy metal content (lead, arsenic, cadmium, and mercury) (Köhler et al., 2019) of silkworm pupae is below the maximum recommended level for human consumption and use in animal feed (National Standardization Management Committee of China, 2005). The mineral content reported in the published literature is highly varied (Köhler et al., 2019; Kouřimská & Adámková, 2016; Longvah et al., 2011; Nowak et al., 2016; Zhou & Han, 2006). These differences might be explained by mineral content varying with geographical location, seasonality, and diet, among other items. In general, edible insects contain a variety of vitamins, but have limited vitamin A (Kouřimská & Adámková, 2016). Silkworm pupae are a good source of thiamin, riboflavin, and niacin (Table 1). They contain about 10 mg tocopherols per 100 g, which is a much higher level than that found in other common foods. Importantly, the mineral and vitamin content of farm‐bred silkworm pupae can be controlled by regulating what they are fed.
Silkworm pupae also contain some antinutrients when they consume mulberry leaves. These antinutrients include phytate (72.89–110.16 mg/g) and phytin phosphorus (20.54–31.03 mg/g), as well as tannic acid, alkaloid, flavonoids, saponin, and oxalate. However, these antinutrients are present at low levels and fall within human tolerance levels. Thus, silkworm pupae are safe for human consumption (Omotoso, 2015).
Overall, silkworm pupae are a good source of protein, lipids, minerals, and vitamins, all of which are all important components of the human diet.
3. FUNCTIONAL PROPERTIES AND APPLICATIONS OF SILKWORM PUPAE
Silkworm pupae have many functional properties that could be utilized in the food and pharmaceutical industries. In recent years, various bioactive compounds have been found in silkworm pupae that have potential functions and health benefits. For instance, silkworm proteins and hydrolyzed peptides have several functions, including improving immunity, and antitumor and antioxidant activity (Table 2). Hydrolyzed peptides of silkworm pupae have multiple physiological functions. However, methods for their extraction, purification, and structural identification need to be developed, and the mechanisms of their pharmacological actions need describing. Current methods for preparing peptides from silkworm pupae by enzymatic hydrolysis generate poor yields. Thus, enzymatic hydrolysis must be optimized to facilitate the commercialization of this process. In addition, after deproteinization and degreasing, silkworm pupae residues contain 2%–8% chitosan, about 4% polysaccharides, and small amounts of antibacterial peptides and other bioactive materials, which have various biological activities (Battampara et al., 2020; Luo et al., 2010; Mishraa et al., 2003; Ni et al., 1998; Wang et al., 2007; Yue et al., 2013; Zhang et al., 2000). The precise functions of chitin and polysaccharides extracted from silkworm pupae in humans need further investigation. A dimethyladenosine compound extracted from silkworm pupae could be used as a vasorelaxant to treat vasculogenic impotence in men (Ahn et al., 2008). Many natural drugs have been isolated from microbes, marine organisms, and plants; however, few drugs isolated from insects are available on the market. The silkworm has long been used in Chinese medicine (Ratcliffe et al., 2011). Scientific studies have demonstrated the health benefits of silkworm pupae, and it has been reported that eating silkworm pupae does not cause mutation or hepatotoxicity (Yang et al., 2010; Zhou & Han, 2006). Thus, silkworm pupae represent a valuable insect source for use in medicines and other healthcare products. Although some active substances in silkworm pupae have been identified, their pharmacological actions remain unclarified. With in‐depth research, silkworm pupae have great potential for use in the pharmaceutical industry.
TABLE 2.
Source | Function | Studies conducted |
---|---|---|
Protein Hydrolysis peptide |
Antifatigue Antifatigue |
|
Hydrolysis peptide | Antihypertensive property | (Wei et al., 2008; Wang et al., 2011; Wu et al., 2011; Zhao et al., 2011; Zhang et al., 2005; Wu et al., 2015; Wang et al., 2014) |
Extract Hydrolysis peptide |
Antioxidant activity Antioxidant activity |
(Deori et al., 2014) (Li et al., 2011; Wang et al., 2012; Min et al., 2009; Xiao et al., 2011; Lu et al., 2013; Zhao et al., 2011; Zhang et al., 2021) |
Protein Hydrolysis peptide |
Enhance/regulate immune responses Enhance/regulate immune responses |
(Yeo et al., 2013) (Li et al., 2019; Liu et al., 2010; Lu et al., 2013; Qi et al., 2009; Yang et al., 2008) |
Hydrolytic amino acid | Antitumor activity | (Hu et al., 2004; Li et al., 2018; Yan et al., 2008; Zhan et al., 2013, 2015) |
Extract Hydrolysis peptide |
Weight reduction Weight reduction |
(Ryu, 2014) (Lee et al., 2012) |
Extract | Alcohol detoxification | (Kwon et al., 2012) |
Hydrolysis peptide Hydrolysis peptide |
Serum glucose reduction Decrease fat accumulation |
(Zhang et al., 2016; Lee et al., 2011) (Lee et al., 2011) |
Hydrolysis peptide | Umami taste enhancement | (Yang et al., 2017) |
A study on the functional properties of silkworm pupae demonstrated their potential for use as food additives (Omotoso, 2015). In addition to direct consumption, the protein powder of silkworm pupae has been used as a food additive in cookies, noodles, bread, and other foods. Kim et al. (2016) used flour from silkworm pupae to replace 10% lean pork as a novel protein ingredient and showed that it enhanced the hardiness and cooking yield of emulsion sausages.
One of the greatest barriers to the adoption of edible insects as a direct food is consumer acceptance (Mlcek et al., 2014). Although consumers recognize the high nutrition value of insects, they prefer to not know what they are eating in this case (Govorushko, 2019). Certain components extracted from insects are preferable for consumers. Thus, extracting the proteins of silkworm pupae, or other bioactive compounds, could increase consumer acceptability. Future research should focus on developing methods to extract and process the proteins of silkworm pupae for use in the food industry.
Compound amino acids prepared by the hydrolysis of silkworm pupae could be easily accepted by consumers. In recent years, degreased silkworm pupae have been used in China to mass‐produce compound amino acids for use in health and medical care. A total of 11 healthcare products using compound amino acids derived from the proteins of silkworm pupae have been approved by the Ministry of Health and the State Food and Drug Administration in China and are commercially available on the Chinese market. Eight of these products enhance immune response, while two products are used to combat fatigue (http://www.samr.gov.cn/fw/wyc/).
Insects successfully substitute many ingredients used in the commercial production of animal feed (Govorushko, 2019). Silkworm pupae are used as fishmeal for breeding poultry, fish, and crustacean species (Konwar et al., 2008; Rahimnejad et al., 2019; Sun et al., 2014). This use of silkworm pupae could help to reduce other sources of protein feedstuffs, with positive effects on molting time, antioxidant capacity, and digestibility. Besides consuming silkworm directly or as ingredients in food, the human need for food can be met by using silkworm pupae as an animal feedstuff.
In recent years, the number of patents for inventions associated with silkworm pupae has increased rapidly in China. According to patent data from the State Intellectual Property Office of China, between 1989 and October 2019, there were 476 invention patents associated with silkworm pupae, of which 257 were issued between 2014 and October 2019. Of these 476 patents, 276 were associated with human needs. Of these 246 patents, 86 patents were for human medicine, veterinary medicine, forestry, agriculture, hunting, animal husbandry, fishing, trapping, and baking. The other 189 patents were for use in foods or food ingredients and their processing (not covered by other categories). Thus, patent applications for silkworm pupae as food and animal feed are rapidly increasing in China. Many patents for silkworm pupae have also been issued in South Korea, with applications including snack manufacturing and the refining of silkworm powder (Han et al., 2017).
4. SILKWORM ALLERGY
4.1. Silkworm‐induced allergy
The possible allergic reactions associated with eating insects are of concern for both consumers and scientists. Safety is a vital factor in food quality, with it being important to build confidence in the consumption of edible insects. Silkworms contain important sources of allergens, including excrement, dander, and silk. These allergens can cause various allergic reactions, such as cutaneous symptoms, respiratory symptoms, cardiovascular symptoms, and, even, anaphylactic shock (Gautreau et al., 2017; Ji et al., 2008; Vovolis & Galatas, 1999). These reactions could limit the use of silkworm pupae in food and feed. Potential silkworm‐induced allergies include respiratory allergy, contact allergy, and food allergy.
The silkworm is widely cultivated, and its silk is widely used. During processing and use, silk particles and wild silk floating in the air might be inhaled, causing allergies (Häcki et al., 1982; Inoue et al., 1997). Furthermore, inhaling the scales of the silkworm moth suspended in the air might cause respiratory allergies (Blanc et al., 1999; Suzuki et al., 1995). People allergic to silkworm might have a reaction when they are in contact with silk products (contact allergy) (Borelli et al., 1999; Ohansson et al., 1985). Silkworm pupae also cause allergic reactions when consumed as food (Ji et al., 2008; Choi et al., 2010). Thus, allergens likely exist at different developmental stages of the silkworm lifecycle; however, it is not clear whether these allergens are the same protein.
Silkworm pupae are consumed raw, boiled, and fried in several Asian countries. Allergic reactions after consuming silkworm pupae include urticaria, dizziness, skin itching, and shock (Feng et al., 2018). In China, many cases of silkworm pupae‐induced allergies have been reported. Each year, at least 1,000 patients have anaphylactic reactions after eating silkworm (Ji et al., 2008). In Korea, 9.4% of patients were found to be allergic to silkworm pupae (Kim et al., 2003). In East Asia, allergic reactions to eating silkworm pupae are considered a common cause of anaphylaxis (van der Poel & Chen, 2009). However, allergic reactions caused by silkworm pupae are no more serious than those caused by conventional foods, such as shrimp and fish (de Gier & Verhoeckx, 2018). Because silkworm pupae are being increasingly incorporated into the daily human diet, the mechanisms driving these allergic reactions need to be elucidated.
4.2. Allergens present in silkworm pupae
To date, 26 silkworm pupae proteins have been identified as allergens (Table 3). The only protein characterized as an allergen in silkworm larvae was an arginine kinase, which cross‐reacted with an arginine kinase in cockroaches (Liu, Wu, et al., 2009; Liu, Xia, et al., 2009). However, except for this arginine kinase (officially named Bomb m 1) (Liu, Wu, et al., 2009; Liu, Xia, et al., 2009), no allergens of silkworm pupae have been officially confirmed and registered by the WHO and International Union of Immunological Societies (WHO/IUIS) Allergen Nomenclature Sub‐committee (www.allergen.org). Five allergen proteins belong to lipoprotein 11 family (30‐kDa family proteins), while three are insect cuticle proteins (Table 3). The other proteins belong to different protein families. According to the WHO/IUIS Allergen Nomenclature Sub‐committee, proteins reported as allergens in other species include heat shock protein, paramyosin, chitinase, profilin, triosephosphate isomerase, and vitellogenin.
TABLE 3.
Allergen | Molecular weight (KDa/PI) | Identification method | GI No | Family | Reference |
---|---|---|---|---|---|
Juvenile hormone epoxy hydrolase | 52.36/6.08 | WB | 255977192 | Abhydrolase 1 superfamily | (Jeong et al., 2016) |
Cell differentiation protein | 32.17/7.06 | WB | 290760296 | Cell differentiation family | (Jeong et al., 2016) |
Chitinase precursor | 61.52/5.78 | WB | 29467722 | Chitinase A N | (Zhao et al., 2015) |
27‐kDa glycoprotein | 24.89/5.12 | WB/ELISA | 19911074 | DUF1397 | (Jeong et al., 2016) |
Cuticular protein RR−2 motif 63 precursor | 18.5/6.61 | WB | 290563229 | Insect cuticle protein | (Liang et al., 2016) |
Putative cuticle protein | 45.68/4.14 | WB | 223671172 | Insect cuticle protein | (Jeong et al., 2016) |
Putative cuticle protein | 28,28/4.63 | WB | 19911074 | Insect cuticle protein | (Jeong et al., 2016) |
Chemosensory protein 5 precursor | 14.26/6.89 | WB/ELISA | 112983054 | Insect pheromone‐binding family | (Ma et al., 2016) |
Cellular retinoic acid binding protein | 14.86/5.66 | WB | 112983600 | Lipocalin/cytosolic fatty acid binding protein | (Liang et al., 2016) |
30‐kDa protein precursor | 29.39/unknown | WB/Murine model of asthma | 112984502 | Lipoprotein 11 | (Zuo et al., 2015) |
30‐kDa lipoprotein precursor | 30/unknown | WB | 154201552 | Lipoprotein 11 | (Cao et al., 2017) |
Mature 30‐kDa lipoprotein | 28.55/6.37 | WB | 1335608 | Lipoprotein 11 | (Zuo et al., 2015) |
LOC114242470 low molecular mass 30‐kDa lipoprotein 21G1 | 30.34/6.33 | WB | 266439 | Lipoprotein 11 | (Zuo et al., 2015) |
Low molecular mass 30‐kDa lipoprotein 19 G1 precursor | 29.65/6.9 | WB | 266438 | Lipoprotein 11 | (Zuo et al., 2015) |
Heat shock protein 20.8 | 20.8/unknown | WB/ELISA | 148298693 | Metazoan ACD (Alpha‐crystallin domain of metazoan) | (Zuo et al., 2015) |
Paramyosin | 10.28/5.43 | WB | 195963325 | Myosin tail 1 | (Zhao et al., 2015) |
Thiol peroxiredoxin | 22/unknown | WB/ELISA/Murine model of asthma | 112982996 | Peroxiredoxin (PRX) family | (Wang et al., 2016) |
AGAP008849‐PA | 35.88/8.09 | WB | 58392734 | Phosphoglycerate dehydrogenases | (Zuo et al., 2015) |
Xanthine dehydrogenase | 147.63/6.38 | WB | 13936381 | PLN02906 superfamily | (Jeong et al., 2016) |
Profilin | 14/unknown | WB | 118500453 | Profilin | (Hu et al., 2017) |
Triosephosphate isomerase | 26.93/5.67 | WB | 125987,66 | PTZ00333 | (Zuo et al., 2015) |
Chymotrypsin inhibitor CI‐8A | 43.91/5.2 | WB | 14028769 | Serpin | (Zuo et al., 2015) |
Tropomyosin | 40/unknown | WB | 195963325 | Tropomyosin | (Liu et al., 2009) |
Uncharacterized protein LOC101743840 | 33/6.76 | WB | 1200729467 | unknown | (Liang et al., 2017) |
Cuticular protein hypothetical 30 | 25/unknown | WB | 290560816 | unknown | (Hu et al., 2016) |
Vitellogenin | 20.35/7.07 | WB | 32526658 | Vitellogenin N | (Zuo et al., 2015) |
Abbreviation: WB, Western blot analysis.
Heat shock protein, tropomyosin, chitinase, and triosephosphate isomerase are also allergens of house dust mites; their official names are Der f 10, Der f 11, Der f 15, and Der f 25, respectively. The National Center for Biotechnology Information (www.ncbi.nlm.nih.gov) showed that the sequence homologies of amino acids in silkworm pupae and house dust mites are 30.77%, 81.94%, 28.33%, and 71.77% for heat shock protein, tropomyosin, chitinase, and triosephosphate isomerase, respectively. Tropomyosin is a well‐known invertebrate pan‐allergen and is a major allergen of crustaceans, house dust mites, cockroaches, and moths (Ivanciuc et al., 2009). Arginine kinase is another well‐known invertebrate pan‐allergen. It is an enzyme found in insects and crustaceans, belonging to the guanidino phosphotransferase family (Azzi et al., 2004). However, arginine kinase has been reported as an allergen of silkworm larvae, but not of silkworm pupae. Wang and Xu (2006) showed that the gene for arginine kinase is also expressed in pupae at a relatively low level, with expression increasing as larvae mature. Thus, studies are needed to examine the allergenicity of arginine kinase in silkworm pupae. Vitellogenin is an allergen of the honey bee (Api m 12), chum salmon (Onc k 5), and yellow jacket (Ves v 6). Profilin is a pan‐allergen (McKenna et al., 2016). The homology of arginine kinases and tropomyosins from different insect species is greater than 70%, while that of other allergenic proteins ranges from 35% to 95%. This phenomenon might induce cross‐reactive reactions between proteins from different insect species and from crustaceans, such as shrimp (de Gier & Verhoeckx, 2018). Thus, the allergens of some silkworm pupae have high homology and structural similarity with those from other species, with cross‐reactive potential. Cross reactions between invertebrate proteins are usually attributed to homologous allergens (Marti et al., 2007). Silkworms belong to the phylum Arthropoda, which includes crustaceans. A comparative proteomic study showed that some pupae proteins are differentially expressed when comparing gender and diet of silkworm larvae (Lamberti et al., 2019). Of note, the levels of known allergens in female silkworm pupae reared on mulberry leaves were lower compared to those reared under other experimental conditions (Lamberti et al., 2019). Thus, the allergen profile of silkworm pupae could be associated with gender and diet and so could be regulated.
In recent years, there has been extensive research to minimize food allergenicity in technical food processing. However, only the 27‐kDa hemolymph glycoprotein has been identified as a heat‐stable allergen in silkworm pupae (Jeong et al., 2016). Knowledge remains limited on how food processing affects the allergenic potential of proteins in silkworm pupae. Methods to minimize allergens in silkworm pupae need to be developed. In the food industry, only hydrolysis and fermentation have achieved a satisfactory reduction in food allergenicity (Lepski & Brockmeyer, 2013; Verhoeckx et al., 2015). These processes might have similar effects on silkworm pupae. Enzymatic hydrolysis represents a promising processing technology for exploiting the bioactive properties of silkworm pupae. This process might also represent an effective means of minimizing allergenicity. Through understanding the structure–allergenicity relationship of allergens in silkworm pupae, effective methods to process hypoallergenic proteins could be developed. Further studies are required to characterize the immunological properties of allergens in silkworm pupae.
5. PERSPECTIVES AND CONCLUSIONS
The silkworm is an insect that can be produced at a large scale. After extracting the silk thread, silkworm pupae are a subproduct of the textile industry. These pupae are rich in nutrients and have high value. The potential uses of silkworm pupae have attracted increasing research interest. Many studies have shown that silkworm pupae are a good source of nutrients for humans, with various potential functions. Although silkworm pupae have many benefits for humans, consumer acceptance remains low, especially in Western countries. Good cooking methods could promote the consumption of insects as food (Feng et al., 2018). Furthermore, the incorporation of insects into everyday food items is a documented strategy that overcomes the challenges associated with the low acceptance of insects as food (Khatun et al., 2021; Bawa et al., 2020; Nyangena et al., 2020). For instance, consuming protein powder and hydrolyzed peptides in a food product might be more acceptable than direct consumption.
However, developing silkworm pupae as a food source requires an effective risk assessment of potential allergenic hazards. Evaluation of the allergies of silkworm pupae is scarce and is primarily based on case reports without the consistent use of standardized tests. Overall, 26 silkworm pupae proteins have been identified as allergens; however, their immunological properties remain poorly characterized.
Potential strong cross reactions of silkworm pupae allergens should be carefully examined. Large‐scale investigations of such cross‐reactions are required. The detection, labeling, and elimination of silkworm pupae allergens is needed to combat allergic reactions. Thus, the allergens present in silkworm pupae, and the mechanisms by which they cause allergic reactions, must be fully elucidated.
CONFLICT OF INTEREST
The authors declared they do not have any conflict of interest.
AUTHOR CONTRIBUTIONS
Xuli Wu: Conceptualization (lead); Funding acquisition (lead); Methodology (lead); Project administration (lead); Resources (lead); Supervision (lead); Validation (lead); Visualization (lead); Writing‐original draft (equal); Writing‐review & editing (lead). Kan He: Investigation (lead); Writing‐original draft (equal). Tanja Cirkovic Velickovic: Conceptualization (equal); Writing‐original draft (equal). Zhigang Liu: Resources (equal); Writing‐original draft (equal).
ETHICAL APPROVAL
This study does not involve any human or animal testing.
ACKNOWLEDGEMENTS
This study was supported in part by the Key‐Area Research and Development Program of Guangdong Province (2019B020213001), Research Funding for Innovation Project of Universities in Guangdong Province (2018KTSCX192), and Research Funding of Shenzhen (JCYJ201803053000708). The authors acknowledge support from the Ministry of Education, Science and Technological Development, GA No. 451‐03‐68/2020‐14/200168.
Wu, X., He, K., Velickovic, T. C., & Liu, Z. (2021). Nutritional, functional, and allergenic properties of silkworm pupae. Food Science & Nutrition, 9, 4655–4665. 10.1002/fsn3.2428
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available on request from the corresponding author.
REFERENCES
- Ahn, M. Y., Shim, S. H., Jeong, H. K., & Ryu, K. S. (2008). Purification of a dimethyladenosine compound from silkworm pupae as a vasorelaxation substance. Journal of Ethnopharmacol, 117, 115–122. 10.1016/j.jep.2008.01.031 [DOI] [PubMed] [Google Scholar]
- Araujo, L. M., Filho, N. A. R., & Riedi, C. A. (2014). Respiratory allergy to moth: The importance of sensitization to Bombyx mori in children with asthma and rhinitis. Journal of Pediatrics (Rio J), 90(2), 176–181. 10.1016/j.jpedp.2013.08.002 [DOI] [PubMed] [Google Scholar]
- Azzi, A., Clark, S. A., Ellington, W. R., & Chapman, M. S. (2004). The role of phosphagen specificity loops in arginine kinase. Protein Science, 13, 575–585. 10.1110/ps.03428304 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Battampara, P., Sathish, T. N., Reddy, R., Guna, V., Nagananda, G. S., Reddy, N., Ramesha, B. S., Maharaddi, V. H., Rao, A. P., Ravikumar, H. N., Biradar, A., & Radhakrishna, P. G. (2020). Properties of chitin and chitosan extracted from silkworm pupae and egg shells. International Journal of Biological Macromolecules, 161, 1296–1304. 10.1016/j.ijbiomac.2020.07.161 [DOI] [PubMed] [Google Scholar]
- Bawa, M., Songsermpong, S., Kaewtapee, C., & Chanput, W. (2020). Effects of microwave and hot air oven drying on the nutritional, microbiological load, and color parameters of the house crickets (Acheta domesticus). Journal Food Processing and Preservation, 44, 1‐12. [Google Scholar]
- Blanc, P. D., Eisner, M. D., Israel, L., & Yelin, E. H. (1999). The association between occupation and asthma in general medical practice. Chest, 115(5), 1259–1264. 10.1378/chest.115.5.1259 [DOI] [PubMed] [Google Scholar]
- Borelli, S., Stern, A., & Wüthrich, B. A. (1999). Silk cardigan inducing asthma. Allergy, 54, 892–902. 10.1034/j.1398-9995.1999.00280.x [DOI] [PubMed] [Google Scholar]
- Cao, H., Cai, D. F., Yang, P. C., Liu, Z. G., & Xia, L. X. (2017). Expression and immunological identification of MBP‐Bmlp7 from Bombyx mori. Journal of Shenzhen University Science and Engineering, 34(2), 117–121. 10.3724/SP.J.1249.2017.02117 (Article in Chinese) [DOI] [Google Scholar]
- Chen, J., Zheng, M. Z., & Wang, H. (2009). Development of a sports beverage of silkworm pupa protein peptide. Food Science, 30(14), 318–320. 10.1360/972009-1551 (Article in Chinese) [DOI] [Google Scholar]
- Choi, G. S., Shin, Y. S., Kim, J. E., Ye, Y. M., & Park, H. S. (2010). Five cases of food allergy to vegetable worm (Cordyceps sinensis) showing cross‐reactivity with silkworm pupae. Allergy, 65(9), 1196–1197. 10.1111/j.1398-9995.2009.02300.x [DOI] [PubMed] [Google Scholar]
- de Castro, R. J. S. , Ohara, A., Aguilar, J. G. D. S., & Domingues, M. A. F. (2018). Nutritional, functional and biological properties of insect proteins: Processes for obtaining, consumption and future challenges. Trends in Food Science & Technology, 76, 82–89. 10.1016/j.tifs.2018.04.006 [DOI] [Google Scholar]
- de Gier, S. , & Verhoeckx, K. (2018). Insect (food) allergy and allergens. Molecular Immunology, 100, 82–106. 10.1016/j.molimm.2018.03.015 [DOI] [PubMed] [Google Scholar]
- Deori, M., Boruah, D. C., Devi, D., & Devi, R. (2014). Antioxidant and antigenotoxic effects of pupae of the muga silkworm antheraea assamensis. Food Bioscience, 5, 108–114. 10.1016/j.fbio.2013.12.001 [DOI] [Google Scholar]
- Dong, Y. P., & Wu, Q. Y. (2010). Research status of development and utilization for silkworm chrysalis protein. Academic Periodical of Farm Products Processing, 211, 17–20. 10.3969/j.issn.1671-9646(X).2010.06.005 (Article in Chinese) [DOI] [Google Scholar]
- Food and Agriculture Organization of the United Nations (FAO) (2013). Edible insects. Future prospects for food and feed security, Vol. 171. Food and Agriculture Organization of the United Nations. [Google Scholar]
- Food and Agriculture Organization of the United Nations (FAO)/World Health Organization(WHO) (1985). Energy & protein requirements. WHO Technical Report Series No. 724. World Health Organization. [Google Scholar]
- Feng, Y., Chen, X. M., Zhao, M., He, Z., Sun, L., Wang, C. Y., & Ding, D. F. (2018). Edible insects in China: Utilization and prospects. Insect Science, 25(2), 184–198. 10.1111/1744-7917.12449 [DOI] [PubMed] [Google Scholar]
- Gautreau, M., Restuccia, M., Senser, K., & Weisberg, S. N. (2017). Familial anaphylaxis after silkworm ingestion. Prehospital Emergency Care, 21(1), 83–85. 10.1080/10903127.2016.1204035 [DOI] [PubMed] [Google Scholar]
- Govorushko, S. (2019). Global status of insects as food and feed source: A review. Trends in Food Science & Technology, 91, 436–445. 10.1016/j.tifs.2019.07.032 [DOI] [Google Scholar]
- Häcki, M., Wüthrich, B., & Hanser, M. (1982). Wild silk: A strong inhalation allergen. Deutsche Medizinische Wochenschrift, 107(5), 166‐169. 10.1055/s-2008-1069892 (Article in German) [DOI] [PubMed] [Google Scholar]
- Han, R., Shin, J. T., Kim, J., Choi, Y. S., & Kim, Y. W. (2017). An overview of the South Korean edible insect food industry: Challenges and future pricing/promotion strategies. Entomological Research, 47, 141–151. 10.1111/1748-5967.12230 [DOI] [Google Scholar]
- Hu, D. C., Liu, Q., Wang, H., Cui, H. R., Han, D. X., & Xu, H. B. (2004). Apoptosis of human hepatoma cells SMMC‐7721 induced by selenium‐abundant amino acids from silkworm pupa. Chinese Pharmacological Bulletin, 20(11), 1287–1292. 10.1016/S0898-6568(03)00096-2 (Article in Chinese) [DOI] [Google Scholar]
- Hu, J. L., & Chen, W. P. (2011). Effect of silkworm chrysalis oil on apoprotein and lipid‐metabolizedenzyme level in hyperlipidemia rats. Chinese Traditional and Herbal Drugs, 42(02), 300–306. 10.1088/1009-0630/13/1/25 (Article in Chinese) [DOI] [Google Scholar]
- Hu, W., Liang, Z. L., Wang, L. L., & Liu, Z. G. (2016). Expression, purification, immunological identification and B cell epitope analysis of allergen CPH30 in silkworm (Bombyx mori) pupae. Acta Entomologica Sinica, 59(04), 377–381. 10.16380/j.kcxb.2016.04.002 (Article in Chinese) [DOI] [Google Scholar]
- Hu, W., Liang, Z. L., Wang, L. L., Zhong, H. L., & Liu, Z. G. (2017). Expression, purification and bioimformatics analysis of allergen protein profilin from silkworm (Bombyx mori). Immunology Journal of Chinese, 33(01), 81–84. 10.3969/j.issn.1000-484X.2017.01.016 (Article in Chinese) [DOI] [Google Scholar]
- Inoue, A., Ishido, I., Shoji, A., & Yamada, H. (1997). Textile dermatitis from silk. Contact Dermatitis, 37(4), 185–187. 10.1111/j.1600-0536.1997.tb00199.x [DOI] [PubMed] [Google Scholar]
- Ivanciuc, O., Garcia, T., Torres, M., Schein, C. H., & Braun, W. (2009). Characteristic motifs for families of allergenic proteins. Molecular Immunology, 46, 559–568. 10.1016/j.molimm.2008.07.034 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jeong, K. Y., Son, M., Lee, J. Y., Park, K. H., Lee, J., & Park, J. (2016). Allergenic characterization of 27‐kDa glycoprotein, a novel heat stable allergen, from the pupa of Silkworm, Bombyx mori . Journal of Korean Medical Science, 31(1), 18–24. 10.3346/jkms.2016.31.1.18 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ji, K. M., Zhan, Z. K., Chen, J. J., & Liu, Z. G. (2008). Anaphylactic shock caused by silkworm pupa consumption in China. Allergy, 63(10), 1407‐1408. 10.1111/j.1398-9995.2008.01838.x [DOI] [PubMed] [Google Scholar]
- Capinera, J. L., & Finke, M. D. (2008). Nutrient content of insects. Encyclopedia of Entomology [M]. Springer. 10.1007/978-1-4020-6359-6_2274 [DOI] [Google Scholar]
- Khatun, H., Claes, J., Smets, R., De Winne, A., Akhtaruzzaman, M., & Van Der Borght, M. (2021). Characterization of freeze‐dried, oven‐dried and blanched house crickets (Acheta domesticus) and Jamaican field crickets (Gryllus assimilis) by means of their physicochemical properties and volatile compounds. European Food Research and Technology, 247, 343‐352. 10.1007/s00217-021-03709-x [DOI] [Google Scholar]
- Kim, H. W., Setyabrata, D., Lee, Y. J., Jones, O. G., & Kim, Y. H. B. (2016). Pre‐treated mealworm larvae and silkworm pupae as a novel protein ingredient in emulsion sausages. Innovative Food Science & Emerging Technologies, 38(Part, A), 116–123. 10.1111/j.1398-9995.2008.01838.x [DOI] [Google Scholar]
- Kim, S. H., Kang, H. R., Kim, K. M., Kim, T. B., Kim, S. S., Chang, Y. S., Kim, C. W., Bahn, J. W., Kim, Y. K., Cho, S. H. et al (2003). The sensitization rates of food allergens in a Korean population: A multi‐center study. Journal of Asthma, 23, 502–514. [Google Scholar]
- Kim, S. A., Kim, K. M., & Oh, B. J. (2008). Current status and perspective of the insect industry in Korea. Entomological Research, 38, S79–S85. 10.1111/j.1748-5967.2008.00178.x [DOI] [Google Scholar]
- Köhler, R., Kariuki, L., Lambert, C., & Biesalski, H. K. (2019). Protein, amino acid and mineral composition of some edible insects from Thailand. Journal of Asia‐Pacific Entomology, 22(1), 372–378. 10.1016/j.aspen.2019.02.002 [DOI] [Google Scholar]
- Konwar, P., Konwar, B. K., Ahmed, H. F., Nath, N. C., & Ghosh, M. K. (2008). Effect of feeding silkworm pupae meal with enzyme supplementation on growth performance of broilers. Indian Veterinary Journal, 85(1), 47–49. 10.1016/j.fsi.2007.08.004 [DOI] [Google Scholar]
- Kotake‐Nara, E., Yamamoto, K., Nozawa, M., Miyashita, K., & Murakami, T. (2002). Lipid profiles and oxidative stability of silkworm pupal oil. Journal of Oleo Science, 51(11), 681–690. 10.5650/jos.51.681 [DOI] [Google Scholar]
- Kouřimská, L., & Adámková, A. (2016). Nutritional and sensory quality of edible insects. Journal of Nutrition and Food Security, 4, 22–26. 10.1016/j.nfs.2016.07.001 [DOI] [Google Scholar]
- Kwon, M. G., Kim, D. S., Lee, J. H., Park, S. W., Choo, Y. K., Han, Y. S., Kim, J. S., Hwang, K. A., Ko, K., & Ko, K. (2012). Isolation and analysis of natural compounds from silkworm pupae and effect of its extracts on alcohol detoxification. Entomological Research, 42(1), 55–62. 10.1111/j.1748-5967.2011.00439.x [DOI] [Google Scholar]
- Lamberti, C., Gai, F., Cirrincione, S., Giribaldi, M., Purrotti, M., Manfredi, M., Marengo, E., Sicuro, B., Saviane, A., Cappellozza, S., Giuffrida, M. G., & Cavallarin, L. (2019). Investigation of the protein profile of silkworm (Bombyx mori) pupae reared on a well‐calibrated artificial diet compared to mulberry leaf diet. Peer Journal, 7, e6723. 10.7717/peerj.6723 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee, H. S., Lee, H. J., & Suh, H. J. (2011). Silk protein hydrolysate increases glucose uptake through up‐regulation of GLUT 4 and reduces the expression of leptin in 3T3‐L1 fibroblast. Nutrition Research, 1(12), 937–943. 10.1016/j.nutres.2011.09.009 [DOI] [PubMed] [Google Scholar]
- Lee, S. H., Park, D., Yang, G., Bae, D. K., Yang, Y. H., Kim, T. K., Kim, D., Kyung, J., Yeon, S., Koo, K. C., Lee, J. Y., Hwang, S. Y., Joo, S. S., & Kim, Y. B. (2012). Silk and silkworm pupa peptides suppress adipogenesis in preadipocytes and fat accumulation in rats fed a high‐fat diet. European Journal of Nutrition, 51(8), 1011–1019. 10.1007/s00394-011-0280-6 [DOI] [PubMed] [Google Scholar]
- Lepski, S., & Brockmeyer, J. (2013). Impact of dietary factors and food processing on food allergy. Molecular Nutrition & Food Research, 57(1), 145–152. 10.1002/mnfr.201200472 [DOI] [PubMed] [Google Scholar]
- Li, G. Y., Cui, T. B., & Chen, L. (2011). Preliminary study of enzymatic hydrolysis of silkworm pupa protein for production of antioxidant peptide. Modern Food Science & Technology, 27(7), 810–814. 10.13982/j.mfst.1673-9078.2011.07.015 (Article in Chinese) [DOI] [Google Scholar]
- Li, X. D., Xie, H. Q., Chen, Y. J., Lang, M. Z., Chen, Y. Y., & Shi, L. G. (2018). Silkworm pupa protein hydrolysate induces mitochondria‐dependent apoptosis and s phase cell cycle arrest in human gastric cancer SGC‐7901 cells. International Journal of Molecular Sciences, 19(4), 1013. 10.3390/ijms19041013 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li, Z. Y., Zhao, S., Xin, X. D., Zhang, B., Thomas, A., Charles, A., Lee, K. S., Jin, B. R., & Gui, Z. Z. (2019). Purification and characterization of a novel immunomodulatory hexapeptide from alcalase hydrolysate of ultramicro‐pretreated silkworm (Bombyx mori) pupa protein. Journal of Asia‐Pacific Entomology, 22(3), 633–637. 10.1016/j.aspen.2019.04.005 [DOI] [Google Scholar]
- Liang, Z. L., Li, P., Liu, Z. G., & Liu, X. Y. (2016). Clone, expression, purification, immunological identification and bioinformatics analysis of allergen cuticular protein RR‐2 motif 63 precursor (CPR63) of silkworm (Bombyx mori) pupae. Immunological Journal, 32(7), 565–569. 10.13431/j.cnki.immunol.j.20160110 (Article in Chinese) [DOI] [Google Scholar]
- Liang, Z. L., Liu, X. Y., Liu, Z. G., & Chen, X. X. (2017). Purification, immunological identification and bioinformatics study of gene: LOC101743840 from Bombyx mori pupae. China Tropical Medicine, 17(7), 641–645. 10.13604/j.cnki.46-1064/r.2017.07.01 (Article in Chinese) [DOI] [Google Scholar]
- Liang, Z. L., Wang, H., Hu, W., Liu, Z. G., & Liu, X. Y. (2016). Cloning, expression and bioinformatics analysis of cellular retinoic acid binding protein (CRABP) in silkworm, Bombyx mori. Journal of Nanchang University (Medical Sciences), 56(5), 15–23. 10.13764/j.cnki.ncdm.2016.05.005 (Article in Chinese) [DOI] [Google Scholar]
- Liu, J. Y., Tao, Q. P., Sun, J. H., Tian, L. Y., & Huang, Y. B. (2010). Effect of oak silkworm chrysalis polypeptide solution on mouse immunity. North Sericulture, 31(2), 10–12. 10.19443/j.cnki.1673-9922.2010.02.004 (Article in Chinese) [DOI] [Google Scholar]
- Liu, Z. G., Wu, Y. L., Yang, R., & Wu, H. Q. (2009). Cloning, expression, and purification of silkworm (Bombyx mori) tropom yosin gene and identifying its immunological characteristics. Journal of Immunology, 25(06), 655–658. 10.13431/j.cnki.immunol.j.20090173 (Article in Chinese) [DOI] [Google Scholar]
- Liu, Z., Xia, L., Wu, Y., Xia, Q., Chen, J., & Roux, K. H. (2009). Identification and characterization of an arginine kinase as a major allergen from silkworm (Bombyx mori) larvae. International Archives of Allergy and Immunology, 150(1), 8–14. 10.1159/000210375 [DOI] [PubMed] [Google Scholar]
- Longvah, T., Manghtya, K., & Qadri, S. S. (2012). Eri silkworm: A source of edible oil with a high content of α‐linolenic acid and of significant nutritional value. Journal of the Science of Food and Agriculture, 92(9), 1988–1993. 10.1002/jsfa.5572 [DOI] [PubMed] [Google Scholar]
- Longvah, T., Mangthya, K., & Ramulu, P. (2011). Nutrient composition and protein quality evaluation of eri silkworm (Samia ricinii) prepupae and pupae. Food Chemistry, 128(2), 400–403. 10.1016/j.foodchem.2011.03.041 [DOI] [PubMed] [Google Scholar]
- Lu, N., Mao, K., Liao, X. Y., Weng, X. C., Song, H. S., & Huang, J. Y. (2013). Antioxidant and immune effect of silkworm pupa peptides in D‐gal‐induced aging mice. Science and Technology of Food Industry, 34(12), 331–334. 10.13386/j.issn1002-0306.2013.12.012 (Article in Chinese) [DOI] [Google Scholar]
- Luo, F. Y., Ning, X. L., Wu, G. Z., Li, B. X., Li, Y. Y., & He, J. F. (2010). Study on antiseptic antibacterial effect of natural antimicrobial peptides from silkworm pupa on the fresh pork. Science and Technology of Food Industry, 3, 117–118. 10.13386/j.issn1002-0306.2010.03.046 (Article in Chinese) [DOI] [Google Scholar]
- Ma, Y. H., Hu, W., Liang, Z. L., Wang, H., & Liu, Z. G. (2016). Immunologica and bioinformatics analysis of a recombinant allergen of silkworm CSP5. Courrent Immunlolgy, 36(6), 466–470. CNKI:SUN:SHMY.0.2016‐06‐005 (Article in Chinese) [Google Scholar]
- Marti, P., Truffer, R., Stadler, M. B., Keller‐Gautschi, E., Crameri, R., Mari, A., Schmid‐Grendelmeier, P., Miescher, S. M., Stadler, B. M., & Vogel, M. (2007). Allergen motifs and the prediction of allergenicity. Immunology Letter, 109, 47–55. 10.1016/j.imlet.2007.01.002 [DOI] [PubMed] [Google Scholar]
- McKenna, O. E., Asam, C., Araujo, G. R., Roulias, A., Goulart, L. R., & Ferreira, F. (2016). How relevant is panallergen sensitization in the development of allergies. Pediatric Allergy & Immunology, 27(6), 560–568. 10.1111/pai.12589 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Min, J. H., Li, J. K., & Chen, T. (2009). Preparation and antioxidant activity in vitro of ailkworm pupa polypeptide. Food Science, 30(14), 123–126. 10.1001/jama.1937.02780520028007 (Article in Chinese) [DOI] [Google Scholar]
- Mishraa, N., Hazarikaa, N. C., Naraina, K., & Mahanta, J. (2003). Nutritive value of non‐mulberry and mulberry silkworm pupae and consumption pattern in Assam. India. Nutrition Research, 23(10), 1303–1311. 10.1016/S0271-5317(03)00132-5 [DOI] [Google Scholar]
- Mlcek, J., Borkovcova, M., Rop, O., & Bednarova, M. (2014). Biologically active substances of edible insects and their use in agriculture, veterinary and human medicine‐a review. Journal of Central European Agriculture, 15(4), 225–237. 10.5513/JCEA01/15.4.1533 [DOI] [Google Scholar]
- National Standardization Management Committee of China . (2005). Maximum levels of contaminants in foods (pp. 2–4). Standard Press of China. [Google Scholar]
- Ni, H., Chen, H. X., & Yang, Y. Y. (2003). The technology of the comprehensive utilization of oak silkworm pupae. Journal of Hubei University (Natural Science Edition), 25(3), 263–266. 10.3969/j.issn.1000-2375.2003.03.018 (Article in Chinese) [DOI] [Google Scholar]
- Ni, H., Chen, H. X., Yang, Y. Y., & Tao, L. (1998). Studies on extraction and preparation technique of silkworm chrysalis (Bombyx mori L.) pupa chitin and chitosan. Journal of Hubei University (Natural Science Edition), 20(1), 94–96. CNKI:SUN:HDZK.0.1998‐01‐021 (Article in Chinese) [Google Scholar]
- Nowak, V., Persijn, D., Rittenschober, D., & Charrondiere, U. R. (2016). Review of food composition data for edible insects. Food Chemistry, 193, 39–46. 10.1016/j.foodchem.2014.10.114 [DOI] [PubMed] [Google Scholar]
- Nyangena, D. N., Mutungi, C., Imathiu, S., Kinyuru, J., Affognon, H., Ekesi, S., Nakimbugwe, D., & Fiaboe, K. K. M. (2020). Effects of traditional processing techniques on the nutritional and microbiological quality of four edible insect species used for food and feed in East Africa. Foods, 9, 1‐16. 10.3390/foods9050574 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohansson, S. G., Wüthrich, B., & Zortea‐Caflisch, C. (1985). Nightly asthma caused by allergens in silk‐filled bed quilts: Clinical and immunologic studies. Journal of Allergy and Clinical Immunology, 75(4), 452–459. 10.1016/S0091-6749(85)80017-8 [DOI] [PubMed] [Google Scholar]
- Omotoso, O. T. (2015). An Evaluation of the nutrients and some anti‐Nutrients in silkworm, Bombyx mori L. (Bombycidae: Lepidoptera). Jordan Journal of Biological Sciences, 8(1), 45–50. 10.12816/0026947 [DOI] [Google Scholar]
- Pali‐Schöll, I., Verhoeckx, K., Mafra, I., Bavaro, S. L., Clare Mills, E. N., & Monaci, L. (2019). Allergenic and novel food proteins: State of the art and challenges in the allergenicity assessment. Trends in Food Science & Technology, 84, 45–48. 10.1016/j.tifs.2018.03.007 [DOI] [Google Scholar]
- Payne, C. L. R., Scarborough, P., Rayner, M., & Nonaka, K. (2016). A systematic review of nutrient composition data available for twelve commercially available edible insects, and comparison with reference values. Trends in Food Science & Technology, 47, 69–77. 10.1016/j.tifs.2015.10.012 [DOI] [Google Scholar]
- Pereira, N. R., Ferrarese‐Filho, O., Matsushita, M., & de Souza, N. E. (2003). Proximate composition and fatty acid profile of Bombyx mori L. chrysalis toast. Journal of Food Composition and Analysis, 24(2), 18–19. 10.1016/S0889-1575(03)00016-4 [DOI] [Google Scholar]
- Qi, Y. X., Meng, J., Cao, B. Y., Fei, B. L., & Wen, Q. L. (2009). Immunoregulation functions of pupa polypeptides in mice. Food Science, 30(23), 419–421. 10.1007/978-3-540-85168-4_52 (Article in Chinese) [DOI] [Google Scholar]
- Rahimnejad, S., Hu, S., Song, K., Wang, L., Lu, K., Wu, R., & Zhang, C. (2019). Replacement of fish meal with defatted silkworm (Bombyx mori L.) pupae meal in diets for pacific white shrimp (Litopenaeus vannamei). Aquaculture, 510, 150–159. 10.1016/j.aquaculture.2019.05.054 [DOI] [Google Scholar]
- Rao, P. U. (1994). Chemical composition and nutritional evaluation of spent silk worm pupae. Journal of Agricultural & Food Chemistry, 42, 2201–2203. 10.1021/jf00046a023 [DOI] [Google Scholar]
- Ratcliffe, N. A., Mello, C. B., Garcia, E. S., Butt, T. M., & Azambuja, P. (2011). Insect natural products and processes: New treatments for human disease. Insect Biochemistry and Molecular Biology, 41(10), 747–769. 10.1016/j.ibmb.2011.05.007 [DOI] [PubMed] [Google Scholar]
- Ryu, S. P. (2014). Silkworm pupae powder ingestion increases fat metabolism in swim‐trained rats. Journal of Exercise Nutrition and Biochemistry, 18(2), 141. 10.5717/jenb.2014.18.2.141 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shanker, K. S., Shireesha, K., Kanjilal, S., Kumar, S. V., Srinivas, C., Rao, J. V., & Prasad, R. B. (2006). Isolation and characterization of neutral lipids of desilked eri silkworm pupae grown on castor and tapioca leaves. Journal of Agricultural and Food Chemistry, 54(9), 3305–3309. 10.1021/jf060581x [DOI] [PubMed] [Google Scholar]
- Sun, Y., Chang, A. K., Wen, Z., Li, Y., Du, X., & Li, S. (2014). Effect of replacing dietary fish meal with silkworm (Bombyx moril) caterpillar meal on growth and non‐specific immunity of sea cucumber Apostichopus japonicus (Selenka). Aquaculture Research, 45(7), 1246–1252. 10.1111/are.12068 [DOI] [Google Scholar]
- Suzuki, M., Itoh, H., Sugiyama, K., Takagi, I., Nishimura, J., Kato, K., Mamiya, S., Baba, S., Ohya, Y., Itoh, H., Yokota, A., Itoh, M., & Ohta, N. (1995). Causative allergens of allergic rhinitis in Japan with special reference to silkworm moth allergen. Allergy, 50(1), 23–27. 10.1111/j.1398-9995.1995.tb02479.x [DOI] [PubMed] [Google Scholar]
- van der Poel, L. , & Chen, J. (2009). Food allergy epidemic ‐is it only a western phenomenon? Current Opinion in Allergy and Clinical Immunology, 22, 121–126. [Google Scholar]
- Verhoeckx, K. C. M., Vissers, Y. M., Baumert, J. L., Faludi, R., Feys, M., Flanagan, S., Herouet‐Guicheney, C., Holzhauser, T., Shimojo, R., van der Bolt, N. , Wichers, H., & Kimber, I. (2015). Food processing and allergenicity. Food and Chemical Toxicology, 80, 223–240. 10.1016/j.fct.2015.03.005 [DOI] [PubMed] [Google Scholar]
- Vovolis, V., & Galatas, L. (1999). Silk‐induced asthma. Allergy & Asthma Proceedings, 2(20), 107–108. 10.2500/108854199778612626 [DOI] [PubMed] [Google Scholar]
- Wang, G. J., Yin, W. F., Wang, J., Tang, J. L., & Huang, Y. P. (2007). Effect of polysaccharide of silkworm pupa on immunological function in mice. Journal of Jiangsu University (Medicine Edition), 17(5), 373–375. 10.13312/j.issn.1671-7783.2007.05.001 (Article in Chinese) [DOI] [Google Scholar]
- Wang, H., Hu, W., Liang, Z., Zeng, L., Li, J., Yan, H., Yang, P., Liu, Z., & Wang, L. (2016). Thiol peroxiredoxin, a novel allergen from Bombyx mori, modulates functions of macrophages and dendritic cells. American Journal of Translational Research, 8(12), 5320–5329. ISSN:1943‐8141/AJTR0030512 [PMC free article] [PubMed] [Google Scholar]
- Wang, H. B., & Xu, Y. S. (2006). cDNA cloning, genomic structure and expression of arginine kinase gene from Bombyx mori (L.). Scientia Agricultura Sinica, 39, 2354–2361. 10.3321/j.issn:0578-1752.2006.11.028 [DOI] [Google Scholar]
- Wang, J., Zhang, J. L., & Wu, F. A. (2013). Enrichment process for alpha‐linolenic acid from silkworm pupae oil. European Journal of Lipid Science and Technology, 115(7), 791–799. 10.1002/ejlt.201200324 [DOI] [Google Scholar]
- Wang, W., Wang, N., Zgou, B., Zhang, Y. U., Wu, X. Q., Xu, L. H., & Wang, J. Q. (2012). Antioxidant activities of silkworm protein hydrolyzates by bienzyme. Acta Agriculturae Zhejiangensis, 24(2), 300–304. 10.3969/j.issn.1004-1524.2012.02.023 (Article in Chinese) [DOI] [Google Scholar]
- Wang, W., Wang, N., & Zhang, Y. (2014). Antihypertensive properties on spontaneously hypertensive rats of peptide hydrolysates from silkworm pupae protein. Food and Nutrition Sciences, 5(13), 1202–1211. 10.4236/fns.2014.513131 [DOI] [Google Scholar]
- Wang, W., Wang, N., Zhou, Y., Zhang, Y., Xu, L. H., Xu, J. F., Feng, F. Q., & He, G. Q. (2011). Isolation of a novel peptide from silkworm pupae protein components and interaction characteristics to angiotensin I‐converting enzyme. European Food Research and Technology, 232(1), 29–38. 10.1007/s00217-010-1358-8 [DOI] [Google Scholar]
- Wang, Y. P., Liu, J., Wu, Y. M., Liu, L. E., Lv, Q. J., & Wu, Y. J. (2009). Analysis of nutrition composition on silkworm pupa. Journal of Zhengzhou University (Medical Sciences), 44(3), 638–641. 10.13705/j.issn.1671-6825.2009.03.005 (Article in Chinese) [DOI] [Google Scholar]
- Wei, W. G., Shen, S. R., Chen, Q. H., Tanga, B., He, G., Ruan, H., & Das, U. N. (2008). Hydrolyzates of silkworm Pupae (Bombyx mori) protein is a new source of angiotensin i‐converting enzyme inhibitory peptides (ACEIP). Current Pharmaceutical Biotechnology, 9, 307–314. 10.2174/138920108785161578 [DOI] [PubMed] [Google Scholar]
- Wen, H. S., Chang, Y. Q., & Cao, B. Y. (2009). Anti‐fatigue function of silkworm pupa protein polypeptides. Food Science, 30(19), 291–293. 10.1007/978-3-540-85168-4_52 (Article in Chinese) [DOI] [Google Scholar]
- World Health Organization (WHO) . (2015). Healthy diet: Fact sheet No.394. Available online: http://www.who.int/nutrition/publications/nutrientrequirements/healthydiet_factsheet394.pdf?ua¼1 [Google Scholar]
- Wu, Q., Jia, J., Yan, H., Du, J., & Gui, Z. (2015). A novel angiotensin‐I converting enzyme (ACE) inhibitory peptide from gastrointestinal protease hydrolysate of silkworm pupa (Bombyx mori) protein. Biochemical characterization and molecular docking study. Peptides, 68, 17–24. 10.1016/j.peptides.2014.07.026 [DOI] [PubMed] [Google Scholar]
- Wu, Q. Y., Xu, J. L., Jia, J. Q., Gui, Z. Z., & Tan, G. X. (2011). Nutrition evaluation of silkworm pupal proteins with various solubility and inhibitory activity of their enzymatic digested products to angiotensin‐converting enzyme. Acta Sericologica Sinica, 37(2), 352–357. 10.1007/s11518-011-5154-1 (Article in Chinese) [DOI] [Google Scholar]
- Xiao, Y. P., Huang, P. X., Dong, Y. P., Xue, J. X., & Wu, Q. Y. (2011). Preparation and purification of antioxidant peptides from silkworm pupae protein. Academic Periodical of Farm Products Processing, 3, 11–13. 10.3969/jissn.1671-9646(X).2011.03.003 (Article in Chinese) [DOI] [Google Scholar]
- Xu, J. Y., & Lu, X. H. (2008). Experimental study on the alleviative effect of protein from silkworm pupae on fatigue induced by exercise. Modern Preventive Medicine, 35(12), 2309–2313. 10.3969/j.issn.1003-8507.2008.12.049 (Article in Chinese) [DOI] [Google Scholar]
- Yan, Q. T., Cao, B. Y., & Chang, Y. Q. (2008). Anti‐tumor effects of silkworm pupa protein polypeptides in vitro and in vivo. Food Science, 29(11), 588–590. 10.3321/j.issn:1002-6630.2008.11.138 (Article in Chinese) [DOI] [Google Scholar]
- Yang, A. S., Chen, H. B., Zheng, G. Y., & Fan, Q. S. (2008). Study on preparation conditions of immuno‐active peptides from silkworm pupa protein by enzyme hydrolysis. Science and Technology of Food Industry, 29(1), 225–227. 10.13386/j.issn1002-0306.2008.01.004 (Article in Chinese) [DOI] [Google Scholar]
- Yang, B., Liu, X. L., & Zhao, M. M. (2017). Effects of pretreatment on silkworm pupae protein hydrolysis and umami‐taste enhancement of hydrolysates. Modern . Food Science and Technology, 33(6), 222–227. 10.13982/j.mfst.1673-9078.2017.6.033 (Article in Chinese) [DOI] [Google Scholar]
- Yang, H. J., Lee, J. W., Lee, S. H., Ryu, J. S., Kwak, D. H., Nam, K. S., Park, Y. I., Lee, Y. C., Jung, K. Y., & Choo, Y. K. (2010). Estrogenic activity produced by aqueous extracts of silkworm (Bombyx mori) pupae in ovariectomized rats. The American Journal of Chinese Medicine, 38(1), 89–97. 10.1142/S0192415X10007683 [DOI] [PubMed] [Google Scholar]
- Yang, Y., Tang, L., Tong, L., & Liu, H. (2009). Silkworms culture as a source of protein for humans in space. Advances in Space Research, 43(8), 1236–1242. 10.1016/j.asr.2008.12.009 [DOI] [Google Scholar]
- Yeo, Y., Cho, M., Jeon, B., Seo, H., Kwon, T., & Ryu, S. (2013). Changes of pupa powder ingestion on inflammatory cytokine in rats. Journal of Exercise Nutrition and Biochemistry, 17(3), 71–80. 10.5717/jenb.2013.17.3.71 [DOI] [Google Scholar]
- Yue, Y., Cui, J. A., & Chen, X. P. (2013). Separation purification antimicrobial peptides from silkworm chrysalis and physical and chemical properties. Food and Fermentation Technology, 49(2), 62–67. 10.3969/j.issn.1674-506X.2013.02-017 (Article in Chinese) [DOI] [Google Scholar]
- Zhan, X. D., Shi, Z. L., & Li, C. P. (2013). Inhibition effect of composite amino acid of silkworm chrysalis on human hepatic cancer cells SMMC‐7721. Natural Product Research and Development, 25(4), 460–465. 10.16333/j.1001-6880.2013.04.007 (Article in Chinese) [DOI] [Google Scholar]
- Zhan, X. D., Shi, Z. L., & Li, Z. P. (2015). Inhibition effect of hydrolytic amino acid of silkworm chrysalis (HAASC) to the HepG2.2.15. Journal of Qiqihar University of Medicine, 4, 469–470. 10.3969/j.issn.1002-1256.2012.17.060 (Article in Chinese) [DOI] [Google Scholar]
- Zhang, F., & Zhang, Z. (2001). Study on edible insect resources and their exploitation and utilization. Resource Science, 23, 21–23. 10.3321/j.issn:1007-7588.2001.02.013 (Article in Chinese) [DOI] [Google Scholar]
- Zhang, L. P., Qu, H. G., Chang, Y. Q., & Zheng, H. Y. (2005). Antifatigued effect of protein in silkworm chrysalis in human sample. Food Science, 26(9), 462–465. 10.3321/j.issn:1002-6630.2005.09.123 (Article in Chinese) [DOI] [Google Scholar]
- Zhang, M., Haga, A., Sekiguchi, H., & Hirano, S. (2000). Structure of insect chitin isolated from beetle larva cuticle and silkworm (Bombyx mori) pupa exuvi. International Journal of Biological Macromolecules, 27(1), 99–105. 10.1016/S0141-8130(99)00123-3 [DOI] [PubMed] [Google Scholar]
- Zhang, M. Q., Han, K. Q., Zhang, Y., Xu, T., & Zhang, J. Y. (2005). Preparation biological active peptide from fresh silkworm chrysalis with method of enzymolysis and ultrafiltration. Food Science, 26(8), 156–158. 10.3321/j.issn:1002-6630.2005.08.032 (Article in Chinese) [DOI] [Google Scholar]
- Zhang, Y., Wang, W., Zhang, Y. F., & Wang, J. H. (2016). The enzymatic hydrolysis condition optimization of α‐Glucosidase inhibitory peptides of silkworm pupa protein by response surface methodology. Journal of Chinese Institute of Food Science and Technology, 16(4), 137–143. 10.16429/j.1009-7848.2016.04.019 (Article in Chinese) [DOI] [Google Scholar]
- Zhang, Y., Wang, J. H., Zhu, Z. Y., Li, X., Sun, S. L., Wang, W., & Sadiq, A. F. (2021). Identification and characterization of two novel antioxidant peptides from silkworm pupae protein hydrolysates. European Food Research and Technology, 247, 343–352. 10.1007/s00217-020-03626-5 [DOI] [Google Scholar]
- Zhao, X., Li, L., Kuang, Z., Luo, G., & Li, B. (2015). Proteomic and immunological identification of two new allergens from silkworm (Bombyx mori L.) pupae. Central European Journal of Immunology, 40(1), 30–34. 10.5114/ceji.2015.50830 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhao, X. Y., Wang, X. D., Liu, X., Zhu, W. J., Mei, Y. Y., Li, W. W., & Wang, J. (2015). Structured lipids enriched with unsaturated fatty acids produced by enzymatic acidolysis of silkworm pupae oil using oleic acid. European Journal of Lipid Science and Technology, 117, 879–889. 10.1002/ejlt.201400438 [DOI] [Google Scholar]
- Zhao, Z. X., Liao, D. K., Sun, J. H., Huang, K. L., Sun, G. S., Qin, W. J., Wu, Z. H., & Tong, Z. F. (2011). Screening for optimal enzyme for preparation of silkworm pupae protein hydrolysate with in vitro antioxidant and antihypertensive activities and process optimization by response surface methodology. Food Science, 32(23), 186–190. 10.1007/s11518-011-5154-1 (Article in Chinese) [DOI] [Google Scholar]
- Zhou, J., & Han, D. (2006). Safety evaluation of protein of silkworm (Antheraea pernyi) pupae. Food and Chemical Toxicology, 44(7), 1123–1130. 10.1016/j.fct.2006.01.009 [DOI] [PubMed] [Google Scholar]
- Zhou, J., & Han, D. (2006). Proximate, amino acid and mineral composition of pupae of the silkworm Antheraea pernyi in China. Journal of Food Composition and Analysis, 19(8), 850–853. 10.1016/j.jfca.2006.04.008 [DOI] [Google Scholar]
- Zhu, L. S. (2004). Exploitation and utilization of the silkworm antheraea pernyi. Northern Sericulture, 25(101), 32–33. 10.3969/j.issn.1673-9922.2004.02.014 [DOI] [Google Scholar]
- Zuo, J., Lei, M., Yang, R., & Liu, Z. (2015). Bom m 9 from Bombyx mori is a novel protein related to asthma. Microbiology & Immunology, 59(7), 410–418. 10.1111/1348-0421.12271 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available on request from the corresponding author.