Toxicological Characteristics of Edible Insects in China: a Historical Review

Accepted Manuscript Toxicological characteristics of edible insects in China: A historical review Yu Gao, Di Wang, Meng-Lei Xu, Shu-Sen Shi, Jin-Feng Xiong PII: S0278-6915(18)30218-7 DOI: 10.1016/j.fct.2018.04.016 Reference: FCT 9705 To appear in: Food and Chemical Toxicology Received Date: 26 January 2018 Revised Date: 1 April 2018 Accepted Date: 7 April 2018 Please cite this article as: Gao, Y., Wang, D., Xu, M.-L., Shi, S.-S., Xiong, J.-F., Toxicological characteristics of edible insects in China: A historical review, Food and Chemical Toxicology (2018), doi: 10.1016/j.fct.2018.04.016. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT 1 2 Toxicological Characteristics of Edible Insects in China: A historical review 3 Yu Gao a, Di Wang a, Meng-Lei Xu b*, Shu-Sen Shi a* , Jin-Feng Xiong c 4 5 a College of Agriculture, Jilin Agricultural University, Changchun, 130118, P. R. 6 China 7 b State Key Laboratory of Supramolecular Structure and Materials, Jilin University, 8 Changchun, 130000, P. R. China 9 c Changchun Institute of Biological Products Co. Ltd., Changchun, 130012, P. R. 10 China 11 12 *Co-Corresponding authors: MANUSCRIPT 13 Meng-Lei Xu, [email protected] 14 Shu-Sen Shi, [email protected] ACCEPTED ACCEPTED MANUSCRIPT 15 Abbreviations 16 ED 50 , median effective doses; 17 SOD, superoxide dismutase; 18 MDA, malondialdehyde; 19 MTD, maximum tolerated dose; 20 PSP, protein from silkworm pupae; 21 LD 50 , median lethal dose; 22 MNEL, maximal no-effect level; 23 ADI, acceptable daily intake. 24 MANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT 25 26 Abstract : Edible insects are ideal food sources, which contain important nutrients and 27 health-promoting compounds. With a rapid development of industrial insect farming, 28 insect-derived food is a novel and emerging food industry. Edible insects have been 29 traditionally consumed in various communities, while continuously gaining relevance 30 in today's society; however, they currently remain underutilized. Although there are a 31 large number of literatures on edible insects, these literatures primarily focus on the 32 nutritional value edible insects. The toxicity assessment data of edible insects remain 33 incomprehensive, especially for the new national standard that is currently in effect; 34 and many data and conclusions are not accurately specified/reported. Therefore, we 35 performed a literature review and summarized the data on the toxicological 36 assessment of edible insects in China. The reviewMANUSCRIPT first describes the research progress 37 on safety toxicological assessment, and then offers references regarding the 38 development of 34 edible insect species in China. These data can be a platform for the 39 development of future toxicological assessment strategies, which can be carried out 40 by a multidisciplinary team, possibly consisting of food engineers, agronomists, 41 farmers, and so on, to improve the acceptability of edible insects. 42 43 Keywords : ACCEPTEDEdible insects; Toxicological assessment; China; Food safety 44 ACCEPTED MANUSCRIPT 45 46 Highlights 47 1. 34 edible insect species with long history in China are reviewed based on 48 toxicology assessment. 49 2. Toxicological assessment methods and testing procedures are briefly 50 summarized. 51 3. Traditional edible insects in China are safe and can potentially be a food 52 resource. 53 TOC MANUSCRIPT 54 55 ACCEPTED ACCEPTED MANUSCRIPT 56 1. Introduction 57 Edible insects have been part of the cultural and genetic heritage in different 58 regions worldwide (Anankware et al., 2015; Belluco et al., 2015). With the increased 59 demand of animal-derived food to feed a continuously growing global population, 60 insects have great potential in dealing with the food crisis because of their diversity, 61 apparent abundance, and low environmental influence required for high-scale 62 production (Yen, 2015; Huis, 2016; Payne et al., 2016). Although edible insects are 63 currently underutilized, they are still consumed traditionally by different communities 64 while gaining relevance in today's society (Domingo, 2017). Thus, edible insects have 65 been valued and dedicated as a source of food by the Food and Agricultural 66 Organization of the United Nations (FAO) in 2013. 67 Edible insects have historically been consumedMANUSCRIPT in China for more than 2000 68 years owing to their medicinal and trophic values (Feng et al., 2018). The most 69 commonly consumed insects includes caterpillars, beetles, bee, wasps, crickets, ants, 70 termites, and flies (Zhang et al., 2008; Chen et al., 2009). In China, food safety, which 71 plays a central role in providing a guidance for the suitability of food for human 72 consumption, is one of the most challenging social issues that need to be addressed 73 (Wu and Chen, 2013; Nongonierma and Fitzgeral, 2017). However, the scientifically 74 based knowledgeACCEPTED to ensure safety of insect food processing, especially in the 75 industrial scale, is still lacking (Schlüter et al., 2017). For instance, the Chinese oak 76 tasar moth ( Antheraea pernyi ), which has traditionally been used as food as well as 77 traditional medicine in some Asian countries, has recently been listed as a novel ACCEPTED MANUSCRIPT 78 common food source by the Ministry of Health P. R. China (Zhu, 2004; Shao et al., 79 2014). Possible hazards from insects are contaminants such as heavy metals, toxins, 80 pesticide residues, and pathogens (Huis, 2015). Currently, most edible insects have 81 not been incorporated into policy documents, while have largely been omitted from 82 the regulatory frameworks. Moreover, in some nations where there are traditions of 83 consuming edible insects, the edible insects do not explicitly appear in their dietary 84 guidelines (Halloran et al., 2015). For this reason, some organizations and researchers 85 have proposed that edible insects should be systematically evaluated by a series of 86 toxicological assessments to ensure its safety as a new available food resource (Zhou 87 and Han, 2006; Poma et al., 2017). 88 Although the nutrient components of edible insects have been largely discussed 89 in a work by Feng et al. (2016), its toxicologicalMANUSCRIPT data are still incomprehensive. 90 Therefore, this article reviews the toxicological characteristics of edible insects in 91 China. The insect species were selected based on toxicological data recalled from 92 memory, such as traditional knowledge and practices in the use of edible insects. 93 94 2. Toxicity Assessment methods and testing procedures 95 Toxicology assessment is a judgment process based on the data/results obtained 96 from standardACCEPTED testing procedures. The standardization of food toxicology testing and 97 assessment in China began in 1980s. The Ministry of Health has promulgated a draft 98 of 'Procedures for toxicological assessment on food safety' in 1994, while national 99 standard 'Procedures for toxicological assessment of food' (GB 15193–1994, GB ACCEPTED MANUSCRIPT 100 15193–2003) in 2003 (Ministry of Health P. R. China, 2003). After the Food Safety 101 law went into effect and the toxicology technology was developed worldwide, all 102 toxicological assessments were complied with these laws and regulations. The 103 National Health and Family Planning Commission of P. R. China 104 (http://www.nhfpc.gov.cn/) gathered experts to revise the above standards, resulting in 105 the current version of 'Procedures for toxicological assessment of food' (GB 106 15193.1–2014). This new standard not only defines the contents of tests for 107 toxicological assessment, the principle of different subjects, the purpose and results 108 determination, and the factors to be considered in the assessment, but also contains 109 improved scientificity and universality. Whereas sperm deformity test was 110 discontinued due to its non-universality, sex-linked recessive lethal test was directly 111 transferred to new version. Nineteen standardsMANUSCRIPT were revised and 6 new standards were 112 developed to fill in the technological gap (Table S1). This China's food toxicology 113 assessment procedures and methods is a mandatory standard that is a particularly 114 important part of the national food safety standards. 115 The food toxicity tests set by this standard include: acute toxicity test, 116 genotoxicity test, twenty-eight days oral toxicity test, ninety days oral toxicity test, 117 teratogenicity study, reproductive toxicity test and reproductive development toxicity 118 test, toxicokinetics,ACCEPTED chronic toxicity test, carcinogenicity tests and combined chronic 119 toxicity with carcinogenicity studies (Fig. S1). The genotoxicity tests should follow 120 the principles, which combined prokaryotic and eukaryotic cells, both in vivo and in 121 vitro . According to the characteristic and the aim of the test, it is recommended as ACCEPTED MANUSCRIPT 122 follows: 123 Group one: Bacterial reverse mutation assay, mammalian erythrocyte 124 micronucleus test or mammalian bone marrow cell chromosome aberration test, 125 mice spermatogonium/spermatocyte chromosome aberration test or rodent

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