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Insight into the proximate composition and microbial diversity of edible insects marketed in the European Union

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Abstract

In recent years, the idea of exploiting edible insects for their industrial production has attracted the attention of media, research institutions and food industry operators, because of the numerous positive factors associated with this food source. Notwithstanding, insects are still underutilized in Western countries. Moreover, edible insects are carriers of natural microorganisms; hence, safety issues may arise from their industrial production. This study was aimed at providing insight into the proximate composition, with a focus in the fatty acid and amino acid composition, and microbial diversity of some processed edible insects marketed in the European Union. A high content of protein and fat was seen, with values ranging from 59.46 to 46.78 and 35.32 to 15.18%, respectively, with nutritionally valuable characteristics in both the lipid fractions and amino acid profiles. Furthermore, a great variation in microbial counts was seen. Both commensal and potential pathogenic microorganisms ascribed to the genera Pediococcus, Weissella, Streptomyces, Acinetobacter, Agrococcus, Arthrobacter, Naxibacter, Planomicrobium, Rufibacter, Bacillus, Clostridium, Vibrio, Desulfovibrio, Loktanella, Escherichia, Tetrapisispora, Aspergillus, Eurotium, Debaryomyces, and Wallemia, were identified by PCR-DGGE. The high diversity in the chemical composition and microbial profile of the marketed edible insects analyzed suggest a role of both the rearing and processing procedures on these variables. The results overall collected encourage the exploitation of edible insects as a valuable large-scale, animal-based commodity.

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References

  1. Van Huis A, Van Itterbeeck J, Klunder H, Mertens E, Halloran A, Vantomme P (2013) Edible insects: future prospects for food and feed security. Food and Agriculture Organization of the United Nations FAO Forestry Paper FAO, Rome

  2. Sogari G (2015) Entomophagy and Italian consumers: an exploratory analysis. Prog Nutr 17:311–316

    Google Scholar 

  3. Regulation (EU) 2015/2283 of the European Parliament and of the Council of 25 November 2015 on novel foods, amending Regulation (EU) No 1169/2011 of the European Parliament and of the Council and repealing Regulation (EC) No 258/97 of the European Parliament and of the Council and Commission Regulation (EC) No 1852/2001. http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32015R2283&from=EN

  4. Belluco S, Losasso C, Maggioletti M, Alonzi C, Ricci A, Paoletti MG (2015) Edible insects: a food security solution or a food safety concern? Anim Front 5:25–30

    Article  Google Scholar 

  5. Klunder HC, Wolkers-Rooijackers J, Korpela JM, Nout MJR (2012) Microbiological aspects of processing and storage of edible insects. Food Control 26:628–631

    Article  Google Scholar 

  6. Rumpold BA, Schlüter OK (2013) Nutritional composition and safety aspects of edible insects. Mol Nutr Food Res 57:802–823

    Article  CAS  Google Scholar 

  7. Gahukar RT (2016) Chapter 4—edible insects farming: efficiency and impact on family livelihood, food security, and environment compared with livestock and crops. In: Dossey AT, Morales-Ramos JA, Rojas MG (eds) Insects as sustainable food ingredients. Elsevier, Amsterdam, pp 85–111

  8. Milanović V, Osimani A, Pasquini M, Aquilanti L, Garofalo C, Taccari M, Cardinali F, Riolo P, Clementi F (2016) Getting insight into the prevalence of antibiotic resistance genes in specimens of marketed edible insects. Int J Food Microbiol 227:22–28

    Article  Google Scholar 

  9. Nowak V, Persijn D, Rittenschober D, Charrondiere UR (2016) Review of food composition data for edible insects. Food Chem 193:39–46

    Article  CAS  Google Scholar 

  10. Zhao X, Vázquez-Gutiérrez JL, Johansson DP, Landberg R, Langton M (2016) Yellow mealworm protein for food purposes—extraction and functional properties. PLoS ONE 11(2):e0147791

    Article  Google Scholar 

  11. Henderson JW, Ricker RD, Bidlingmeyer BA, Woodward C (2006) Rapid, accurate, sensitive, and reproducible HPLC analysis of amino acids. Agilent application note. 5980-1193EN. pp 1–10

  12. Osimani A, Babini V, Aquilanti L, Tavoletti S, Clementi F (2011) An eight-year report on the implementation of HACCP in a university canteen: impact on the microbiological quality of meals. Int J Environ Health Res 21:120–132

    Article  CAS  Google Scholar 

  13. Ampe F, Ben Omar N, Moizan C, Wacher C, Guyot JP (1999) Polyphasic study of the spatial distribution of microorganisms in Mexican pozol, a fermented maize dough, demonstrates the need for cultivation-independent methods to investigate traditional fermentations. Appl Environ Microbiol 65:5464–5473

    CAS  Google Scholar 

  14. Sheffield VC, Cox DR, Lerman LS, Myers RM (1989) Attachment of a 40-base pairs G + C rich sequence (GC clamp) to genomic DNA fragments by the polymerase chain reaction results in improved detection of single-base changes. Proc Natl Acad Sci USA 86:297–303

    Article  Google Scholar 

  15. Osimani A, Garofalo C, Aquilanti L, Milanović V, Clementi F (2015) Unpasteurised commercial boza as a source of microbial diversity. Int J Food Microbiol 94:62–70

    Article  Google Scholar 

  16. Ezeokoli OT, Gupta AK, Mienie C, Popoola T-O, Bezuidenhout CC (2016) PCR-denaturing gradient gel electrophoresis analysis of microbial community in soy-daddawa, a Nigerian fermented soybean (Glycine max (L.) Merr.) condiment. Int J Food Microbiol 220:58–62

    Article  CAS  Google Scholar 

  17. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  Google Scholar 

  18. Chen X, Feng Y, Chen Z (2009) Common edible insects and their utilization in China. Entomol Res 39:299–303

    Article  Google Scholar 

  19. van Huis A (2016) Edible insects are the future? Proc Nutr Soc 75:294–305

    Article  Google Scholar 

  20. Vieira Alves A, Sanjinez-ArgandoñaEJ Linzmeier AM, Lima Cardoso CA, Rodrigues Macedo ML (2016) Food value of mealworm grown on Acrocomia aculeata pulp flour. PLoS ONE 11:e0151275

    Article  Google Scholar 

  21. de Barroso FG, Haro C, Sánchez-Muros M-J, Venegas E, Martínez-Sánchez A, Pérez-Bañón C (2014) The potential of various insect species for use as food for fish. Aquaculture 422–423:193–201

    Article  Google Scholar 

  22. Food and Agriculture Organization of the United Nations (FAO) (2010) In: Heinz G, Hautzinger P (eds) Meat processing technology for small-to medium-scale producers. http://www.fao.org/docrep/010/ai407e/AI407E03.htm

  23. Shockley M, Dossey AT (2014) Insects for human consumption. In: Morales-Ramos JA, Guadalupe Rojas M, Shapiro-Ilan DI (eds) Mass production of beneficial organisms. Academic Press, London

    Google Scholar 

  24. Sun-Waterhouse D, Waterhouse GIN, You L, Zhang J, Liua Y, Ma L, Gao J, Dong Y (2016) Transforming insect biomass into consumer wellness foods: a review. Food Res Int 89:129–151

    Article  Google Scholar 

  25. Ramos-Bueno RP, González-Fernández MJ, Sánchez-Muros-Lozano MJ, García-Barroso F, Guil-Guerrero JL (2016) Fatty acid profiles and cholesterol content of seven insect species assessed by several extraction systems. Eur Food Res Technol 242:1471–1477

    Article  CAS  Google Scholar 

  26. van Broekhoven S, Oonincx DGAB, van Huis A, van Loon JJA (2015) Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by-products. J Insect Physiol 73:1–10

    Article  Google Scholar 

  27. Makkar HPS, Tran G, Henze V, Ankers P (2014) State-of-the-art on use of insects as animal feed. Anim Feed Sci Technol 197:1–33

    Article  CAS  Google Scholar 

  28. Zheng L, Hou Y, Li W, Yang S, Li Q, Yu Z (2013) Exploring the potential of grease from yellow mealworm beetle (Tenebrio molitor) as a novel biodiesel feedstock. Appl Energy 101:618–621

    Article  CAS  Google Scholar 

  29. Tzompa-Sosa DA, Yi L, van Valenberg HJF, van Boekel MAJS, Lakemond CMM (2014) Insect lipid profile: aqueous versus organic solvent-based extraction methods. Food Res Int 62:1087–1094

    Article  CAS  Google Scholar 

  30. Siemianowska E, Kosewska A, Aljewicz M, Skibniewska KA, Polak-Juszczak L, Jarocki A, Jędras M (2013) Larvae of mealworm (Tenebrio molitor L.) as European novel food. Agric Sci 4:287–291

    Google Scholar 

  31. Oonincx DGAB, van Broekhoven S, van Huis A, van Loon JJA (2015) Feed conversion, survival and development, and composition of four insect species on diets composed of food by-products. PLoS ONE 10(12):e0144601

    Article  Google Scholar 

  32. Vanhercke T, Shrestha P, Green AG, Singh SP (2011) Mechanistic and structural insights into the regioselectivity of an acyl-CoA fatty acid desaturase via directed molecular evolution. J Biol Chem 286:12860–12869

    Article  CAS  Google Scholar 

  33. Tomčala A, Bártů I, Šimek P, Kodrík D (2010) Locust adipokinetic hormones mobilize diacylglycerols selectively. Comp Biochem Physiol B Biochem Mol Biol 156(1):26–32

    Article  Google Scholar 

  34. Ulbricht TLV, Southgate DAT (1991) Coronary heart disease: seven dietary factors. Lancet 338:985–992

    Article  CAS  Google Scholar 

  35. Fernández M, Ordóñez JA, Cambero I, Santos C, Pin C, de la Hoz L (2007) Fatty acid compositions of selected varieties of Spanish dry ham related to their nutritional implications. Food Chem 101:107–112

    Article  Google Scholar 

  36. Wood JD, Enser M, Richardson RI, Whittington FM (1992) Fatty acids in meat products. In: Chow CK (ed) Fatty acids in foods and their health implications. CRC Press, Taylor and Francis Group, New York

    Google Scholar 

  37. Simopoulos AP (2002) The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 56:365–379

    Article  CAS  Google Scholar 

  38. Yi L, Lakemond CM, Sagis LM, Eisner-Schadler V, van Huis A, van Boekel MA (2013) Extraction and characterisation of protein fractions from five insect species. Food Chem 141(4):3341–3348

    Article  CAS  Google Scholar 

  39. Food and Agriculture Organization of the United Nations (FAO) (1989). Protein quality evaluation. Food and nutrition paper 51. Report of the Joint FAO/WHO Expert Consultation Bethesda, Md, USA, 4–8 Dec

  40. Regulation (EC) No. 2073/2005 (2005) of the European Parliament and the Councilof 15 November 2005 on microbiological criteria for foodstuffs. Off J Eur Union. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2005:338:0001:0026:EN:PDF

  41. Kramer JM, Gilbert RJ (1989) Bacillus cereus and other Bacillus species. In: Doyle MP (ed) Foodborne bacterial pathogens. Marcel Dekker, New York, pp 21–70

    Google Scholar 

  42. Ali A, Mohamadou BA, Saidou C, Aoudou Y, Tchiegang C (2010) Physico-chemical properties and safety of grasshoppers, important contributors to food security in the far North Region of Cameroon. Res J Anim Sci 4:108–111

    Article  Google Scholar 

  43. Stoops J, Crauwels S, Waud M, Claes J, Lievens B, Van Campenhout L (2016) Microbial community assessment of mealworm larvae (Tenebrio molitor) and grasshoppers (Locusta migratoria migratorioides) sold for human consumption. Food Microbiol 53:122–127

    Article  CAS  Google Scholar 

  44. Garofalo C, Osimani A, Milanović V, Taccari M, Cardinali F, Aquilanti L, Riolo P, Ruschioni S, Isidoro N, Clementi F (2017) The microbiota of marketed processed edible insects as revealed by high-throughput sequencing. Food Microbiol 62:15–22

    Article  CAS  Google Scholar 

  45. Opara MN, Sanyigha FT, Ogbuewu IP, Okoli IC (2012) Studies on the production trend and quality characteristics of palm grubs in the tropical rainforest zone of Nigeria. Int J Agric Technol 8:851–860

    CAS  Google Scholar 

  46. Liberti J, Sapountzis P, Hansen LH, Sørensen SJ, Adams RM, Boomsma JJ (2015) Bacterial symbiont sharing in Megalomyrmex social parasites and their fungus-growing ant hosts. Mol Ecol 24:3151–3169

    Article  Google Scholar 

  47. Wang WW, He C, Cui J, Wang HD, Li ML (2014) Comparative analysis of the composition of intestinal bacterial communities in Dastarcus helophoroides fed different diets. J Insect Sci 14:111

    Article  Google Scholar 

  48. İnce İA, Demirbağ Z, Katı H (2014) Arthrobacter pityocampae sp. nov., isolated from Thaumetopoea pityocampa (Lep., Thaumetopoeidae). Int J Syst Evol Microbiol 64:3384–3389

    Article  Google Scholar 

  49. Hanshew AS, McDonald BR, Díaz Díaz C, Djiéto-Lordon C, Blatrix R, Curie CR (2015) Characterization of actinobacteria associated with three ant–plant mutualisms. Microb Ecol 69:192–203

    Article  Google Scholar 

  50. Collignon C, Uroz S, Turpault M-P, Frey-Klett P (2011) Seasons differently impact the structure of mineral weathering bacterial communities in beech and spruce stands. Soil Biol Biochem 43:2012–2022

    Article  CAS  Google Scholar 

  51. Zhang JY, Liu XY, Liu SJ (2010) Agrococcus terreus sp. nov. and Micrococcus terreus sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 60:1897–1903

    Article  CAS  Google Scholar 

  52. Zhang ZD, Gu MY, Zhu J, Li SH, Zhang LJ, Xie YQ, Shi YH, Wang W, Li WJ (2015) Rufibacter roseus sp. nov., isolated from radiation-polluted soil. Int J Syst Evol Microbiol 65:1572–1577

    Article  CAS  Google Scholar 

  53. Polkade A, Ramana VV, Joshi A, Pardeshi L, Shouche YS (2015) Rufibacter immobilis sp. nov., a novel strain isolated from high altitude saline Lake. Int J Syst Evol Microbiol 65:1592–1597

    Article  CAS  Google Scholar 

  54. Abaydulla G, Luo X, Shi J, Peng F, Liu M, Wang Y, Dai J, Fang C (2012) Rufibacter tibetensis gen. nov., sp. nov., a novel member of the family Cytophagaceae isolated from soil. Antonie Van Leeuwenhoek 101:725–731

    Article  CAS  Google Scholar 

  55. Gupta AK, Rastogi G, Nayduch D, Sawant SS, Bhonde RR, Shouche YS (2014) Molecular phylogenetic profiling of gut-associated bacteria in larvae and adults of flesh flies. Med Vet Entomol 28:345–354

    Article  CAS  Google Scholar 

  56. Banjo AD, Lawal OA, Adeyemi AJ (2006) The microbial fauna associated with the larvae of Oryctes Monocerus. J Appl Sci Res 2:837–843

    Google Scholar 

  57. Egert M, Sting U, Bruun LD, Pommerenke B, Brune A, Friedrich MW (2005) Structure and topology of microbial communities in the major gut compartments of Melolontha melolontha larvae (Coleoptera: Scarabaeidae). Appl Environ Microbiol 71:4556–4566

    Article  CAS  Google Scholar 

  58. Olofsson TC, Alsterfjord M, Nilson B, Butler E, Vásquez A (2014) Lactobacillus apinorum sp. nov., Lactobacillus mellifer sp. nov., Lactobacillus mellis sp. nov., Lactobacillus melliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov. and Lactobacillus kullabergensis sp. nov., isolated from the honey stomach of the honeybee Apis mellifera. Int J Syst Evol Microbiol 64:3109–3119

    Article  Google Scholar 

  59. Oh SJ, Shin NR, Hyun DW, Kim PS, Kim JY, Kim MS, Yun JH, Bae JW (2013) Weissella diestrammenae sp. nov., isolated from the gut of a camel cricket (Diestrammena coreana). Int J Syst Evol Microbiol 63:2951–2956

    Article  CAS  Google Scholar 

  60. Hou Y, Ma Z, Dong S, Chen YH, Yu X (2013) Analysis of yeast-like symbiote diversity in the brown planthopper (BPH), Nilaparvata lugens Stål, using a novel nested PCR-DGGE protocol. Curr Microbiol 67:263–270

    Article  CAS  Google Scholar 

  61. Lachance M-A, Bowles JM, Starmer WT (2003) Metschnikowia santaceciliae, Candida hawaiiana, and Candida kipukae, three new yeast species associated with insects of tropical morning glory. FEMS Yeast Res 3:97–103

    CAS  Google Scholar 

  62. Suh S-O, Blackwell M (2004) Three new beetle-associated yeast species in the Pichia guilliermondii clade. FEMS Yeast Res 5:87–95

    Article  CAS  Google Scholar 

  63. Foley K, Fazio G, Jensen AB, Hughes WOH (2014) The distribution of Aspergillus spp. opportunistic parasites in hives and their pathogenicity to honey bees. Vet Microbiol 169:203–210

    Article  Google Scholar 

  64. Phoku JZ, Barnard TG, Potgieter N, Dutton MF (2014) Fungi in housefly (Musca domestica L.) as a disease risk indicator-A case study in South Africa. Acta Trop 140:158–165

    Article  CAS  Google Scholar 

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Osimani, A., Garofalo, C., Milanović, V. et al. Insight into the proximate composition and microbial diversity of edible insects marketed in the European Union. Eur Food Res Technol 243, 1157–1171 (2017). https://doi.org/10.1007/s00217-016-2828-4

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