Evaluation of Edible Insects in terms of Sustainable Nutrition and Health

Abstract

In parallel with the increase in the human population, the demand for food has also increased, which has made the problems of malnutrition and the search for new food sources important, especially in underdeveloped countries today. The global increase in food demand and the limited land area available have led to the search for alternative protein sources. As a result of this search; In the future, entomophagy as an alternative food source has received serious attention. The potential use of insects as a new food source has many environmental and nutritional advantages and is seen as a sustainable source of animal protein. Edible insects have approximately the same protein content as conventional meat and contain higher levels of polyunsaturated fatty acids and various vitamins and minerals. The findings of various in vitro and in vivo animal studies have demonstrated the beneficial effects of entomophagy in the prevention of cardiovascular, gastrointestinal and non-communicable diseases, as well as in immune functions and carcinogenesis. Despite the many positive effects of insects, there are potential food safety hazards. Moreover; in countries where insect consumption is not traditional, there is a lack of acceptance and skill in preparing food with insects. For this reason, a number of strategies have been proposed to encourage insect consumption. It is pointed out by the World Food and Agriculture Organization that increasing the consumption of edible insects under safe conditions can positively affect the natural environment and reduce the problem of malnutrition in the world. With this; there is a need for high-quality clinical studies evaluating the efficacy, oral safety and allergy risk of this alternative food source and the development of consumption standards through authorities. The aim of this review is to evaluate entomophagy as an alternative food source in terms of sustainable nutrition and health.

Keywords

• Entomophagy
• Edible insects
• Nutrition
• Sustainability
• Alternative protein source

Yenilebilir Böceklerin Sürdürülebilir Beslenme ve Sağlık Açısından Değerlendirilmesi

Abstract

Günümüzde insan nüfusunun artmasına paralel olarak gıda talebi artmış, bu durum az gelişmiş ülkeler başta olmak üzere yetersiz beslenme sorunlarına neden olmuştur. Gıda talebindeki küresel artış ve mevcut sınırlı arazi alanı, alternatif protein kaynakları arayışına yol açmıştır. Bu durumda alternatif bir gıda kaynağı olarak entomofajiye olan ilgi artmıştır. Yeni bir gıda kaynağı olarak böceklerin potansiyel kullanımı, sürdürülebilirlik ve besinsel avantajlara sahiptir. Yenilebilir böcekler, geleneksel et ile yaklaşık olarak aynı protein içeriğine sahip olup daha yüksek seviyelerde çoklu doymamış yağ asitleri ile çeşitli vitamin ve mineralleri içermektedir. Çeşitli hayvan çalışmaların bulguları, entomofajinin kardiyovasküler, gastrointestinal ve diğer bulaşıcı olmayan hastalıkları önlemenin yanı sıra bağışıklık fonksiyonları ve karsinogenez açısından yararlı etkilerini ortaya koymuştur. Böceklerin birçok olumlu etkilerine rağmen potansiyel gıda güvenliği tehlikeleri de bulunmaktadır. Ayrıca; böcek tüketiminin yaygın olmadığı ülkelerde, böceklerle yemek hazırlama konusunda kabul ve beceri eksikliği görülmektedir. Bu sebeple böcek tüketimini teşvik etmek için bir dizi stratejiler önerilmektedir. Gıda Tarım Örgütü tarafından, güvenli koşullarda, yenilebilir böceklerin tüketiminin arttırılmasının, doğal çevreyi olumlu yönde etkileyebileceği ve dünyadaki yetersiz beslenme sorununu azaltabileceğine dikkat çekilmektedir. Bununla birlikte bu alternatif gıda kaynağının etkinliğini, oral alım güvenliğini ve alerji riskini değerlendiren yüksek kaliteli klinik çalışmalara ve otoriteler aracılığıyla tüketim standartlarının geliştirilmesine ihtiyaç vardır. Bu derlemenin amacı, entomofajinin altenatif bir gıda kaynağı olarak sürdürülebilir beslenme ve sağlık açısından değerlendirilmesidir.

Keywords

• Entomofaji
• Yenilebilir böcekler
• Beslenme
• Sürdürülebilirlik
• Alternatif protein kaynağı

References

1. Ademolu K., Idowu AB. Nutritional value assessment of variegated grasshopper, zonocerus variegatus (L.) (Acridoidea: Pygomorphidae), during post-embryonic development. African Entomology 2010; 18, 360-364.
2. Aguilar JGdS. An overview of lipids from insects. Biocatalysis and Agricultural Biotechnology 2021; 33, 101967.
3. Ahn MY., Ryu KS., Lee YW., Kim YS. Cytotoxicity and L-amino acid oxidase activity of crude insect drugs. Archives of Pharmacal Research 2000; 23, 477-481.
4. Anankware J., Fening K., Osekre E., Obeng-Ofori D. Insects as food and feed: A review. International Journal of Agricultural Research and Review 2015; 3, 143-152.
5. ANSES. Opınıon of the french agency for food. Environmental and Occupational Health & Safety. 2015. Access date, 02 March 2022. Retrieved from, https://www.anses.fr/en/system/files/bıorısk2014sa0153en.pdf.
6. Ayensu J., Annan R., Edusei A., Lutterodt H. Beyond nutrients, health effects of entomophagy: a systematic review. Nutrition & Food Science 2018; 49.
7. Banjo A., Lawal O., Adeyemi A. The microbial fauna associated with the larvae of oryctes monocerus. Journal of Applied Sciences Research 2006; 2.
8. Barbera F., Verneau F., Amato M., Grunert KG. Understanding Westerners’ disgust for the eating of insects: The role of food neophobia and implicit associations. Food Quality and Preference 2018; 64, 120-25.

9. Baş Aksoy A., Nehir El S. Geleceğin protein kaynağı yenilebilir böcekler. Turkish Journal of Agriculture - Food Science and Technology 2021; 9(5): 887-96.
10. Bauserman MS., Lokangaka A., Gado J., Close K., Wallace D., Kodondi KK., Bose CL. A cluster-randomized trial determining the efficacy of caterpillar cereal as a locally available and sustainable complementary food to prevent stunting and anaemia. Public Health Nutrition 2015; 18, 1785-92.
11. Bednářová M. Possibilities of using ınsects as food in the czech republic dissertation. Thesis, Mendel University, Brno. 2013.
12. Caparros Megido R., Gierts C., Blecker C., Brostaux Y., Haubruge É., Alabi T., Francis F. Consumer acceptance of insect-based alternative meat products in Western countries. Food Quality and Preference 2016; 52, 237-43.
13. Cerritos R. Insects as food: an ecological, social and economical approach. Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2009; 4 (27).
14. Cito A., Botta M., Francardi V., Dreassi E. Insects as source of angiotensin converting enzyme inhibitory peptides. Journal of Insects as Food and Feed 2017; 3(4):231-240.
15. de Carvalho NM., Madureira AR., Pintado ME. The potential of insects as food sources - a review. Crit Rev Food Sci Nutr 2020; 60(21): 3642-3652.
16. Di Mattia C., Battista N., Sacchetti G., Serafini M. Antioxidant activities in vitro of water and liposoluble extracts obtained by different species of edible ınsects and ınvertebrates. Frontiers in Nutrition 2019; 6.
17. EFSA Scientific Committee. Risk profile related to production and consumption of insects as food and feed. EFSA Journal 2015; 13(10): 4257.
18. Ersin M., Beyhan Y. Toplu beslenme sistemlerinde hijyen sanitasyonu sağlama önerileri. TTB Mesleki Sağlık ve Güvenlik Dergisi 2001; 2(8); 19-26.
19. FAO. Edible insects future prospects for food and feed security. 2013. Access date, 02 March 2022. Retrieved from, https://www.fao.org/3/i3253e/i3253e.pdf.
20. FAO. The future of food and agriculture – Trends and challenges. 2017. Access date, 02 March 2022. Retrieved from, https://reliefweb.int/sites/reliefweb.int/files/resources/a-i6583e.pdf.
21. FAO. Looking at edible insects from a food safety perspective. Challenges and Opportunities For The Sector. 2021 Access date, 02 March 2022. Retrieved from, http://www.fao.org/3/cb4094en/cb4094en.pdf.
22. Finke MD. Complete nutrient content of three species of wild caught insects, pallid-winged grasshopper, rhinoceros beetles and white-lined sphinx moth. J. Insects as Food Feed 2015; 1(4): 281-292.
23. Grabowski NT., Klein G. Microbiology of cooked and dried edible Mediterranean field crickets (Gryllus bimaculatus) and superworms (Zophobas atratus) submitted to four different heating treatments. Food Science and Technology International 2017; 23(1): 17-23.
24. Govorushko S. Global status of insects as food and feed source: A review. Trends in Food Science & Technology 2019; 91, 436-445.
25. Guo Z., Döll K., Dastjerdi R., Karlovsky P., Dehne HW., Altincicek B. Effect of fungal colonization of wheat grains with fusarium spp. on food choice, weight gain and mortality of meal beetle larvae (Tenebrio molitor). PLoS One 2014; 9(6): e100112.
26. Hall F. Functional properties of whole tropical banded crickets (Gryllodes Sigillatus) protein hydrolysates. (In Partial Fulfillment of the Requirements for the degree of Master of Science). Submitted to the Faculty of Purdue University, West Lafayette, Indiana, 2017.
27. Hartmann C., Shi J., Giusto A., Siegrist M. The psychology of eating insects: A cross-cultural comparison between Germany and China, Food Quality and Preference 2015; 44: 148-156.
28. Hong KS., Yun SM., Cho JM., Lee DY., Ji SD., Son JG., Kim EH. Silkworm (Bombyx mori) powder supplementation alleviates alcoholic fatty liver disease in rats. Journal of Functional Foods 2018; 43: 29-36.
29. Hou L., Shi Y., Zhai P., Le G. Inhibition of foodborne pathogens by Hf-1, a novel antibacterial peptide from the larvae of the housefly (Musca domestica) in medium and orange juice. Food Control 2007; 18(11): 1350-57.
30. Huis A. Conference on ‘The future of animal products in the human diet : health and environmental concerns’ Boyd Orr Lecture Edible insects are the future ? Proceedings of The Nutrition Society 2016; 1(3):1-12.
31. Ji K., Chen J., Li M., Liu Z., Wang C., Zhan Z., Xia Q. Anaphylactic shock and lethal anaphylaxis caused by food consumption in China. Trends in Food Science & Technology 2009; 20(5): 227-231.
32. Kauppi SM., Pettersen IN., Boks C. Consumer acceptance of edible insects and design interventions as adoption strategy. International Journal of Food Design 2019; 4(1):39-62.
33. Kaymaz E., Ulema Ş. Yenilebilir böceklerin menülerde kullanılması üzerine bir araştırma-Kapadokya örneği. Journal of Travel and Tourism Research 2020; 14, 46-64.
34. Klunder HC., Wolkers-Rooijackers J., Korpela JM., Nout MJR. Microbiological aspects of processing and storage of edible insects. Food Control 2012; 26(2): 628-631.
35. Konyole S., Kinyuru J., Owuor B., Kenji G., Onyango C., Estambale B., Owino V. Acceptability of amaranth grain-based nutritious complementary foods with dagaa fish (Rastrineobola argentea) and edible termites (Macrotermes subhylanus) compared to corn soy blend plus among young children/mothers dyads in Western Kenya. Journal of Food Research 2012; 1(3).
36. Kouřimská L., Adámková A. Nutritional and sensory quality of edible insects. NFS Journal 2016; 4: 22-26.
37. Kowalczewski PŁ., Walkowiak K., Masewicz Ł., Bartczak O., Lewandowicz J., Kubiak P., Baranowska HM. Gluten-Free Bread with Cricket Powder—Mechanical Properties and Molecular Water Dynamics in Dough and Ready Product. Foods 2019; 8(7):240.
38. Lange K., Nakamura Y. Edible insects as a source of food bioactives and their potential health effects. Journal of Food Bioactives 2021; 14:4-9.
39. Lategan A. An assessment of the potential of edible insect consumption in reducing human nutritional deficiencies in South Africa while considering food and nutrition security aspects. Masters’s Thesis, Stellenbosch University, Stellenbosch, South Africa, 2019.
40. Lee KP., Simpson SJ., Wilson K. Dietary protein‐quality influences melanization and immune function in an insect. Functional Ecology 2008; 22, 1052-61.
41. Menozzi D., Sogari G., Veneziani M., Simoni E., Mora C. Eating novel foods: an application of the theory of planned behaviour to predict the consumption of an insect-based product. Food Quality and Preference 2017; 59, 27-34.
42. Mentang F., Maita M., Ushio H., Ohshima T. Efficacy of silkworm (Bombyx mori L.) chrysalis oil as a lipid source in adult Wistar rats. Food Chemistry 2011; 127(3): 899-904.
43. Michaelsen KF., Hoppe C., Roos N., Kaestel P., Stougaard M., Lauritzen L., Friis H. Choice of foods and ingredients for moderately malnourished children 6 months to 5 years of age. Food and Nutrition Bulletin 2009; 30(3): 343-404.
44. Mlcek J., Rop O., Borkovcová M., Bednářová M., A comprehensive look at the possibilities of edible insects as food in Europe – A review. Polish Journal of Food and Nutrition Sciences 2014; 64(3): 147–157.
45. Muslu M. Sağlığın geliştirilmesi ve sürdürülebilir beslenme için alternatif bir kaynak yenilebilir böcekler / An alternative source for improvement of health and sustainable nutrition: edible insects, Gıda / The Journal Of Food 2020; 45, 1009-1018.
46. Navarro Del Hierro J., Gutiérrez-Docio A., Otero P., Reglero G., Martin D. Characterization, antioxidant activity, and inhibitory effect on pancreatic lipase of extracts from the edible insects Acheta domesticus and Tenebrio molitor. Food Chem 2020; 309, 125742.
47. Nguyen P., Kim KY., Kim AY., Kim NS., Kweon H., Ji SD., Koh YH. Increased healthspan and resistance to Parkinson's disease in Drosophila by boiled and freeze-dried mature silk worm larval powder. Journal of Asia Pacific Entomology 2016; 19(2): 551-561.
48. Nowak V., Persijn D., Rittenschober D., Charrondiere UR. Review of food composition data for edible insects. Food Chem 2016; 193, 39-46.
49. Ogbuagu MN., Emodi NV. Fatty acid and amino acid compositions of the larva of oil palm weevil (Rhyncophorous Ferrugineus). Elixir Appl. Chem 2014; 67, 21560-25164.
50. Ordoñez-Araque R.., Egas-Montenegro E. Edible insects: A food alternative for the sustainable development of the planet. International Journal of Gastronomy and Food Science 2021; 23, 100304.
51. Orkusz A. Edible ınsects versus meat—nutritional comparison: Knowledge of their composition ıs the key to good health. Nutrıents 2021; 13(4): 1207.
52. Orsi L., Voege LL., Stranieri S. Eating edible insects as sustainable food? Exploring the determinants of consumer acceptance in Germany. Food Res Int 2019; 125, 108573.
53. Paoletti MG., Buscardo E., Vanderjagt DJ., Pastuszyn A., Pizzoferrato L., Huang YS., Cerda H. Nutrient content of termites (Syntermes soldiers) consumed by Makiritare Amerindians of the Alto Orinoco of Venezuela Ecology of Food and Nutrition 2003; 42(2): 177-191.
54. Payne CLR., Scarborough P., Rayner M., Nonaka K. A systematic review of nutrient composition data available for twelve commercially available edible insects, and comparison with reference values. Trends in Food Science & Technology 2016; 47, 69-77.
55. Pettit GR., Meng Y., Herald DL., Knight JC., Day JF. Antineoplastic agents. 553. The Texas grasshopper brachystola magna. Journal of Natural Products 2005; 68(8): 1256-1258.
56. Phiriyangkul P., Srinroch C., Srisomsap C., Chokchaichamnankit D., Punyarit P. Effect of food thermal processing on allergenicity proteins in bombay locust (Patanga Succincta). International Journal of Food Engineering 2015; 1, 23-8.
57. Pippinato L., Gasco L., Di Vita G., Mancuso T. Current scenario in the European edible-insect industry: a preliminary study. Journal of Insects as Food and Feed 2020; 6(4): 371-381.
58. Raheem D., Raposo A., Oluwole OB., Nieuwland M., Saraiva A., Carrascosa C. Entomophagy: Nutritional, ecological, safety and legislation aspects. Food Research International 2019; 126, 108672.
59. Ramos-Elorduy J. Energy Supplied by Edible Insects from Mexico and their Nutritional and Ecological Importance. Ecology of Food and Nutrition 2008; 47(3): 280-297.
60. Research and Markets. Global $7.95Bn edible ınsects market by 2030: Analysis by Product Type & Application - ResearchAndMarkets.com. 2019. Access date, 02 March 2022. Retrieved from, https://www.researchandmarkets.com/research/xrqhr7/7_95_billion?w=12.
61. Ruby MB., Rozin P. Disgust, sushi consumption, and other predictors of acceptance of insects as food by Americans and Indians. Food Quality and Preference 2019; 74, 155-162.
62. Rumpold BA., Schlüter OK. Nutritional composition and safety aspects of edible insects. Molecular Nutrition & Food Research 2013; 57(5): 802-823.
63. Seo M., Goo TW., Chung MY., Baek M., Hwang JS., Kim MA., Yun EY. Tenebrio molitor Larvae Inhibit Adipogenesis through AMPK and MAPKs Signaling in 3T3-L1 Adipocytes and Obesity in High-Fat Diet-Induced Obese Mice. International Journal of Molecular Sciences 2017; 18(3): 518.
64. Sirimungkararat S., Saksirirat W., Nopparat T., Natongkham A. Edible products from eri and mulberry silkworms in Thailand In P. B. Durst, D. V. Johnson, R. L. Leslie, & K. Shono (Eds.), Forest insects as food: humans bite back, proceedings of a workshop on Asia-Pacific resources and their potential for development (pp. 189-200). Regional Office for Asia and the Pacific, Bangkok: FAO. 2010.
65. Skau JK., Touch B., Chhoun C., Chea M., Unni US., Makurat J., Roos N. Effects of animal source food and micronutrient fortification in complementary food products on body composition, iron status, and linear growth: a randomized trial in Cambodia. Am J Clin Nutr 2015; 101(4): 742-751.
66. Slocinska M., Marciniak P., Rosinski G. Insects Antiviral and Anticancer Peptides: New Leads for the Future? Protein and peptide letters 2008; 15, 578-585.
67. Stone AK., Tanaka T., Nickerson MT. Protein quality and physicochemical properties of commercial cricket and mealworm powders. J Food Sci Technol 2019; 56(7): 3355-3363.
68. Stull VJ., Finer E., Bergmans RS., Febvre HP., Longhurst C., Manter DK., Weir TL. Impact of edible cricket consumption on gut microbiota in healthy adults, a double-blind, randomized crossover trial. Scientific Reports 2018; 8(1): 10762.
69. Sun-Waterhouse D., Waterhouse GIN., You L., Zhang J., Liu Y., Ma L., Dong Y. Transforming insect biomass into consumer wellness foods: A review. Food Research International 2016; 89(1): 129-151.
70. Tan HSG., Fischer ARH., Tinchan P., Stieger M., Steenbekkers LPA., van Trijp H CM. Insects as food: Exploring cultural exposure and individual experience as determinants of acceptance. Food Quality and Preference 2015; 42, 78-89.
71. Tan HSG, Fischer ARH, van Trijp HCM, Stieger M. Tasty but nasty? Exploring the role of sensory-liking and food appropriateness in the willingness to eat unusual novel foods like insects. Food Quality and Preference 2016; 48, 293-302.
72. Tuccillo F., Marino MG., Torri L. Italian consumers’ attitudes towards entomophagy: Influence of human factors and properties of insects and insect-based food. Food Research International 2020; 137, 109619.
73. Van der Fels-Klerx HJ., Camenzuli L., Belluco S., Meijer N., Ricci A. Food safety ıssues related to uses of ınsects for feeds and foods. Comprehensive Reviews in Food Science and Food Safety 2018; 17(5): 1172-1183.
74. Van Der Spiegel M., Noordam MY., van der Fels-Klerx HJ. Safety of novel protein sources (ınsects, microalgae, seaweed, duckweed, and rapeseed) and legislative aspects for their application in food and feed production. Comprehensive Reviews in Food Science and Food Safety 2013; 12(6): 662-678. Van Huis A. Nutrition and health of edible insects. Curr Opin Clin Nutr Metab Care 2020; 23(3): 228-231.
75. Van Huis A., van Itterbeeck J., Klunder HC., Mertens E., Halloran A., Muir G., Vantomme P. Edible ınsects–future prospects for food and feed security. 2013. Access date, 02 March 2022. Retrieved from, www.fao.org/docrep/018/i3253e/i3253e.pdf.
76. Verbeke W. Profiling consumers who are ready to adopt insects as a meat substitute in a Western society. Food Quality and Preference 2015; 39, 147-155. Verneau F., La Barbera F., Kolle S., Amato M., Del Giudice T., Grunert K. The effect of communication and implicit associations on consuming insects: An experiment in Denmark and Italy. Appetite 2016; 106, 30-36.
77. WHO. Protein and amino acid requirements in human nutrition: report of a joint FAO/WHO/UNU expert consultation. 2007. Access date, 02 March 2022. Retrieved from, http://whqlibdoc.who.int/trs/who_trs_935_eng.pdf.
78. Xia Z., Chen J., Wu S. Hypolipidemic activity of the chitooligosaccharides from Clanis bilineata (Lepidoptera), an edible insect. International Journal of Biological Macromolecules 2013; 59, 96-98.
79. Yüksel E., Canhilal R. A survey of public opinion about entomophagy in erciyes university. Uluslararası Tarım ve Yaban Hayatı Bilimleri Dergisi 2018; 4(2): 203-208.