Selected aspects of edible insect rearing and consumption-A review

149 Czech Journal of Food Sciences, 39, 2021 (3): 149–159 Review https://doi.org/10.17221/288/2020-CJFS Supported bythe Tomas Bata University (TBU) inZlín, theCzech Republic (Internal grant No.IGA/FT/2021/008) andtheBrno University ofTechnology (BUT) inBrno, theCzech Republic (Project No.FEKT-S-20-6215). Selected aspects ofedible insect rearing and consumption –Areview Jiří Mlček1, Anna Adámková1*, Martin Adámek2,3, Marie Borkovcová1, Martina Bednářová4, Lenka Kouřimská5, Veronika Hlobilová1 1Department ofFood Analysis and Chemistry, Faculty ofTechnology, Tomas Bata University, Zlín, Czech Republic 2Department ofMicroelectronics, Faculty ofElectrical Engineering and Communication, Brno University ofTechnology, Czech Republic 3Department ofPhysics and Materials Engineering, Faculty ofTechnology, Tomas Bata University, Zlín, Czech Republic 4Department ofInformation Technology, Mendel University, Brno, Czech Republic 5Department ofMicrobiology, Nutrition and Dietetics, Faculty ofAgrobiology, Food and Natural Resources, Czech University ofLife Sciences Prague, Prague, Czech Republic *Corresponding author: [email protected] Citation: Mlček J., Adámková A., Adámek M., Borkovcová M., Bednářová M., Kouřimská L., Hlobilová V. (2021): Selected aspects ofedible insect rearing and consumption –Areview. Czech J. Food Sci., 39: 149–159. Abstract: Thepresented work brings acomprehensive study ofedible insect farming with animpact onthe environment and human health. Thereview focuses not only oncommonly monitored parameters such ascarbon footprint orfeed conversion but also onwaste management. Italso highlights thepositive and negative aspects ofeating edible insect regarding human health. Compared toother livestock, therearing ofedible insect brings less environmental burden and higher environmental protection. This review aimed tosummarise current knowledge and broaden thecomplex view ofthe issue. Keywords: allergy; carbon footprint; chitin; global warming potential Insects asanimal species exist inthe world for more than 300millionyears, and since thebeginning ofmankind, they are considered a"miracle ofnature" for medical, religious, and food use purposes (Ramos-Elorduy 1998; Meyer-Rochow 2017). Edible insects have been used byhumans since time immemorial and have been one ofthe most available food ingredients of animal origin (Sponheimer et al. 2005; Lesnik 2014). Currently, edible insects are consumed bymore than one-third ofthe world's population (more than 2billionpeople) (vanHuis etal. 2013). Considering thegrowing world population [according toUN(2015), itmay beupto10billion people in2050], theneed tolook for alternative sources offood implies, and edible insects appear tobeasuitable alternative source ofprotein. The nutritional value ofedible insects varies greatly, mainly due tothe variability ofspecies and consumption possible atdifferent developmental stages. Theprotein content in the insect body ranges from 13% to 81% of dry matter (Ramos-Elorduy et al. 1997; Xiaoming etal. 2008). Edible insects contain nutritionally valuable amino acids, including ahigh content ofphenylalanine and tyrosine. According toXiaoming etal. (2008), 150 Review Czech Journal of Food Sciences, 39, 2021 (3): 149–159 https://doi.org/10.17221/288/2020-CJFS thecontent ofessential amino acids may be46–96% ofthe total amino acids. Some insect species also contain large amounts oflysine, tryptophan, and threonine, which are deficient insome cereal proteins (Kouřimská and Adámková 2016). Therefore, itispossible tofortify conventional bakery products toincrease their content. Fat variability depends onmany factors and isusually inthe range of10% to55% ofdry matter (Bednářová etal. 2013). Insect fat can bewidely used, e.g.for food purposes in terms of saturated fatty acids (palmitic acid) content. The total content of polyunsaturated fatty acids, which provide prophylaxis against cardiovascular diseases, such asoleic, linoleic, orlinolenic, can beup to70% oftotal fatty acids (Tzompa-Sosa etal. 2014). Some species ofedible insects can beavaluable source ofminerals, e.g.iron and zinc contents are especially important indeveloping countries (Rumpold and Schlüter 2013; Manditsera 2019). Inthe case ofcommonly bread mealworm larvae, Zielińska etal. (2015) report azinc content of11.2mgkg –1 and Finke (2004) 137mgkg –1 . Edible insects also contain vitamins such asBvitamins, vitaminsA, D, E, K, andC. Ingeneral, most edible insect species provide sufficient energy and protein, meet amino acid requirements for humans, have ahigh content ofmono and polyenoic fatty acids, and are rich intrace elements such ascopper, iron, magnesium, manganese, phosphorus, selenium, andzinc, aswell asriboflavin, pantothenic acid, biotin and insome cases folic acid (Rumpold and Schlüter 2013). InCentral European countries, theinsect iscurrently most often sold aspart ofbakery products, protein bars, mixtures for the preparation of meatballs orvegetable cakes with insects, orasadelicacy prepared byroasting orother cooking techniques. Edible insect asafood bears certain positives and negatives, like other food commodities. VanHuis etal. (2013) listed thefollowing benefits ofedible insect rearing: – Insects can high feed conversion (Mancini etal.2019; Chow etal. 2020; Imathiu 2020); – Insect rearing can be environmentally friendly, reducing environmental pollution (Chow etal. 2020); – Insects can convert organic waste; – Insects produce relatively low quantities of greenhouse gases and ammonia (Mancini etal. 2019; Orsi etal. 2019); – Insect farming requires much less water and land than livestock farming (Garino etal. 2019); – Insects pose alow risk ofzoonotic transmission; – Insects are more efficient inrearing. Van Huis etal. (2013) stated that conversion ofthe house cricket (Acheta domestica) feed istwice aseffective aschicken, fourtimes higher than apig, and more than twelvetimes higher than cattle. Fortheproduction of1kg oflive weight ofinsect, feed consumption of1.7kg for domestic cricket (Acheta domestica) isneeded (Collavo etal. 2005). For comparison, Ayieko (2007) stated the feed requirements to produce 1kg ofmeat asfollows: 7.7kg for beef, 6.3kg for lamb, 3.6kg for pork, and 2.2kg for chicken. Pimentel and Pimentel (2003) calculated aneven lower conversion rate for conventional livestock. Schlup and Brunner (2018) mention that insect needs up to ten times less feed incomparison tocattle toproduce thesame amount ofanimal protein. One ofthe basic advantages ofinsect isthe conversion oforganic waste into protein. Forexample, black soldier fly (Hermetia illucens), mealworm (Tenebrio molitor), and house fly (Musca domestica) are very effective inorganic waste biodegradation. Together, they can process 1.3billiontons ofbio-waste peryear (Veldkamp etal. 2012). Insect farming also has anenvironmental impact (Figure1). In the study of Premalatha et al. (2011) on greenhouse gas and ammonia emissions, greenhouse gasses production ofpig and bovine breeding were compared tothe rearing ofmealworm (Tenebrio molitor), migratory locust (Locusta migratoria), house cricket (Acheta domesticus), and orange-spotted cockroach (Blaptica dubia). The study has shown that insects produced comparable oreven lower amounts ofboth greenhouse gases and CO2 alone, perkilogram ofmeat obtained, when compared topigs, and much less than cattle. Ammonia formation inall four insect species was lower than that ofthe farm animals. Thefact that insect rearing requires much less water and soil than livestock breeding is also significant (Pimentel and Pimentel 2003; Oonincx and de Boer 2012). Entomophagy may also involve some risks that must beconsidered. Collecting thefreely living insect could seriously interfere with thelandscape ecosystem. Itis therefore recommended toconsume insect reared under controlled and defined conditions. Byselecting anappropriate and safe Starving people reduction Safe food (EFSA)Employment increase Controlled farming Nature conservation Figure 1. Impact ofcontrolled farming onthe environment (inspired byHalloran etal. 2018) 151 Czech Journal of Food Sciences, 39, 2021 (3): 149–159 Review https://doi.org/10.17221/288/2020-CJFS feed, theconsequent health ofedible insect isensured. Other possible hazards ofeating edible insect include eating unsuitable developmental stages, inadequate handling, and inappropriate culinary treatment. Eating can also trigger anallergic response. Theinsect has anexternal skeleton made ofchitin, which isdifficult for humans todigest. Today, due tochitin-free food, there isadecrease inchitinase production inhumans. Some people have such asmall amount ofthe enzyme that anallergic reaction occurs after eating aninsect (Mlček etal. 2014). Themost threatened are people suffering from allergies toseafood, such asshrimps. If thecorrect starving, heat treatment, and appropriate storage conditions are not ensured, theedible insect can become dangerous, even from themicrobiological point of view (Giaccone 2005; Klunder et al. 2012). EFSA (2015) recommends further research ofedible insects while focusing on rearing safety and health risks for consumers. This review aimed tosummarise thefindings and spread information onedible insects asapossible alternative source ofprotein for food and feed. INSECT REARING FOR FOOD AND FEED PURPOSES, AND ITS ECONOMIC AND ENVIRONMENTAL EFFICIENCY At present, livestock production is the single largest anthropogenic use ofland. Itmakes up 70% ofall agricultural land use (including feed crop production) and 30% ofthe land surface area on Earth. Itis also alarge source ofgreenhouse gases and themain cause of biodiversity loss through land degradation, water pollution, and soil erosion (Steinfeld etal. 2006). Furthermore, indeveloped countries, resources, including vast areas ofland, are used togenerate animal protein for pet animals. Another advantage is the fact that theedible insects also contain micronutrients (minerals and vitamins) (Dreassi etal. 2017; Montowska etal. 2019; Yoo etal. 2019; Kwon etal. 2020; Wu etal. 2020). A further benefit of edible insects may be the number oflipids contained therein. Forexample, Berezina (2017) claimed that theamount oflipids inthe insect is30–50% onadry matter basis. Megido etal. (2018) mentioned that mealworm contains ~33% of lipids. Having this knowledge, the potential of the insect ashuman food should not beignored any longer, especially its ability to provide the needed protein for hungry people all around theworld. Thesignificance ofentomophagy ishighlighted even more bythe fact that every sixth person onEarth dies from malnutrition and hunger (FAO etal. 2017). Incase theinsect isused asamajor food resource, itwill benecessary tohave aconsiderable amount available. Freely living insect will probably not meet thedemand; moreover, ecosystems may be damaged if we will be using wildlife sources (Mitsuhashi 2010). For food use, insect used should be reared on farms, which would produce a clean specimen with known nutritional values. This will help tocontribute tosustainable ecosystems while avoiding overexploitation offreely living insect. Several farms already produce insect inlarge quantities, for example, projects toeradicate fruit flies and screwworms. Most ofthe larvae raising procedures are automatic, and insect continuous cell lines have been created. This could beamodel for thevast scale edible insect production inthe future (Mitsuhashi 2002). Therearing procedures are well developed, for example, for silkworms, mealworm, and others (Finke 2004; Katayama etal. 2005). Silkworm feeds onmulberry leaves, and mulberry has many cultivars available. Silkworm can bemade polytrophic. Artificial feed tasting like mulberry has already been developed. Pupa inacocoon oradult moth might be suitable as a food source (Katayama et al. 2005). However, it is not possible to cultivate some insect group cells using nowadays techniques, but inthe future, wemay find asolution tothis (Mitsuhashi 2010). Carbon Footprint. Greenhouse gasses (GHG) production isone ofthe possible causes ofclimate change. Themost important greenhouse gases are nitrous oxide(N2O), carbon dioxide(CO2), and methane(CH4). Up to18% oftotal anthropogenic GHGemissions and 64% ofall anthropogenic NH3emissions are produced bythe livestock sector (Steinfeld etal. 2006). Byassigning aCO2value of1global warming potential (GWP), the warming potentials can be expressed on a CO2- -equivalent basis: CH4 has aGWPof25, and N2O has aGWPof298(IPCC 2007). Avast amount ofNH3, produced bylivestock, leads tosoil acidification and nitrification. Increased practice ofentomophagy could help with this problem (Premalatha etal. 2011). Furthermore, other factors that lead togreenhouse gas emissions are closely linked with theproduction offoods from animal products or animal husbandry (production of greenhouse gases infeed production, energy for theproduction and processing ofanimal products, transportation). Oonincx and Dierenfeld (2012) evaluated thecontribution tothe GWP and energy utilisation (EU) and compared them with other animal products – milk, pork, chicken, and beef. Thecontribution toGWP was lower for mealworm than for other commodities –reduced bytwelvetimes, compared tobeef (Figure2). Theenergy used toproduce 1kg ofedible mealworm 152 Review Czech Journal of Food Sciences, 39, 2021 (3): 149–159 https://doi.org/10.17221/288/2020-CJFS protein was comparable toor higher than other commodities (e.g.upto79% for milk) (Figure3). Thereason isthe heating ofthe insect farms atlow ambient temperatures. Considering this, mitigation measures have been proposed, whereby larger larvae produce theexcess ofmetabolic heat, thereby heating thesmaller larvae that require it(Oonincx and Dierenfeld 2012). Oonincx and Dierenfeld (2012) also compared thearea utilisation ofinsect farming with other animal food commodities (Figure 4). The utilisation of area isagain lower for edible insect than for other compared commodities (uptofourteentimes). Oonincx etal. (2010), who also dealt with greenhouse gasses production, states inhis work that GHGemissions of4ofthe5insect species were much lower than ofpigs when expressed perkg ofmass gain and only about 1% from GHG emissions produced by ruminants. Themeasured NH3emission levels ofall insect species inthis experiment were lower than reported NH3emission levels for conventional livestock. Moreover, insect average daily gain(ADG) inthis study was higher than inconventional livestock, while CO2production related toweight gain was comparable orlower, suggesting higher insect feed conversion efficiency. CH4was produced only bytermites, cockroaches, and scarab beetles. Thereason ishindgut Methanobacteriaceae fermentation (Oonincx etal. 2010). Nutrient conversion. Thebody growth: CO2production ratio indicates thefeed conversion efficiency, and thereby itisarelevant environmental impact indicator. Themain three factors that cause thedifference inlife cycle assessment are: feed conversion efficiency, enteric CH4 emissions, and reproduction rates (de Vries and deBoer 2010). Many studies show that insects and small animals, in general, are relatively efficient converters (Beets 1997). Theinsect ismore effective than macrolivestock inassimilating matter –more than tentimes asmany plant resources are needed toproduce one kilogram ofmeat than toproduce one kilogram ofinsect zoomass. Thus, the production of insect-based foods puts much less pressure on ecosystem services than livestock-based foods (Premalatha etal. 2011). Theexplanation ofthis difference isquite simple. Theinsect ispoikilothermic and therefore does not spend asmuch food energy and nutrients as the warm-blooded livestock (Lindroth 1993). Therefore, insect produces much more animal protein perkilogram ofphytomass consumed than ordinary livestock. Insects have much higher fertility and a much faster growth rate: thousands ofoffspring are produced byasingle insect individual, while only afew are produced bynormal livestock. These Figure 2. Contribution toglobal warming potential (GWP) bymealworm (Tenebrio molitor) production with comparison toother commodities Data were normalised to1kg ofdigestible proteins from mealworm larvae [processed according toOonincx and Dierenfeld (2012)] Figure 3. Energy utilisation toproduce 1kg ofdigestible proteins ofmealworm larvae (Tenebrio molitor) compared toother commodities Data were normalised to1kg ofdigestible proteins from mealworm larvae [processed according toOonincx and Dierenfeld (2012)] Figure 4. Energy utilisation toproduce 1kg ofdigestible proteins ofmealworm larvae (Tenebrio molitor) compared toother commodities Data were normalised to1kg ofdigestible proteins from mealworm larvae [processed according toOonincx and Dierenfeld (2012)] Larvae TM Milk Pork Chicken Beef 0 4 8 12 16 Utilised area Normal According to Oonincx and Dierenfeld (2012) Larvae TM Milk Pork Chicken Beef 0 2 4 6 8 10 12 14 Contribution to GWP Normal According to Oonincx and Dierenfeld (2012) 0.0 0.4 0.8 1.2 1.6 Larvae TM Milk Pork Chicken Beef Energy utilisation Normal According to Oonincx and Dierenfeld (2012) 153 Czech Journal of Food Sciences, 39, 2021 (3): 149–159 Review https://doi.org/10.17221/288/2020-CJFS offspring mature within afew days, while inpoultry and ruminants, it takes months or even years. Combined with avery good nutritive value, these properties have impressed space scientists toinclude theuse ofinsect ashuman food into space travel and habitation plans (Huetal. 2010). That isnot all, asbymodelling thesituation inspace modules, where theneed will betoensure food sources within a much smaller space, proposals were also made tosupport and develop asustainable civilisation onEarth (Katayama etal. 2005). There isaneven better outcome for insect while comparing thepossibilities ofbiomass production inan area. Some collectively living insect species are very successful animals regarding biomass and diversity (Hunter 2010). Social insects – notably termites, wasps, bees, and ants have developed theability tolive in colonies with much higher population density than beetles, often since they are "clones" –individuals genetically identical. Although social insects makeup only twopercent ofinsect species, they makeup more than half ofthe total insect mass (Wilson 1990). Thesocial insect needs toutilise resources more effectively toincrease biomass, which isaccomplished bycreating communities that work together tocollect food inwide areas (Hunter 2010). THE RISKS, ALLERGIES, TOXICITY, AND MICROBIAL RISKS OF EDIBLE INSECT Consumption and handling ofinsects are not without risk. Collecting insect inunsuitable areas, wrong culinary preparation, the consumption of inappropriate developmental stages, and handling without protective equipment may result inunfavourable reactions. Risks. Bouvier (1945) observed inhis research that consuming grasshoppers and locusts without removing thelegs may lead tointestinal constipation, caused bythe large spines onthe tibia. Often theonly solution isthe surgical removal ofthese legs. Theautopsy showed that thedeaths ofthe monkeys during thelocus raids had thesame cause. Toxicity. TheAfrican silkworm pupae Anaphespp. has a high activity of relatively heat resistant thiaminase (Nishimune etal. 2000). Insouthwestern Nigeria, acute ataxic syndrome epidemics occur annually during therainy season. Reported symptoms, which appeared after theconsumption ofacarbohydrate meal, were impaired consciousness, intention tremors, and ataxia (Adamolekun etal. 1997). Enzyme reaction can decrease cellular free thiamine concentration orinfluence carbohydrate metabolism or energy production. Theenzyme could influence themetamorphosis ofthe insect. Its gene expression inthe different steps ofsilkworm metamorphosis, which has many apoptosis-like steps, is interesting. A thiaminase I gene has already been sequenced using a cloned bacterial gene (Abe etal. 1987; Costello etal. 1996). Theactivity ofthiaminase inJapanese silkworms (Bombyx mori) ismore than two-thirds lower that of Anaphe spp. This suggests theneed for proper heat treatment for detoxificationofthe African silkworm ifitshould beasafe source ofhigh-quality protein (Nishimune etal. 2000). Pesticide applications against locusts and grasshoppers must also betaken into consideration, asitcan cause problems due totoxic residues (vanHuis 2003; Yen 2009). Allergy. Overly zealous T-helper type 2 response to environmental antigens is the cause of the allergy, which can have fatal consequences. Our bodies constantly encounter potential allergens, either through breathing oreating. Sensitivity toinsect proteins may manifest itself, for example, byasthma, rhinitis, conjunctivitis, dermatitis, contact urticaria, orrhinoconjunctivitis (Bernstein et al. 1983; Schroeckenstein etal. 1990; Freye et al. 1996). In extreme cases, a strong allergic reaction may occur –anaphylactic shock. Itisaserious allergic reaction that occurs quickly and can cause death (Belluco etal. 2013). Allergies usually occur inthe work environment where theemployee encounters insects. Allergic reactions toinsect are mostly reported concerning chitin, which isthe second most abundant biopolymer in nature. Its role in nature is mostly the protection of parasites, fungi, and crustaceans from the dangers in their environments (Elias et al. 2005). Chitin isnot considered acommon allergen; however, it can cause sensitisation due to frequent exposure (Burton and Zaccone 2007). Itisalso arecognition element for tissue infiltration byinnate cells implicated in allergic and helminth immunity, and this process can be negatively regulated by a vertebrate chitinase (Reeseetal. 2007). Theamount ofchitin inedible insects isintherange of2–5% ofdry matter (Berezina 2017). Allergic reactions have been documented mainly for mealworm andOrthoptera, either for contact orrespiratory form (Linares etal. 2008; Garino etal. 2019). Combined allergies tomore than one species ofinsect are not uncommon (Bleßmann-Gurk et al. 2007). Studies show that inhaled particulates from mealworm exoskeletons are potent sensitisers and elicit IgE-mediated occupational asthma, which confirms thefact that Tenebrionid family beetles are potentially significant allergens for employees working with grains orgrain products (Bernstein etal. 1983; Schroeckenstein etal. 1990). 154 Review Czech Journal of Food Sciences, 39, 2021 (3): 149–159 https://doi.org/10.17221/288/2020-CJFS For themealworm, Marono etal. (2015) report anaverage of 5% of chitin, unlike Finke (2015), who states 1.2%. Thecontent ofchitin infield cricket (Gryllus Testaceus Walker) determined byWang etal. (2004) was 8.7% ofchitin onadry matter. Finke (2007) detected 81.5gkg–1 on a dry matter of chitin in the nymph of the house cricket (Acheta domesticus). Goodman (1989) reports anaverage of10%chitin ininsects. However, chitin does not appear inthe pure form but isbound tomany amino acids, most likely cuticular protein. Yet, thechitin content isusually evaluated asthe total content ofthese chitinous substances (Barker etal. 1998; Finke 2002). Chitin exposure originating from shellfish, moulds, dust mites, orinsects might bethe primary external trigger inallergy development. Discontinuous low-level exposure can cause allergies inpeople with agenetic predisposition. It is crucial to understand the allergenic role ofchitin, partially because ofits abundance intheenvironment but also because itiscommonly used inhealthcare and cosmetics. Various studies suggest chitin can quicken wound healing; its molecules are already used inmedicines today (Muzzarelli 1997). Chitin can activate macrophages, which is beneficial for stimulating tissue repair; yet chitin might also recruit polymorphonuclear leukocytes, which starts the allergic reactions (Kodelja et al. 1997). Toxicological tests are mostly performed onanimals whose chitinase activity could be higher. Therefore, further research isrequired toreveal thegenetic basis ofdifferences inchitinase functions and allergy inhumans. Moreover, chitinase has animportant role inthe innate immunity tovarious infectious agents, including parasites. Therefore, we can hypothesise that, when produced in a dysregulated fashion, they also have a relevant role inthe pathogenesis of allergy and/or asthma (Elias etal. 2005). It has also been found that aprototypic chitinase, acidic mammalian chitinase, was induced during TH2inflammation byanIL-13-dependent mechanism. Ithas also been shown tohave acrucial role inthe pathogenesis ofTH2inflammation and activation oftheIL-13effector pathway and isoverexpressed inhuman asthmatic tissues. Thefinding that chitinases contribute tothe host's antiparasitic responses and asthmatic TH2inflammation supports thenotion that asthma could beaparasite with anindependent antiparasitic response (Elias etal. 2005; Burton and Zaccone 2007; Sutherland etal. 2009). Chitin isarecognition element for tissue infiltration bycongenital cells involved innematode allergy and immunity, and this process may benegatively regulated by vertebrate chitinases. Mammalian chitinase (AMCase) and chitotriosidase (ChT) have chitinolytic activity, but theknowledge about their role innasal polyps isscarce. Nasal polyps appear toeliminate chitinase levels, and thepresence orgrowth ofpathogens with thecontent ofchitin may increase chitinase expression, which leads totheformation and growth ofnasal polyp insusceptible individuals (Park etal. 2009). Another potential allergen is tropomyosin protein, which isfound inmuscle and non-muscle cells ofall vertebrate and invertebrate species. Itmay have more isoforms (Belluco etal. 2013). Cross-reaction studies incrustaceans show that tropomyosin isone oftheir major allergens, responsible for the immunological relationship between crustaceans, house dust mites and cockroaches. Shrimps can cross-react with arthropods such asmites and insect species, including cockroaches, grasshoppers, and fruit flies (Leung etal. 1996; Reese etal. 1999). Verhoeckx etal. (2014) and vanBroekhoven etal. (2016) also report similar findings intheir study. Theresults ofvanBroekhoven etal. (2016) further show that heat treatment can weaken allergies, but therisk isnot always ruled out. Microbial risk. Insects, especially their intestines, can beasuitable environment for thegrowth ofmicrobial fauna (Rumpold and Schlüter 2013), which may beharmful tohumans. Therefore, therisk oftransmission of infectious diseases must also be considered. However, from thepoint ofview ofhuman nutrition, thecomposition ofthe microflora oflive edible insect species may not behazardous tothe final food if theinsect isproperly reared and processed using preservation and storage techniques such ascooking orrefrigeration (Belluco etal. 2013). Edible insects can become microbiologically dangerous if proper rearing, shedding, heat treatment, and suitable storage conditions are not ensured (Giaccone 2005; Klunder etal. 2012). Klunder etal. (2012) documents the microbiological content offresh, processed, and stored edible insects. Thestudy focused onthe larvae ofmealworm (Tenebrio molitor) and crickets (Acheta domesticus and Brachytrupes sp.). Theresults showed that infresh insects, various species ofbacteria ofthe family Enterobacteriaceae can bedetected and subsequently isolated, aswell assporulating bacteria, which are most likely toenter theinsect upon contact with thesoil. Cooking insects for 5min isaneffective procedure for removing Enterobacteriaceae (Klunder etal. 2012). Grabowski (2017) documents that cooking for 10min and drying for 24h at80°C reduced thetotal number ofmicroorganisms [total microbial count (TMC)] below adangerous level for 5days ofstorage. If thedrying 155 Czech Journal of Food Sciences, 39, 2021 (3): 149–159 Review https://doi.org/10.17221/288/2020-CJFS temperature was 60°C, theTMC was not reduced below themaximum allowable limit, and thefood remained unfit for human consumption. Thelast heat treatment tested was cooking for 30min followed bydrying at80°C for 12h and drying at100°C for 12h. Interestingly, this heat treatment reduced theTMC below themaximum allowable limit only on the first day of storage, and inthe following days, theTMC rose above theallowed safe limit. Onthe other hand, Staphylococcus was not detected inthese samples, incontrast toother thermal treatments. Microbial analyses performed byAdámek et al. (2018) show that, from a microbiological safety point of view, killing, drying, and subsequent storage are more appropriate than killing and freezing samples. INSECT IN WASTE MANAGEMENT Modern agriculture involves the keeping of many dairies, pigs, chickens, and other animals. This causes theaccumulation ofasignificant amount ofmanure, and that ishazardous totheenvironment (Lietal. 2011b). On the other hand, manure and bio-waste can also beused asaprincipal resource for larvae ofmany insect species such asthe black soldier fly, Hermetia illucens (Booram etal. 1977; Bondari and Sheppard 1981; St-Hilaire etal. 2007; Myers etal. 2008; Lietal. 2011b; Rabani etal. 2019). Such information can provide anincentive for establishing anadequate method for themass production ofprotein-rich dipterous larvae (Larde 1990). Black soldier fly larvae (BSFL) possess another advantage –besides manure liquidation, they can reduce Escherichia coli counts (Liu etal. 2008). Very promising inmany aspects appears tobethe finding that BSFL not only can help us with thedisposing ofthe manure but atthe same time being asource ofquality protein and fats; they are also useful for theproduction ofbiodiesel instead ofcrop oil, which isalimited and expensive food resource. 1000BSFL growing on1kg ofcattle manure can beused toproduce 35.5g ofbiodiesel. Forpig manure, itis57.8g, and for chicken manure, 91.4g (Lietal. 2011a). Petroleum ether could beused toextract grease from BSFL; then, thetwo-step method isapplied toproduce biodiesel. The"waste" from this process, thedry matter residues of BSFL can be utilised as a protein feed (Lietal. 2011a). Theintegration oflarge-scale insect rearing into small-scale farming ventures may pose aninteresting challenge. Anexample can betoinclude insect into organic waste recycling systems (DeFoliart 1995; Ramos-Elorduy 2008). Insects are a basic substance that feeds on organic matter in nature. They make efficient use of all organic resources and feed onall levels ofplants and animals. Duetothese properties and theneed torecycle vast amounts ofwaste generated byup-to-date lifestyles, theinsects could beused asbio-transformers for converting organic waste into protein-rich animal biomass suitable for use inanimal nutrition (Ramos-Elorduy 1996). Thenutritional value ofthe insects increased. There were differences based onthe medium used, but itwas generally slightly better than the control. The recycling time of the waste depended on the species of insect and the substrate used. Forsubstrates that provide abalanced diet, 92% to95% ofthe medium was consumed and transformed into insect tissues (Ramos-Elorduy and Pino 1990). The degree of protein transformation ranged from 5%to8% for poor quality proteins insubstrates to43% to 61% for higher quality proteins (Ramos-Elorduy etal. 1988). Allthese facts show thepossibilities ofrecycling organic matter asaculture medium for insects toobtain nutritious insect biomass. Experiments with insects inanimal nutrition show that they can replace soy orfishmeal when fed poultry orfish with thesame orbetter results (DeFoliart etal. 1982; Ramos-Elorduy etal. 1988; Ramos-Elorduy 1996). Black soldier fly (Hermetia illucens) could be successfully used to reduce animal waste inbreeding facilities and produce animal feed highinprotein and fat, which isthanks toahigh rate ofconversion ofbiomass toprotein and fats (Rabani etal. 2019). If their diet contains fish offal, theflies contain eicosapentaenoic acid (EPA), α-linolenic acid (ALA), and docosahexaenoic acid (DHA). St-Hilaire etal. (2007) examined thedifference infeeding with fish offal and cow manure, where theresults showed that ifthelarvae were fed byfish offal, thelipid amount was onaverage 30%, which was 43% more than if thelarvae were fed bycow manure. Besides, theomega-3fatty acid content reached this level within 24h after feeding theoffal. Omega-3fatty acid elevated pre-pupae may beaswell usable asfish meal and fish oil substitution for carnivorous fish and other animal feeds. This could also beanefficient way toreduce and recycle fish offal from processing factories (St-Hilaire etal. 2007). CONCLUSION The review summarises existing information on the impact of edible insect on the environment, including waste management, and compares thebenefits and risks ofthis food commodity with other commodities ofanimal origin. Thestudy demonstrates alower environmental burden by insect farming, evaluating the need for theproduction of1kg ofprotein compared toother live- 156 Review Czech Journal of Food Sciences, 39, 2021 (3): 149–159 https://doi.org/10.17221/288/2020-CJFS stock. Inparticular, itproves lower greenhouse gas emissions and higher feed conversion. Italso draws attention tothe risks and safety ofrearing and eating edible insect that is comparable to other livestock. The key is controlled insect farming, which ensures significant protection ofthe environment without disturbing its diversity. The review provides acomprehensive view ofthis issue. Ingeneral, themain advantages ofinsect rearing are fast feed conversion, high insect reproduction capacity, low demands onthe rearing area, and theability torear insects on multiple floors. On the contrary, a negative energy load incolder rearing areas ispossible. Inthe food industry and human nutrition, thebasic disadvantages ofconsuming edible insects are thepossibility ofsevere allergic reactions (chitin), possible toxicity, aswell ascomplicated legislation intherearing ofinsects for food purposes and theassociated current high price. Onthe contrary, theadvantages are nutritional values such ashigh protein content, good digestibility, and appropriate representation ofessential amino acids and polyunsaturated fatty acids, and avaluable source ofminerals. REFERENCES Abe M., Ito S., Kimoto M., Hayashi R., Nishimune T. (1987): Molecular studies onthiaminaseI. Biochimica et Biophysica Acta (BBA) –Gene Structure and Expression, 909:213–221. Adámek M., Mlček J., Adámková A., Suchánková J., JanalíkováM., Borkovcová M., Bednářová M. (2018): Effect ofdifferent storage conditions onthe microbiological characteristics ofinsect. Potravinarstvo Slovak Journal ofFood Sciences, 12:248–253. Adamolekun B., Mc Candless D.W., Butterworth R.F. (1997): Epidemic ofseasonal ataxia inNigeria following ingestion ofthe African silkworm Anaphe venata: Role ofthiamine deficiency? Metabolic Brain Disease, 12:251–258. Ayieko A.M. (2007): Nutritional value ofselected species ofreproductive Isoptera and Ephemeroptera within theASAL ofLake Victoria basin. Discovery and Innovation, 19:126–130. Barker D., Fitzpatrick M.P., Dierenfeld E.S. (1998): Nutrient composition ofselected whole invertebrates. Zoo Biology, 17:123–134. Bednářová M., Borkovcová M., Mlček J., Rop O., Zeman L. (2013): Edible insects –Species suitable for entomophagy under condition ofCzech Republic. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 61:587–593. Beets W.C. (1997): Theneed for anincreased use ofsmall and mini livestock inintegrated smallholder farming systems. Ecology ofFood Nutrition, 36:237–245. Belluco S., Losasso C., Maggioletti M., Alonzi C.C., PaolettiM.G., Ricci, A. (2013): Edible insects inafood safety and nutritional perspective: Acritical review. Comprehensive Reviews inFood Science and Food Safety, 12:296–313. Berezina N. (2017): Insects:Novel source oflipids for afan ofapplications. Oilseeds and Fats, Crops and Lipids, 24:1–9. Bernstein D.I., Gallagher J.S., Bernstein I.L. (1983): Mealworm asthma: Clinical and immunologic studies. Journal ofAllergy and Clinical Immunology, 72:475–480. Bleßmann-Gurk B., Hoffmann B., Bayerl C. (2007): Allergic contact urticaria inareptile owner (Allergische Kontakturtikaria bei einem Reptilienhalter). Akt Dermatol, 33:166–167. (in German) Bondari K., Sheppard D.C. (1981): Soldier fly larvae asfeed incommercial fish production. Aquaculture, 24:103–109. Booram C.V., Newton G.L., Hale O.M., Barker R.W. (1977): Manure asasubstrate for protein production via Hermetia illucens larvae. In:Food, Fertilizer & Agricultural Residues: Proceedings ofthe 9th Cornell Agricultural Waste Management Conference, Ann Arbor Science Publishers, Ann Arbor, MI, USA, 1977: 599–604. Bouvier G. (1945): Some questions ofveterinary entomology and thefight against certain arthropods intropical Africa (Quelques questions d'entomologie vétérinaire etlutte contre certains arthropodes enAfrique tropicale). Acta Tropica, 2:42–59. (in French) Burton O.T., Zaccone P. (2007): Thepotential role ofchitin inallergic reactions. Trends inimmunology, 28:419–422. Chow C.Y., Riantiningtyas R.R., Sørensen H., Frøst M.B. (2020): School children cooking and eating insects aspart ofateaching program –Effects ofcooking, insect type, tasting order and food neophobia onhedonic response. Food Quality and Preference, 87: 1–6. Collavo A., Glew R.H., Huang Y.S., Chuang L.T., Bosse R., Paoletti M.G. (2005): House cricket small-scale farming. In:PaolettiM.G.(ed.): Ecological Implications ofMinilivestock: Potential ofInsects, Rodents, Frogs and Snails. Enfield, NH, USA, Science Publishers: 519–544. Costello C.A., Kelleher N.L., Abe M., McLafferty T.W., BeyloyT.P. (1996): Mechanistic studies onThiaminaseI: Overexpression and identification ofthe active site nucleophile. Journal ofBiological Chemistry, 271:3445–3452. De Foliart G.R., Finke M.D., Sunde M.L. (1982): Potential value ofthe mormon cricket (Orthoptera: Tettigoniidae) harvested asahigh-protein feed for poultry. Journal ofEconomic Entomology, 75:848–852. De Foliart G.R. (1995): Edible insects asmini livestock. Biodiversity and Conservation, 4:306–321. deVries M., deBoer I.J.M. (2010): Comparing environmental impacts for livestock products: Areview oflife cycle assessments. Livestock Science, 128:1–11. 157 Czech Journal of Food Sciences, 39, 2021 (3): 149–159 Review https://doi.org/10.17221/288/2020-CJFS Dreassi E., Cito A., Zanfini A., Materozzi L., Botta M., Francardi V. (2017): Dietary fatty acids influence thegrowth and fatty acid composition ofthe yellow mealworm Tenebrio molitor (Coleoptera: Tenebrionidae). Lipids, 52:285–294. EFSA (2015): Risk profile related toproduction and consumption ofinsects asfood and feed. European Food Safety Authority (EFSA) Scientific Committee. EFSA Journal, 13:1–60. Elias J.A., Homer R.J., Hamid Q., Chun G.L. (2005): Chitinases and chitinase-like proteins inTH2 inflammation and asthma. Journal ofAllergy and Clinical Immunology, 116:497–500. FAO, IFAD, UNICEF, WFP, WHO (2017): TheState ofFood Security and Nutrition inthe World 2017: Building Resilience forPeace and Food Security. Rome, Italy, FAO: 117. Finke M.D. (2002): Complete nutrient composition ofcommercially raised invertebrates used asfood for insectivores. Zoo Biology, 21:269–285. Finke M.D. (2004): Nutrient content ofinsects. In:CapineraJ.L.(ed.): Encyclopedia ofEntomology. Dordrecht, theNetherlands, Kluwer Academic Publishers: 1563–1575. Finke M.D. (2007): Estimate ofchitin inraw whole insects. Zoo Biology, 26:105–115. Finke M.D. (2015): Complete nutrient content offour species ofcommercially available feeder insects fed enhanced diets during growth. Zoo Biology, 34:554–564. Freye H.B., Esch R.E., Litwin C.M., Sorkin L. (1996): Anaphylaxis tothe ingestion and inhalation ofTenebrio molitor (mealworm) and Zophobas morio (superworm). Allergy and Asthma Proceedings, 17:215–219. Garino C., Zagon J., Braeuning A. (2019): Insects infood and feed –Allergenicity risk assessment and analytical detection. EFSA Journal, 17:1–12. Giaccone V. (2005): Hygiene and health features of"minilivestock". In: Paoletti M.G. (ed.): Ecological Implications ofMinilivestock: Potential ofInsects, Rodents, Frogs and Snails. Enfield, NH, USA, Science Publishers: 579–598. Goodman W.G. (1989): Chitin: Amagic bullet? Food Insects Newsletter, 2:6–7. Grabowski N.T., Klein G. (2017): Microbiology ofprocessed edible insect products –Results ofapreliminary survey. International Journal ofFood Microbiology, 243:103–107. Halloran A., Flore R., Vantomme P., Roos N. (2018): Edible Insects inSustainable Food Systems. Switzerland, Springer International Publishing: 479. Hu E., Bartsev S.I., Liu H. (2010): Conceptual design ofabioregenerative life support system containing crops and silkworms. Advances inSpace Research, 45:929–939. Hunter P. (2010): Massing life. Research into biomass and food chains attracts increasing attention, given thebiosphere's capacity tosequester CO2 from theatmosphere. European Molecular Biology Organization (EMBO) reports, 11:511–514. Imathiu S. (2020): Benefits and food safety concerns associated with consumption ofedible insects. Nutrition and Food Science (NFS) Journal, 18:1–11. IPCC (2007): Summary for policymakers. In:Solomon S., QinD., Manning M., Chen Z., Marquis M., Averyt K.B., Tignor M., Miller H.L. (eds.): Climate Change 2007: ThePhysical Science Basis. Contribution ofWorking GroupI tothe Fourth Assessment Report ofthe Intergovernmental Panel onClimate Change (IPCC). Cambridge, UK, Cambridge University Press: 3–18. Katayama N., Yamashita M., Wada H., Mitsuhashi J. (2005): Space agriculture task force; entomophagy aspart ofaspace diet for habitation onMars. TheJournal ofSpace Technology and Science, 21:27–38. Klunder H.C., Wolkers-Rooijackers J., Korpela J.M., Nout M.J.R. (2012): Microbiological aspects ofprocessing and storage ofedible insects. Food Control, 26:628–631. Kodelja V., Müller C., Tenorio S., Schebesch C., OrfanosC.E., Goerdt S. (1997): Differences inangiogenic potential ofclassically vs alternatively activated macrophages. Immunobiology, 197:478–493. Kouřimská L., Adámková A. (2016): Nutritional and sensory quality ofedible insects. Nutrition and Food Science (NFS) Journal, 4:22–26. Kwon G.T., Yuk H.G., Lee S.J., Chung Y.H., Jang H.S., YooJ.S., Cho K.H., Kong H., Shin D. (2020): Mealworm larvae (Tenebrio molitor L.) exuviae asanovel prebiotic material for BALB/c mouse gut microbiota. Food Science Biotechnology, 29:531–537. Larde G. (1990): Recycling ofcoffee pulp byHermetia illucens (Diptera: Stratiomyidae) larvae. Biological Wastes, 33:307–310. Lesnik J.J. (2014): Termites inthe hominin diet: Ametaanalysis oftermite genera, species and castes asadietary supplement for South African robust australopithecines. Journal ofHuman Evolution, 71:94–104. Leung P.S., Chow W.K., Duffey S., Kwan H.S., Gershwin M.E., Chu K.H. (1996): IgEreactivity against across-reactive allergen incrustacea and mollusca: Evidence for tropomyosin asthe common allergen. Journal ofAllergy and Clinical Immunology, 98:954–961. Li Q., Zheng L., Cai H., Garza E., Yu Z., Zhou S. (2011a): From organic waste tobiodiesel: Black soldier fly, Hermetia illucens, makes itfeasible. Fuel, 90:1545–1548. Li Q., Zheng L., Qiu N., Cai H., Tomberlin J.K., Yu Z. (2011b): Bioconversion ofdairy manure byblack soldier fly (Diptera: Stratiomyidae) for biodiesel and sugar production. Waste Management, 31:1316–1320.