2. Insect Consumption Preferences in Europe

Nutritional neophobia occurs as an evolutionary adaptation aimed at avoiding potential hazards resulting from the consumption of novel foods. This situation affects various aspects of human nutritional behaviour, including nutritional preferences and choices ^[8]. The approach to edible insects is particularly negative for consumers in countries with no tradition of insect consumption. Insects arouse disgust and aversion ^[9]. It is worth stressing, however, that a significant number of edible insects are herbivores that feed on fresh leaves or wood. From this perspective, they are more hygienically safe than the seafood or frogs that are popular in Europe ^[10]. However, the barrier is culinary practice and the difficulty in the integration of insects into existing dietary practices. It seems that marketing efforts and attempts to combine insect products with traditional eating habits have not brought the expected results yet. The cultural, social, and psychological aspects in consumers may be crucial when they decide to try novel food of insect origin. Consumers are not certain of safety and pay attention to possible hazards associated with insect diseases and the conditions resulting from consuming them. It is noteworthy that Americans or Asians ^[11][12][13] are more inclined to introduce insects into their diet than the inhabitants of Europe ^[13][14][15] or Australia ^{[16][17][18][19]}.

The decision to introduce insects into the diet, particularly in Europe, is linked to the understanding of the wider context: social, economic, and ecological. In routine consumer studies, it is the same determinants, i.e., the price, flavor, availability and habit, that usually determine the choice of a food product. However, as regards insect-based products, consumers are guided by different criteria. The main emphasis is placed on the aspect of the so-called higher necessity in the name of the common good. This establishes completely new tasks and expectations for producers and the market ^[20]. Table 1 provides current research into the preferences with regard to and acceptance of insects or insect-based products among the inhabitants of European countries.

Table 1.

Summary of studies on implementation of insects as functional additives to food in Europe.

Kind of Insect	Reference	Research	Counrty	Results
(T. molitor L.) (A. domesticus) Insects flour Whole insects	[99]	insect chips, insect bar, whole insects	Italy n = 62	The highest palatability rating for a bar with insect meal (6.95), followed by whole crickets (6.64, crisps with insect meal (6.33). The lowest rating for insects in carmel (6.02).
(A. domesticus) Insects flour	[100]	Acceptability and sensory evaluation of energy bars and protein bars enriched with edible insect	Czech n = 96	The bars are acceptable to consumers in the Czech Republic, with the best rating for bars with the addition of a tropical flavor
(A. domesticus) Insects flour Whole inscets	[95]	Two types of jelly 1—with the addition of whole insects 2—with the addition of cricket flour	Italy n = 88	Insect jellies were rated better than before tasting. Jellies with the addition of cricket powder were better shaded than those with a visible insect.
(T. molitor L.) Insect flour	[69]	Addition of insect flour to bread dough in the amount of 5%, 10%	Italy n = 9	Bread with the addition of mealworm powder scored worse than the control sample. Bread with 5% insect flour was assessed slightly better
(A. domesticus) Cricket powder	[44]	Addition of powder to bread dough in the amount of 10%, 30%	Italy n = 9	Bread with the addition of cricket powder was evaluated worse than the control sample. Bread with 10% insect flour was rated slightly better
(T. molitor) Mealworm powder	[101]	50% addition to beef and green lentil burgers	Belgium n = 79	The mealworm burgers scored lower than the beef burger, but better than the lentil burger. The mixture of mealworm with beef was rated slightly better than with lentils.
(T. molitor) (A. diaperinus) Mealworm powder	[102]	Addition of insect powder to bread dough	Spain n = 327	Bread with the addition of mealworm powder was better rated than the bread with the addition of buffalo larvae powder and comparable to the control bread. The greater addition of mealworm powder (10%) made the bread with its addition the tastiest among the analyzed variants.
(A. domesticus) Cricket powder	[103]	Addition of 5%, 10%, 15% cricket powder to pasta	Poland n = 20	A consumer evaluation showed that the use of the CP additive was well received. The color of the pasta sample with 5% CP was described by consumers as resembling wholemeal pasta.
(B. mori) Silkworm powder	[83]	Addition of silkworm powder 5 and 10 g to buckwheat pasta	Hungary n = 98	The highest acceptance was obtained for pasta with a higher content of silkworm powder = 10 g
(A. domesticus) Cricket powder	[104]	Addition of cricket powder 5%, 10%, 15% to oat biscuits	Hungary n = 100	The biscuits with the addition of 5%/100 g CP obtained the highest acceptance, but the other variants also obtained the acceptance level

In general, it needs to be stressed that the unwillingness to consume insects is mainly related to concerns about the flavor, aroma and structure of the product as well as health safety. The gathered insects are usually scalded with hot water following a starvation period of 1–3 days. Further culinary processing includes cooking, roasting, frying or drying. All additional technological operations result in changes to the flavor and aroma while offering the possibility of modifying them. Insects’ flavors are very diverse, which is supposedly due to the pheromones found on the insect body. The flavor can also be modelled using properly prepared feed and farming conditions as well as the thermal processing method. Roasted or fried insects are considered to be the tastiest. Consumers point out that the most common flavors include nutty, mushroom, forest, fish or baked potato flavor. In order to improve the acceptability on the European market, it is possible to purchase freeze-dried insects enriched with various flavorings and spices, for example, curry powder, garlic, paprika or fried onion flavor. The offer is not limited only to savoury flavors, as producers also offer insects in salty caramel or with chocolate. The color of a meal prepared from insects is of significance as well. Raw insects are usually dark-grey to grey, which, from the consumer’s perspective, is not an attractive feature. On the other hand, due to thermal processing, they take on a red color with shades of brown. Properly dried or freeze-dried insects take on a golden color ^[21].

The texture of insects ranges from crunchy to soft ^[22]. Some of them are very hard and have an irregular structure, which may considerably limit the placing on the market and the consumers’ acceptance. Insects with exoskeletons are crunchier due to the presence of chitin. On the other hand, larvae and caterpillars have a more delicate structure. The acquisition method and technological processing are of significance as well. In Europe, insects are most often sold in whole, freeze-dried or as a powder. It appears that the use of insect flour or protein concentrates as a food ingredient is by far most likely to be successful on the market ^[23] used the addition of insect protein hydrolysate in the production of sausages. Many positive functional characteristics were noted. Enrichment with insect flour decreased the moisture content in the sausage, which contributed to a change in rheological characteristics. Protein has repeatedly been the subject of research into the possibility for using it in bakery and confectionery production ^[24][25]. In one of the studies, grasshopper and mealworm beetle flours were added to traditional Turkish egg noodles. The assessed samples of egg noodles exhibited better functional effects, but the sensory assessment indicated lower acceptance towards the control sample. However, the rating was not disqualifying ^[26]. Insect proteins are also used as concentrates and isolates in designing functional food. Solubility is one of the major functional properties which regulate the food modelling processes. The degree of protein solubility in an aqueous solution determines its foaming, gelling and emulsifying abilities ^[27]. Having considered all functional characteristics of insect protein, they are recognized as distinguishable among other protein sources in food. What is more, the introduction of insect protein into designed food may prolong the feeling of satiety. This aspect is rarely addressed in such studies. Having considered the problem of world hunger, on the one hand, and the obesity epidemic on the other, it appears appropriate to carry out further research into the satiating properties of insect protein ^[28].

3. Hazards Related to the Production and Consumption of Insects in Europe

The rapidly developing industry involving insects as food is increasingly promoted as a sustainable alternative to other animal protein production systems. However, it is not completely clear if the European food market is ready for this type of food. The exact technological, economic, ecological and health-related advantages are not clear due to an overwhelming lack of knowledge on almost all of these aspects (Figure 1). It is essential to select appropriate species and the conditions for their growth, particularly as regards rooms, climatic factors and the entire control and surveillance system. It is necessary to examine whether or not the forced selection in one stage of an insect’s life has an adverse effect on other stages, for example through reducing the survival rate, reproductive functions or potential nutritional value. The system for controlling sick individuals and methods of their treatment, particularly the use of antibiotics and growth-promoting substances, is a gap in the knowledge. The system of insect feeding which includes the striving for breeding maximization while ensuring physical, biochemical and microbiological safety of insect-based food products, must also be subject to standardization.

Figure 1.

Gaps in the areas of knowledge concerning the edible insect market.

From a technological perspective, not only the breeding process but also the method for preparing insects for the consumption, packing methods and effective distribution needs to be safeguarded. This, in turn, will determine the form of the sales system. The production of insects should be based on economic prerequisites of sustainable development. It should provide sufficient quantities of food of acceptable quality and appropriate efficiency, which, due to certain constraints, is extremely difficult. It is necessary to calculate the costs related to the production, breeding and transport. It appears that this can be one of the barriers to the introduction into the global and European food market. Nowadays, most industrial production is based on high-efficiency drying or freeze-drying processes, which considerably increase the production costs.

If sustainable environmental development is to be the paramount feature of the mass production of insects for the consumption, it is necessary to conduct research related to sustainable development criteria, which are directly linked to crucial aspects of industrial development ^[29]. First of all, breeding may directly affect the adjacent natural systems. What is particularly dangerous is the possibility of an uncontrolled, extensive spread of insects into areas where they are an endemic species or are not found in a particular ecosystem at all, which can have very serious consequences, both environmentally and economically. Moreover, there are no accurate data on the emissions of greenhouse gases released during insect production. It is indisputable that insect breeding on a mass scale generates fewer pollutants and residues than the breeding of other animals ^[30]. Moreover, the biomass conversion rate is lower and the production duration is much shorter than for any other animals. The use of water and land is lower than that for conventional breeding. Sometimes edible insects are crop pests and gathering them in the fields ensures both a source of food and lasting protection of crops without the use of chemical pesticides which must also be considered ^[31].

Another aspect is the thorough examination of the effect of insect consumption on health. As the subject of hazards to human health following the consumption of insects is new, there are few studies concerning this area of knowledge ^[29].

It follows from the available data that the emerging concerns can be considered in terms of chemical and microbiological hazards. The dynamic development of production raises questions about methods of killing insects and related ethical dilemmas. It will be necessary to develop a code and / or regulation setting morally accepted standards on insects’ welfare.

The most common chemical hazards include the presence of heavy metal and the residues of veterinary drugs, halogenated organic compounds and pesticides. Since the main passage of chemical exposure will be the substrate on which the insect grows, it is important to use a suitable substrate and ensure continuous monitoring during breeding ^[32]. Studies into insect heavy metal concentrations have mostly concerned insects bred in the feed industry and not as human nutrition products. Few studies report on increased levels of certain heavy metals such as cadmium, arsenic, lead and mercury ^[33][34][35]. This problem more often concerns insects gathered using a traditional method, where the natural environment of the particular area, in which the insects are found, is of crucial importance.

Moreover, problems resulting from the presence of toxins and veterinary drug residues were identified as well. Toxins contained in insects are most often the result of either the spontaneous synthesis of a natural toxin characteristic of the particular species or its accumulation, most often from a substrate. One of the studies analyzed 69 mycotoxins in flies. The study detected only three mycotoxins (enniatin A—12.5 µg/kg, A1—7.3 µg/kg, and beauvericin) ^[36][37]. It is believed, however, that the identified mycotoxin levels did not pose a health hazard, which was also confirmed by studies by ^[38][39].

The substrate quality is also linked to the presence of residues of veterinary drugs, mainly antibiotics, which could also pose an actual health hazard. Unfortunately, there is insufficient data on this subject ^[32]. Apart from drugs, agricultural waste residues, including pesticides and dioxins, can be hazardous as well, particularly when using a plant substrate ^[40].

Insects are a habitat of numerous microorganisms, including certain human pathogenic bacteria. Over the last few years, the focus has been on the microbiological safety of insects intended for consumption. It was assumed that the major hazard were zoonoses transmitted by insects. On the other hand, this is not supposed to happen under controlled breeding conditions. A greater hazard is posed by the microflora which may result from inappropriate breeding and the failure to comply with basic sanitary recommendations concerning processing and transport. Although it is believed that the viruses borne by insects are not dangerous to humans ^[41], mention a wide range of viruses that may pose a health hazard to humans.

Little is known about microbiology of processed insect products. One study examined a total of n = 38 samples subjected to various types of thermal processing. The presence of Enterobacteriaceae, staphylococci, bacilli as well as numerous yeasts and molds was detected. Even though each product type exhibited its own microbiological profile, the results for all samples were negative for the presence of Salmonella, L. Monocytogenes, E. Coli and Staphylococcus aureus, dried and powdered insects and dust particles contained B. cereus, coliform bacteria, Serratia liquefaciens, Listeria ivanovii, Mucor spp., Aspergillus spp., Penicillium spp. and Cryptococcus neoformans. Having compared the results with hygienic criteria for edible insects proposed by Belgium and the Netherlands, Class I products failed to meet many limits for bacterial count despite the absence of classical food pathogens. Therefore, it is recommended that Class I products should always be consumed following additional thermal processing ^[42].

Scarce studies show that the priority for microbiological purity includes the processing method and appropriate conditions for the storage of insects in each breeding farm ^[43]. Moreover, insects, just like all animals, can hide and transmit parasites, e.g., the nematodes Gongylonema pulchrum ^[44][45]. There is, however, insufficient data to determine whether such a hazard occurs under controlled industrial breeding conditions.

To sum up, the hazards to human health following the consumption of insect meat are largely induced by the quality of the breeding substrate and the proper implementation of all production stages, i.e., the processing, storage and distribution. Microbiological safety appears to be the biggest knowledge gap and that needs to be thoroughly investigated in the near future.

Edible insects are an important source of food worldwide. However, insufficient attention is paid to the undesirable allergic reactions caused by the consumption of insects, as insect protein is mentioned as a possible allergenic component ^[46]. Allergies to insect protein can be divided into the primary allergy to insects and susceptibility to cross-reactions with other allergens. There are few studies based on clinical trials on humans. Tests have been conducted on rats, mice and guinea pigs. The irritating agent was the proteins of the Japanese beetle, the mealworm beetle, and the cricket. Allergy to the mealworm beetle was only demonstrated on a mouse model. It was recognized that insect protein binds chitin and troponin, which may indicate that allergy to insects may also occur in humans ^[47]. A study by Francis et al. ^[48] suggests that exposure to insect allergy is not only oral but also includes inhalation or contact. Arginine kinase, paramyosin and chitin were responsible for allergic reactions in patients consuming silkworms. Similar study results were obtained by identifying the potential allergens in the mealworm beetle: arginine kinase, tropomyosin and both heavy and light myosin chain ^[49].

Certain researchers also indicate the possibility of cross allergies. One of the studies tested patients allergic to crustaceans and house dust mites. The entire test group, which exhibited allergy to crustaceans, exhibited allergy to mealworm beetle protein as well ^[50]. Leung et al. ^[51] reported a cross allergy between insects (grasshopper, cockroach, common fruit fly) and prawns for n = 9 subjects. In this case, tropomyosin was identified as the main allergen, probably because insects are closely related to crustaceans and HDM, in which the main allergens include tropomyosin and arginine kinase. Unfortunately, due to the scarce knowledge on this subject and the lack of diagnostic test consistency, it is not possible to clearly identify allergic relationships ^[52]. Additionally, the changes in insect proteins during thermal and further processing need to be examined ^[53]. As long as allergies to insects are poorly understood, it is necessary to be particularly careful and the information on packaging should include information on possible allergens. In addition, edible insects contain significant amounts of purines (adenine, guanine, xanthine, and hypoxanthine) and uric acid, which may limit the possibility of consumption in patients with gout ^[54].

4. Conclusions

Associating insects with food for humans triggers two completely different mental reactions. In countries where entomophagy is traditionally, or commonly, practised, insects are perceived as a valuable and traditional source of food, the knowledge of which is passed from generation to generation. Indeed, through globalization, insect consumption can sometimes be viewed, especially by younger people, as backward. On the other hand, in Western cultures, insects may provoke strong negative mental reactions, for example, repulsion.

In conclusion, the approach to entomophagy is determined by several major factors of a psychological, social, religious and anthropological nature. Since certain nutritional habits develop in childhood, it is suggested that in the future this will be the target group in highly developed countries.

Many supporters of the entomophagy sector believe that, in the years to come, a new emerging market of insects or their components (e.g., bakery products and snacks) may appear in many European countries, particularly in Northern Europe where certain insects had been available on the market even before the full application of the Regulation on new foods.

However, for such a trend to be sustained, it is necessary to understand the needs of consumers, therefore consumer acceptance is one of the most important challenges for food producers. Intensive marketing efforts and long-term educational strategies are needed to reduce uncertainty, ignorance and consumer reluctance and allow insects to be slowly introduced into the daily diet. In the case of European countries, it should be assumed that changes in eating habits in the context of the consumption of edible insects take time. Therefore, the method of small steps should be used here, in order to first target young Europeans who care about the environment and health, but who are also open and willing to change their eating habits. With the above in mind, an analysis of consumer preferences is required. The key to increasing interest in entomophagy is the development of products that are characterized by high trust, sensory appeal and health safety.

Future research should focus on finding the optimal conditions for breeding and processing insects into various forms with desirable functional properties and accepted sensory characteristics while maintaining a positive economic balance and environmental sustainability. One of the major challenges is the safety of consumption. This requires the development of precise legislation concerning production, distribution, sales and health safety. Therefore, further analysis should target these identified areas.