Edible insects are a well-appreciated food source (entomophagy) in many regions of Africa, Asia, and the Americas.[1] In Western countries, the use of insects as food and feed is gaining attention as consumers learn of the nutritional and environmental benefits associated with them.[2] Globally, over 2,000 species are known to be edible and consumed by approximately 2 billion people.[3] According to a global estimation, the most commonly consumed insects by humans are beetles (31%), caterpillars (18%), and bees, wasps, and ants (14%). In addition, consumption of grasshoppers, locusts, and crickets is about 13 percent, followed by cicadas, leafhoppers, plant hoppers, scale insects, and true bugs (10%), termites (3%), dragonflies (3%), flies (2%), and others (5%) (Figure 1).[3]

Insect consumption is usually promoted for three major reasons: nutritional value, environmental benefits, and livelihood improvement (social and economic factors).[4] The nutritional value (relative amount of proteins, fat, vitamins, and calories) compares favorably with that of meat and fish[3] and can reduce nutrient deficiencies in populations consuming them. Furthermore, edible insects can be used in fortified blended foods in countries with food insecurity mainly because of their high protein and micronutrient content and the high bioavailability of nutrients.[5] In terms of environmental benefits, insects emit less greenhouse gas and ammonia[6] as they are mostly omnivorous and therefore could be raised on various organic waste/agricultural side streams. Edible insects have also been reported to contribute significantly to food security and livelihoods in most African countries where they are consumed. For instance, some communities trade the harvested insects to nearby markets, generating income to improve their livelihood.

The demand for affordable, alternative, and sustainable protein sources is surging globally due to the increase in the world’s population, which is projected to reach 9.7 billion by 2050. From this perspective, the Food and Agriculture Organization (FAO) of the United Nations proposed a global initiative to increase use of insects as food and feed to ensure future food security.[3] The potential of insect food has generated global interest to develop and use insect-food products, such as those shown in Figure 2, and has promoted more research and development on edible insects. Since many countries have a history of using insects as food, this traditional knowledge should be an essential contributor to the future development of insects as a food ingredient worldwide.

Risks Associated with Edible Insects
Just like vertebrates, insects can contain biological agents and substances that can represent a health threat to consumers. In an opinion on the risks associated with using insects as a food and feed, the European Food Safety Authority[7] concluded that the risks highly depended on the species of insect, the feed they consume, environment they inhabit, and the production and processing methods adopted. This complexity is the reason consumers are advocating for assurance of the safety of edible insects. The risks can be greater when edible insects are harvested from the wild, as is the case in most African countries. This makes it difficult to control the hazards emanating from the food that the insects consume in the wild. However, in most European countries, or in cases where the insects are farmed, the insects are reared in controlled environments, in which sanitary techniques are usually employed, thus reducing some hazards such as microbiological contamination.[8] Therefore, the differences in the habitats the edible insects are harvested from can contribute to differences in their safety.

Microbial Hazards
Insects both collected in nature and raised on farms may be infected with pathogenic microorganisms, such as bacteria (Staphylococcus, Bacillus, Campylobacter, Pseudomonas, Micrococcus, Acinetobacter, Proteus, Escherichia, Enterobacteriaceae, and other spore-forming bacteria), viruses, fungi, and protozoa.[9] However, specific studies on the microbiological safety of insects specifically reared versus wild-harvested for food or feed production are rare in the scientific literature.

In West Africa, three rhinoceros beetle species of the genus Oryctes are commonly consumed: Oryctes monoceros and Oryctes owariensis, which breed in dead-standing coconut and oil palms, and Oryctes boas, which is found in rotting vegetation and manure heaps. Pathogenic bacteria including Staphylococcus aureus, Pseudomonas aeruginosa, and Bacillus cereus that may pose a risk to the health of consumers have also been reported in association with these insects.[10] In Botswana, the inner flesh of the wild-harvested mopane caterpillar, Imbrasia belina, has been observed disintegrating due to mold growth with fungal isolates Aspergillus, Penicillium, Fusarium, Cladosporium, and Phycomycetes.[11] Wild-harvested raw grasshoppers (Ruspolia differens) from Eastern Africa were found to be highly contaminated by Enterobacteriaceae, lactic acid bacteria, yeast and molds, and bacterial endospores.[12]

A study on four farmed commercial insect species (superworm larvae, mealworm larvae, greater wax moths, and house crickets) showed a high total microbial charge (10⁵–10⁶ CFU/g) on samples originating from a closed-cycle farm. It was mainly composed of Gram-positive bacteria (fecal and total coliforms). However, Salmonella spp. and Listeria monocytogenes were not isolated from the tested samples. Similarly, in fresh-farmed insects (mealworm larvae, house crickets, and Brachytrupes spp.), spore-forming bacteria and Enterobacteriaceae were isolated.[9] Furthermore, a study in Belgium reported high microbial contamination in mealworm larvae (Tenebrio molitor) and crickets (Acheta domesticus and Gryllodes sigillatus), with average counts for both types of insects above 7.6–8.8-log CFU/g. The identified bacteria include Enterobacteriaceae, lactic acid bacteria, yeast and molds, and aerobic bacterial endospores.[13] A study involving A. domesticus, Gryllus assimilis, Gryllus bimaculatus, Locusta migratoria, Blaptica dubia, Galleria mellonella, Chilecomadia moorei, Pachnoda marginata, T. molitor, Zophobas atratus, and Apis mellifera reported the presence of B. cereus, S. aureus, Escherichia coli, Salmonella, Shigella, and Campylobacter.[14]

In a risk assessment study in the Netherlands,[15] the results of a small-scale survey on the microbiological status of 55 insect products (locusts, lesser mealworms, mealworms, and a mealworm snack) that had undergone no treatment apart from freeze-drying found that 59 percent of the insect products exceeded the process hygiene criterion for aerobic bacteria in raw materials used in meat preparation (10⁶ CFU/g), while the concentration of Enterobacteriaceae in 65 percent of the samples exceeded the criterion for raw materials used in meat preparations (10³ CFU/g). The study investigated the presence of Clostridium perfringens, Salmonella, and Vibrio, and none of these were detected. In 93 percent of the samples, the concentrations of the spore-forming bacterium B. cereus were less than 100 CFU/g.

Chemical Hazards
Like products from other animals, insect-derived food and feed products may contain hazardous chemicals. Some of these chemicals may be present in the substrates for insects, such as environmental contaminants like heavy metals, organochlorines such as dioxins, mycotoxins, and plant toxins, for example.

Harmful metals from the environment have been found in the insects’ fat, exoskeleton, reproductive organs, and digestive tracts, where they accumulate. Concentrations of heavy metals in insects depend on the characteristics of the elements and their concentrations in the substrates, the insect species, and their growth stage. However, there are limited data available regarding the influence of different substrates on the heavy metal concentration in farmed insects. A study on the yellow mealworm (T. molitor) and black soldier fly (Hermetia illucens) larvae showed that the insects accumulate cadmium, lead, and arsenic when they feed on contaminated substrates, such as organic matter in soils that contain these metals.[16] The European Union specified the maximum content for cadmium in feed materials of animal origin to be 2 mg/kg (88% dry matter); the insect samples analyzed had concentrations below this limit. High lead content was found in dried grasshoppers, and the dehydration increased lead concentration, while extreme accumulation of selenium was found in T. molitor larvae.[16]

Pesticides used against invading insects are potentially dangerous for consumers, particularly if the insects and insect products have been obtained by wild harvesting rather than controlled farming. It is a real problem in some developing countries, where edible, even dead insects, mainly locusts and grasshoppers, are collected and consumed after insecticide treatment. For instance, according to a study in Kuwait, the collected locusts contained no chlorinated pesticides, but a relatively high amount of organophosphorus pesticides were found, possibly due to the pesticides that were used in that area.[17] However, in cases of pesticide treatment, only about less than 0.1 percent of pesticides applied reaches the target pests; the remaining 99.9 percent moves into the environment and may accumulate in the beneficial biota, soil, and water, therefore accumulating in edible insects through the substrate used for feeding.[18]

Information is scarce on the mycotoxin contamination of edible insects. Low levels of aflatoxin B1 were reported in edible stinkbugs that were collected in the forest and stored in traditionally woven wooden dung-smeared baskets and gunny bags previously used to store cereals.[19] Aflatoxin contamination was reported in edible mopane caterpillar (I. belina), and the level of total aflatoxins varied from 0 to 50 μg/kg of product.[11]

Efficacy of Processing Methods in Reducing Risks
Processing of edible insects can help lower the microbial load and the chemical hazards present in the insect. In addition, processing could increase the acceptability, palatability, and digestibility of insects and insect-based products. A recent study showed that drying, boiling or blanching, roasting, frying, fermenting, smoking, and milling of dried insects are the most commonly used processing methods.[20] The processing methods can be applied solely or in combination; for example, boiling preceded most of the other processes like frying, roasting, and drying.[20]

When wild-harvested grasshoppers (R. differens) were either deep-fried, smoked, or toasted, Enterobacteriaceae and lactic acid bacteria were completely eliminated, while bacterial endospores were not, highlighting the importance of good handling practices during harvesting and transportation.[12] Another study reported that boiling followed by open-pan roasting and hot-ash roasting of mopane worms is the most effective process to reduce microbial contamination.[20] In addition, a combination of wet heating and dry heating (boiling and open-pan roasting) as compared with dry heating (hot-ash roasting), as well as hygienic handling (using gloves during degutting), helped lower E. coli and S. aureus in mopane worms.[21] Normally, dry heat is usually associated with a lower heat transfer rate that will be insufficient in eliminating some the bacteria.

A study on the effect of processing fresh samples of farmed mealworm larvae (T. molitor) and house crickets (A. domesticus) showed that a short heating step was sufficient to eliminate Enterobacteriaceae, while spore-forming bacteria were not eliminated.[9] In addition, simple processing methods such as drying/acidification were considered promising in controlling Enterobacteriaceae and bacterial endospores.[9]

When the effects of blanching (for 10, 20, or 40 seconds), followed by either chilled storage or industrial microwave drying, on microbial counts of yellow mealworm larvae (T. molitor) were studied, considerable log reductions were obtained (total viable count, Enterobacteriaceae, lactic acid bacteria, yeasts and molds, and psychrotrophs) at whatever time applied, except for aerobic endospores. No major growth was observed during subsequent chilled storage for 6 days, while blanching for 40 seconds followed by industrial microwave drying for 8, 10, or 13 minutes did not yield larvae with a water activity below 0.60, which is necessary to eliminate all microbial growth.[22]

A study that characterized the effects of different household cooking methods (boiling, panfrying, vacuum cooking, and oven cooking) on the microbial load and nutritive value of mealworms, with a focus on protein digestibility and fatty acid composition, showed that boiling and cooking under vacuum were the most efficient techniques to reduce microbial load while maintaining the high levels of protein and polyunsaturated fatty acids of mealworms.[23] Cooking method-related changes were very low on macronutrient content except for panfried mealworms, which exhibited the highest lipid content.[23] A study microbiologically analyzed a total of 38 samples of deep-fried and spiced (A. domesticus, L. migratoria, and Omphisa fuscidentalis), cooked-in-soy-sauce (“tsukudani”; Oxya yezoensis, Vespula flaviceps, and Bombyx mori), dried (A. domesticus, L. migatoria, Alphitobius diaperinus, T. molitor, B. mori, H. illucens, and Musca domestica), powdered (H. illucens and T. molitor), and other (deep-frozen B. mori and honeybee pollen) insect products.[14] Although each product type revealed a microbiological profile of its own, dried and powdered insects displayed markedly higher counts than the deep-fried and cooked ones. All samples were negative for salmonellae, L. monocytogenes, E. coli, and S. aureus, but dried and powdered insects, as well as pollen, contained B. cereus, coliforms, Serratia liquefaciens, L. ivanovii, Mucor spp., Aspergillus spp., Penicillium spp., and Cryptococcus neoformans.[14]

Boiling and drying lowered the amount of anti-nutrients (oxalates, phytates) in Encosternum delegorguei, while a decrease in the anti-nutritional factors of degutted, boiled, and milled wild-harvested Cirina forda (Westwood moth) larvae was reported in Zimbabwe.[24] As shown in the studies above, the processing methods adopted may contribute greatly toward improving the safety of edible insects and insect-based products.

Conclusion
Generally, the levels of hazards are higher in fresh insects than in processed insects/insect-based products. In addition, it’s highly likely that insects that are farmed under controlled, hygienic conditions may have lower levels of hazards as compared with wild-harvested insects. However, in the literature, there is little information regarding the hazards related to human consumption of insects. The available information is not very detailed or relies on the extrapolation of information on the consumption of other foodstuffs. Nevertheless, the common processing methods adopted in edible insects (drying, boiling or blanching, roasting, deep-frying, toasting, fermentation, smoking, and milling) are sufficient in eliminating common foodborne pathogens such as salmonellae, L. monocytogenes, E. coli, and S. aureus.

However, using the above-discussed processing methods (e.g., heat treatment below sterilization conditions), spore-producing bacteria may not be eliminated, and the spores may survive and germinate, leading to an important potential hazard—botulism. Thus, whatever way edible insects are processed and whatever insect species is considered, bacterial spores and their survival need special attention. In addition to a thermal treatment, appropriate storage conditions are consequently important. Furthermore, during processing of insects, toxic substances or process contaminants, such as heterocyclic aromatic amines, polyaromatic hydrocarbons, acrylamide, chloropropanols, and furans, can be formed by chemical reactions between the insects and other ingredients. However, this requires further research. Good Manufacturing Practices will be critical in the use of insects as food ingredients to eliminate the physical hazards in addition to biological and chemical hazards.   

John N. Kinyuru, Ph.D., RNutr, and Jeremiah Ng’ang’a are from the Department of Food Science and Technology at Jomo Kenyatta University of Agriculture and Technology, Kenya.

References
1. Christensen, DL, et al. 2006. “Entomophagy among the Luo of Kenya: A Potential Mineral Source?” Int J Food Sci Nutr 57:198–203.
2. Megido, RC, et al. 2014. “Edible Insects Acceptance by Belgian Consumers: Promising Attitude for Entomophagy Development.” J Sensory Stud 29:14–20.
3. Van Huis, A. 2013. “Potential of Insects as Food and Feed in Assuring Food Security.” Annu Rev Entomol 58(1):563–583.
4. Roos, N and A van Huis. 2017. “Consuming Insects: Are There Health Benefits?” J Insects Food Feed 3(4):225–229.
5. FAO. Edible Insects. Future Prospects for Food and Feed Security (2013).
6. Oonincx, DGAB, et al. 2010. “An Exploration on Greenhouse Gas and Ammonia Production by Insect Species Suitable for Animal or Human Consumption.” PLoS One 5(12):1–7, e1445.doi: 10.1371/journal.pone.0014445.
7. E. S. Committee. 2015. “Risk Profile Related to Production and Consumption of Insects as Food and Feed.” EFSA J 13(10):4257.
8. Rumpold, BA and OK Schluter. 2013. “Nutritional Composition and Safety Aspects of Edible Insects.” Mol Nutr Food Res 57(5):802–823.
9. Klunder, HC, et al. 2012. “Microbiological Aspects of Processing and Storage of Edible Insects.” Food Contr 26(2):628–631.
10. Banjo, AD, et al. 2006. “The Microbial Fauna Associated with the Larvae of Oryctes monoceros.” J Appl Sci Res 2(11):837–843.
11. Mpuchane, S, et al. 2000. “Quality Deterioration of Phane, the Edible Caterpillar of an Emperor Moth Imbrasia belina.” Food Contr 11(6):453–458.
12. Ng’ang’a, J, et al. 2018. “Microbial Quality of Edible Grasshoppers Ruspolia differens (Orthoptera: Tettigoniidae): From Wild Harvesting to Fork in the Kagera Region, Tanzania.” J Food Safe August:1–6.
13. Vandeweyer, D, et al. 2017. “Microbial Counts of Mealworm Larvae (Tenebrio molitor) and Crickets (Acheta domesticus and Gryllodes sigillatus) from Different Rearing Companies and Different Production Batches.” Int J Food Microbiol 242:13–18.
14. Grabowski, NT and G Klein. 2017. “Microbiology of Processed Edible Insect Products – Results of a Preliminary Survey.” Int J Food Microbiol 243:103–107.
15. Netherlands Food and Consumer Product Safety Authority. Advisory Report on the Risks Associated with the Consumption of Mass-Reared Insects. zenodo.org/record/439001#.XRu3qOtKgdU (2014).
16. Vijver, M, et al. 2003. “Metal Uptake from Soils and Soil–Sediment Mixtures by Larvae of Tenebrio molitor (L .) (Coleoptera).” Ecotoxicol Environ Safe 54:277–289.
17. Saeed, T, et al. 1993. “Analysis of Residual Pesticides Present in Edible Locusts Captured in Kuwait.” Arab Gulf J Sci Res 11:1–5.
18. Pimentel, D, et al. 1995. “Amounts of Pesticides Reaching Target Pests: Environmental Impacts and Ethics.” J Agric Environ Ethics 8(1):17–29.
19. Musundire, R, et al. 2016. “Aflatoxin Contamination Detected in Nutrient and Anti-Oxidant Rich Edible Stink Bug Stored in Recycled Grain Containers.” PLoS One 11(1):1–16.
20. Murefu, TR, et al. 2019. “Safety of Wild Harvested and Reared Edible Insects: A Review.” Food Contr 101:209–224.
21. Mujuru, FM, et al. 2014. “Microbiological Quality of Gonimbrasia belina Processed under Different Traditional Practices in Gwanda, Zimbabwe.” Int J Curr Microbiol Appl Sci 3(9):1085–1094.
22. Vandeweyer, D, et al. 2017. “Effect of Blanching Followed by Refrigerated Storage or Industrial Microwave Drying on the Microbial Load of Yellow Mealworm Larvae (Tenebrio molitor).” Food Contr 71:311–314.
23. Caparros Megido, R, et al. 2018. “Effect of Household Cooking Techniques on the Microbiological Load and the Nutritional Quality of Mealworms (Tenebrio molitor L. 1758).” Food Res Int 106 (2017):503–508.
24. Musundire, R, et al. 2014. “Nutrient and Anti-Nutrient Composition of Henicus whellani (Orthoptera: Stenopelmatidae), an Edible Ground Cricket, in South-Eastern Zimbabwe.” Int J Trop Insect Sci 34(4):223–231.