Food Control 108 (2020) 106877

Contents lists available at ScienceDirect

Food Control
journal homepage: www.elsevier.com/locate/foodcont

Review

Insects as food: A review on risks assessments of Tenebrionidae and T

Gryllidae in relation to a first machines and plants development
Alessio Cappellia,∗, Enrico Cinia, Chiara Lorinib, Noemi Olivaa, Guglielmo Bonaccorsib
a
Department of Agriculture, Food, Environment and Forestry (DAGRI), University of Florence, Piazzale Delle Cascine 16, 50144, Florence, Italy
b
Department of Health Sciences, University of Florence, Viale GB Morgagni 48, 50134, Florence, Italy

A R T I C LE I N FO A B S T R A C T

Keywords: The demand for protein food with low environmental impact is currently a major challenge for food production.
Novel food Insects represent a potential source of good quality food, that is rich in nutrients, cheaper, and easier to produce,
Food safety with potentially lower environmental impact. Nevertheless, insects could present significant risks for the con-
Insect protein sumers' safety and for the workers of this emerging production chain. This highlights the need for a specific
Mealworm
comprehensive approach that can guarantee safe working conditions and risk-free products. The aim of this
Cricket
review is to summarize the current knowledge pertaining to the potential microbial, chemical, physical, and
Food industry
allergenic risks in the breeding, transformation, and consumption of edible insects. In particular, given the lack
of specific studies, the purpose of this paper is to suggest strategies to orient the development of machines and
plants in the emerging production chain of insects for food, with ameliorative effects on both finished product
and workers’ safety. Despite a very appealing nutritional profile that is rich in high quality proteins, lipids,
vitamins, minerals, and fiber, insects present several risks, mainly related to microbial contamination, accu-
mulation and production of chemical contaminants like toxins and heavy metals, allergenicity through inhala-
tion or food ingestion by workers and consumers. This paper, according to the findings achieved by the sys-
tematic review, suggests strategies, processes, and treatments, which could guide the development of ad hoc
machines aimed to guarantee safety in the production chain of insects for food.

1. Introduction between 2005 and 2050 (from 258 to 455 million tons). Meeting this
demand will require innovative solutions (Alexandratos & Bruinsma,
The world population is constantly increasing and it is expected that 2012; Van Huis, 2015).
the world will host 9 billion people by 2050 (Alexandratos & Bruinsma, Several studies suggest that edible insects may be a viable alter-
2012). Feeding this growing mass of more demanding consumers will native or supplement to conventional protein sources (Belluco et al.,
necessarily require an increase in food production, particularly in 2013; Mlcek, Borkovcova, & Bednarova, 2014; Payne, Scarborough,
protein sources, which are also the most expensive for the environment. Rayner, & Nonaka, 2016; Schlüter et al., 2017; Van Huis, 2015). Edible
This will inevitably put more pressure on the planet's already limited insects are already popular foodstuffs in many areas, mainly Asia,
resources: land, oceans, water, and energy. If food production is to be Africa, Latin America and Oceania. The eaten insects species vary ac-
obtained by means of current techniques, increases in green house gas cording to the geographical distribution (Patel, Suleria, & Rauf, 2019).
(GHG) and ammonia emissions, deforestation, soil erosion, loss of plant Despite Tenebrionidae and Gryllidae families are widely studied in
biodiversity, and water pollution are set to continue. These environ- literature, each country has its own niche of insect and tries to valorize
mental problems, especially those associated with raising livestock, such source of protein (e.g. Mopane warm in South Africa (Stack et al.,
need urgent attention: according to FAO, livestock is, in fact, the 2003)). Furthermore, the collecting and processing methods are able to
world's largest user of agricultural land (67.3%) (FAOSTAT, 2013). The influence safety, nutritional values and technological performances of
global demand for meat products is expected to increase by 76.4% whole and powdered insects (Vandeweyer, Lenaerts, Callens, and Van

Abbreviations: (GHG), Green House Gas; (PCB), Poly-Chlorinated Biphenyl; (OCP), Organo-Chlorine Pesticide; (PBDE), Poly-Brominated Diphenyl Ether; (HFR),
Halogenated Flame Retardant; (PFRs), Phosphorous Flame Retardants; (PPE), Personal Protective Equipment; (SERS), Surface-Enhanced Raman Scattering; (FET),
Field-Effect Transistor
∗
Corresponding author.
E-mail address: alessio.cappelli@unifi.it (A. Cappelli).

https://doi.org/10.1016/j.foodcont.2019.106877
Received 4 July 2019; Received in revised form 3 September 2019; Accepted 4 September 2019
Available online 06 September 2019
0956-7135/ © 2019 Elsevier Ltd. All rights reserved.
A. Cappelli, et al. Food Control 108 (2020) 106877

Campenhout (2017b), De Gier & Verhoeckx, 2018; Vandeweyer et al. regarding machines, plants, and integrated supply chain approaches
(2017b); EFSA, 2015). Insect eating is estimated to be regularly prac- regarding the production chain of insects for food, thus motivating this
ticed by at least 2 billion people worldwide (FAO, 2014). Thousands of work. For this reason, the aim of this review is to summarize the current
insect species have been documented in literature as edible, most of knowledge related to the potential microbial, chemical, physical, and
them from tropical countries (Jongema, 2017). The most commonly allergenic risks related to the breeding, transformation, and consump-
eaten insect groups are beetles, caterpillars, wasps, bees, ants, grass- tion of edible insects for food.
hoppers, locusts, crickets, cicadas, termites, dragonflies, and flies (Van
Huis, 2015; Sun-waterhouse et al., 2016). However, Tenebrionidae and 2. Search strategy
Gryllidae families are seen as more suitable for consumption and pro-
cessing (Marberg, van Kranenburg, & Korzilius, 2017). Furthermore, The review considers the EFSA scientific opinion (EFSA, 2015) as
these families are widely studied in literature (Bednarska et al., 2016; the starting point, which is why the years from 2016 onwards (till begin
Borremans, Lenaerts, Crauwels, Lievens, & Van Campenhout, 2018; of 2019 included) have been chosen as a time frame. Three databases
Broekman et al., 2015; Caparros Megido et al., 2018; Fernandez-Cassi, were explored by means of ad hoc search strings: Science direct,
Supeanu, Jansson, Boqvist, & Vagsholm, 2018; Francis et al., 2019; PubMed, and Web of Science. For the microbiological, chemical, and
Grau, Vilcinskas, & Joop, 2017; Han et al., 2016; Osimani et al., 2017a; physical risks, a unique search string was used for all the databases,
Osimani et al., 2018b; Vandeweyer, Crauwels, Lievens, & Van while for the risk related to allergenicity, two different search strings
Campenhout, 2016). In most Western countries, consumer acceptance were used: one for Science direct and one for PubMed and Web of
of entomophagy is still limited by disgust (appearance, taste, sense of Science. The search strings used are as follows:
dirtiness and danger perception) (Cicatiello, Franco, Pancino, & Blasi,
2016; Shelomi, 2015; Sogari, 2015; Sun-waterhouse et al., 2016; Van • “Food AND (Insect* OR “novel food*" OR mealworm* OR cricket*
Huis, 2015). Nonetheless, even in these regions, insect rearing is in- OR entomophagy OR “edible insect*") AND (microbiota OR “mi-
creasing and more and more insect-based food products are being stu- crob* community” OR “microb* count*" OR “microb* load” OR
died (Fasolato et al., 2018; Osimani et al., 2018b). “microb* risk” OR “microb* hazard” OR “microb* saf*" OR “food
The potential benefits of insect consumption include their nutri- safety”)” for microbiological risk,
tional properties: most insects are rich in high quality proteins (with an • “Food AND (Insect* OR “novel food*” OR mealworm* OR cricket*
essential amino acid score ranging from 46 to 96%), good quality lipids OR entomophagy OR “edible insect*“) AND (“chemical risk*” OR
(rich in alpha-linolenic acid and linoleic acid), vitamins, minerals (such “chemical hazard*” OR “chemical safety” OR radionuclide* OR ar-
as calcium, iron, and zinc) and fiber (due to the presence of chitin) senic OR cadmium OR copper OR zinc OR chrome OR toxin*)” for
(Belluco et al., 2013; Mlcek et al., 2014; Payne et al., 2016; Rumpold & chemical risk,
Schlüter, 2013; Schlüter et al., 2017; Sun-waterhouse et al., 2016). • “Food AND (Insect* OR “novel food*” OR mealworm* OR cricket*
These nutritional benefits are well-known and pursued in developing OR entomophagy OR “edible insect*“) AND (“physical risk*” OR
countries, where for a long time, the combination of the richest avail- “physical hazard*” OR “physical safety” OR “foreign bod*” OR
ability of edible insects and the presence of malnutrition have de- “breeding substrate*” OR vegetable* OR ran OR flour*)” for phy-
termined their largely diffused consumption (Garofalo et al., 2017; sical risk,
Klunder, Wolkers-Rooijackers, Korpela, & Nout, 2012). However, it is • “Food AND (Insect* OR “novel food*” OR mealworm* OR cricket*
important to highlight that the nutritional value of insects varies sig- OR entomophagy OR “edible insect*“) AND (allergen*)” for aller-
nificantly among species and development stages. Apart from nutri- genicity risk on Science direct and “Food AND (Insect* OR “novel
tional qualities, the rearing of insects for food is also linked to potential food*” OR mealworm* OR cricket* OR entomophagy OR “edible
economic, social, and ecological proceeds. Harvesting or farming in- insect*“) AND (allerg*)” on PubMed and Web of Science.
sects can offer new employment and income-earning opportunities,
including some of the poorest segments of society (FAO, 2014). Insect All articles considering insects belonging to the families of Tenebrio
breeding seems to have a lower ecological footprint than livestock molitor and Acheta domesticus, Tenebrionidae and Gryllidae, respec-
production: insects multiply faster, cause lower GHG and ammonia tively, were included. Among all insects species, these families are seen
emissions, require less land area and water use, have higher feed con- as more suitable for consumption and processing (Marberg et al., 2017).
version efficiency, and can potentially be bred on organic by-products No language restriction was imposed. No restriction regarding the
(Garofalo et al., 2017; Klunder et al., 2012; Van Huis, 2015). publication status was enforced. All duplications have been excluded
Owing to the same properties, insects, like many food products that from the obtained results. In addition to the studies that mainly deal
are rich in nutrients and moisture, also provide a favorable environ- with the types of risk mentioned above, those in which they are treated
ment for microbial survival and growth (EFSA, 2015; Garofalo et al., in a non-exclusive but exhaustive manner were also included. However,
2017; Klunder et al., 2012; Stoops et al., 2016; Van Huis, 2015). Since, despite the EFSA report (EFSA, 2015) mentioned other kinds of risk
as of January 2018, insects are considered as categories of food to (such as hormones), according to the obtained results the authors
which the European Union legislation on novel foods (Regulation (EU) decided to discuss only microbiological, chemical, physical, and aller-
2015/2283 on novel foods) is applied, more data on the microbial, genic risks, to which a great amount of literature was found. The search
chemical, and physical safety of edible insects reared or imported in results were first screened by title and abstract reading (excluding, at
Europe are necessary (European Union, 2015). Despite this, is it im- this step, the articles in the form of abstract and/or index), and then by
portant to highlight that insects are not allowed for human consump- full text reading. For each of the four types of risk investigated, a flow
tion in all the European countries. Furthermore, additional microbial chart was produced to synthetize the obtained results, which were
hazard data are needed to set up microbiological criteria for edible subsequently summarized in Table 1 (for reviews and book chapters)
insects in future, as for other food products (Regulation (EC) N° 2073/ and Table 2 (for articles).
2005 on microbiological criteria for foodstuffs) (Belluco et al., 2013;
European Commission, 2005; Vandeweyer et al., 2017b). Moreover, 3. Main findings
little is known about the potential risks derived from the breeding
systems, as well as those potentially derived from the transformation 3.1. Results of the systematic review
processes (in particular physical and allergenic risks for food chain
operators and consumers). In fact, this systematic review of the existing A total of 4593 results were obtained: 1871 for microbiological risk,
bibliography highlights the lack of scientific articles and reviews 639 for chemical risk, 660 for physical risk and 1423 for allergenicity

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A. Cappelli, et al. Food Control 108 (2020) 106877

Table 1
Reviews and book chapters collected with the systematic review.
Author and year Risk type Main results

De Castro R. J. S. et al., 2018 Microbiological Allergenic Enterobacteriaceae and sporulating bacteria were isolated in fresh insects. No pathogen was found.
Boiling eliminates the Enterobacteriaceae but not sporulating bacteria. Roasting cannot eliminate
Enterobacteriaceae. Arthropods can induce allergic reactions. 238 allergens present in arthropods have
been identified (few processes can reduce their allergenicity).
Walia K. et al., 2018 Microbiological If porridge fortified with cricket powder is boiled prior to consumption, the food safety risk is low for S.
aureus; low to moderate for B. cereus, C. perfringens Type A, C. sakazakii, enterohemorrhagic E. coli, L.
monocytogenes, and Salmonella spp., and moderate to serious for C. Perfringens Type C. No outbreaks of B.
cereus, C. perfringens, C. sakazakii, L. monocytogenes and Salmonella spp. were recorded. No E. coli, was
isolated from cricket powder.
Kouřimská L. & Adámkova A., Microbiological Chemical Insects may produce or contain toxic bioactive compounds, residues of pesticides and heavy metals (e.g.
2016 Allergenic cadmium and lead). The consumption of insects can lead to allergic reactions due to the presence of
chitin. If insects are not subjected to fasting, heat treatment, and storage, they can become dangerous
from a microbiological point of view.
Marshall D. L. et al., 2016 Microbiological Chemical Gut of house cricket contains Citrobacter, Klebsiella, Yersinia, Bacteroides, and Fusobacterium. The yellow
Physical mealworm hosts Actunobacillus, Propionibacterium, Citrobacter, Serratia, Bacillus, Dermabacter,
Brachybacterium, Clavibacter, and Exiguobacterium. Appropriate breeding techniques must be used to
control the pathogens dangerous to humans.
Grau T. et al., 2017 Microbiological Chemical Mealworms are not reported to contain pathogens (L. monocytogenes and Salmonella spp.). A short heating
Allergenic treatment or blanching significantly reduces total bacterial counts and enterobacteria counts. No
documented evidence of infections during the mass rearing of mealworms, however, this risk cannot be
excluded due to similar situations occurring in other insects such as house cricket. The accumulation of
hazardous chemicals originating from contaminated insect diets can occur. Regarding the risk of
allergies, mealworm proteins cross-react in vitro with IgE in response to tropomyosin. Mealworm allergy
can occur in shrimp-allergic patients. A heating treatment and in vitro digestion reduce the allergic
reaction but do not eliminate it completely.
Schlüter O. et al., 2016 Microbiological The transmission of microorganisms can occur mechanically (through contact) or if they resist and
Chemical multiply inside the insect. Toxins and antinutrients can be absorbed or synthesized by the insect. The
Allergenic cross-reactivity effect of tropomyosin has been confirmed. Tropomyosin and arginine kinase have been
identified as cross-reactive proteins. People allergic to crustaceans and dust mites can manifest allergic
reactions.
Van der Fels-Klerx H. J. et al., Microbiological Chemical Potential accumulation of chemical contaminants depends on the type of insect and the growth phase.
2018 Allergenic The substrate and the farming environment strongly influence the microflora and the contamination of
insects. Insects are characterized by high counts of total vital bacteria and Enterobacteriaceae. A suitable
heating treatment can eliminate a good part of microbiological risk (except for bacterial spores). The pan-
allergen tropomyosin was identified in mealworm. Arginine kinase and α-amylase play a role in cross-
reactivity between crustaceans and insects.
Fernandez-Cassi X. et al., 2018 Microbiological Chemical The minor risks deriving from the consumption of Acheta domesticus are those related to viruses, prions,
Allergenic fungi, and parasites. The medium risks are high microbial counts, sporulating bacteria, and their growth
after heat treatment, bioaccumulation of heavy metals (especially cadmium) and allergenicity. No
pathogenic microorganisms such as L. monocytogenes or Salmonella spp. were found; however, species
belonging to the genera Clostridium spp., Listeria spp., and Bacillus spp. have been detected.
Grabowski N. T. & Klein G., 2017b Microbiological Insects can act as carriers for human pathogens. The exclusion of clinically diseased specimens, hygienic
obtention, washing, and thorough heating seem suitable procedures to reduce the risk of food-borne
diseases by bacteria. Raw consumption of insects should be evaluated thoroughly. The phyla most
present in the intestinal microbiota of insects are Proteobacteria and Firmicutes.
Grabowski N. T. et al., 2017a Microbiological Many fungi associated with arthropods do not survive in humans due to body temperature. The
prevalence of pathogenic fungi for humans varies from 0 (dragonflies, orthoptera, termites, hemiptera,
cockroaches, ephemeral and flies) to above 4 (hemiptera) and 7 (hymenoptera) to 17 (moths) and 71%
(cockroaches).
Sun-Waterhouse D. et al., 2016 Chemical Physical risks such as glass, stones, plastics, and metal fragments can be present in insects. Chemical
Physical contaminants could be naturally present, synthesized, accumulated or generated during the production
Allergenic process. Some insects may contain cross-reactive allergens: proteins (such as tropomyosin),
carbohydrates (such as chitin) and other components that are yet to be identified. Arginine kinases,
myosin heavy chains, myosin light chain kinases, hemocyanin, amylase, and sarcoplasmatic calcium-
binding proteins are other allergens that may be present in edible insects.
Gallo, 2018 Chemical Allergenic The different chemical contaminants that can contaminate insects are heavy metals, veterinary drugs,
hormones, pesticides, toxins, and mycotoxins. Insect consumption can lead to the development of allergic
reactions in people allergic to crustaceans, because of the morphological similarity between them and
insects.
Liu & Zhao, 2018 Chemical Physical Physical and chemical risks can occur in insects. Many poisonous substances could be present in
Tenebrionidae cockroaches. Some chemical risks can be removed or deactivated by cooking or digestion.
Antinutrients of plant origin found in feed can be accumulated in insects.
Varelas & Langton, 2017 Chemical Physical Allergenic Chemical hazards include substances that are toxic to insects, antibiotics, contaminants and anti-
nutrients. Physical hazards derive from parts of insects or from foreign materials, while allergens are
associated with enzymes and allergenic substances present in insects.
Van Huis, 2017 Chemical Yellow mealworms reared on a mycotoxin-contaminated diet (mainly deoxynivalenol) are able to
partially excrete them through faeces in an unmetabolized form and the remaining part as metabolized in
different compounds.
Marone P. A., 2016 Chemical Physical Insects can bioaccumulate chemical residues and heavy metals, and produce harmful substances. Insects
can contain anti-nutrients that interfere with physiological processes. The major physical risk is
suffocation, so insect powder is more suitable and is considered safe compared to the raw and whole
insect.
Van Huis A. & Dunkel F. V., 2017 Allergenic
(continued on next page)

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A. Cappelli, et al. Food Control 108 (2020) 106877

Table 1 (continued)

Author and year Risk type Main results

Cross-reaction between insects and crustacean is possible. Arginine kinase and tropomyosin were found
as the major cross-reactive proteins in yellow mealworm. Patients allergic to dust mites and crustaceans
can react to foods containing proteins of the yellow mealworm.
Pali- Schöll I. et al., 2018b Allergenic Edible insects can cause allergic cross-reactions in patients allergic to shrimp or dust mites. Pan-allergen
identified in arthropods are tropomyosin and arginine kinase. Breeders of yellow mealworm developed a
primary sensitization to this insect that evolved in food allergy.
Downs M. et al., 2016 Allergenic The most relevant cross-reactivity is between insects and crustaceans. The protein hydrolysis and heating
treatments, can reduce allergic reactions.
De Gier & Verhoeckx, 2018 Allergenic Cases of primary allergy to insects and cross-reactivity (related to tropomyosin and arginine kinase) are
reported. Heat treatment can lead to a reduction, increase, or no change in the allergenicity. Digestion
can also have an effect on allergenicity.
Van der Spiegel, 2016 Allergenic The consumption of insects can lead to allergic reactions due to cross-reactivity of insect proteins with
shrimps and dust mites. An allergen present in the exoskeleton is chitin. Insects can carry anti-nutritional
factors with them, but they are minimized or eliminated by cooking.
Van Huis, 2016 Allergenic Insects can generate allergic reactions due to cross-reactivity with the phylum of arthropods. Frying
might alter the allergenicity of edible insects.
Pali-Schöll I. et al., 2018a Allergenic A long-term exposure of insect breeders leads to respiratory sensitivity. The potential cross-reactivity has
been highlighted in patients allergic to crustaceans and dust mites due to the consumption of mealworm
or grasshopper.
Ribeiro J. C et al., 2018 Allergenic In this systematic review, 25 articles were revised: eight studied the cross-reactivity or co-sensitization
between edible insects, crustaceans, and house dust mite, three identified and characterized allergens of
edible insects, 10 were cases reports or case series of food allergy caused by insects, three assessed the
frequency of anaphylaxis caused by entomophagy, and one assessed the prevalence of allergy among
insect-eaters. Many studies report the cross reactivity of the yellow mealworm with crustaceans and dust
mites. The heating treatment changes the solubility of mealworms allergens. Boiling or in vitro digestion
does not significantly alter the ability of tropomyosin to bind IgE contrary to frying.

risk. After removing duplicates within each database, screening by title studies (Garofalo et al., 2017; Grabowski & Klein, 2017a; Osimani et al.,
and abstract reading, screening by full text reading, and removing du- 2018a, 2017b; Vandeweyer et al., 2016; Vandeweyer et al., 2018;
plicates between the three databases, 77 were selected as the sum of the Wynants et al., 2018). Despite the latter two were not detected in the
results of all the search strings. By removing the articles in common selected studies, this does not mean that insects are safe and free from
between the results of the different search strings, the items selected these pathogens. In fact, their monitoring still remains important for
were brought down to 64. Of these 64, two were systematic reviews, 14 consumers’ safety.
were other forms of review, eight were book chapters, one was an Vandeweyer et al. (2017b) studied the effect of refrigerated storage
epidemiological retrospective cohort study, and 38 were descriptive and microwave drying, after a blanching treatment, on microbial load
studies by laboratory researchers (32 on contaminants in insect samples in yellow mealworm larvae. It was observed that, except for spores,
and six on patients’ sera). Flow charts developed according to PRISMA blanching leads to a significant reduction of all microbial counts at any
statement (Moher, Liberati, Tetzlaff, & Altman, 2009) related to mi- time interval. Except for one batch (in which a slight growth of meso-
crobiological (Fig. 1a), chemical (Fig. 1b), physical (Fig. 1c), and al- philic and psychrotrophic organisms was observed), no microbial
lergenic risks (Fig. 1d) are shown in Fig. 1. Reviews and book chapters growth occurred during refrigerated storage. After blanching, the
are listed in Table 1 and search articles are listed in Table 2. chilled conditions allowed mealworms to be stored for at least six days
without spoilage, as the numbers remained well below the level con-
sidered for food spoilage (7 log cfu/g). Long drying times after
3.2. Microbiological risks
blanching led to large reductions in total counts until a plateau was
reached. Drying after blanching resulted in Enterobacteriaceae, LAB,
The bacterial communities found in mealworms are composed of
yeast and molds counts below or very close to the detection limit. For
Actinobacteria, Firmicutes, Proteobacteria, and Tenericutes (Garofalo
bacterial endospore counts, blanching and drying resulted in lower
et al., 2017; Yang et al., 2018), while those present in house crickets
reductions (between 0.3 and 1.0 log cfu/g).
(both in whole and in powder form) are Proteobacteria, Firmicutes, and
Regarding the fungal biota, Vandeweyer et al. (2016) report a dif-
Bacteroidetes (Garofalo et al., 2017). In a study by Garofalo et al.
ference between mealworms and crickets: molds were dominant in
(2017), the microbiological profile of certain insect species has been
mealworm larvae and yeasts in crickets. Fungi present in feed may
examined, including mealworm and house cricket. The total mesophilic
contaminate insects and the major risk concerns those able to produce
aerobic count was the highest in powdered cricket (4.80 ± 0.06 log cfu
mycotoxins as Aspergillus, Penicillium, Mucor and Rhizopus, as insects are
g−1) and the lowest in mealworm larvae (< 2.00 log cfu g−1). Whole
able to metabolize and accumulate these compounds (Van der Spiegel,
crickets were characterized by the higher Lactic Acid Bacteria (LAB)
2016). However, good hygiene procedures during the production chain
counts, while the lowest values were recorded in mealworm larvae and
can reduce the risk of fungi in insects (Gallo, 2018). Moreover, a
powdered crickets. Yeast counts were the highest in whole crickets and
blanching treatment significantly reduces the presence of fungi
molds were the highest in powdered crickets and lowest in whole
(Vandeweyer et al., 2017b; (Wynants et al., 2018); Grabowski, Pingen,
crickets. The Enterobacteriaceae count varied in the selected studies:
Grootaert, & Klein, 2017).
high in some (Osimani et al., 2018a) while in others low, and, in two
Viruses that are pathogenic for insects are not a risk for humans
cases, below the limit of detection (Fasolato et al., 2018; Garofalo et al.,
because they are specific to invertebrates and because of the genetic
2017). However, a heat treatment (e.g. blanching or boiling) reduces
difference between human and insect. However, although there is no
the Enterobacteriaceae count without sporulating bacteria and bacterial
evidence of pathogenic viruses in insect, they may be able to act as
spores (De Castro, Ohara, Aguilar, dos, & Domingues, 2018; Gallo,
mechanical vectors for human pathogenic viruses (Gallo, 2018; Van der
2018; Liu & Zhao, 2018; Van der Fels-Klerx, Camenzuli, Belluco, Meijer,
Fels-Klerx et al., 2018). EFSA (EFSA, 2015) reports that lower risks
& Ricci, 2018; Van Huis, 2016; Van Huis & Dunkel, 2017). Salmonella
regarding house cricket consumption are those related to viruses,
spp. and Listeria monocytogenes were not detected in any of the selected

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Table 2
Research articles collected with the systematic review.
Author, year and country Aim Type of risk Main results

Yang S. S. et al., 2018 (USA, To investigate the ability of Tenebrio molitor larvae to Microbiological Significant taxonomic shifts for mealworms fed with diets
China, UK) digest and biodegrade polystyrene. of polystyrene plus bran and polystyrene alone. The 99%
abundance in the measured bacterial communities were
Actinobacteria, Firmicutes, Proteobacteria and Tenericutes.
The six most abundant families were Bacillaceae,
Enterobacteriaceae, Enterococcaceae, Lactobacillaceae,
Leuconostocaceae, and Streptococcaceae.
Stoops J. et al., 2017 To investigate the effect of the production process and Microbiological Fresh living mealworm larvae contain a high number of
(Belgium) the storage conditions (air, 60% CO2/40% N2) on the microorganisms. Both production methods affected the
microbial and bacterial counts of a minced meat-like microbiota of the finished products. Modified atmosphere
product from yellow mealworm larvae during storage reduces bacterial growth compared to
storage in air. The initial load of bacterial spores of both
product types remained constant during the entire storage
period. After 35 days of storage in air, a statistically
significant decrease in OTU richness was noticed for both
product types.
Garofalo C. et al., 2017 (Italy) Assessing the microbial species in some processed Microbiological Relatively low counts of total mesophilic aerobes,
marketed edible insects (powdered and whole), through Enterobacteriaceae, lactic acid bacteria, Clostridium
classical microbiological analyses and pyrosequencing. perfringens spores, yeasts, and molds were found. Food
spoilage bacteria were also identified, as well as
Spiroplasma spp. in mealworm larvae. Salmonella and L.
monocytogenes were not detected. The presence of Listeria
spp., Staphylococcus spp., Clostridium spp., and Bacillus spp.
was also found through pyrosequencing.
Ong S. Y. et al., 2018 Recovering PHA from Cupriavidus necator, incorporating Microbiological In the gut of mealworms fed with wheat bran and freeze-
(Malaysia, Germany, the use Tenebrio molitor as partial purification dried cells a remarkably high relative abundance of
Japan) machinery, followed by washing on the fecal pellets with Firmicute–89% and 86% respectively. In guts of the
distilled water and sodium hydroxide. mealworms fed with freeze-dried cells, it was as high as
55% of Proteobacteria dominated the gut. The gut of
mealworms fed with cells produced from waste animal fats
was dominated by Bacillus, the gut of mealworms fed with
cells produced from palm olein was dominated by
Oxalobacteraceae and the gut of mealworm fed with wheat
bran by Enterococcus.
Osimani A. et al., 2017a (Italy) Assessing the resistance to tetracyclines, macrolide- Microbiological Spore-forming bacteria have been detected in both fresh
lincosamide-streptogramin B, vancomycin, beta-lactams, and processed mealworms. Regarding total mesophilic
and aminoglycosides in 40 samples of Tenebrio molitor. aerobes, mean counts ranged between < 1 and 6.73 log
cfu/g. For spore-forming bacteria, viable counts were
between < 1 and 4.24 log cfu/g. For lactic acid bacteria,
viable counts varied between < 1 and 2.99 log cfu/g.
Osimani A. et al., 2018a (Italy) To study the bacterial biota characterizing a pilot Microbiological Larvae and frass were characterized by high loads of
production chain of fresh Tenebrio molitor larvae. Enterobacteriaceae, lactic acid bacteria, and several species
of mesophilic aerobes. Spore-forming bacteria were
detected to a lesser extent. The combined molecular
approach confirmed the low microbial contamination of
wheatmeal and allowed the detection of Enterobacter spp.,
Erwinia spp., Enterococcus spp., and Lactococcus spp. as
dominant genera in both larvae and frass.
Entomoplasmatales constituted a major fraction of the
microbiota of one batch of larvae. From the real-time PCR
assays, no sample was positive for either C. burnetii or
STEC, whereas P. aeruginosa was detected in one sample of
frass. No Salmonella spp. or Listeria monocytogenes were
detected.
Osimani et al., 2018b (Italy) To evaluate cricket (Acheta domesticus) powder in bread- Microbiological Cricket powder was characterized by high counts of both
making to obtain bread with enhanced nutritional value. LAB and spore-forming bacteria that attested at up to 3.8
log cfu/g and 5 log cfu/g, respectively. Yeasts counts were
< 1 log cfu/g.
Wynants E. et al., 2018 To characterize the microbial dynamics in the insect, Microbiological Enterobacteriaceae, LAB, and fungi dropped significantly to
(Netherlands) insect feed and substrate, during a production cycle of close to or below the detection limit with blanching
lesser mealworms (Alphitobius diaperinus) treatment, except for aerobic endospores. The starvation
treatment did not significantly alter the microbial count.
Salmonella, L. monocytogenes, Bacillus cereus, and coagulase-
positive staphylococci were not detected. Fungal isolates
corresponding to the genera Aspergillus and Fusarium were
recovered.
Fasolato L. et al., 2018 (Italy) To investigate the microbial traits of insects available Microbiological Quantities of Staphylococcus, molds, yeasts, LAB, and
online (mealworms, crickets, mole crickets and Enterobacteriaceae was predominantly below the limits of
silkworms). detection. The characterization of strains from the Bacillus
cereus group, 17% of the isolated strains presented nine of
the 10 toxin targets.
Wynants E. et al., 2017 To assess the effect on the microbiota of starvation and Microbiological The results obtained do not show considerable changes in
(Belgium) rinsing at the end of the rearing period of Tenebrio microbial numbers of mealworm larvae during the
molitor. starvation period. Metagenetic analyses show an average
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5
A. Cappelli, et al. Food Control 108 (2020) 106877

Table 2 (continued)

Author, year and country Aim Type of risk Main results

number of OTUs from 21 to 57 per sample. The phyla

mainly present were Proteobacteria and Firmicutes.
Rinsing and starvation did not have any influence on the
microbial counts of larvae.
Vandeweyer D. et al., 2017b Study the effect of blanching, followed by chilled storage Microbiological For all total counts, log reductions of 4.4, 6.4 and 5.6 log
(Belgium) or microwave drying, on microbial counts of the larvae. cycles were observed for blanching times of 10, 20 and 40 s
respectively. Long drying times caused strong reductions on
total count, until a plateau was reached after 20 min of
drying. No major growth was observed during subsequent
chilled storage.
Borremans A. et al., 2018 To apply marination and fermentation processes on Microbiological Marination can increase the shelf life of this products up to
(Belgium) larvae of the yellow mealworm Tenebrio molitor. seven days. Regarding fermentation, a microbial growth
was observed only at the seventh day of fermentation. LAB
were the major part of the bacterial community (the other
microbial counts were low).
Vandeweyer D. et al., 2016 To generate an overview of intrinsic parameters (pH, Microbiological The microbial counts of the fresh insects were high. The
(Belgium) water activity and moisture content) and microbial largest variations were found in numbers of bacterial
quality of fresh mealworm larvae and crickets. endospores, psychrotrophs, and fungi. Salmonella spp. and
L. monocytogenes were not detected in batches from
individual breeders. Comparing mealworms and crickets,
mealworms were dominated by molds and crickets by
yeasts.
Milanović V. et al., 2016 To investigate the occurrence of 11 transferable Microbiological Microbial counts of total mesophilic aerobes showed a wide
(Italy) antibiotic resistance genes in 11 species of marketed variability among samples (104–107 cfu/g). The high
edible insects in order to provide a first baseline for risk microbial load suggest the survival of spore-forming
assessment. bacteria, due to ineffective boiling or cross-contamination.
Tet(K), erm(B), tet(S), and blaZ were the most frequent
antibiotic resistance genes, suggesting that insect's
consumption might be related to a significant risk.
Li L. et al., 2016 (China) To study the effects of rearing yellow mealworm Microbiological Samples from the open environment had higher
(Tenebrio molitor L.) in a closed artificial ecosystem on abundances of Bacillus, Lactococcus, Weissella, Escherichia,
their associated microbial communities. and Clostridiaceae, compared with the three samples from
the closed ecosystem. In samples from the closed ecosystem
Enterococcus and some unclassified Enterobacteriaceae
were identified as the predominant bacteria. Some classes
that were found in the feed disappeared in the samples of
both groups.
Buϐler S. et al., 2016b To investigate the protein extractability and techno- Microbiological Tenebrio molitor larvae was highly contaminated with
(Germany) functionality of insect flour fractions recovered from microorganisms. Pureeing, freeze-drying, and grinding of
Tenebrio molitor and Hermetia illucens. the larvae at low temperatures were found to be
inappropriate for production of microbiologically safe
insect fractions. Extreme pH conditions apparently do not
lead to a reduction in microorganisms but only to a mild
effect.
Caparros Megido R. et al., To characterize the effects of different cooking methods Microbiological Boiling and cooking under vacuum were the most efficient
2018 (Belgium) (boiling, pan-frying, vacuum cooking and oven cooking) techniques to reduce microbial load while maintaining the
on the microbial load and nutritive value of mealworms high levels of protein and polyunsaturated fatty acids of
mealworms. Total aerobic count was higher in crude
larvae, followed by larvae cooked in oven, larvae cooked
under vacuum, larvae subjected to pan-frying, and larvae
subjected to boiling.
Caparros Megido R. et al., To characterize the microbial load of edible insects Microbiological Blanching step has led to a reduction of the total aerobic
2017 (Belgium) found in Belgium and to evaluate the efficiency of count for all insect species, except for one caterpillar
different processing methods in reducing microorganism species. Freeze-drying and sterilization treatments were
counts. effective in reducing the total aerobic count. Sterilization
resulted the most efficient treatment than blanching and
freeze-drying.
Grabowski N. T. & Klein G., To study different drying techniques on cooked edible Microbiological T3 was the most effective of the drying treatments,
2016 (Germany) insects in relation to microbiological quality. excepted Bacilli for which T2 was more efficient. Treatment
T1 was the less efficient treatment. In cricket, Staphylococci
count was in the same range for T1 and T2 and different
from T3. Regarding the larva, each treatment was
characterized by a different range of Staphylococci count.
Bacillus cereus was not isolated in any sample. Treatment T4
resulted the most efficient treatment in the reduction of
microbial count.
Grabowski N. T & Klein G., To analyze processed insect products using classical food Microbiological All samples were free of salmonellae, L. monocytogenes, E.
2017a (Germany) microbiology methods. coli and S. aureus. Dried and powdered insects contained B.
cereus, coliforms, Serratia liquefaciens, Listeria ivanovii,
Mucor spp., Aspergillus spp., and Cryptococcus neoformans.
Three cricket samples and two mealworm samples did not
respect the process hygiene criteria imposed by Belgium
and the Netherlands.
Stoops J. et al., 2016 Microbiological The most abundant operational taxonomic unit in
(Belgium) mealworm larvae was Propionibacterium. Proteobacteria,
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6
A. Cappelli, et al. Food Control 108 (2020) 106877

Table 2 (continued)

Author, year and country Aim Type of risk Main results

To characterize the microflora of fresh edible mealworm Firmicutes, and Actinobacteria were found as dominant
larvae and grasshoppers in a quantitative and qualitative phyla in yellow mealworm. Regarding the structure of
way. bacterial community, in the yellow mealworm a total of 50
different OTUs was found, the most abundant OUT was that
of Propionibacterium sp.
Vandeweyer D. et al., 2018 To investigate the microbial dynamics, from industrial Microbiological None of the investigated food pathogens were found. Some
(Belgium) rearing to processing and storage, of the tropical house possible mycotoxin-producing fungi were isolated from the
cricket reared for human consumption. crickets. A postharvest heat treatment reduced microbial
numbers, but an endospore load of 2.4 log cfu/g remained.
An increase in microbial counts was observed for the dried
and smoked/dried crickets. The microbial numbers
remained constant over a six-month storage period,
whether frozen or at ambient temperature.
Vandeweyer D. et al., 2017a To increase the knowledge on the microbial quality of Microbiological The bacterial community composition of the investigated
(Belgium) edible insects by comparing the bacterial community crickets was similar among different companies and
composition of mealworms and crickets. between both crickets species. Mealworms communities
were dominated by Spiroplasma and Erwinia species, while
crickets were abundantly colonized by (Para)bacteroides
species. Only a few OTUs could be associated with potential
human pathogens.
Osimani A. et al., 2017b (Italy) To provide insight into the proximate composition and Microbiological It was seen a great variation in microbial counts. L.
microbial diversity of some processed edible insects monocytogenes and Salmonella spp. were not detected.
marketed in the European Union. Cricket powder was characterized by significantly higher
viable counts for all microorganisms investigated. It was
seen a great microbial diversity in quantitative and
qualitative terms among all products analyzed.
Buϐler S. et al., 2016a To investigate the possible use of the CAPP technology Microbiological Following CAPP treatment, the total microbial load of
(Germany) for the decontamination and modification of flour Tenebrio flour of 7.72 log10 cfu/g was reduced to 7.10
produced from mealworms. (1 min), 6.72 (2.5 min), 5.79 (5 min), 5.19 (7.5 min), 5.21
(10 min) and 4.73 (15 min) log10 cfu/g. In conclusion, the
CAPP treatment seems to be effective for the
decontamination of mealworm flours.
Han. S. R et al., 2016 (Korea) To evaluate subchronic toxicity, including potential Chemical + Allergenic The administration of Tenebrio molitor larvae freeze-dried
hypersensitivity, of freeze-dried powdered T. molitor did not lead to adverse or toxic effects in rats, including
larvae in male and female Sprague-Dawley rats. allergologic evaluation.
Poma G. et al., 2017 (Belgium) To provide a comprehensive overview of the residual Chemical In the two larvae were found PCBs levels of 26.5 and
levels of different chemical compounds, in insects and 33.8 pg/g ww, whereas in insect-based products values
insect-based food intended for human consumption, and were higher. PBDEs levels were low. The untargeted
to compare these levels to those measured in common screening analysis revealed the presence of vinyltoluene,
animal products. tributylphosphate and pirimiphos-methyl. The levels of Cu
and Zn in insects were similar to those measured in meat
and fish in other studies, whereas As, Co, Cr, Pb, Sn levels
were relatively low in all samples. Results suggest the
possibility to consume these insect species with no
additional hazards in comparison to the more commonly
consumed animal products.
Van der Fels-Klerx H. J. et al., To investigate the accumulation of cadmium, lead and Chemical Bioaccumulation was seen in all treatments in Hermetia
2016 (The Netherlands) arsenic provided to larvae of Tenebrio molitor and illucens larvae and for three arsenic treatments in Tenebrio
Hermetia illucens, using contaminated feed. molitor larvae. Development of Tenebrio molitor larvae was
not influenced by the treatment applied. Results showed
that yellow mealworm larvae can accumulate arsenic in the
body, instead of cadmium and lead, of which
concentrations were found higher in feed.
Camenzuli L. et al., 2018 To investigate the potential accumulation of mycotoxins Chemical No differences were observed between larvae reared on
(Belgium, The in the lesser mealworm (Alphitobius diaperinus) and black mycotoxins individually or as a mixture with regard to
Netherlands) soldier fly (Hermetia illucens) larvae. either larvae development or mycotoxin accumulation/
excretion. For all applied treatments, the concentration
values of mycotoxins and their metabolites in Alphitobius
diaperinus larvae were below the detection limit.
Bednarska A. J. & Świątek Z., To compare the sequestration processes of cadmium and Chemical The concentration of cadmium in the flour affected the
2016 (Poland) zinc in Tenebrio molitor larvae and to assess the potential concentration of cadmium in the larval subcellular fraction,
availability of the metals to higher trophic levels. whereas the concentration of zinc only affected the zinc
concentration in S2 and G fractions. Larvae sequestered
approximately 30% of cadmium and zinc in the S1 fraction,
which is important for the transport of metals to higher
trophic levels.
Chomchai & Chomchai, 2018 To investigate the connection between histamine Chemical Out of 227 students, 18 developed illness, which included
(Thailand) poisoning and insect consumption. flushing, pruritus, urticarial rashes, headache, nausea,
vomiting, diarrhea, dyspnea and bronchospasm. Three
students begin to develop the symptoms within 1 h and half
after ingestion, the other 25 after 2–7 h. The highest attack
rate was associated with the consumption of locusts and
silkworms. Histamine poisoning can therefore also occur
with the consumption of insects.
Chemical
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7
A. Cappelli, et al. Food Control 108 (2020) 106877

Table 2 (continued)

Author, year and country Aim Type of risk Main results

Bosch G. et al., 2017 (The To evaluate the tolerance and accumulation of aflatoxin Both insects tolerated the presence of aflatoxin B1 in feed
Netherlands) B1 in two insect species to determine whether they could up to the highest level of 0.415 mg/kg. Feed contaminated
be used to retain condemned mycotoxin contaminated with aflatoxin B1 did not affect survival and body weight in
crops in the food chain. both insects, indicating a high tolerance. The residues of
yellow mealworm contained aflatoxin M1 when larvae
were fed with levels of aflatoxin B1 of 0.023, 0.084 mg/kg
or more, with levels of aflatoxin B1 excreted from 0.9 to
1.7%. This suggests that aflatoxin B1 was partially
transformed in the yellow mealworm in aflatoxin M1.
Van Broekhoven et al., 2017 To study the degradation and excretion of Fusarium Chemical No deoxynivalenol derivates were found in samples.
(The Netherlands) toxin deoxynivalenol in Tenebrio molitor reared with Deoxynivalenol was not present at detectable levels either
wheat flour naturally contaminated with mycotoxins. in the larvae harvested directly or for those held fasting for
24 h. The results show that diets containing deoxynivalenol
do not affect the mortality or weight of the larvae, which is
partially excreted in the frass and does not remain in an
unmetabolized form in the body.
Broekman H. C. H. P. et al., To address the risk of mealworm sensitization and Allergenic All four subjects had developed an allergy during
2017a (The Netherlands) allergy in subjects without shrimp allergy. professional or domestic mealworm breeding. The two
professional breeders had inhalant allergy symptoms when
they entered the room where they were raised but did not
develop symptoms when they ate them (sporadically). A
domestic breeder after two years of exposure developed
rhinoconjunctivitis that evolved into dyspnea.
Broekman H. et al., 2016 (The To investigate the potential allergenicity of mealworm in Allergenic The DBPCFC test confirmed allergy to mealworm in 13
Netherlands) shrimp-allergic patients. subjects out of 15. The symptoms were oral allergy (7/13),
urticaria (6/13), nausea (8/13), abdominal cramps (4/13),
vomiting (1/13) and dyspnea (2/13). It has been concluded
that allergy to this insect is highly probable shrimp-allergic
patients with potentially serious outcome.
Hall F. et al., 2018 (USA) To evaluate the effect of enzymatic hydrolysis on the Allergenic All sera reacted to tropomyosin in unhydrolyzed cricket
bioactive properties of cricket protein hydrolysates and in protein hydrolysates with a hydrolysis degree of
before and after simulated gastrointestinal digestion. 15–50%. There was no reaction in the case of cricket
protein hydrolysates with a degree of hydrolysis from 60 to
85%. Cricket protein hydrolysates had the greatest
bioactive potential and less reactivity to tropomyosin than
other cricket protein hydrolysates and control.
Francis F. et al., 2019 To investigate arginine kinase known as allergens Allergenic Positive responses were obtained with sera from Acheta
(Belgium) mainly from shrimps and to investigate the cross- domesticus samples for both protein extracts and purified
reactivity of these allergens taken from A. domesticus and arginine kinase, while a diversity of sample bands from
T. molitor. protein extracts from Tenebrio molitor. Regarding arginine
kinase, low specific allergenicity was here illustrated and
discussed in relation to the development of safe insect
consumption by humans.
Van Broekhoven S. et al., 2016 To assess IgE cross-reactivity of protein, isolated from Allergenic Results obtained reveal that IgE from crustaceans and
(The Netherlands) three edible mealworm species, with sera from patients house dust mite allergic patients showed cross-reactivity to
allergic to either crustaceans or house dust mite, and to mealworm tropomyosin or α-amylase, hexamerin 1B
determine the effect of processing and in vitro digestion precursor and muscle myosin. The major protein identified
of whole mealworms on IgE-reactivity. to cross-react with IgE from crustacean allergic patients
was tropomyosin. Heat processing as well as in vitro
digestion did diminish, but not eliminate, house dust mite
or tropomyosin IgE cross-reactivity. Tropomyosin
allergenicity appeared decreased in fried samples and
disappeared in fried in vitro digested samples.
Broekman H. C. H. P. et al., To investigate the allergenic potential of edible insects in Allergenic The most IgE-binding proteins were tropomyosin and
2017b (The Netherlands, both the shrimp and primary mealworm allergic arginine kinase. Subjects with primary mealworm allergy
Italy) population. showed sensitization to the tested insect extracts.
Tropomyosin and arginine kinase were identified in all
insect extracts and many subjects have shown reactivity to
these two allergens. From the results obtained, it can be
concluded that shrimp-allergic patients are probably at risk
not only for food allergy to mealworm but also from other
insects.

prions, fungi, and parasites (Fernandez-Cassi et al., 2018). There is no conditions: in fact, in controlled breeding, the elements needed to
evidence of the presence of parasites in bred insects, but it can be as- complete their lifecycle are lacking, and processing (freezing and
sumed that this risk can be eliminated under controlled breeding cooking) can contribute in the elimination of this risk (Gallo, 2018).

8
A. Cappelli, et al. Food Control 108 (2020) 106877

Fig. 1. Flow charts regarding the selection of papers on microbiological (a), chemical (b), physical (c), and allergenic (d) risks obtained according to the results of the
systematic review.

The prions of insects have not been described and no diseases caused by Broekhoven, Gutierrez, De Rijk, De Nijs, and Van Loon (2017) shows
them have ever been observed (Grau et al., 2017; Van der Fels-Klerx that Tenebrio molitor larvae are able to metabolize deoxynivalenol be-
et al., 2018). The risk related to prions is linked to the substrate: if the cause the remaining fraction of this compound, i.e. the portion excreted
substrate is contaminated, the insects may be able to act as mechanical through faeces, has not been detected. Cooking or digestion can remove
vectors in their transmission to humans (Gallo, 2018; Van der Fels-Klerx or deactivate some chemical hazards (Liu & Zhao, 2018). However,
et al., 2018; Van der Spiegel, 2016). collecting insects for the production of food and food ingredients must
be done in such a way as to prevent or minimize the accumulation of
toxins, drugs, and antinutrients coming from outside (Schlüter et al.,
3.3. Chemical risks 2016). In particular, the most critical steps regard the breeding phase,
which is crucial to control the chemical risk, and the transformation
Chemical contaminants, like toxins, can be absorbed by insects from process.
the feed or the insects themselves can synthesize these compounds
(Schlüter et al., 2016). It is reported that darkling beetles, from the
3.4. Physical risks
Tenebrionidae family, produce quinones and alkanes, but the risk
arising from these substances needs to be better investigated (Schlüter
In none of the selected articles is the physical risk treated specifi-
et al., 2016). However, it is important to highlight that darkling beetles
cally for yellow mealworm larvae or house cricket. Only general in-
are not usually consumed as food. In a study by Poma et al. (2017), the
formation is given for all insects. Choking is the greatest physical ha-
levels of different chemical contaminants in different insects and insect
zard associated with insects consumption: in fact, the insect body is
products were analyzed. Poly-Chlorinated Biphenyl (PCB) levels were
inhomogeneous because it has appendages like spines or cuticles, which
higher in cricket croquettes (1712 pg/g ww) than in Alphitobius dia-
make insects a foreign texture to those with which Western palates are
perinus-based food (783 and 156 pg/g ww), Alphitobius diaperinus larvae
accustomed (it is particularly hazardous for elderly people and chil-
(33.8 pg/g ww) and Tenebrio molitor larvae (26.5 pg/g ww). In the
dren, owing to greater difficulty in ingestion) (Marone, 2016). For this
products mentioned, the level of Organo-Chlorine Pesticide (OCP) was
reason, powdered insects are considered safer than whole insects and it
higher in Tenebrio molitor larvae (156 pg/g ww). Poly-Brominated Di-
is also the form that mostly facilitates consumer acceptance (Marone,
phenyl Ether (PBDE) and Halogenated Flame Retardant (HFR) were
2016). The control of physical hazards when the risk is identified as a
below the limit of quantification, except for one Alphitobius diaperinus-
part or an ingredient of the food, in our case represented by the whole
based food (16.2 pg/g ww). A total of six Phosphorous Flame Re-
insect or a part of it, is particularly difficult; the best way to prevent it is
tardants (PFRs) were detected and their concentration in samples were
to follow good manufacturing practices (e.g. IPIFF guide on Good Hy-
higher than the other compounds analyzed, which might be due to their
giene Practices) and increase the awareness of employees in controlling
use in treatment processes and packaging.
all the steps of the food chain (Marshall, Dickson, & Nguyen, 2016).
Zinc was the most abundant metal in samples, followed by copper
However, according to the degree of risk exposure, the adoption of
Poma et al. (2017). In a study on contaminated substrates with different
personal protective equipment (PPE), such as filtering facepiece re-
heavy metal levels, it was observed that Tenebrio molitor larvae can
spirator, could protect the workers during the processing phases.
accumulate arsenic but not cadmium and lead (Van der Fels-Klerx,
Camenzuli, Van Der Lee, & Oonincx, 2016). Regarding mycotoxin
contamination, the results of Bosch, van der Fels-Klerx, De Rijk, and 3.5. Allergenic risks
Oonincx (2017) suggest that aflatoxin B1 is rapidly catabolized and
excreted by yellow mealworm larvae, either by conversion into afla- Based on the number of results obtained and the fact that most of
toxin M1 or simply as aflatoxin B1. This highlights a significant risk the articles confirm the likelihood of developing food allergy to insects,
related to bioaccumulation. Moreover, the study reported by Van it can be stated that the risk of allergic reactions related to the

9
A. Cappelli, et al. Food Control 108 (2020) 106877

consumption of insects is significant. People allergic to crustaceans and insects in the refrigerator.
house dust mites can develop allergic reactions to insects due to the Another heat treatment that can be applied to insects is blanching.
close taxonomic relationship between insects and arthropods, which In the study by Vandeweyer et al. (2017b), it is shown to lead to a
helps to predict allergens (Downs, Johnson, & Zeece, 2016). The major significant reduction of microbial counts. Particularly for blanching
allergens that cause cross-reactivity in insects are tropomyosin and times of 10, 20, and 40 s, log reductions for total counts of 4.4, 6.4, and
arginine kinase, but there are also other allergens such as sarcoplasmic 5.6 log cycles were observed (no relationship between the magnitude of
calcium-binding protein, myosin light chain, troponin C, sarcoplasmic the reduction and blanching times was observed). Blanching followed
endoreticulum calcium ATPase, hemocyanin, and phospholipase by refrigerated storage can preserve mealworms without spoilage for at
(Downs et al., 2016). In a study by Broekman et al. (2017a), it has been least six days (Vandeweyer et al., 2017b). In the same study, it was
observed that mealworm breeders (both domestic and professional) observed that a blanching treatment followed by microwave drying
develop inhalant allergy and food allergy to this insect, and binding IgE represents a pasteurization treatment because of the killing of vegeta-
were found towards allergens as tropomyosin, arginine kinase, myosin tive cells but not of the spores. Moreover, blanching preceded by
light chains, and myosin heavy chains. In shrimp-allergic patients, roasting leads to a strong reduction in the number of En-
mealworm consumption shows different symptoms like oral allergy, terobacteriaceae (FASFC, 2014), although Klunder et al. (2012) observe
urticaria, nausea, abdominal cramping, vomiting, and dyspnea that roasting alone is not able to completely eliminate En-
(Broekman et al., 2016). More in general, insect food allergy can occur terobacteriaceae. No treatment was found to be capable of significantly
in different ways (from a mild localized reaction to anaphylactic shock) reducing the count of sporulating bacteria and bacterial spores: in the
and symptoms are subdivided into cutaneous, gastrointestinal, and re- reviewed studies, no one was able to eliminate them with heat treat-
spiratory (De Gier & Verhoeckx, 2018). ment (De Castro et al., 2018; Gallo, 2018; Liu & Zhao, 2018; Van der
Regarding cricket allergenicity, Hall, Johnson, and Liceaga (2018) Fels-Klerx et al., 2018; Van Huis, 2016; Van Huis & Dunkel, 2017).
studied cross-reactivity between human shrimp-allergic sera and tro- After heat treatments, insects may be frozen or freeze-dried: these
pomyosin in crickets (Gryllodes sigillatus) at different degrees of hy- two treatments are applied to obtain an extension of the shelf life of the
drolysis: cricket protein hydrolysates with a degree of hydrolysis of product, but it was observed in a preliminary study that they barely
60–85% had the lowest reactivity to tropomyosin compared to those influence the total aerobic bacterial count of the insects (FASFC, 2014).
with a degree of hydrolysis of 15–50% and to the unhydrolyzed cricket. The crushing of the larvae leads to the release of microorganisms
Processing can affect insect allergenicity. In fact, tropomyosin aller- contained in the intestine and to their distribution across the whole
genicity seems to be decreased in fried samples and disappeared in fried insect; this leads to an increase in viable bacteria count (Klunder et al.,
and in vitro digested samples (Van Broekhoven, Bastiaan-net, de Jong, 2012). According to Rumpold and Schlüter (2013), a crushing step
& Wichers, 2016). Apart from proteins, there is also an allergen of in- before thermal treatment (boiling or roasting) does not improve the
sects among carbohydrates, namely chitin. Chitin is a fiber present in efficacy but results in a higher microbial content in comparison with
the exoskeleton of insects (also in crustaceans) (Van der Spiegel, 2016). the whole insect. However, confirmation studies which test several
The effect of processing on allergens can be understood from studies time-temperature ratios and different methods of heating application
devoted to closely related arthropod species, as there is not much in- (e.g. direct and indirect heating) are necessary to validate this state-
formation regarding insect-specific allergens (Downs et al., 2016). ment. One possibility to reduce the contamination resulting from the
However, data from recent literature about the effect of thermal microbiota of insect gut, is to adopt a starvation period before insect
treatment are contradictory because highlight that the allergenicity harvest. However, the effect of a starvation period of 48 h has been
may decrease, increase, or remain the same (Broekman et al., 2015; De studied; there is no significant effect of reducing the microbial content
Gier & Verhoeckx, 2018; Van Broekhoven et al., 2016). Contradictory of insect gut (Wynants et al., 2017). Further studies are needed to
results may be explained by the fact that processing changes the solu- clarify the effect of starvation in edible insects.
bility of proteins (De Gier & Verhoeckx, 2018). Although digestion has Fermentation of insects is also documented. It is used to increase the
an effect on food allergenicity due to the acidic environment, protein shelf-life and microbial safety of ground insects (FASFC, 2014). It was
degradation does not always occur completely and sometimes does not observed that fermentation deactivates Enterobacteriaceae and main-
occur at all (De Gier & Verhoeckx, 2018). tains spore-forming bacteria under 103 cfu/g (Klunder et al., 2012).
During fermentation, spores were unable to germinate and grow
4. Discussion (Klunder et al., 2012). Borremans et al. (2018) studied fermentation of
insects, specifically in Tenebrio molitor larvae; their results suggest that
From the selected studies chosen by means of the systematic process to obtain rapid acidification with the aim to inhibit undesirable mi-
of review emerges the exigence of developing machines and processes croorganisms, a starter culture should be added. In this study, mar-
to reduce the microbiological, chemical, physical, and allergenic risks ination of insects was also investigated; it was observed that it can
related to emerging production chain of insects for food. This is ne- prolongs the shelf life of fresh mealworms for at least seven days due to
cessary in order to lay the foundations for the development of a spe- a reduction of pH which inhibits microbial growth during storage
cifically designed supply chain of insects for food, which can guarantee (Borremans et al., 2018).
the safety and health for workers and consumers. Cold atmospheric pressure plasma is a treatment that can be applied
without the use of heat. Buβler et al. (2016a) studied the effect of cold
4.1. Strategies for reducing the microbiological risks atmospheric plasma on the microbial load of Tenebrio molitor flour. It
led to a reduction in the microbial content, the magnitude of which
The microbiological content of Tenebrio molitor and Acheta domes- increased with the prolongation of treatment time: the initial microbial
ticus (fresh, processed, or stored) was evaluated in the study by Klunder load of 7.72 log10 cfu/g was reduced to 7.10 log10 cfu/g after 1 min and
et al. (2012), along with the effect of certain processes on it. The effect to 4.73 log10 cfu/g after 15 min of treatment (Buβler et al., 2016a).
of boiling was observed to completely eliminate Enterobacteriaceae According to present knowledge, the most interesting strategies to re-
after 5 min of treatment. In crickets, however, prolonging the boiling duce the microbial contamination would include the addition of
time to 10 min does not affect the level of the remaining bacteria blanching machine in the production chain, followed by refrigeration in
(Klunder et al., 2012). Boiling and cooking under vacuum were seen to the case of whole insect conservation, or microwave treatment before
be the most efficient treatments for reducing the microbial load in processing. However, after the blanching and/or microwaves treat-
mealworms (Caparros Megido et al., 2018). Based on the obtained re- ments, which reduce the microbial load, the fermentation with selected
sults, Klunder et al. (2012) recommend applying boiling before storing strains of yeasts and LAB might significantly reduce the microbiological

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risk, exalting the efficacy and efficiency of the blanching and/or mi- The operators involved in the production must follow correct personal
crowaves treatments. hygiene practices (in particular the good manufacturing practices in
force (e.g. IPIFF guide on Good Hygiene Practices)) and wear suitable
4.2. Strategies for reducing the chemical risks clothing and protections to prevent the introduction of foreign bodies
and the risk of inhalation.
Regarding chemical contaminants, EFSA (2015) reports that pro- In agreement with the scarceness of data collected, with the utili-
cessing conditions (e.g. heating or freeze-drying) have only minimal zation of an effective insect-sorting machine, it is possible to effectively
effect on them. The best way to control the levels of chemical con- reduce the risk of foreign-body contamination in the product. An im-
taminants is fractionation because they are accumulated in specific portant focus should regard the physical risk related to the workers’
insect fractions (EFSA, 2015). For the prevention of chemical risk, it is activities. In particular, the selection of machines optimized in ergo-
important to control insect breeding substrates, feed, and the environ- nomics and usability terms, as automated as possible, would reduce the
ment in which insects are bred, because of the ability of insects to ac- cutting and contusion risks along the production chain of insects for
cumulate chemical contaminants. In addition to breeding, a check food. Furthermore, in order to guarantee workers safety, another im-
could be applied for the presence of chemical contaminants during the portant focus might regard the adoption of specific PPE, such as fil-
process. For the rapid detection of chemical contamination, several tering facepiece respirator, which could protect the workers from in-
methods can be used: immunodetection (which is based on the inter- halation risk during the processing phases.
action between an antigen and an antibody, it is used in pesticide de-
tection, for example), chemistry method (in presence of metallic ion, 4.4. Strategies for reducing the allergenic risks
organic agrochemical of phosphorous hydrolyze giving rise to a hy-
drolysis product that leads to color change) and biosensor (the con- As previously reported, there are in literature contradictory data
centration of the contaminant is converted into a measurable electrical about the effect of thermal treatment on the food allergenicity of insects
signal) (Tang, Lu, Zhao, & Wang, 2009). For heavy metal analysis, the (De Gier & Verhoeckx, 2018). In fact, EFSA (EFSA, 2015) also reported
common techniques employed are different types of spectrometry that the allergenicity of certain compounds can be triggered or blocked
(Zukowska & Biziuk, 2008); however, these methods require a labor- through heat treatment that alters the structure of proteins (Fernandez-
ious phase of sample preparation and are not possible in time restric- Cassi et al., 2018). Although, the understanding of the effect of pro-
tions. cessing on insect-allergens can be found in studies devoted to closely
Recently, nanotechnology is often used to provide sensors for heavy related arthropod species (Downs et al., 2016), there are some studies
metal detection in the environment, such as fluorescent sensors, plas- that investigate allergenicity. Broekman et al. (2015) were the first to
modic sensors, surface-enhanced raman scattering (SERS) sensors, op- study the effect of heat treatment on mealworm allergenicity: they
tofluidic sensors, electrochemical sensors, field-effect transistor (FET) observed that the IgE-binding capacity and IgE cross-linking function-
sensors (Li, Gou, Al-Ogaidi, & Wu, 2013). Due to the fact that the ac- ality of mealworm allergens were not lowered by the processing, while
cumulation of heavy metals in insects comes mainly from feed, these the solubility of proteins was strongly influenced. As the heat treatment
sensors could be used for heavy metal detection in the breeding en- seems to increase the solubility of tropomyosin, it was hypothesized
vironment. Apart from feed and breeding, control should be maintained that this phenomenon happened when the bonds with proteins were
throughout the production process because chemical contaminants broken or when the formation of soluble aggregates took place during
could be introduced during unit operations, for example migration from the treatment (Broekman et al., 2015). Tropomyosin allergenicity, in
the machines used. From this point of view, in the choice of the ma- the study by Van Broekhoven et al. (2016), decreased in fried samples
chines to be included in the production process, the evaluation of the and disappeared in fried and in vitro digested samples. On the other
usability of the machines is important. An example of the migration of hand, heating causes the arginine kinase to unfold, exposing the hy-
chemical contaminants in food during a unit operation, specifically the drophobic amino acids and leading to the formation of larger protein
grinding, is reported by Yahaya, Aremu, and Abdullahi (2012): in aggregates that, in most cases, are insoluble (Broekman et al., 2015).
ground food samples, an increase in iron content was observed, so it Regarding the allergenicity of crickets, in a study by Hall et al.
was recommended to subject the grinding discs to heat treatment to (2018), it was observed that the enzymatic hydrolysis of proteins had
minimize metal contaminants in ground foods. In accordance with the an effect on tropomyosin allergenicity: in fact, cricket protein hydro-
findings, possible strategies intended to reduce the chemical risk could lysates with a major degree of hydrolysis showed the lowest reactivity
start by preventive approach in the breeding phase, followed by careful of tropomyosin. Given the consistency of information in the references,
fractionation and finally rapid detection strategies during the critical it is advisable not to encourage people who are allergic to crustaceans
control points of the process with nanosensors. and house dust mite to consume insects. It is, therefore, essential that
the information accompanying the product must be clear: on the label,
4.3. Strategies for reducing the physical risks it should be reported a warning addressed to people allergic to crus-
tacean and house dust mites, informing them of the allergenic risk that
As previously mentioned, the major physical hazard present in in- they run in case of consumption of the product. However, frying and
sects is choking: the way to limit this risk is to grind insects (Marone, enzymatic hydrolysis seems to be the most interesting strategies to re-
2016). For an optimal control of physical risks, critical points should be duce the tropomyosin allergenicity. Finally, further investigations are
identified throughout the production process. In particular, the HACCP needed to assess the effect on workers' health connected with the risk of
system should be focused on the most critical phases (sorting, grinding, developing allergenicity due to inhalation during the grinding unit
and packaging) to guarantee safe working conditions and product free operation and in others phases of the production chain (Broekman
from foreign bodies. Moreover, unit operations are crucial so it would et al., 2017a). In particular, a clarification is necessary regarding the
be advisable to use machines that prevent the introduction of foreign effects on workers’ health to understand if single exposure is sufficient
bodies, such as closed grinders, with significant reduction in the in- to produce damages on health or if prolonged exposure is needed.
halation risk for the workers. To verify the good functioning of the most
critical unit operations, of the HACCP plan and of the identified critical 5. Conclusions & future trends
points, the installation of instruments capable of detecting the presence
of foreign bodies during the process and in the product might be useful. The growing demand of protein food with reduced environmental
The presence of foreign bodies such as metals and glass can be verified impacts is currently a big challenge for food production. Insects re-
by installing metal detectors or X-ray machines (Marshall et al., 2016). present a potential frontier of good quality food, rich in nutrients and

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easy to be produced, at cheaper costs and with possible lower en- Caparros Megido, R., Desmedt, S., Blecker, C., Béra, F., Haubruge, É., Alabi, T., et al.
vironmental impact. Nonetheless, it is fundamental for the consumers' (2017). Microbiological load of edible insects found in Belgium. Insects, 8(1), 12.
Caparros Megido, R., Poelaert, C., Ernens, M., Liotta, M., Blecker, C., Danthine, S., et al.
safety to conduct prospective studies on the risks raised by them, since (2018). Effect of household cooking techniques on the microbiological load and the
in the majority of the EU Countries, as well as in the Northern part of nutritional quality of mealworms (Tenebrio molitor L. 1758). Food Research
America, their use is too recent to have solid evidences on the impact on International, 106, 503–508.
Chomchai, S., & Chomchai, C. (2018). Histamine poisoning from insect consumption: An
health, as well as on the effectiveness of the processes used to control outbreak investigation from Thailand. Clinical Toxicology, 56(2), 126–131.
the described risks. As for all the novelties, insects will also require Cicatiello, C., Franco, S., Pancino, B., & Blasi, E. (2016). The value of food waste: An
specific surveillance systems that can promptly record any unfavorable exploratory study on retailing. Journal of Retailing and Consumer Services, 30, 96–104.
De Castro, R. J. S., Ohara, A., Aguilar, J. G., dos, S., & Domingues, M. A. F. (2018).
episode for consumers’ health, which can address the private and public Nutritional, functional and biological properties of insect proteins: Processes for
control to improve the safety of the whole production chains, so as to obtaining, consumption and future challenges. Trends in Food Science & Technology,
ensure safe products on the market. Many other primary studies are 76, 82–89.
De Gier, S., & Verhoeckx, K. (2018). Insect (food) allergy and allergens. Molecular
necessary to untie these nodes, but this review is a preliminary proof
Immunology, 100, 82–106.
that authorized novel foods can, at least partially, represent a possible Downs, M., Johnson, P., & Zeece, M. (2016). Insects and their connection to food allergy.
answer to the increasing demand of protein food by a population that is Insects as sustainable food ingredients (pp. 255–272). Academic Press.
forecast to grow significantly and whose food demand will not be re- EFSA Scientific Committee (2015). Risk profile related to production and consumption of
insects as food and feed. EFSA Journal, 13(10), 4257.
duced in the future. This paper suggests strategies to orient the devel- European Commission (2005). Commission Regulation (EC) No 2073/2005 of 15 November
opment and improvement of specific machines for the emerging pro- 2005 on microbiological criteria for foodstuffs, Vol.50, Off. J. Eur. Union1–26.
duction chain of insects for food, with ameliorative effects on workers European Union (2015). Regulation (EU) 2015/2283 of the European parliament and of the
council of 25 November 2015 on novel foods, amending regulation (EU) No 1169/2011 of
and finished products safety. In particular, this review aims to lay down the European parliament and of the council and repealing regulation (EC) No 258/97 of
the foundations for the development of the production chain of insects the European parliament and of the council and commission regulation (EC) No 1852/
for food which should be based on integrated supply chain approaches, 2001. European Parliament.
FAO (2014). State of food insecurity in the world 2013: The multiple dimensions of food
specific self-regulations and HACCP plans, development of ad hoc ma- security. FAO.
chines, and defined processes flowcharts that might lead to a specific FAOSTAT, D. (2013). Food and agriculture organization of the united nations. Statistical
European Regulation for edible insects. database.
FASFC (2014). Food safety aspects of insects intended for human consumption Sci Com
dossier 2014/04. SHC dossier n°, 9160(9160), 1–22.
Funding Fasolato, L., Cardazzo, B., Carraro, L., Fontana, F., Novelli, E., & Balzan, S. (2018). Edible
processed insects from e-commerce: Food safety with a focus on the Bacillus cereus
group. Food Microbiology, 76, 296–303.
This research did not receive any specific grant from funding
Fernandez-Cassi, X., Supeanu, A., Jansson, A., Boqvist, S., & Vagsholm, I. (2018). Novel
agencies in the public, commercial, or not-for-profit sectors. foods: A risk profile for the house cricket (Acheta domesticus). EFSA Journal,
16(July), 1–15.
Declarations of interest Francis, F., Doyen, V., Debaugnies, F., Mazzucchelli, G., Caparros, R., Alabi, T., et al.
(2019). Limited cross reactivity among arginine kinase allergens from mealworm and
cricket edible insects. Food Chemistry, 276, 714–718.
The authors declare no conflict of interest. Gallo, M. (2018). Novel foods: Insects - safety issues. Encyclopedia of Food Security and
Sustainability. Elsevier, 1, 294–299.
Garofalo, C., Osimani, A., Milanović, V., Taccari, M., Cardinali, F., Aquilanti, L., et al.
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