ABSTRACT

Edible insects are a novel food in most countries; their popularity is growing because of their high-protein and low-fat content, ease of cultivation, and small environmental impact. To our knowledge, this is the first report that addresses both microbiological and chemical hazards in edible insects. Samples were collected from retail stores or purchase through e-commerce. A total of 51 samples of dried whole insects or insect powder were tested for Escherichia coli, which serves as an indicator of the overall sanitation conditions throughout the food production chain, and the bacterial pathogen Salmonella spp. Neither Salmonella spp. nor E. coli (>100 CFU/g) was found in the samples analyzed. A total of 43 samples of crickets (protein bars, powders, flour, and whole insects) and 4 samples of silkworm (whole insects) were analyzed for up to 511 pesticides. Of these, 39 samples contained up to four pesticides; 34 samples were compliant and 5 samples were noncompliant with Canadian regulations. Seven pesticide residues were detected, with glyphosate and its metabolite, aminomethylphosphonic acid, as the predominant residues. Nineteen of the samples tested for pesticides were also analyzed for arsenic, cadmium, mercury, and lead; there was insufficient material remaining to allow testing of pesticides and metals. The positive rates for arsenic, cadmium, lead, and mercury were 100, 79, 58, and 74%, respectively. The detected concentrations ranged from 0.030 to 0.34 mg/kg for arsenic, from 0.031 to 0.23 mg/kg for cadmium, 0.019 to 0.059 mg/kg for lead, and from 0.94 to 28 μg/kg for mercury. Based on the lack of detection of microbiological contamination, and the positive rates and levels of pesticides and metals observed in the products, Health Canada determined that all insect products analyzed were safe for human consumption. This is a limited study; the Canadian Food Inspection Agency will continue to monitor this novel food.

HIGHLIGHTS
  • Edible insects were tested for potential microbiological and chemical health hazards.

  • No Salmonella spp. or E. coli (>100 CFU/g) was detected.

  • 89% compliance was found with Canadian pesticide regulations.

  • Glyphosate and its metabolite, AMPA, were the most commonly detected pesticides.

  • All insect products tested were deemed safe for human consumption.

Edible insects and food products containing insect ingredients are not commonly consumed by humans in North America and Europe. By contrast, people in Africa, Asia, and Latin America have been consuming insects for centuries. There are 1,000 to 2,000 species of insects consumed globally (22). The Food and Agriculture Organization of the United Nations (10) and other organizations have been promoting the cultivation and consumption of edible insects as alternative sources of protein (food security) and as sustainable forms of agriculture. Edible insects have high protein-to-fat ratios relative to plants or traditional meats, making insects a healthier and more nutritious food. The environmental footprint of insect production is minimal compared with the production of beef, pork, and chicken (31).

In response, a growing number of edible insect products have appeared on the Canadian market in recent years, such as whole and powdered insects and processed insect products. Dried whole insects (roasted, smoked, and flavored) are intended to be consumed as is, whereas powdered insects are used as ingredients in other foods. Processed products, such as protein bars, chips, crackers, and cookies, are manufactured with insects as the principal source of protein. Edible insect products can be purchased online, at specialty stores, and at mainstream grocery stores.

To date, there are no specific regulations, standards, or guidelines regarding potential microbiological or chemicals hazards established in Canada for edible insects or insect-containing foods. Internationally, the European Food Safety Authority requires premarket approval of individual edible insect species (8). A few countries in the European Union permit the marketing and sale of certain edible insect species (25). Edible insects produced for human consumption and available to Canadian consumers must meet the same safety and hygiene standards as other foods available in Canada (6). All pesticide residues in insect products are subject to the general maximum residue limit (MRL) of 0.1 mg/kg (7). Each pesticide is assessed separately against the MRL, including cases with multiple pesticides per sample. Notable exceptions are a pesticide and its metabolite or metabolites or multiple forms of a pesticide (e.g., spinosyn A and spinosyn D, assessed as spinosad), which are summed and then compared against the MRL. There are no regulations regarding permissible levels of arsenic, cadmium, lead, or mercury in insect products in Canada (7). In this context, this article presents baseline surveillance data on the prevalence and levels of chemical and microbiological hazards of edible insects. These data are important in the assessment of potential human health risks.

Insect samples

Each sample consisted of a single or multiple unit or units (e.g., individual consumer-sized packages) from a single lot with a total weight of at least 50 g for microbiological analysis or at least 200 g for chemical analysis. All samples were acquired from online retailors or collected at retail establishments located in Ottawa, Canada, with the intent of capturing as wide a range of retail forms (i.e., brand and product type) and insect types as possible. The samples included dried whole insects, insects in powdered form, or insects incorporated into finished products (e.g., protein bars). The products included domestically cultivated and processed products, domestically processed products, and imported products. Some products were labeled organic. To be included in the study, the products had to be intended for human consumption. Therefore, insects available for purchase as animal or pet feed were excluded. A total of 51 samples of dried whole insects or insect powder were collected for microbiological hazard testing. A total of 43 samples of crickets (protein bars, powders, flour, and whole insects) and 4 samples of silkworm (whole insects) were collected for chemical hazard testing.

Microbiological analyses

Samples were analyzed for Salmonella spp. and Escherichia coli by the Canadian Food Inspection Agency (CFIA) using methods published in Health Canada's Compendium of Analytical Methods for the Microbiological Analysis of Foods (15). Specifically, MFLP-29 and MFHPB-20 were used for Salmonella spp. and MFHPB-34 was used for E. coli analysis (15).

Chemical analyses

Samples were analyzed in an external, ISO/IEC 17025–accredited laboratory under contract with the Government of Canada. The methods have been demonstrated to provide accurate results via internationally accredited proficiency testing programs, as well as interlaboratory sample comparison. In addition, when the laboratories identify pesticide residue levels within 80% of the MRL for a particular commodity, they are required to repeat the assay to verify the results. Four analytical methods were used (and will be individually described later): a multiresidue pesticide method (505 pesticides), a phenoxy herbicide method (2 pesticides: 2,4-dichlorophenoxyacetic acid [2,4-D] and 2-methyl-4-chlorophenoxyacetic acid [MCPA]), a quat screen (diquat/paraquat) method, and a glyphosate method (parent compound plus metabolite) for a total of 511 pesticides. Metal method analyses were used for up to 18 metals, but only the toxic metals (arsenic, cadmium, lead, and mercury) are discussed in this article.

Chemical analysis: multiresidue pesticide method

The multiresidue pesticide method began with soaking in water for 2 h (1). Then, the sample was extracted in 1% acetic acid in acetonitrile in the presence of isotopically labeled internal standards. Cleanup was performed using dispersive solid-phase extraction with primary-secondary amine and C18. The extract was then analyzed by gas chromatography–tandem mass spectrometry (GC-MS/MS) and liquid chromatography–tandem mass spectrometry (LC-MS/MS).

GC-MS/MS was performed using electron impact ionization, with helium as the carrier gas (1). The samples were also analyzed using reverse-phase liquid chromatography with gradient conditions. Detection was performed by tandem mass spectrometry with electrospray ionization in positive or negative mode with multiple reaction monitoring (1). A total of 505 pesticides were analyzed by these two methods. Two transitions were monitored per pesticide residue, regardless of detection method. Supplemental Table S1 contains a list of all pesticides screened as part of this method.

Chemical analysis: phenoxy herbicide method

With the phenoxy herbicide method (2), the sample was extracted in 0.007 M HCl, pH was adjusted to 2, and ethyl ether was added. After centrifugation, the ethyl ether layer was evaporated to near dryness, diluted to volume with methanol, centrifuged again, and then analyzed with LC-MS/MS. The samples were analyzed using reverse-phase liquid chromatography with isocratic conditions. Detection was performed by tandem mass spectrometry with electrospray ionization in negative mode with single reaction monitoring. For MCPA, m/z 199 and 201 were monitored, whereas for 2,4-D, m/z 219.2 and 221.2 were monitored. Table S2 contains a list of all pesticides screened as part of this method and their limits of detection (LODs).

Chemical analysis: quat method

With the quat method (9), samples were extracted in acidic methanol (2% HCl). After incubation, two rounds of centrifugation, and filtration, the samples were ready for analysis by LC-MS/MS.

The samples were analyzed using reverse-phase, ion pair liquid chromatography with gradient elution. Detection was performed by tandem mass spectrometry with electrospray ionization in positive mode. Two transitions were monitored for each analyte. For paraquat, m/z 171.0 to 155.0 and 171.0 to 103.0 were monitored. For diquat, m/z 183.0 to 157.0 and 183.0 to 130.0 were monitored. Table S3 contains a list of all pesticides screened as part of this method and their LODs.

Chemical analysis: glyphosate method

With the glyphosate method (26), the sample was extracted in 0.05 M KOH in the presence of an isotopically labeled internal standard. After centrifugation, the extract was adjusted to pH 7.0 ± 0.5 with 0.1 M HCl. Following addition of 5% sodium thiosulfate and sodium tetraborate, the sample extract was derivatized with fluorenylmethyloxycarbonyl chloride. The reaction was quenched, filtered, and analyzed by LC-MS/MS (26). The samples were analyzed using reverse-phase liquid chromatography with gradient elution. Detection was performed by tandem mass spectrometry with electrospray ionization in negative mode. Two marker residues were analyzed (glyphosate and its metabolite, aminomethylphosphonic acid [AMPA]), and two transitions were monitored for each analyte. For glyphosate, m/z 390.0 to 150.0 and 390.0 to 168.0 were monitored. For AMPA, m/z 110.0 to 63.0 and 110.0 to 79.0 were monitored. Table S4 contains a list of all pesticides screened as part of this method and their LODs.

Multimetal analysis

In addition, where there was sufficient quantity of sample, the samples were analyzed by inductively coupled plasma mass spectrometry (ICP-MS) for 18 metal contaminants (28, 30). The sample was extracted with 7.5 mL of concentrated nitric acid at room temperature for 12 h. The extract was then heated, and hydrogen peroxide and hydrochloric acid were added sequentially. The last step was the addition of water to a volume of 50 mL. The sample was thus ready for analysis by ICP-MS.

For determination of arsenic, cadmium, and lead by ICP-MS, the digestate was introduced into the Argon plasma with a temperature between 6,000 to 8,000 K. Ions were filtered based on mass-to-charge ratio and detected by a discrete dynode electron multiplier. The output from the detector was proportional to the concentration of the element in the sample. The reporting limits were 0.02 mg/kg for arsenic, 0.01 mg/kg for cadmium, and 0.015 mg/kg for lead. Table S5 contains a list of all metals screened as part of this method and their LODs.

Mercury (29) was analyzed by cold vapor atomic fluorescence spectroscopy. Mercury atoms were excited by a UV light source at a wavelength of 254 nm; the fluorescence was detected by photomultiplier tube or UV photodiode. Argon was used as the carrier gas. The reporting limit was 0.5 μg/kg.

Statistical analysis

The sample population consisted of all units of the targeted commodities available at retail to Canadian consumers as per the sampling design. Because all units of the population could not be assumed to have an equal probability of selection, the commodity units at a store or online were drawn as randomly as possible to be reasonably representative of the population. The sampling method used for this study was a nonprobability sampling method, which does not allow standard statistical inferential methods to be invoked. Nevertheless, the random selection approach provide a snapshot on the presence of microbiological and chemical hazards in the selected foods.

A total of 51 samples of dried whole insects or insect powder were tested for microbiological hazards. A total of 43 samples of crickets (protein bars, powders, flour, and whole insects) and 4 samples of silkworm (whole insects) were tested for chemical hazard testing. The results are discussed below in the appropriate sections “Microbiological testing” and “Chemical testing.”

Microbiological testing

All 51 products sampled as part of this study were analyzed for the presence of Salmonella spp. and E. coli. Table S6 presents the species of whole and powdered insects tested as part of this study. Of the 51 samples, 18 (35%) were domestically produced and 33 (65%) were imported from five countries (France, Thailand, the United Kingdom, the United States, and Zambia). Salmonella spp. and E. coli (>100 CFU/g) were not detected in the samples tested. Similar to the results of this survey, a preliminary study in Germany did not detect the presence of Salmonella or E. coli (>100 CFU/g) in 38 samples of edible insects available at retail between 2014 and 2015 (12). In 2015 to 2016, a Dutch study found that genetic material from Salmonella spp. was absent from the processed edible insect samples from one Dutch company (11). However, these studies identified Bacillus cereus, Pseudomonas spp., (12), Listeria spp., and Staphylococcus spp. (11) in the samples analyzed, respectively.

Several studies have indicated that the total bacterial load of unprocessed raw insects was higher than that found in raw ground meat and that an effective heat treatment (sterilization) is needed to reduce the total bacterial load (3, 13, 24). The Federal Agency for the Safety of the Food Chain of Belgium requires all insects for human consumption to undergo heat inactivation or sterilization to ensure the safety of the food products (25).

Because the samples we tested were picked up at retail, no information is available on whether a heat-inactivation step was used or on the conditions from breeding stage to final product. Our preliminary bacterial testing results indicate that the edible insects analyzed in this study appear to have been produced under sanitary conditions.

Chemical testing

A total of 47 samples were tested for up to 511 pesticides. The residue levels of the pesticides were assessed against Canadian MRLs for pesticide residues in food. The MRL is the maximum amount of residue that is expected to remain in or on food products when a pesticide is used according to label instructions. Product compliance was determined by comparison of the reported level of a pesticide and metabolites to the MRLs published in Health Canada's Pesticide MRL database (14). Many food-pesticide combinations do not have specific MRLs in Canada. In those cases, a default MRL (0.1 mg/kg) is used for assessments. There are no MRLs in place for insect products, so the default MRL was used for assessment.

Table 1 shows a summary of the number of samples tested, the number of nondetects, the number of detects (the concentration is at or below the default MRL of 0.1 mg/kg), and the number of noncompliances (the concentration exceeds 0.1 mg/kg). The detection rate for pesticides was 50% in silkworms and 89% in cricket-based products (with variation depending on product format). Of the 47 samples, 5 samples (4 cricket products and 1 silkworm product, 11%) had one or more noncompliant pesticide residues.

TABLE 1

Distribution of sample positives and noncompliances as a function of product type

Distribution of sample positives and noncompliances as a function of product type
Distribution of sample positives and noncompliances as a function of product type

As demonstrated in Table 1 and Figure 1, most samples (64%) contained a single pesticide residue per sample. Eight samples contained no detectable pesticide residues per sample, and seven samples contained two pesticide residues per sample (one sample was associated with two noncompliances). Only one sample contained three pesticide residues (all compliant), and one sample contained four pesticide residues (one compliant and three noncompliant residues).

FIGURE 1

Frequency of detection of pesticide residues per sample.

FIGURE 1

Frequency of detection of pesticide residues per sample.

Close modal

Phenoxy herbicides, diquat, and paraquat were not detected in the samples. Table 2 presents the seven pesticides and one metabolite that were detected in the insect products. Four of the pesticides were detected only in one sample each. Residues of glyphosate (including its metabolite, AMPA, observed singly or in combination) were the most frequently detected pesticide residues. Glyphosate and AMPA co-occurred in eight samples. AMPA alone was detected in two samples. All detections of glyphosate and/or AMPA occurred in cricket-based products.

TABLE 2

Pesticides and metabolites detected in insect samples

Pesticides and metabolites detected in insect samples
Pesticides and metabolites detected in insect samples

The levels of all pesticides observed were quite low, suggesting that the pesticides are not directly applied to the insects being raised for human consumption but rather originate from the materials used for feeding the insects (e.g., grains, seeds, and grass) or other ingredients in the products. Because the samples are being picked up at retail, it is not possible to determine whether, when, or how the pesticides came to be in the products tested.

Few studies in the literature examine the levels of pesticides in retail-level insect products. One study tested locusts for pesticides (23). In that study, five pesticides were detected (β-hexachlorocyclohexane; lindane; aldrin; fenitrothion, also known as sumithion; and malathion) at concentrations ranging from 2.20 to 740 μg/kg. These pesticides are included in the scope of the multiresidue analysis used in this study but were not detected in the samples. Another survey examined 393 pesticides in fly larvae and found only chlorpyrifos (n = 1) and piperonyl butoxide (n = 1) (4). Chlorpyrifos was also detected in this study in a cricket-based protein bar, but piperonyl butoxide was not detected. A recent study of edible insects detected nine pesticides in one or more of the samples, but none of these coincided with the pesticides detected in this study (21). Another study suggests that 99.9% of a pesticide application is absorbed by the environment and may accumulate in the feed materials for insects (20). Articles have suggested that the degree of pesticide accumulation depends on the type of insect, its growth stage, the concentration of the pesticide in the feed or environment, and whether the insects were caught from the wild or farmed. All articles, including the present study, are in agreement that pesticides in insect products do not pose a human health risk.

In the final part of this study, where sufficient sample was collected, multimetal analysis was performed. This subset included 15 samples of cricket-based products and 4 silkworm-based products. The concentrations of the metals in the insect products depend on numerous factors, including the levels in the environment (soil, water, and air), the type of insect, its growth phase at harvest, its lifespan, and the types of chemicals used on the feed materials (e.g., arsenic-containing pesticides). Tables S11 through S22 contain summaries of the metal levels as a function of metal, insect, and product type. Antimony, beryllium, and tin were not detected in the insect samples. Only the results for the toxic metals (arsenic, cadmium, lead, and mercury) are discussed in this article.

Arsenic, cadmium, lead, and mercury are of concern because they are associated with harmful human health effects, ranging from affecting the brains of infants and children to causing cancer or death from exposure to high levels (27). The health effects vary according to the metal, its form, and the concentration. These metals typically are not deliberately added to foods (except as components of pesticides licensed for use in Canada). They may be present as environmental contaminants from natural or industrial sources. The laboratory cannot distinguish the source of the metal.

As shown in Table 3, all insect products tested contained a detectable level of arsenic. The concentrations detected ranged from 0.030 mg/kg (whole silkworm pupae) to 0.34 mg/kg (cricket powder), with an average concentration of 0.094 mg/kg. The average level of arsenic was 0.12 mg/kg in cricket products and 0.049 mg/kg in silkworm pupae. These values do not concur with the reported result of no more than 0.03 mg/kg for cricket samples (18, 21). Table S7 provides a listing of the arsenic content of each of the 19 samples tested.

TABLE 3

Occurrence of arsenic in insect products

Occurrence of arsenic in insect products
Occurrence of arsenic in insect products

Table 4 indicates that none of the silkworm pupae–based products and all cricket-based samples contained detectable levels of cadmium. The levels of detected cadmium ranged from 0.031 to 0.23 mg/kg, with an average level of 0.083 mg/kg. This does not concur with previously reported cadmium levels of no more than 0.03 mg/kg (21). Table S8 provides a listing of the cadmium content of each of the 19 samples tested.

TABLE 4

Occurrence of cadmium in insect products

Occurrence of cadmium in insect products
Occurrence of cadmium in insect products

The positive rate for lead was 58% overall, 25% for silkworm pupae–based products, and 67% for cricket-based products (Table 5). The concentrations of lead ranged from 0.019 to 0.059 mg/kg, with an average concentration of 0.034 mg/kg. The detected level in silkworm pupae–based samples was 0.020 mg/kg versus an average level of 0.033 mg/kg in cricket products. These values do not concur with the reported result of no more than 0.03 mg/kg for cricket samples (21). Table S9 provides a listing of the lead content of each of the 19 samples tested.

TABLE 5

Occurrence of lead in insect products

Occurrence of lead in insect products
Occurrence of lead in insect products

As with cadmium, none of the silkworm pupae–based products and all cricket-based samples contained detectable levels of mercury (Table 6). The levels of detected mercury ranged from 0.94 to 28 μg/kg, with an average level of 6.2 μg/kg. These levels of mercury in crickets are low relative to the 125 ± 62 and 109 ± 73 μg/kg observed in one study (19). Table S10 provides a listing of the mercury content of each of the 19 samples tested.

TABLE 6

Occurrence of mercury in insect products

Occurrence of mercury in insect products
Occurrence of mercury in insect products

The lack of concurrence with literature data for some metal content may relate to the type of insect product sampled, the degree of processing, the growth phase of the insect, the concentrations of heavy metals in the cultivation or harvest environment, and whether the insects are wild caught or farmed. This information is not available, because the samples are picked up at the retail level, rather than the producer level. The data provided in this article, in agreement with all other articles cited, does not indicate that there is a human health risk associated with the levels of toxic metals detected in insect products.

Canada has not established maximum levels (MLs) for heavy metals in insect products. However, Canada has established MLs for arsenic, lead, and mercury in commodities with higher consumption rates than insect products. Specifically, none of the insect samples exceeded the Canadian MLs of 0.35 mg/kg for inorganic arsenic in brown rice or 0.2 mg/kg for lead in beverages (16). The highest level of mercury detected in insect products was almost 18 times lower than the Canadian ML of 0.5 mg/kg for mercury in fish (17). There are no Canadian regulations for cadmium; however, the highest level of cadmium in insect products was almost two times lower than the ML of 0.4 mg/kg for cadmium in rice (5) set by the Codex Alimentarius Commission, an international standard-setting body. This confirms that this novel food (insect products) is safe for consumption.

Edible insect products in the Canadian market were tested for a limited number of hazards. Although the number of insect species and product types was limited, both the microbiological and the chemical data assembled point to no human health risks from the consumption of insect products.

The authors thank Jeffrey van de Riet, Annie Locas, Dugane Quon, and Dingding Huang for their expertise and support in carrying out these studies and/or preparing this manuscript for publication. Studies carried out by CFIA, a federal government body, whose mandate is to safeguard the Canadian food supply, are funded by the CFIA.

Supplemental material associated with this article can be found online at: https://doi.org/10.4315/JFP-21-099.s1

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Supplementary data