Next Article in Journal
Anticancer Potential of Valencia Peanut (Arachis hypogaea L.) Skin Extract against Cervical Cancer Cells In Vitro and in Nude Mouse Xenograft Models
Previous Article in Journal
Effects of Tea Seed Oil Extracted by Different Refining Temperatures on the Intestinal Microbiota of High-Fat-Diet-Induced Obese Mice
Previous Article in Special Issue
Tracking Trace Elements Found in Coffee and Infusions of Commercially Available Coffee Products Marketed in Poland
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Multi-Elemental Analysis of Edible Insects, Scorpions, and Tarantulas from French (Online) Market and Human Health Risk Assessment Due to Their Consumption: A Pilot Study

1
Department of Chemistry, Queen’s University, 90 Bader Lane, Kingston, ON K7L 3N6, Canada
2
Laboratory for Food Safety, University Paris East Creteil, Anses, F-94700 Maisons-Alfort, France
*
Author to whom correspondence should be addressed.
Foods 2024, 13(15), 2353; https://doi.org/10.3390/foods13152353
Submission received: 19 June 2024 / Revised: 24 July 2024 / Accepted: 24 July 2024 / Published: 26 July 2024
(This article belongs to the Special Issue Trace Elements in Food: Nutritional and Safety Issues)

Abstract

:
Edible insects are becoming increasingly popular as protein alternatives to traditional animal-based products. As such, information on their elemental composition is important to ensure they are safe for human consumption. This article describes the development and validation of a rapid, reliable method for the simultaneous determination of 19 elements (Al, As, B, Ba, Ca, Cd, Co, Cr, Cu, Fe, K, Mg, Mn, Mo, Na, Pb, Se, Sr, and Zn) in edible insects by inductively coupled plasma mass spectrometry (ICP-MS) following closed vessel microwave digestion. The method was validated using three insect certified reference materials, namely black soldier fly larvae meal (BFLY-1), cricket flour (KRIK-1), and mealworm powder (VORM-1). The method was applied to analyze twelve different (whole) insect species. The maximum amount of each sample was calculated for As, Cd, and Pb with respect to their provisional tolerable daily intake values established by the Food and Agricultural Organization/World Health Organization. Most of the samples, except for scorpions and tarantulas, were safe to consume at large doses (1000–10,000 insects per day). Furthermore, most of the samples contained high levels of Fe, K, Na, and Zn, providing a preliminary overview of the nutritional profile of these novel protein alternatives.

1. Introduction

Entomophagy is a term used to describe the practice of eating insects [1]. While common in some countries, Western regions are still overcoming psychological and cultural barriers [2]. Recent efforts have been made to eliminate these barriers and promote the consumption of insects as an alternative protein source, given that the world’s population is estimated to reach approximately 9.7 billion by 2050 and a shortage of current animal-based proteins is expected [3,4,5]. An increasing number of edible insect products are emerging on the market, providing consumers with environmentally friendly and nutritious options, taking into account that insects consume less water and land, emit less greenhouse gases compared to livestock, and they contain proteins, essential vitamins, and minerals [6,7,8,9,10]. However, information on the total elemental composition of these commercially available edible insects is required to ensure their safety for human consumption.
Trace elements in the human body, which are generally present at levels < 250 μg g−1 are classified as essential, nonessential, and potentially toxic, depending on the dose and duration of intake [11,12,13]. Essential trace elements play a vital role in human health and functions. They include Cu and Fe, which participate in energy metabolism via oxidation-reduction reactions, and Fe enables transport of oxygen throughout the body via the formation of hemoglobin [11,13]. Meanwhile, potentially toxic elements (PTEs) include As, Cd, Hg, and Pb, which can lead to cancer and damage to the nervous system and organs when consumed at high doses for long periods of time [11,13,14,15,16]. There is a possibility that insects, such as the black soldier fly larvae (BSFL, Hermetia illucens) that convert organic matter into biomass, are bioaccumulating these PTEs from their feed, posing health risks for humans if ingested [17,18]. To minimize these risks, trace element levels in edible insects must be monitored.
As the emergence of insect-based proteins is relatively new, there is little information on their elemental composition in the current literature. Although techniques such as particle-induced X-ray emission (micro PIXE), instrumental neutron activation analysis (INAA), and wavelength dispersive X-ray fluorescence (WDXRF) spectrometry [19,20,21,22,23,24] have been previously used for the determination of elements in various insect samples, inductively coupled plasma optical emission spectrometry (ICP-OES) and inductively coupled plasma mass spectrometry (ICP-MS) allow for simultaneous multi-elemental analysis [17,18,25,26,27,28,29]. Notably, ICP-MS provides lower detection limits and greater sensitivity, making it the suitable choice for this type of research [30,31].
The aim of this study was to develop and validate a rapid and reliable method for the determination of minor, major, potentially toxic, and essential elements in a selection of commercially available edible insects using ICP-MS. For this purpose, nineteen trace elements were studied: Al, As, B, Ba, Ca, Cd, Co, Cr, Cu, Fe, K, Mg, Mn, Mo, Na, Pb, Se, Sr, and Zn. As the proposed method has not previously been applied to such matrices, it was validated through the analysis of several insect certified reference materials (CRMs) before being applied to the analysis of real-life insect samples.

2. Materials and Methods

2.1. Instrumentation

The samples were digested using a closed microwave system (Mutiwave 7000, Anton Paar, Courtaboeuf, France).
An Agilent 8900 ICP tandem mass spectrometry (ICP-MS/MS) instrument (Agilent Technologies, Courtaboeuf, France) equipped with a MicroMist concentric nebulizer and Scott-type double-pass quartz spray chamber was used for analysis. Sample digests were introduced directly into the instrument via a peristaltic pump from tubes connected to an SPS 4 autosampler (Agilent Technologies, Courtaboeuf, France). The operating conditions are detailed in Table 1. These parameters were optimized daily by performing short-term stability tests with the tuning solution (1 mg L−1) in both detection modes (standard and collision mode) to ensure maximum sensitivity and minimal interference from oxide (CeO+/Ce+ < 1.2%) and doubly charged ions (Ce2+/Ce+ < 2%). The signals were obtained using Scientific MassHunter software (Agilent Technologies) and the raw data were processed using Excel.

2.2. Chemicals and Reagents

Ultrapure water (18.2 MΩ cm, Millipore Milli-Q™, Merck Millipore, Saint Quentin en Yvelines, France) and HNO3 (67% v/v, Suprapur, VWR, Fontenay sous-Bois, France) were used throughout the study. High purity argon (99.996%, Linde Gas, Montereau-Fault-Yonne, France) was used for the plasma, auxiliary, and nebulizer gases.
Stock solutions containing 1000 mg L−1 of each analyte (Al, As, B, Ba, Ca, Cd, Co, Cr, Cu, Fe, K, Mg, Mn, Mo, Na, Pb, Se, Sr, and Zn) were purchased from LGC Standards (Molsheim, France) and were used to prepare calibration standard solutions daily in 6% (v/v) HNO3.
Internal standard solutions were prepared using 1000 mg L−1 standard stock solutions of Y, Re, and Bi that were purchased from LGC Standards. These solutions were added to all samples, calibration standards, and blanks to compensate for drift.
A tuning solution and a Factor P/A solution were prepared separately using multi-element solutions (Agilent Technologies) to ensure optimal instrument sensitivity over a wide range of masses and linear response of the detector between pulse and analog detection modes, respectively.
Solutions of HNO3 at 6% (v/v) and 10% (v/v) were used for rinsing the ICP-MS/MS system between analyses.

2.3. Reference Materials and Samples

Three insect-based CRMs provided by the National Research Council Canada (Ottawa, ON, Canada) were used throughout the study to validate the method, namely: BFLY-1 (black soldier fly larvae meal), KRIK-1 (cricket flour), and VORM-1 (mealworm powder). The mussel tissue ERM-CE278k CRM from the Institute for Reference Materials and Measurements (LGC Standards) was also used throughout the study as an internal quality control sample.
Fourteen dry samples including authorized edible crickets (Acheta domesticus), worms (Tenebrio molitor), ants (Atta laevigata), water bugs (Nepidae), locusts (Locusta migratoria), scorpions (Heterometrus longimanus), and tarantulas (Haplopeima albostriatum) were purchased from the French market and online. To ensure sufficient quantities for analysis, multiple packages of some samples were purchased. Although these packages originated from the same batch, they were each treated as a single sample to distinguish any variations between packages, which led to the analysis of 27 samples (see Table 2 for details). Information on the life stage and origin of the samples is not available.

2.4. Analytical Procedures

2.4.1. Sample Preparation

Each sample was removed from its original packaging and stored at room temperature in a closed polyethylene tube while awaiting preparation for analysis. As most packages contained multiple insects, the total weight (in g) was measured. From this, the weight per insect (in g) was approximated by weighing 20 whole insects.
Each sample was then homogenized using a BM500 benchtop laboratory ball mill (Anton Paar, Courtabœuf, France) and three 10 mm agate beads. The grinding frequency and time varied depending on the type of insect. Those with hard exoskeletons (scorpions, water bugs, and tarantulas) were ground at 30 Hz for 2 min, whereas others were ground at 25 Hz for 45 s.

2.4.2. Multi-Elemental Analysis by ICP-MS/MS

Approximately 0.3 g of homogenous sample was weighed in a quartz digestion vial, to which 3 mL of HNO3 (67%, v/v) and 3 mL of ultrapure water were added. The samples were then completely digested using a closed microwave digestion system for 30 min at 250 °C and a pressure of 140 bar. Once cooled to room temperature, the sample solutions were transferred into 50 mL polyethylene flasks and 100 µL of a mixture of internal standard solution (Y, Re, and Bi) were added before final dilution to 50 mL with ultrapure water and subsequent analysis by ICP-MS.

2.4.3. Data Processing

Concentrations were expressed in mg kg−1. Calibration curves were produced for each analysis series to verify linearity (R2 ≥ 0.995). Humidity was measured in all three insect CRMs to correct the result. A Grubbs test at the 95% confidence level was performed to identify and remove any outliers in the experimentally obtained data.
To determine the method’s accuracy when analyzing the three insect CRMs, the difference between the certified and measured values (Δm) were compared to their combined uncertainties (UΔ) using the Equations (1)–(3) [32,33]:
m = c m c C R M
u = s m 2 + s C R M 2
U = k · u
where cm is average measured concentration, cCRM is certified concentration, sm is standard deviation of the measured value, and sCRM is uncertainty of the certified value. Note, a coverage factor (k) of 2 was used, corresponding to 95% confidence level.

3. Results and Discussion

3.1. Method Validation

To ensure that the proposed method is applicable to insect matrices, three CRMs (BFLY-1, KRIK-1, and VORM-1) were analyzed in triplicates on three different days (n = 9, unless otherwise specified) over a period of seven weeks. The comparison of the average total concentration and standard deviation determined for each of the 19 elements in the three CRMs and the corresponding certified value is provided in Figure 1.
Overall, most of the elements had average percent recoveries ranging from 90 to 110% for all three CRMs, hence confirming the method’s fit for the analysis of insects. Furthermore, upon comparing Δm with UΔ (Table S1), all the elements except for Co, K, and Se in BFLY-1, were found to have Δm values lesser than UΔ, indicating that there were no statistically significant differences between the measured and certified concentrations.

3.2. Analysis of Commercially Available Edible Insects

The levels of 19 elements measured in commercially available edible insects are presented as the following: PTEs, major elements, essential elements, and others (see Table 3, Table 4, Table 5 and Table 6, respectively). It is worth to note that amongst the species analyzed in this study, only four are currently authorized as novel food in the European Union (EU), namely the mealworm (Tenebrio molitor), the lesser mealworm (Alphitobius diaperionus), the locust (Locusta migratoria), and the cricket (Acheta domesticus) [34].
The Food and Agricultural Organization/World Health Organization established provisional tolerable daily intake (PTDI) values for As, Cd, and Pb of 2.10 µg kg−1, 0.82 µg kg−1, and 3.57 µg kg−1 bodyweight per day, respectively, in this type of foodstuffs [35,36]. The maximum amount of whole edible insects that can be safely consumed daily for a 60 kg adult and an 18 kg child was calculated using the approximated weight per insect (in g) and is summarized in Table 3.
Based on the measured concentrations, it appears that most of the samples, notably the crickets, locusts, and worms, can be safely consumed at rather large quantities (from 1000 to 100,000 individuals) by both children and adults. However, the maximum number of scorpions that can be consumed in terms of Cd were significantly lower than the other samples, with 12–32 recommended for adults and 4–10 for children.
Moreover, in the case of tarantula samples, the consumption of only 1 individual per day is recommended for children and 2–3 for adults. However, this finding should not pose too much concern considering the context in which insects are being considered as a protein alternative. For instance, in Europe, insects are marketed as a food ingredient, to be added in crackers, pasta, etc. [34].
With regard to the samples originating from the same lot, similar contamination patterns were observed for the ants, crickets 1–3 and 7–8, and worms 4–6 samples. Contrarily, measured results varied significantly between the following samples (see Table 3, Table 4, Table 5 and Table 7): crickets 5–6, locusts 1–2, scorpions 3–4, tarantulas 1–3, water bug 1–2, and worms 1–3. Larger variances observed in scorpions, tarantulas, and water bugs can be explained by the number of individuals in each lot. In fact, especially for these species, one lot was composed of only one or two individuals.
Table 4 summarizes the levels of major (naturally abundant) elements (Na, K, Ca, and Mg) in each sample. Overall, high levels of K were observed for all the samples (from 4- to 10-fold compared to Ca, Mg, and Na), suggesting that insects are rich in this element. This is beneficial as K plays a role in proper kidney and heart regulation, muscle contraction, and nerve transmission [37].
Table 3. Concentrations ± standard deviation (n = 2; µg kg−1) of potentially toxic elements in edible insects, scorpions, and tarantulas (with corresponding sample name) by ICP-MS as well as the number of individual of each type that can be safely consumed (per day) in relation to provisional tolerable daily intake (PTDI) a for human adults b and children c.
Table 3. Concentrations ± standard deviation (n = 2; µg kg−1) of potentially toxic elements in edible insects, scorpions, and tarantulas (with corresponding sample name) by ICP-MS as well as the number of individual of each type that can be safely consumed (per day) in relation to provisional tolerable daily intake (PTDI) a for human adults b and children c.
SampleAsCdPb
MeasuredMaximum Recommended Consumption
(Number per Day)
MeasuredMaximum Recommended Consumption
(Number per Day)
MeasuredMaximum Recommended Consumption
(Number per Day)
AdultsChildrenAdultsChildrenAdultsChildren
Ants
143.86 ± 0.6640112085.4 ± 1.78024106.8 ± 5.428084
244.13 ± 0.7742912979.60 ± 0.159328104.1 ± 1.230993
Crickets
17.70 ± 0.40145,19643,55936.89 ± 0.3911,834355018.296 ± 0.018103,88231,165
26.97 ± 0.18178,10353,43138.95 ± 0.7212,445373315.18 ± 0.51139,02141,706
36.449 ± 0.084182,93954,88229.35 ± 0.9215,696470916.7 ± 2.9120,09736,029
412.42 ± 0.6541,39912,42013.75 ± 0.1114,602438136.62 ± 0.8123,8707161
53.6 ± 2.7271,38981,41773 ± 105182155553.6 ± 2.430,7299219
62.622 ± 0.086423,019126,90665.90 ± 0.496572197233.4 ± 3.856,45416,936
719.57 ± 0.7313,757412776.07 ± 0.92138241596.9 ± 3.047231417
821.07 ± 0.6712,726381876.6 ± 3.8136741062.0 ± 5.673522206
Locusts
135.0 ± 1.08137244131.78 ± 0.343499105050.194 ± 0.06096452894
247.44 ± 0.124912147440.9 ± 2.3222566773.4 ± 1.953971619
Scorpions
1725 ± 366219539 ± 223210235 ± 1432497
2383.5 ± 2.4200602272 ± 19134123.6 ± 3.11053316
3233.1 ± 3.3226681001 ± 38216162 ± 17554166
4192.20 ± 0.2312738771.406 ± 0.04612464.6 ± 9.7643193
Tarantulas
193.78 ± 0.51651913,200 ± 9721633.3 ± 6.316349
2191.8 ± 4.2326989650 ± 19031464.79 ± 0.8922969
3120.8 ± 1.34761438582 ± 48311064 ± 279228
Water bug
159.31 ± 0.646812043.46 ± 0.154556136760.96 ± 0.981126338
286.4 ± 2.64161256.98 ± 0.142009603104.9 ± 1.4582175
Worms
139.73 ± 0.7675,96222,78982.6 ± 2.114,267428010.8 ± 1.7475,050142,515
2470 ± 15148344553.9 ± 4.25049151587.3 ± 5.213,5714071
321.25 ± 0.6220,567617016.777 ± 0.06110,17230527.425 ± 0.011100,06430,019
425.65 ± 0.79119,52035,85679.25 ± 0.7615,10545327.5 ± 2.5694,891208,467
526.50 ± 0.53138,01841,40583.5 ± 2.917,10451316.03 ± 0.281,031,129309,339
625.66 ± 0.12103,37631,01377.7 ± 2.813,33139996.32 ± 0.39713,524214,057
a PTDI levels for As, Cd, and Pb are 2.10, 0.82, and 3.57 µg kg−1 bw−1 day−1, respectively. b weight of 60 kg. c weight of 18 kg.
Although natural samples (free from additives or other ingredients besides the insect) were purchased for this study, some were found to have salt added to them (see ingredients listed in Table 2). This was reflected by high levels of Na being reported in the scorpion and tarantula samples (up to 10,597 and 40,454 mg kg−1, respectively). Sodium, being an essential nutrient, helps maintain plasma volume, acid-base balance, nerve transmissions, and healthy cell functions [38].
Table 4. Concentrations ± standard deviation (n = 2; mg kg−1) of major elements in edible insects, scorpions, and tarantulas (with corresponding sample name) measured by ICP-MS.
Table 4. Concentrations ± standard deviation (n = 2; mg kg−1) of major elements in edible insects, scorpions, and tarantulas (with corresponding sample name) measured by ICP-MS.
SampleCaKMgNa
Ants
1539 ± 62681 ± 2187 ± 21135 ± 5
2458 ± 87677 ± 5184 ± 31117 ± 22
Crickets
11268 ± 137567 ± 1501215 ± 112577 ± 9
21399 ± 168308 ± 1201316 ± 342835 ± 66
31397 ± 218538 ± 791314 ± 432874 ± 33
41798 ± 125263 ± 61727 ± 11771 ± 12
51053 ± 669116 ± 330746 ± 122424 ± 130
61034 ± 539078 ± 220801 ± 102448 ± 15
7496 ± 27017 ± 26867 ± 131259 ± 12
8411 ± 86559 ± 1777 ± 21162 ± 6
Locusts
1559 ± 246510 ± 150749 ± 34937 ± 57
2481 ± 216350 ± 460658 ± 4860 ± 19
Scorpions
11149 ± 525946 ± 510430 ± 710,597 ± 1009
21792 ± 145101 ± 37542 ± 74152 ± 23
32102 ± 426903 ± 4784 ± 286150 ± 7
41163 ± 44883 ± 53417 ± 44495 ± 28
Tarantulas
15372 ± 141298 ± 101944 ± 4332,232 ± 320
22518 ± 741794 ± 381984 ± 1227,079 ± 620
32748 ± 262220 ± 121765 ± 4040,454 ± 260
Water bug
1632 ± 23950 ± 4695 ± 53150 ± 2
2865 ± 184041 ± 18614 ± 105113 ± 49
Worms
1401 ± 104474 ± 2501894 ± 69521 ± 8
21132 ± 17462 ± 1302565 ± 11126 ± 1
3788 ± 676040 ± 291343 ± 17670 ± 6
4499 ± 18335 ± 3003074 ± 6980 ± 10
5492 ± 68533 ± 4002896 ± 70982 ± 38
6501 ± 158294 ± 502959 ± 3976 ± 10
Table 7 compares the results obtained in previous studies with those obtained in this work for potential toxic and major elements. Many results are comparable despite the samples being from different origins, prepared differently, etc. For example, two out of three samples of cricket in the previous study had up to 10–38% of seasonings, whereas only whole dehydrated crickets were analyzed in this work. Yet, except for As, the levels of Cd, Pb, Ca, Mg, K, and Na are fairly similar. The largest differences were observed for water bugs, which were from India in the previous study.
As can be seen in Table 5, high Cu levels were measured in the scorpion (81–130 mg kg−1) and tarantula samples (80–121 mg kg−1). Copper is involved in energy production, iron metabolism, brain development, and immune system functioning [39]. Most of the samples (crickets, locusts, worms, scorpions, ants, tarantulas, and water bugs) also contained high levels of Fe, ranging from 33 to 474 mg kg−1. This element is necessary for human growth and development, with it circulating oxygen throughout the body [40]. Lastly, high levels of Zn were observed for all the samples (from 100 mg kg−1 to 1000 mg kg−1). This is noteworthy, as zinc is involved in cellular metabolism (catalytic activities of enzymes, protein and DNA synthesis), immune health, and growth and development [41]. Table 8 shows that the levels of several essential elements are consistent with those previously obtained in similar samples. Differences may be attributed to different sample origin, sample preparation, etc. The systematically lower concentrations in water bugs reported previously might be a result of the legs and antennas having been removed prior to analysis, whereas the whole insect was analyzed in this work.
Table 5. Concentrations ± standard deviation (n = 2; mg kg−1) of essential elements in edible insects, scorpions, and tarantulas (with corresponding sample name) by ICP-MS.
Table 5. Concentrations ± standard deviation (n = 2; mg kg−1) of essential elements in edible insects, scorpions, and tarantulas (with corresponding sample name) by ICP-MS.
SampleCoCrCuFeMnMoSeZn
Ants
10.05241 ± 0.000740.12074 ± 0.0008919.463 ± 0.042147 ± 336.39 ± 0.390.5309 ± 0.00121.01 ± 0.00113 ± 2
20.0519 ± 0.00320.114 ± 0.01119.34 ± 0.35146 ± 535.32 ± 0.410.5188 ± 0.00371.001 ± 0.012113 ± 3
Crickets
10.0615 ± 0.00530.0561 ± 0.009621.50 ± 0.6055.80 ± 0.2355.2 ± 1.60.5318 ± 0.00260.616 ± 0.023191 ± 2
20.0611 ± 0.00170.0390 ± 0.008819.54 ± 0.9050.5 ± 2.559.3 ± 1.20.5382 ± 0.00150.631 ± 0.024197 ± 2
30.0557 ± 0.00120.0406 ± 0.004220.891 ± 0.04855.2 ± 2.558.2 ± 1.30.560 ± 0.0150.6384 ± 0.0027202 ± 8
40.03363 ± 0.000920.0915 ± 0.003119.98 ± 0.3350.9 ± 1.863.5 ± 1.30.6071 ± 0.00510.3087 ± 0.0035155 ± 2
50.0108 ± 0.00130.02712 ± 0.0003124.2 ± 1.554.69 ± 0.02930.262 ± 0.0520.723 ± 0.0250.1234 ± 0.0064239 ± 24
60.0102 ± 0.00210.0164 ± 0.002626.0 ± 2.449.3 ± 3.330.1 ± 2.90.755 ± 0.0280.1311 ± 0.0017256 ± 9
70.0835 ± 0.00130.1380 ± 0.008153.09 ± 0.4283.58 ± 0.177.69 ± 0.201.4969 ± 0.00530.19229 ± 0.00045150 ± 37
80.0880 ± 0.00700.122 ± 0.01749.31 ± 0.4068.7 ± 1.44.937 ± 0.0481.531 ± 0.0300.200 ± 0.011135 ± 15
Locusts
10.1218 ± 0.00490.0836 ± 0.007760.300 ± 0.03090.33 ± 0.556.77 ± 0.180.678 ± 0.0180.3341 ± 0.0071177 ± 25
20.1246 ± 0.00470.2066 ± 0.009392.7 ± 7.7164 ± 236.46 ± 0.180.574 ± 0.0210.2160 ± 0.0068173 ± 17
Scorpions
10.683 ± 0.0300.1658 ± 0.002381.8 ± 7.4139 ± 11166 ± 120.206 ± 0.0142.136 ± 0.081381 ± 25
21.0358 ± 0.00580.1609 ± 0.0029130.64 ± 0.60199 ± 4203.0 ± 4.00.3230 ± 0.00402.62 ± 0.14624 ± 10
30.4908 ± 0.00890.2082 ± 0.0068128.0 ± 1.1107 ± 1269.1 ± 2.00.28131 ± 0.000351.512 ± 0.011609 ± 1
40.1637 ± 0.00230.24 ± 0.16102.87 ± 0.4062.07 ± 0.7368.9 ± 2.70.14280 ± 0.000991.083 ± 0.012552 ± 2
Tarantulas
10.4964 ± 0.00210.1479 ± 0.0029112.33 ± 0.28157 ± 1735.9 ± 7.60.07640 ± 0.000251.079 ± 0.0141011 ± 10
20.2461 ± 0.00420.3393 ± 0.0016121.0 ± 2.8218 ± 1351.3 ± 1.10.1178 ± 0.00201.179 ± 0.020821 ± 2
30.5862 ± 0.00490.2992 ± 0.003180.3 ± 1.2224.2 ± 0.4275.6 ± 4.90.1194 ± 0.00762.013 ± 0.028734 ± 8
Water bug
10.10819 ± 0.000330.179 ± 0.03112.69 ± 0.36129 ± 110.03 ± 0.140.15052 ± 0.000420.469 ± 0.010147.2 ± 0.4
20.2217 ± 0.00540.211 ± 0.02511.199 ± 0.080474 ± 34014.674 ± 0.0530.2358 ± 0.00860.5047 ± 0.0076119 ± 1
Worms
10.04598 ± 0.000430.0231 ± 0.004516.6 ± 1.346.6 ± 5.010.72 ± 0.120.960 ± 0.0100.819 ± 0.012106 ± 6
20.001978 ± 0.0000150.0203 ± 0.00199.12 ± 0.1132.85 ± 0.9719.390 ± 0.0550.3557 ± 0.00350.6344 ± 0.0096175 ± 4
30.048699 ± 0.0000320.0504 ± 0.00749.714 ± 0.09651.8 ± 2.417.7 ± 1.60.699 ± 0.0110.2437 ± 0.002273.5 ± 3.0
40.01844 ± 0.000230.0237 ± 0.004319.08 ± 0.2056.7 ± 9.711.762 ± 0.0240.55998 ± 0.000630.10654 ± 0.00047105 ± 1
50.01959 ± 0.000730.0798 ± 0.009620.02 ± 0.7351.3 ± 1.811.187 ± 0.0570.573 ± 0.0140.1073 ± 0.0067107 ± 3
60.0198 ± 0.00240.0223 ± 0.006718.45 ± 0.1249.34 ± 0.4911.10 ± 0.150.5681 ± 0.00890.10155 ± 0.00046101 ± 1
Table 6. Concentrations ± standard deviation (n = 2; mg kg−1) of remaining elements in edible insects, scorpions, and tarantulas (with corresponding sample name) measured by ICP-MS.
Table 6. Concentrations ± standard deviation (n = 2; mg kg−1) of remaining elements in edible insects, scorpions, and tarantulas (with corresponding sample name) measured by ICP-MS.
SampleAlBBaSr
Ants
199.5 ± 2.50.742 ± 0.02417.54 ± 0.374.828 ± 0.091
2105 ± 100.715 ± 0.03114.753 ± 0.0294.24 ± 0.23
Crickets
15.49 ± 0.740.757 ± 0.0730.5008 ± 0.00192.794 ± 0.077
23.06 ± 0.430.5543 ± 0.00560.464 ± 0.0132.75 ± 0.10
34.3 ± 1.70.553 ± 0.0110.489 ± 0.0382.9160 ± 0.0040
420.4 ± 1.20.398 ± 0.0120.786 ± 0.0432.472 ± 0.048
512.3 ± 7.60.690 ± 0.0431.06 ± 0.162.54 ± 0.13
63.79 ± 0.720.314 ± 0.0210.773 ± 0.0672.40 ± 0.33
76.29 ± 0.320.771 ± 0.0181.4569 ± 0.00651.861 ± 0.039
84.07 ± 0.600.714 ± 0.0411.171 ± 0.0481.636 ± 0.043
Locusts
155.3 ± 2.40.387 ± 0.0310.9767 ± 0.00551.895 ± 0.028
2119 ± 150.400 ± 0.0201.298 ± 0.0491.0888 ± 0.0059
Scorpions
1283 ± 170.659 ± 0.0208.23 ± 0.644.80 ± 0.45
264.25 ± 0.540.3993 ± 0.004211.071 ± 0.01810.58 ± 0.11
369.0 ± 2.00.763 ± 0.0347.078 ± 0.06217.99 ± 0.11
4103.7 ± 0.50.429 ± 0.0174.269 ± 0.0285.436 ± 0.055
Tarantulas
1132.8 ± 0.050.898 ± 0.04028.83 ± 0.1731.22 ± 0.14
2169 ± 31.0023 ± 0.003623.78 ± 0.4131.08 ± 0.93
3167 ± 11.068 ± 0.04928.57 ± 0.1221.73 ± 0.21
Water bug
181.1 ± 1.4nd1.0085 ± 0.00631.2820 ± 0.0020
2144 ± 3nd1.492 ± 0.0161.424 ± 0.036
Worms
114.2 ± 2.30.758 ± 0.0122.238 ± 0.0533.71 ± 0.20
21.406 ± 0.029nd0.857 ± 0.0500.901 ± 0.016
314.86 ± 0.961.184 ± 0.0282.22 ± 0.143.222 ± 0.069
40.490 ± 0.0702.28 ± 0.233.974 ± 0.0713.619 ± 0.064
51.5 ± 1.22.128 ± 0.0703.83 ± 0.203.57 ± 0.11
60.4421 ± 0.00202.49 ± 0.364.003 ± 0.0433.5216 ± 0.0024
nd: not detected.
Table 7. Comparison of concentrations previously reported for potentially toxic and major elements with those obtained in this work.
Table 7. Comparison of concentrations previously reported for potentially toxic and major elements with those obtained in this work.
InsectAs
(µg kg−1)
Cd
(µg kg−1)
Pb
(µg kg−1)
Ca
(mg kg−1)
K
(mg kg−1)
Mg
(mg kg−1)
Na
(mg kg−1)
Reference
Cricket
(n = 3)
300–40022–28n.d.-19612–26308100–13,500740–18801130–15,900[27]
Cricket
(n = 8)
3.6–21.113.8–76.616.7–96.9411–17985263–9116727–13161162–2874This work
Locust
(n = 1)
300n.d.1686460604902160[27]
Locust
(n = 2)
35.0–47.431.8–40.950.2–73.4481–5596350–6510658–749860–937This work
Mealworm
(n = 3)
200–62030–200n.d.-100,000941–23807560–10,000870–14501290–1510[27]
Mealworm
(n = 5)
25.7–39.779.3–83.86.0–10.8401–7884474–85331343–3074521–982This work
Silkworm
(n = 1)
200n.d.962210904803650[27]
Silkworm
(n = 1)
47053.947.3113274622565126This work
Water bug
(n = 5)
320.9–561.5220–346336–420197.4–286.2[23]
Water bug
(n = 2)
632–8553950–4041614–6953150–5113This work
Table 8. Comparison of concentrations (mg kg−1) previously reported for essential elements with those obtained in this work.
Table 8. Comparison of concentrations (mg kg−1) previously reported for essential elements with those obtained in this work.
InsectCoCrCuFeMnMoSeZnReference
Cricket
(n = 3)
n.d.-0.0450.174–0.26716.3–23.940.9–80.79.62–45.80.327–17.20.474–0.899125–173[27]
Cricket
(n = 8)
0.0102–0.08800.0164–0.138019.54–53.0949.3–83.67.7–63.50.560–1.5310.123–0.638135–256This work
Locust
(n = 1)
n.d.0.14035.742.44.440.7340.307140[27]
Locust
(n = 2)
0.1218–0.12460.0836–0.206660.3–92.790.3–1646.46–6.770.574–0.6780.216–0.334173–177This work
Mealworm
(n = 3)
0.018–0.0330.164–0.62411.3–28.236.2–2535.36–4100.37–0.8970.474–0.54793.8–126[27]
Mealworm
(n = 5)
0.01844–0.048700.0223–0.07989.71–20.0246.6–56.710.7–17.70.560–0.9600.102–0.81973.5–107This work
Silkworm
(n = 1)
n.d.0.0543.9011.75.710.1180.35738.6[27]
Silkworm
(n = 1)
0.0019780.02039.1232.8519.3900.35570.6344175This work
Water bug
(n = 5)
22.2–420253–112119.8–42.2 49.8–72.2[23]
Water bug
(n = 2)
11.2–12.7129–47410.03–14.67 119–147This work

4. Conclusions

This study addresses the assessment of potentially toxic, major, and essential elements (19 trace elements in total) in a variety of edible insects, scorpions, and tarantulas by ICP-MS. The method accuracy was verified by analyzing several insect certified reference materials. Based on the provisional tolerable daily intake (PTDI) values for As, Cd, and Pb, it was concluded that most of the samples were safe to consume for both children and adults at relatively high amounts (number of individuals ranging from 1000 to 100,000 insects per day). However, the maximum number of scorpions that can be safely consumed is much lower (up to ~30 for adults and up to 10 for children), while in the case of tarantulas, consumption of only 1 individual per day is recommended for children and 2–3 for adults.
Lastly, high levels of Cu were found in the tarantula and scorpion samples as well as K, Na, Fe, and Zn in most of the insect samples, suggesting that edible insects have a nutritional value.
A limitation of this study is that it included no information available on the insects’ developmental stage, environmental exposition, bioaccumulation of pesticides and chemicals, which parts of the insects were used in previous studies, and the origin of the following samples: crickets 5–6, locusts 1–2, and water bug 1–2.
The work will be pursued by increasing the replicate size in order to assess the samples’ heterogeneity and also extending the study to other edible insect species in order to provide a more extensive database regarding the benefit–risk balance related to trace elements via consumption of this type of foodstuffs.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/foods13152353/s1, Table S1: Statistical comparison of measured concentrations in insect CRMs with their certified values.

Author Contributions

Conceptualization: Y.H., A.L., D.B. and P.J.; data curation: Y.H., A.L., D.B. and P.J.; formal analysis: Y.H. and C.M.; funding acquisition: D.B. and P.J.; investigation: Y.H., A.L., D.B. and P.J.; methodology: Y.H., A.L., C.M., D.B. and P.J.; project administration: D.B. and P.J.; resources: D.B. and P.J.; supervision: A.L., D.B. and P.J.; validation: Y.H., C.M. and A.L.; writing—original draft preparation: Y.H.; writing—review and editing: D.B., A.L. and P.J. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by a Mitacs Globalink Research Award (Canada) (funding number FR101710).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Materials; further inquiries can be directed to the corresponding author.

Acknowledgments

The authors gratefully acknowledge the National Research Council Canada for providing the certified reference materials. They appreciate the support from the Metallic Trace Elements and Minerals Unit at ANSES as the research was carried out in their laboratory.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Van Huis, A.; Van Itterbeeck, J.; Klunder, H.; Mertens, E.; Halloran, A.; Muir, G.; Vantomme, P. Edible Insects: Future Prospects for Food and Feed Security; Food and Agriculture Organization of the United Nations: Rome, Italy, 2013. [Google Scholar]
  2. Van Huis, A. Edible insects contributing to food security? Agric. Food Secur. 2015, 4, 20. [Google Scholar] [CrossRef]
  3. Henchion, M.; Hayes, M.; Mullen, A.M.; Fenelon, M.; Tiwari, B. Future protein supply and demand: Strategies and factors influencing a sustainable equilibrium. Foods 2017, 6, 53. [Google Scholar] [CrossRef]
  4. United Nations Department of Economic and Social Affairs. World Population Prospects 2022: Summary of Results; Report No. 3; United Nations: New York, NY, USA, 2022. [Google Scholar]
  5. Wood, P.; Tavan, M. A review of the alternative protein industry. Curr. Opin. Food Sci. 2022, 47, 100869. [Google Scholar] [CrossRef]
  6. Cappellozza, S.; Leonardi, M.G.; Savoldelli, S.; Carminati, D.; Rizzolo, A.; Cortellino, G.; Terova, G.; Moretto, E.; Badaile, A.; Concheri, G.; et al. A first attempt to produce proteins from insects by means of a circular economy. Animals 2019, 9, 278. [Google Scholar] [CrossRef]
  7. Kusch, S.; Fiebelkorn, F. Environmental impact judgments of meat, vegetarian, and insect burgers: Unifying the negative footprint illusion and quantity insensitivity. Food Qual. Prefer. 2019, 78, 103731. [Google Scholar] [CrossRef]
  8. de Koning, W.; Dean, D.; Vriesekoop, F.; Aguiar, L.K.; Anderson, M.; Mongondry, P.; Oppong-Gyamfi, M.; Urbano, B.; Luciano, C.A.G.; Jiang, B.; et al. Drivers and inhibitors in the acceptance of meat alternatives: The case of plant and insect-based proteins. Foods 2020, 9, 1292. [Google Scholar] [CrossRef]
  9. McClements, D.J.; Barrangou, R.; Hill, C.; Kokini, J.L.; Lila, M.A.; Meyer, A.S.; Yu, L. Building a resilient, sustainable, and healthier food supply through innovation and technology. Annu. Rev. Food Sci. Technol. 2021, 12, 1–28. [Google Scholar] [CrossRef] [PubMed]
  10. Hadi, J.; Brightwell, G. Safety of alternative proteins: Technological, environmental and regulatory aspects of cultured meat, plant-based meat, insect protein and single-cell protein. Foods 2021, 10, 1226. [Google Scholar] [CrossRef]
  11. National Research Council (US) Committee on Diet and Health. Diet and Health; National Academies Press: Washington, DC, USA, 1989. [Google Scholar]
  12. World Health Organization. Trace Elements in Human Nutrition and Health; World Health Organization: Geneva, Switzerland, 1996. [Google Scholar]
  13. Mehri, A. Trace elements in human nutrition (ii)—An update. Int. J. Prev. Med. 2020, 11, 2. [Google Scholar] [CrossRef]
  14. Türkdoğan, M.K.; Kilicel, F.; Kara, K.; Tuncer, I.; Uygan, I. Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ. Toxicol. Pharmacol. 2003, 13, 17–179. [Google Scholar] [CrossRef]
  15. Islam, M.S.; Islam, A.R.M.T.; Phoungthong, K.; Ustaoğlu, F.; Tokatli, C.; Ahmed, R.; Ibrahim, K.A.; Idris, A.M. Potentially toxic elements in vegetable and rice species in Bangladesh and their exposure assessment. J. Food Compos. Anal. 2022, 106, 104350. [Google Scholar] [CrossRef]
  16. Islam, M.S.; Ahmed, M.K.; Idris, A.M.; Phoungthong, K.; Habib, M.A.; Mustafa, R.A. Geochemical speciation and bioaccumulation of trace elements in different tissues of pumpkin in the abandoned soils: Health hazard perspective in a developing country. Toxin Rev. 2022, 41, 1124–1138. [Google Scholar] [CrossRef]
  17. Proc, K.; Bulak, P.; Wiącek, D.; Bieganowski, A. Hermetia illucens exhibits bioaccumulative potential for 15 different elements—Implications for feed and food production. Sci. Total Environ. 2020, 723, 138125. [Google Scholar] [CrossRef] [PubMed]
  18. Bessa, L.W.; Pieterse, E.; Marais, J.; Dhanani, K.; Hoffman, L.C. Food safety of consuming black soldier fly (Hermetia illucens) larvae: Microbial, heavy metal and cross-reactive allergen risks. Foods 2021, 10, 101934. [Google Scholar] [CrossRef]
  19. Migula, P.; Przybyłowicz, W.J.; Mesjasz-Przybyłowicz, J.; Augustyniak, M.; Nakonieczny, M.; Głowacka, E.; Tarnawska, M. Micro-PIXE Studies of Elemental Distribution in Sap-Feeding Insects Associated with Ni Hyperaccumulator, Berkheya coddii. Plant Soil 2007, 293, 197–207. [Google Scholar] [CrossRef]
  20. Orłowski, G.; Mróz, L.; Kadej, M.; Smolis, A.; Tarnawski, D.; Karg, J.; Campanaro, A.; Bardiani, M.; Harvey, D.J.; Méndez, M.; et al. Breaking down Insect Stoichiometry into Chitin-Based and Internal Elemental Traits: Patterns and Correlates of Continent-Wide Intraspecific Variation in the Largest European Saproxylic Beetle. Environ. Pollut. 2020, 262, 114064. [Google Scholar] [CrossRef]
  21. Momoshima, N.; Sugihara, S.; Hibino, K.; Nakamura, Y. Elemental Concentrations of Aquatic Insect Larvae and Attached Algae on Stone Surfaces in an Uncontaminated Stream. J. Radioanal. Nucl. Chem. 2009, 280, 107–111. [Google Scholar] [CrossRef]
  22. Köksal Erman, Ö. Elemental Composition in Two Water Beetles (Dytiscus thianschanicus, Dytiscus persicus) (Dytiscidae: Coleoptera) as Revealed by WDXRF Spectroscopy. Biol. Trace Elem. Res. 2011, 143, 1541–1563. [Google Scholar] [CrossRef] [PubMed]
  23. Sarmah, M.; Bhattacharyya, B.; Bhagawati, S.; Sarmah, K. Nutritional Composition of Some Commonly Available Aquatic Edible Insects of Assam, India. Insects 2022, 13, 976. [Google Scholar] [CrossRef]
  24. Momoshima, N.; Toyoshima, T.; Matsushita, R.; Fukuda, A.; Hibino, K. Metal Concentrations in Japanese Medaka, Mosquitofish and Insect Larvae Living in Uncontaminated Rivers in Kumamoto, Japan. J. Radioanal. Nucl. Chem. 2007, 272, 495–499. [Google Scholar] [CrossRef]
  25. Bessa, L.W.; Pieterse, E.; Marais, J.; Hoffman, L.C. Why for feed and not for human consumption? The black soldier fly larvae. Compr. Rev. Food Sci. Food. Saf. 2020, 19, 2747–2763. [Google Scholar] [CrossRef] [PubMed]
  26. Braun, M.; Simon, E.; Fábián, I.; Tóthmérész, B. The Effects of Ethylene Glycol and Ethanol on the Body Mass and Elemental Composition of Insects Collected with Pitfall Traps. Chemosphere 2009, 77, 1447–1452. [Google Scholar] [CrossRef] [PubMed]
  27. Sikora, D.; Proch, J.; Niedzielski, P.; Rzymski, P. Elemental Content of the Commercial Insect-Based Products Available in the European Union. J. Food Compos. Anal. 2023, 121, 105367. [Google Scholar] [CrossRef]
  28. Chen, Y.A.; Forschler, B.T. Elemental Concentrations in the Frass of Saproxylic Insects Suggest a Role in Micronutrient Cycling. Ecosphere 2016, 7, e01300. [Google Scholar] [CrossRef]
  29. Simon, E.; Baranyai, E.; Braun, M.; Fábián, I.; Tóthmérész, B. Elemental Concentration in Mealworm Beetle (Tenebrio molitor L.) during Metamorphosis. Biol. Trace Elem. Res. 2013, 154, 81–87. [Google Scholar] [CrossRef]
  30. Kohlmeyer, U.; Jantzen, E.; Kuballa, J.; Jakubik, S. Benefits of high resolution IC-ICP-MS for the routine analysis of inorganic and organic arsenic species in food products of marine and terrestrial origin. Anal. Bioanal. Chem. 2003, 377, 6–13. [Google Scholar] [CrossRef]
  31. Beauchemin, D. Sample Introduction Systems in ICPMS and ICPOES; Elsevier: Amsterdam, The Netherlands, 2020. [Google Scholar]
  32. Linsinger, T. Comparison of a Measurement Result with the Certified Value; Application Note 1; European Reference Materials: Geel, Belgium, 2010. [Google Scholar]
  33. Sánchez, R.; Todolí, J.L. Assessment of total sample consumption infrared-heated system for minimization of matrix effects in ICP-tandem mass spectrometry. Spectrochim. Acta Part B At. Spectrosc. 2023, 208, 106779. [Google Scholar] [CrossRef]
  34. Approval of Fourth Insect as a Novel Food. Available online: https://food.ec.europa.eu/safety/novel-food/authorisations/approval-insect-novel-food_en (accessed on 24 June 2023).
  35. Joint FAO/WHO Expert Committee on Food Additives. Evaluation of Certain Food Additives and Contaminants; World Health Organization: Geneva, Switzerland, 1989. [Google Scholar]
  36. Joint FAO/WHO Expert Committee on Food Additives. Evaluation of Certain Food Additives and Contaminants; World Health Organization: Geneva, Switzerland, 2014. [Google Scholar]
  37. Potassium. Available online: https://ods.od.nih.gov/factsheets/Potassium-HealthProfessional/#h13 (accessed on 9 December 2023).
  38. Sodium Reduction. Available online: https://www.who.int/news-room/fact-sheets/detail/salt-reduction (accessed on 10 December 2023).
  39. Copper. Available online: https://ods.od.nih.gov/factsheets/Copper-HealthProfessional/ (accessed on 10 December 2023).
  40. Iron. Available online: https://ods.od.nih.gov/factsheets/Iron-HealthProfessional/ (accessed on 10 December 2023).
  41. Zinc. Available online: https://ods.od.nih.gov/factsheets/Zinc-HealthProfessional/ (accessed on 10 December 2023).
Figure 1. Average recovery factors (%) and the relative standard deviation (n = 8, patterned bars or n = 9) obtained for the analysis of BFLY-1, KRIK-1, and VORM-1 CRMs by ICP-MS.
Figure 1. Average recovery factors (%) and the relative standard deviation (n = 8, patterned bars or n = 9) obtained for the analysis of BFLY-1, KRIK-1, and VORM-1 CRMs by ICP-MS.
Foods 13 02353 g001
Table 1. Operating conditions of the ICP-MS/MS instrument (Agilent 8900).
Table 1. Operating conditions of the ICP-MS/MS instrument (Agilent 8900).
ParameterSetting
RF power1550 W
Plasma gas flow rate (Ar)15.0 L min−1
Auxiliary gas flow rate (Ar)0.9 L min−1
Nebulizer gas flow rate (Ar)~1.0 L min−1
Collision gas flow rate (He)~5.0 mL min−1
Sampling/skimmer conesNickel
Monitored isotopesNo gas mode: 11B, 75As, 111Cd, 137Ba, 208Pb
Collision mode (He): 23Na, 24Mg, 27Al, 39K, 44Ca, 52Cr, 55Mn, 56Fe, 59Co, 63Cu, 66Zn, 77Se, 88Sr, 95Mo
Internal standards: 89Y, 185Re, 209Bi
Table 2. List of edible insects, scorpions, and tarantulas samples used in the study with corresponding code number, sample name, ingredients, and origin (if available).
Table 2. List of edible insects, scorpions, and tarantulas samples used in the study with corresponding code number, sample name, ingredients, and origin (if available).
Sample NameInsectSpeciesInformationOrigin
Ants 1Columbia antsAtta laevigataWith saltColumbia
Ants 2Columbia antsAtta laevigataWith saltColumbia
Crickets 1CricketsAcheta domesticusWhole dehydrated
crickets
Toulouse, France
Crickets 2CricketsAcheta domesticusWhole dehydrated
crickets
Toulouse, France
Crickets 3CricketsAcheta domesticusWhole dehydrated
crickets
Toulouse, France
Crickets 4CricketsGryllus bimaculatus-Thailand
Crickets 5CricketsN/AWhole dehydrated
crickets
N/A
Crickets 6CricketsN/AWhole dehydrated
crickets
N/A
Crickets 7CricketsN/AWhole dehydrated
crickets
Netherlands
Crickets 8CricketsN/AWhole dehydrated
crickets
Netherlands
Locusts 1LocustsLocusta migratoriaWith saltN/A
Locusts 2LocustsLocusta migratoriaWith saltN/A
Scorpions 1Black scorpionsHeterometrus longimanusWith saltThailand
Scorpions 2Black Asian forest
scorpions
Heterometrus longimanusWith saltThailand
Scorpions 3Black Asian forest
scorpions
Heterometrus longimanusWith saltThailand
Scorpions 4Black Asian forest
scorpions
Heterometrus longimanusWith saltThailand
Tarantulas 1TarantulaHaplopeima albostriatum-Thailand
Tarantulas 2TarantulaHaplopeima albostriatum-Thailand
Tarantulas 3TarantulaHaplopeima albostriatum-Thailand
Water bug 1Giant water bugNepidaeWith oil and saltN/A
Water bug 2Giant water bugNepidaeWith oil and saltN/A
Worms 1MealwormsTenebrio molitor-EU
Worms 2Silk wormsBombyx mori-Thailand
Worms 3Morio wormsZophobas moriosWith saltThailand
Worms 4MealwormsTenebrio molitorWhole dehydrated
mealworm
Toulouse, France
Worms 5MealwormsTenebrio molitorWhole dehydrated
mealworm
Toulouse, France
Worms 6MealwormsTenebrio molitorWhole dehydrated
mealworm
Toulouse, France
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Holowaty, Y.; Leufroy, A.; Mazurais, C.; Beauchemin, D.; Jitaru, P. Multi-Elemental Analysis of Edible Insects, Scorpions, and Tarantulas from French (Online) Market and Human Health Risk Assessment Due to Their Consumption: A Pilot Study. Foods 2024, 13, 2353. https://doi.org/10.3390/foods13152353

AMA Style

Holowaty Y, Leufroy A, Mazurais C, Beauchemin D, Jitaru P. Multi-Elemental Analysis of Edible Insects, Scorpions, and Tarantulas from French (Online) Market and Human Health Risk Assessment Due to Their Consumption: A Pilot Study. Foods. 2024; 13(15):2353. https://doi.org/10.3390/foods13152353

Chicago/Turabian Style

Holowaty, Yulianna, Axelle Leufroy, Clément Mazurais, Diane Beauchemin, and Petru Jitaru. 2024. "Multi-Elemental Analysis of Edible Insects, Scorpions, and Tarantulas from French (Online) Market and Human Health Risk Assessment Due to Their Consumption: A Pilot Study" Foods 13, no. 15: 2353. https://doi.org/10.3390/foods13152353

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Article metric data becomes available approximately 24 hours after publication online.
Back to TopTop