Food Control 138 (2022) 109030

Contents lists available at ScienceDirect

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

Implementation of the HACCP system for production of Tenebrio molitor

larvae meal
Helbert Antonio Arévalo Arévalo a, Edna Magaly Menjura Rojas a,
Karol Bibiana Barragán Fonseca a, b, c, Sandra Milena Vásquez Mejía c, *
a
Centro de Investigación de Artrópodos Terrestres - CINAT. Universidad Nacional de Colombia, Sede Bogotá. Facultad de Medicina Veterinaria y de Zootecnia, Postal
code, 11001, Bogotá D.C, Colombia
b
Spin-Off Company, Insect Farming Technologies – EntoPro SAS, Calle 30 # 32A-75, Bogotá D.C, Colombia
c
Universidad Nacional de Colombia. Sede Bogotá. Facultad de Medicina Veterinaria y de Zootecnia. Departamento de Producción Animal, Bogotá D.C, Carrera 30 #45-
03 Edificio 561A, Postal code, 111321, Colombia

A R T I C L E I N F O A B S T R A C T

Keywords: Background: The hazard analysis and critical control point (HACCP) system allows for guaranteeing provision of
Mealworm safe food to consumers.
Edible insects Scope and approach: This article is intended to explain the principal aspects of implementing the HACCP system in
Insect processing
production of Tenebrio molitor meal, which may be used as food for humans and animals.
Physical hazard
Biological hazard
Key findings: Several microorganisms which are biological hazards were found to be associated with this meal,
Chemical hazard and a variety of allergens as well as chemical and physical hazards were identified during production of the
larvae. These hazards are a risk principally when the processor receives the Tenebrio larvae. Hazards identified
may be avoided by implementing preventive measures, and eliminated or reduced during processing through a
variety of strategies presented in this document. Specifically, during grinding of the larvae, physical hazards may
occur due to pieces of metal from the mill, as well as biological hazards due to exposition of the larvae’s in­
testines, which in turn exposes other microorganisms that may survive grinding. Several Critical Control Points
(CCPs) were identified during the various stages of processing Tenebrio molitor larvae, and parameters of control
and their critical limits were established. Monitoring systems for maintaining CCPs within acceptable limits were
determined and corrective actions proposed in case a CCP is surpassed.
Conclusions: We conclude that those hazards associated with production of Tenebrio molitor meal may be
controlled through effective implementation of the HACCP system.

1. Introduction significantly (Global Market Insights Inc, 2019). The principal challenge
of the edible insect industry is to consistently produce large volumes of
Over the past decade, mass production of insects has significantly high-quality biomass at competitive prices. Technology may signifi­
increased, particularly in North America, Europe, and Africa, as several cantly improve insect production systems and the quality of the product
insects have been demonstrated to be an excellent human and animal while lowering costs of production, including feeding, watering,
food (Dicke, 2017; Varunjikar et al., 2022). Given their nutritional handling, harvest, hygiene, processing, packaging, and storage (Cortes
profile - rich in high-quality protein and fats, essential amino acids, vi­ et al., 2016).
tamins, and minerals (Baiano, 2020; Secci et al., 2021), they are a viable The nutritional value and safety of edible insects depend on the
food for confronting malnutrition in the global south. Furthermore, in­ species and the conditions in which they are raised and processed.
sect production has a low environmental impact (Grau et al., 2017). In Currently, information is lacking regarding their production using
2019, the global market for edible insects surpassed 112 million dollars, different substrates or diets, as well as possible physical, biological, and
and this sector of the agricultural market is predicted to grow chemical hazards related to consuming these species when used live as

* Corresponding author. Universidad Nacional de Colombia. Sede Bogotá. Facultad de Medicina Veterinaria y de Zootecnia. Departamento de Producción Animal,
Postal code, 111321, Bogotá D.C, Colombia.
E-mail address: [email protected] (S.M. Vásquez Mejía).

https://doi.org/10.1016/j.foodcont.2022.109030
Received 16 February 2022; Received in revised form 3 April 2022; Accepted 9 April 2022
Available online 13 April 2022
0956-7135/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

animal feed or processed into meal. In general, human and animal foods molitor meal.
should be processed to avoid potential hazards resulting from raw ma­
terials during primary production (including breeding, fattening, culti­
vation, harvesting), thereby assuring its safety. The Hazard Analysis and 2.2. Review of HACCP system pre-requisites
Critical Control Points System (HACCP) allows for identifying,
analyzing, and controlling physical, chemical, and biological hazards The HACCP team began with the assumption that any company
during food processing. Governments demand HACCP implementation producing food for human consumption has a sanitary plan that com­
in most food industries (Wallace & Mortimore, 2016; EFSA European plies with food safety standards and good manufacturing practices
Food Safety Authority, 2017), although according to the International (GMP) (EFSA European Food Safety Authority, 2021; IPIFF.Interna­
Platform of Insects for Food and Feed (IPIFF), some industries are just tional Platform of Insects for Food and Feed, 2019). Considering stan­
beginning to apply this system to companies that process and market dards that should be met in processing insect meal as an ingredient for
insects (IPIFF.International Platform of Insects for Food and Feed, the food industry, a diagram was made to represent the pre-requisites
2019). According to EFSA European Food Safety Authority (2017), it is programs (PRPs) of the HACCP system, such as cleaning and disinfec­
still necessary guidance on how to select, implement and validate the tion, pest control, solid waste, potable water, preventive maintenance,
most efficient approaches to control the hazards identified in small supplier control, and traceability.
companies.
Development of legislation and regulations addressing hygiene dur­
ing production and marketing will contribute to the future success of the 2.3. Description of the final product in a datasheet and use of Tenebrio
insect production sector (Hubert, 2019). In 2015, the European Union molitor meal
passed EU Regulation 2015/2283 acknowledging and regulating insects
as food for human consumption. Furthermore, the European Food Se­ Although insect meal may be used in a variety of food products, for
curity Authority (EFSA) – which considers insects to be a “novel food,” this study Tenebrio molitor meal was considered to be the final product
whether dried whole or ground into meal - has recommended a review of which should comply with safety standards before being used by any
regulations and of authorization of use of insect protein in farm animal food industry in order to avoid health risks to consumers. Following the
feed (EFSA European Food Safety Authority, 2015; 2021). In Latin recommendations of the Codex Alimentarius Commission (1997), Wal­
America, raising, processing, and marketing invertebrates (particularly lace and Mortimore (2016), EFSA European Food Safety Authority,
insects) for human and animal consumption is still incipient. Existing 2017, and IPIFF.International Platform of Insects for Food and Feed
regulations are based on the international Codex Alimentarius guide­ (2019), a datasheet was developed with information on potential uses of
lines, which does not yet consider insects to be food for human con­ the product, possible allergies, instructions for use to be included on the
sumption (Bugsolutely, 2020). While interest in insect production and label, and preparation prior to use.
marketing is increasing, various technological, environmental, political,
economic, and cultural factors may limit its development (De Brauw
2.4. Development of a flow chart
et al., 2019).
Several species of invertebrates may be produced on organic waste,
A flow chart for production of Tenebrio molitor meal was designed,
resulting in high-quality proteins. These include the mealworm (Tene­
including each stage of the production process. The flow chart specified
brio molitor, Tenebrionidae) (Liu et al., 2020). According to Rumbos
the sequence of the stages of production, addressing input of raw ma­
et al. (2020), Tenebrio molitor contains a large quantity of raw protein
terials, variables to be controlled during each stage, flows of products,
(58–66% dry matter), and its nutrients are easily digestible. Given that
and outputs considering recommendations by IPIFF.International Plat­
Tenebrio molitor meal has a high nutritional value and a prolonged shelf
form of Insects for Food and Feed (2019) and the Codex Alimentarius
life, it has potential in the food industry as an ingredient in a variety of
(1997).
products. Additionally, its mild flavor, texture, aroma, and color as
compared to whole insects improves its acceptability (Kooh et al., 2020).
In order to be used in the food industry, Tenebrio molitor meal must be 2.5. Analysis of potential hazards and preventive measures
processed according to food safety standards. The objective of the pre­
sent study is to present a guide for implementing the HACCP system by Based on the experience of the HACCP team and an exhaustive re­
companies producing insect meal for human and animal consumption. view of recent literature, physical, chemical, and biological hazards
This study was carried out specifically for the production of Tenebrio associated with production of Tenebrio molitor meal were identified.
molitor meal. Although production process of Tenebrio molitor can be Later, a hazard analysis was carried out using a consequence/probability
divided into three main parts, i.e. farming, harvest and post-harvest matrix consisting of 5 scales of assessment. The HACCP team assessed
processing (EFSA European Food Safety Authority, 2021), this work potential hazards by multiplying the probability of the hazard (risk) by a
focuses on post-harvest processing. value assigned to the potential severity of its consequences on consumer
health. Following this, the HACCP team discussed preventive measures –
2. Methodology or “good practices” - for minimizing the likelihood of each possible
hazard in Tenebrio molitor meal production, establishing hazard control
2.1. Creation of the HACCP team and compilation of information strategies according to recommendations by the Codex Alimentarius
regarding the HACCP plan (1997), Wallace and Mortimore (2016), and EFSA European Food Safety
Authority (2017).
The HACCP team constituents the authors of this document
comprising a multi-disciplinary of professionals from Colombia in
diverse areas of animal production, with experience in production of 2.6. Identification of CCPs
Tenebrio molitor, veterinary medicine, food science and technology, and
quality control according to the recommendations of the Codex Ali­ After the hazard analysis, the high and medium risk hazards and the
mentarius Commission (1997), Wallace and Mortimore (2016), and CCPs were identified according to the decision tree methodology, as
IPIFF.International Platform of Insects for Food and Feed (2019). An recommended by the Codex Alimentarius (1997), Wallace and Morti­
exhaustive literature review was carried out to identify physical, more (2016), IPIFF.International Platform of Insects for Food and Feed
chemical, and biological hazards associated with production of Tenebrio (2019), and EFSA European Food Safety Authority (2017).

2
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

2.7. Establishing critical limits, a monitoring system, and corrective 3.2. Description of the final product (datasheet) and expected use
actions
Table 1 presents the datasheet elaborated for Tenebrio molitor meal.
Critical limits, a monitoring system, and corrective actions were The powder obtained by grinding a plant or animal product is termed
established according to that recommended by the Codex Alimentarius “meal” and several studies have used this meal as an ingredient in ani­
(1997), IPIFF.International Platform of Insects for Food and Feed mal feed (Dalmoro et al., 2021; Secci et al., 2021). While Tenebrio molitor
(2019), and Wallace and Mortimore (2016). has been recognized as a “novel food” by The European Food Safety
Authority (EFSA European Food Safety Authority, 2021), this species - as
2.8. Establishing a verification system for the HACCP plan with other invertebrates consumed by humans - has not yet been
addressed in the standards of the Codex Alimentarius; those mentioned
A verification system of the HACCP plan was established to ensure in the existing code to date are only addressed as parasites of some foods.
that hazards are maintained under control and the proposed HACCP However, the utilization of edible insects as human food has received
plan is strictly followed. increasing attention in recent years and they have been recommended as
a sustainable alternative to the traditional livestock (Liu et al., 2020).
2.9. Documentation necessary for endorse the HACPP plan
3.3. Elaboration of the flow chart
Finally, we made a list of the documents and minimum records that
should be kept in concordance with the HACCP plan to allow for The flow chart (see Fig. 2) describes the following principal stages of
adequate audits. production of Tenebrio molitor meal. Before processing, larvae are sub­
mitted to a 24 h fast to clean their gastrointestinal tract (Fraqueza &
3. Results and discussion Patarata, 2017, pp. 89–113). They are then sifted to separate them from
exuvias, feces, and foreign particles (Purschke et al.,0.2018). Following
3.1. Pre-requisites of the HACCP system this, larvae are washed with potable water to remove impurities; sacri­
ficed by freezing at − 18 ◦ C for 24 h (Fraqueza & Patarata, 2017, pp.
Fig. 1 summarizes the principal pre-requisites for implementing the 89–113); and unfrozen at room temperature for 1 h (Purschke et al.,
HACCP system for foods. Good manufacturing practices (GMP) are the 2018). Next, the larvae are scalded at 60 ◦ C for 5 min (Mancini et al.,
basic general principles of hygiene to adequately comply with sanitary 2020) to reduce microbiological contamination and deactivate enzymes
conditions, such that inherent hazards to production are reduced (EFSA responsible for browning (Purschke et al., 2018). After scalding, the
European Food Safety Authority, 2017). For this study, the HACCP team larvae are oven-dried at 60 ◦ C for 24 h (Purschke et al., 2018). Grinding
assumed that any processor of Tenebrio molitor meal must complies with and sifting the dehydrated larvae follows indications by Purschke et al.
over 80% of the pre-requisites (sanitary facilities, GMP, and (2018), for a granule size of 355–500 μm. Upon grinding, the intestine of
pre-requisite programs) and then, may proceed to evaluate the hazards the larvae liberates its microbial content, which contaminates the meal
and classify them. (Klunder et al., 2012). Therefore, thermal treatment is applied to reduce

Fig. 1. Flow chart of GMP as pre-requisites of the HACCP systemSource

Original diagram by the authors, based on (Colombia, 2013; EFSA European Food Safety Authority, 2017; 2021; Fraqueza & Patarata, 2017; IPIFF.International
Platform of Insects for Food and Feed, 2019).
* Basic sanitation programs and complementary programs.

3
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

Table 1 Table 1 (continued )

Datasheet for Tenebrio molitor meal. Insects for Food and Feed (2019)
Product Identification recommends labeling it as possibly
Product name and description Tenebrio molitor meal is a balanced source of containing gluten as the insects are grain-fed.
natural proteins, fats, and fibers obtained by Label instructions The product label should warn of possible
processing the beetle’s larvae, which are fed allergies to Tenebrio molitor meal (Mancino
with wheat bran, fruits, and vegetables in a et al., 2021; Colombia. Instituto de
controlled environment (Morales- Ramos Vigilancia de Medicamentos y Alimentos
et al., 2020; Rumbos et al., 2020). The meal INVIMA, 2020).
is obtained by drying and grinding. Declaration of nutrients should comply with
Raw material and origin Larvae to be processed are eleven weeks old ( that established by Resolución 810/2021 (
EFSA European Food Safety Authority, Colombia, 2021).
2021), with an average length of 2 cm, raised Preparation prior to consumption The meal may be used as an ingredient in
on farms that exclusively produce insects and food products for human consumption. No
later in laboratories under controlled prior treatment or cooking is necessary for
conditions. consumption (Camara et al., 2018).
Ingredients and additives No additives or additional ingredients are Special considerations Primary production of Tenebrio molitor larvae
used in the meal. should be carried out on insect farms
Expected proximate composition of Moisture: 7.5 g; Protein: 44.6 g; Cholesterol: established exclusively for this species,
100 g of Tenebrio molitor meal 0.002 mg, Fiber: 3.0 g, avoiding contamination by other insects (
Fat: 39.4 g (saturated: 8.6 g), Carbohydrates: EFSA European Food Safety Authority, 2021;
< 0.10 g, Total sugar: < 0.10 g, Amino acids: IPIFF.International Platform of Insects for
5.4 g, Sodium: 142 mg, Calories: 539 kcal Food and Feed, 2019; Colombia. Instituto de
(2242 Kj) (Mota de Carvalho et al., 2019). Vigilancia de Medicamentos y Alimentos
Chemical composition may vary according to INVIMA, 2020).
feeding, stage of development, and habitat (
Source: Original table by the authors, based on sources cited in the datasheet.
Akhtar & Isman, 2018).
Physicochemical characteristics Water holding capacity (WHC): 1.29 ± 0.19
(g/g); Oil holding capacity (OHC): 1.71 ± microbiological hazards. The larvae meal is packaged in multi-layer
0.13 (g/g); Foaming capacity: 31.0 ± 1.41%. opaque plastic bags and hermetically sealed (Kooh et al., 2020). Qual­
Stability of foam: 26.0 ± 0.94%. Emulsion
capacity: 65.96 ± 1.5%. Stability of
ity control of the finished product is carried out before marketing.
emulsion: 27.59 ± 1.18% (Zielińska et al.
2018).
PH: 6.5 to 7.0.
3.4. Analysis of potential hazards and preventive measures
Humidity content <6%
Granulometry: 355–500 μm (Purschke et a., Hazards associated with each stage of Tenebrio molitor meal pro­
2018) duction are presented according to recent literature in Table 2.
Food security: microbiological The meal should have <100 ufc/g of Listeria
Biological hazards associated with insect production are principally
characteristics monocytogenes during the product’s shelf life;
absence of Salmonella and Cronobacter spp. in a result of inadequate feeding and the production environment, and may
25 g and 10 g, respectively; absence of be controlled through biosecurity and proper management practices.
staphylococcal enterotoxins in 25 g; < 10 ufc/ According to IPIFF, hazards identified for insect-based products may be
g of enterobacteria; and <400 mg/kg controlled through PRPs and HACCP procedures during processing
histamine (Cámara et al., 2018; IPIFF.
International Platform of Insects for Food
(IPIFF.International Platform of Insects for Food and Feed, 2019).
and Feed, 2019). According to Selaledi and Mabelebele (2021), although insects are
Packaging The meal should be packaged in multi-layer associated with high microbial growth that might result from unhy­
opaque plastic bags, hermetically sealed to gienic processing methods, bacterial contamination of insects may be
avoid rehydration, labeled, and stored at
controlled. In this sense, Klunder et al., (2012) addressed the topic of
room temperature (Kooh et al., 2020).
Useful life Shelf life of the meal is six months from date edible insects from a food security perspective through an exploratory
of fabrication, based on insect meal available study with reared mealworms (Tenebrio molitor) and crickets (Acheta
on the market (Kooh et al., 2020) and domesticus) as well as Brachytrupes spp. harvested from nature. The in­
estimations for other insect meals (Kamau sects were analyzed under the following conditions: fresh, boiled (10
et al., 2018).
Conservation Conserve in a cool dry place, isolated from
min), roasted (10 min), and stir-fried (5 min). In this study, high counts
soil, with a relative humidity <80% ( of total viable bacteria such as Enterobacteriaceae and bacteria that
Fraqueza & Patarata, 2017, pp. 89–113; form spores on or inside fresh insects were isolated. The authors found
Kooh et al., 2020). that processing the insects - whether by freezing or drying - eliminates a
Use of Tenebrio molitor meal
large part of their bacterial contamination. Prions, viruses, parasites,
Use by consumers It may be used in cookies, bread, empanadas,
arepas, pasta, desserts, sausages, and fungus, and yeasts have not been reported to be significant hazards
hamburgers; in smoothies as no further associated with insect production (Errico et al., 2022; Kooh et al., 2020),
processing or cooking is required and as an nor with production of Tenebrio molitor meal. However, given that
ingredient in high-protein diets; Cámara mealworm larvae are fed with grain and the meal is stored in ware­
et al., 2018).
Target population Food processing companies and the public in
houses, risks such as gluten and mycotoxins should be considered.
general Additionally, Table 2 lists the probabilities and consequences of the
Allergies/food sensitivities People with known allergies to invertebrates hazards, and controls or preventive measures that should be imple­
(seafood, powder mites, crustaceans) should mented in the processing plant to reduce the risk of their occurrence.
not consume Tenebrio molitor meal due to its
Various microbiological, physical, and chemical hazards were found to
chitin content (Cámara et al., 2018; EFSA
European Food Safety Authority, 2021). be associated with raising Tenebrio molitor larva, before reaching the
Gluten allergies: Mancini et al. (2020) processing plant. These hazards may be reduced during processing of the
reported gluten contents less than 20 ppm, meal. Of the biological hazards mentioned in Table 2, the bacteria of the
considering the meal to be gluten-free. Enterobacteriaceae family are the most significant. Salmonella and Lis­
However, IPIFF.International Platform of
teria monocytogenes are present in the gastrointestinal tract of the larvae
and - along with Staphylococcus aureus - are associated with poor

4
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

handling (Errico et al., 2022; Klunder et al., 2012; Stoops et al., 2016).
Even though the microbial counts could be within health and food,
standard specifications, their occurrence is still worrying (Errico et al.,
2022; Selaledi & Mabelebele, 2021). These biological hazards may be
prevented mainly by implementing GMP and thermal treatment during
production of the meal (IPIFF.International Platform of Insects for Food
and Feed, 2019; Errico et al., 2022).
Regarding chemical hazards, based on the literature as well as the
experience of the HACCP team in producing Tenebrio molitor, we iden­
tified the presence of pesticides (organochlorines, organophosphates,
and others), heavy metals (lead, cadmium, selenium, arsenic), and
mycotoxins arising during larvae production (Baiano, 2020; Belluco
et al., 2013; Bosch et al., 2017; Errico et al., 2022; Grau et al., 2017;
IPIFF.International Platform of Insects for Food and Feed, 2019).
However, in recent studies, it has been identified that all metal con­
centrations found in different feeding substrates were below the legal
limit of undesirable substances in animal feed and only the mercury (Hg)
is bioaccumulative. Therefore, the risk of exposure to metals from con­
sumption of mealworm larvae is relatively low (Truzzi et al., 2019).
Additionally, according to the experience of the HACCP team, hazards as
residues of soaps and disinfection products – may be avoided with GMP.
As shown in Table 2, chemical hazards decreased as the stages of pro­
cessing the meal progressed.
Pieces of metal, stones, plastic, and other foreign particles are the
principal physical hazards, principally resulting from production of
larvae in metal or plastic beds and breakage of the mesh upon sifting the
meal (EFSA European Food Safety Authority, 2017; IPIFF.International
Platform of Insects for Food and Feed, 2019). Physical hazards identified
may be prevented with adequate technical maintenance and calibration
programs (EFSA European Food Safety Authority, 2017), visual in­
spection of the mesh, use of metal detectors during reception of the
larvae, and use of X-ray equipment during packaging to detect all the
foreign particles (Einarsdóttir et al., 2016). Other physical hazards
identified were presence of insect parts such as wings and legs, as well as
insect pests such as mites associated with other contaminants. These
hazards may be prevented with proper feeding of the larvae and a pest
control program, as well as rigorous visual inspection upon sifting.
As shown in Table 2, allergens - which have a variety of causes - are
another common hazard of this type of food (Belluco et al., 2013;
Cámara et al., 2018; EFSA European Food Safety Authority, 2021; Errico
et al., 2022; Grau et al., 2017; Mancini et al., 2020). Since it is difficult to
avoid allergens as contaminants in Tenebrio molitor meal, and heat
treatment can reduce but not eliminate the allergenicity (Errico et al.,
2022), the best preventive measure is to mention possible presence of
allergens on the label. To prevent contamination by gluten due to
feeding the larvae with cereals, an adequate fasting period is necessary
to assure that gluten levels decrease to acceptable levels (Mancini et al.,
2020). In any case, the label must state that the product “may contain
gluten”, and gluten levels of the meal must be monitored to assure the
effectiveness of the imposed fast.

3.5. Identification of CCPs, critical limits, the monitoring system, and

corrective actions to be implemented in production of Tenebrio molitor
meal

Table 3 contains information on the CCPs and Table 4 shows the

critical limits, the proper monitoring system for production of Tenebrio
molitor meal, and corrective actions that must be implemented if the
control variables surpass the limits permitted.
The most critical stage for controlling hazards (CCP) – particularly
pieces of metal - is upon reception of the larvae. It is also crucial to
establish a supplier control program by which suppliers are required to
Fig. 2. Flow chart of production of Tenebrio molitor mealSource offer safe raw materials (EFSA European Food Safety Authority, 2017;
Original diagram by the authors, based on (Mancini et al., 2020; Purschke et al.,
Wallace & Mortimore, 2016). In those cases, in which the processor of
2018; Fraqueza & Patarata, 2017; Kooh et al., 2020; IPIFF.International Plat­
the flour also raises the larvae, this control point is expected to allow for
form of Insects for Food and Feed, 2019).
elimination of pieces of metal, since this hazard will be easier to control.

5
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

Table 2
Hazards analysis in production of Tenebrio molitor meal and preventive measures.
Stage Classification Type of Hazard Probability Severity Classification Control/Preventive measures
of hazard

Stage 1. Biological Enterobacteriaceae* 4- 3 - Severe 12 - High Improve biosecurity and hygiene measures of
Reception of Moderate personnel. Apply heat treatment at some point
larvae during the processing.
Taenia (Hymenolepis diminuta) 2 - Remote 3 - Severe 6 - Medium Reinforce biosecurity and hygiene measures for
personnel and pest control programs.
Staphylococcus aureus 3- 4 - Critical 12 - High Reinforce biosecurity and hygiene measures for
Occasional personnel. Reinforce cleaning and disinfection
protocols in larvae packing and transport. Apply
heat treatment.
Clostridium botulinum 2 - Remote 5- 10 - High Avoid contamination of substrate by soil.
Catastrophic Reinforce supplier control program. Apply heat to
control the microorganism and its toxins.
Clostridium perfringens 2 - Remote 4 - Critical 8 - Medium See recommendations for Clostridium botulinum.
Salmonella 3- 5- 15 - High Request supplier to adequately separate organic
Occasional Catastrophic residues that will be used as substrate for the
larvae from other waste contaminated with soil
and feces to avoiding cross-contamination.
Increase control of raw materials. Reinforce
hygiene measures.
Campylobacter spp. 2 - Remote 3 - Severe 6 - Medium Assure supplier produces a suitable substrate for
the larvae and assure use of potable water
throughout the process.
Hepatitis A. virus 2 - Remote 4 - Critical 8 - Medium Assure supplier produces a suitable substrate for
the larvae and assure use of potable water
throughout the process. Improve biosafety and
personal hygiene measures. Implement a
vaccination schedule. Apply a heat treatment to
control the virus.
Escherichia coli - Shiga toxin 2 - Remote 5- 10 - High Assure substrate of larvae are not contaminated.
Catastrophic Assure proper hygiene and biosecurity measures
by personnel. Apply heat treatment to control the
microorganism and their toxins.
Listeria monocytogenes 2 - Remote 5- 10 - High See recommendations for Escherichia coli.
Catastrophic
Chemical Pesticides (including 1 - Unlikely 3 - Severe 3 - Medium Assure substrate and food are not contaminated
organochlorines and by pesticides. Strictly follow supplier control
organophosphates) program. Carry out random tests for pesticides in
batches of larvae.
Heavy metals (lead, cadmium, 2 - Remote 4 - Critical 8 - Medium Assure substrate and food are not contaminated
selenium, arsenic) with pesticides. Strictly follow control program.
Carry out random detection tests on batches of
larvae.
Cleaning and disinfection chemicals 2 - Remote 3 - Severe 6 - Medium Assure larvae are raised in immaculate boxes
without traces of soap or disinfectant. Strictly
follow proper cleaning and hygiene practices.
Mycotoxins and aflatoxins 2 - Remote 4 - Critical 8 - Medium Assure substrate of larvae are fresh. Strictly follow
supplier control program. Improve operator
training on storage of raw materials. Carry out
tests of mycotoxins and aflatoxins.
Physical Pieces of metal 3- 3 - Severe 9 - Medium Carry out rigorous visual inspection of larvae
Occasional upon reception, as well as supplier audits (review
equipment and facilities, carry out rigorous
maintenance program). Install metal detector.
Other foreign particles, including 2 - Remote 2 - Minor 4 - Medium Carry out rigorous visual inspection of larvae
stones and plastic upon reception, as well as supplier audits (review
equipment and facilities, carry out rigorous
maintenance program). Install X-ray equipment
for use in packaging stage.
Insect wings and legs; insect pests 5- 2 - Minor 10 - Medium Control reception. Carry out supplier inspections
(mites) Frequent and rigorous visual inspection.
Allergens Mites, mold, dust, other substances 5- 4 - Critical 20 - High Include recommendations regarding allergens on
derived from Arthropod chitin Frequent label.
(larval cuticle protein A1A and
A2B)
Tropomyosin 5- 4 - Critical 20 - High Include recommendations regarding allergens on
Frequent label.
a-amilase 5- 4 - Critical 20 - High Include recommendations regarding allergens on
Frequent label.
Arginina quinasa 5- 4 - Critical 20 - High Include recommendations regarding allergens on
Frequent label.
Gluten 5- 2 - Minor 10 - Medium Include recommendations regarding allergens on
Frequent label. Ensure sufficient fasting and washing of
larvae before processing.
(continued on next page)

6
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

Table 2 (continued )
Stage Classification Type of Hazard Probability Severity Classification Control/Preventive measures
of hazard

Stage 2. Selection Biological Enterobacteriaceae* 4 3 - Severe 12 - High See recommendations for stage 1.
of larvae -Moderate
Salmonella 1 - Unlikely 5- 5- Medium Assure adequate treatment of organic residues to
Catastrophic be used as food for the larvae, avoiding cross-
contamination. Carry out strict control of raw
materials. Assure strict hygiene measures by
personnel.
Escherichia coli - Shiga toxins 1 - Unlikely 5- 5 - Medium See recommendations for stage 1.
Catastrophic
Hepatitis A. virus 1 - Unlikely 4 - Critical 4 - Medium See recommendations for stage 1.
Physical Plastic or latex 1 - Unlikely 2 - Minor 2 - Low Use new gloves to handle each batch. Carry out
visual inspection to detect deterioration of gloves.
Train personnel regarding personal safety and
food safety.
Stage 3. Fasting Biological Enterobacteriaceae* 4- 3 - Severe 12 - High See recommendations for stage 1.
of larvae Moderate
Salmonella 2 - Remote 5- 10 - High See recommendations for stage 2.
Catastrophic
Escherichia coli - 2 - Remote 5- 10 - High Apply heat treatment at some point during
Catastrophic processing.
Listeria monocytogenes 3- 5- 15 - High Apply heat treatment at some point during
Occasional Catastrophic processing.
Allergens Gluten 5- 2 - Minor 10 - Medium See recommendations for stage 1.
Frequent
Stage 4. 1st Biological Enterobacteriaceae* 1 - Unlikely 3 - Severe 3 - Medium Assure proper hygiene and biosecurity measures
sifting by personnel. Carry out training regarding GMP.
Apply heat treatment at some point during
processing.
Salmonella 1 - Unlikely 5- 5 - Medium See recommendations for stage 2.
Catastrophic
Escherichia coli - 1 - Unlikely 5- 5 - Medium See recommendations for Enterobacteriaceae
Catastrophic
Hepatitis A. Virus 1 - Unlikely 4 - Critical 4 - Medium See recommendations for stage 1.
Listeria monocytogenes 1 - Unlikely 5- 5 - Medium See recommendations for stage 1.
Catastrophic
Physical Pieces of metal 1 - Unlikely 4 - Severe 4 - Medium Carry out visual inspection of sieves each time
before sifting. Update preventive equipment
maintenance program. Use a metal detector
toward the end of processing.
Insect parts such as legs, exuviae 3- 2 - Minor 6 - Medium Assure mesh size of 750 μm (μ) for sifting.
Occasional
Other foreign particles, including 2 - Remote 2 - Minor 4 - Medium Carry out a rigorous visual inspection of larvae
stones and plastic upon reception. Install X-ray equipment for use in
the packaging stage.
Stage 5. Washing Biological Enterobacteriaceae* 1 - Unlikely 3 - Severe 3 - Medium See recommendations for stage 4
larvae Listeria monocytogenes 1 - Unlikely 5- 5 - Medium See recommendations for stage 1.
Catastrophic
Stage 6. Sacrifice Biological Salmonella 1 - Unlikely 5- 5 - Medium See recommendations for stage 4.
by freezing Catastrophic
Escherichia coli - 1 - Unlikely 5- 5 - Medium See recommendations for stage 4.
Catastrophic
Stage 7. For this stage, no biological, physical, or chemical hazards were identified.
Unfreezing
Stage 8. Biological Survival of bacteria and spores that 1 - Unlikely 3 - Severe 3 - Medium Assure proper hygiene and biosecurity measures
Blanching survive blanching by personnel. Provide proper training on GMP
and equipment maintenance. Apply heat
treatment during some stage of processing.
Stage 9. Heat Biological Survival of bacteria and spores that 1 - Unlikely 3 - Severe 3 - Medium Provide proper training on GMP. Permanently
treatment. (1st survive high temperatures. monitor time and temperature. Carry out proper
hot air drying) maintenance of drying equipment. Apply heat
treatment toward the end of processing.
Stage 10. Biological Enterobacteriaceae 1 - Unlikely 3 - Severe 3 - Medium Assure proper hygiene and biosecurity measures
Grinding by personnel. Apply heat treatment during some
stage of processing.
Salmonella, E Coli. 1 - Unlikely 5- 5 - Medium Provide proper training on GMP. Apply heat
Catastrophic treatment during some stage of processing.
Physical Pieces of metal 1 - Unlikely 3 - Severe 3 - Medium Continually update preventive equipment
maintenance procedures. Install a metal detector
for use toward the end of processing
Stage 11. Heat Biological Survival of bacteria and spores 1 - Unlikely 3 - Severe 3 - Medium Provide proper training on GMP. Permanently
treatment (2nd despite high temperatures monitor time and temperature during this stage.
hot air drying) Carry out adequate maintenance of drying
equipment.
Stage 12. 2nd Physical Pieces of metal 1 - Unlikely 3 - Severe 3 - Medium Before each sifting, visually inspect sieves.
sifting Continually update preventive equipment
(continued on next page)

7
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

Table 2 (continued )
Stage Classification Type of Hazard Probability Severity Classification Control/Preventive measures
of hazard

maintenance procedures. Install metal detector or

X-ray equipment for use toward the end of
processing.
Stage 13. Physical Foreign particles, such as pieces of 2 - Remote 3 - Severe 6 - Medium Evaluate quality of final product. Carry out
Packaging and metal and plastic equipment maintenance. Suitably package the
labeling product. Install X-ray detector equipment for use
toward the end of processing.
Allergens Allergens that remain in the final 5- 4 - Critical 20 - High See recommendations for stage 1.
product (e.g. gluten) Frequent
Stage 14. Storage Biological Development of microorganisms 1 - Unlikely 3 - Severe 3 - Medium Vacuum pack and inventory final product to avoid
due to product deterioration given deterioration. Include expiration date on label
long storage time and monitor microorganisms in the final product

Source: Original proposal by the authors. Biological hazards based on review literature (Klunder et al.,2012; Shostak, 2014; Stoops et al., 2016; Grau et al., 2017; IPIFF.
International Platform of Insects for Food and Feed, 2019; Kooh et al., 2020). Chemical Hazards based on review literature (Belluco et al. 2013; van der Spiegel et al.,
2013; Poma et al., 2017; Grau et al., 2017; Bosch et al., 2017; IPIFF.International Platform of Insects for Food and Feed, 2019; Baiano, 2020, Errico et al., 2022).
Physical hazards based on review literature (Einarsdóttir et al., 2016; EFSA European Food Safety Authority, 2017; IPIFF.International Platform of Insects for Food and
Feed, 2019). Allergens based on review literature (Belluco et al., 2013; Verhoeckx et al., 2014; Grau et al., 2017; De Gier & Verhoeckx, 2018; Camara et al., 2018;
Beaumont et al., 2019; Garino et al. 2020; Mancini et al., 2020, EFSA European Food Safety Authority, 2021; Errico et al., 2022).
Note: The causes of the hazards and the rationale behind the classification of each risk were discussed by the HACCP team according to reported by recent literature and
the experience of the HACCP team members for the production of Tenebrio molitor meal.

Table 3
CCPs for production stages of Tenebrio molitor meal.
Stages Classification of Type of Hazard Q1 Q2 Q3 Q4 Decision
hazard

Stage 1. Reception of larvae Biological Microorganism identified in Table 2 YES NO NO YES PRP
Chemical Pesticides, heavy metals, and mycotoxins YES NO NO YES PRP
Physical Pieces of metal YES YES CCP
Other foreign particles, including stones and plastic and insect parts YES NO NO YES PRP
Allergens Microorganisms identified in Table 2 YES NO NO YES PRP
Stage 2. Selection of larvae Biological Microorganism identified in Table 2 YES NO NO YES PRP
Stage 3. Fasting of larvae Biological Microorganism identified in Table 2 YES NO NO YES PRP
Allergens Allergens identified in Table 3 YES YES CCP
Stage 4. Biological Microorganism identified in Table 2 YES NO NO YES PRP
1st sifting Physical Pieces of metal YES NO SI YES PRP
Insect parts and exuviae YES YES CCP
Other foreign particles, including stones, plastic and insect parts YES YES CCP
Stage 5. Washing of larvae Biological Microorganism identified in Table 1 YES NO NO YES PRP
Stage 6. Sacrifice by freezing Biological Microorganism identified in Table 2 YES NO NO YES PRP
Stage 8. Blanching Biological Survival of bacterial agents and spores that could survive blanching YES NO NO YES PRP
temperatures
Stage 9. Biological Bacteria and spores that could survive drying temperatures. YES NO NO YES PRP
Heat treatment. (1st hot air
drying)
Stage 10. Grinding Biological Microorganism identified in Table 2 YES NO YES YES PRP
Physical Pieces of metal YES NO YES YES PRP
Stage 11. Biological Bacteria and spores that could survive drying temperatures. Presence of YES YES CCP
Heat treatment. (2nd hot air Enterobacteriaceae due to grinding
drying)
Stage 12. Physical Pieces of metal YES YES CCP
2nd sifting
Stage 13. Packaging and Physical Foreign particles (e.g. plastic) that were not eliminated by sifting YES YES CCP
labeling Allergens Allergens that remain in the final product (e.g. gluten) YES YES CCP
Stage 14. Storage Biological Development of microorganisms due to deterioration of the product given YES NO YES NO CCP
prolonged storage
a
Note: For stage 7 (unfreezing), no biological, physical, or chemical hazards were identified.
PRP = Prerequisite Program.
Q1, Q2, Q3, Q4: Questions asked upon carrying out the decision tree methodology.

The fasting stage has been identified as a CCP due to the importance size of 710–1400 μm so that it be small enough to eliminate this hazard
of assuring reduction in gluten levels during this period. With the (Purschke et al., 2018). The next CCP in Tenebrio molitor meal produc­
induced fast and washing of the larvae, gluten decreases to less than 20 tion is heat treatment (2nd drying stage). Due to the temperature and
ppm (the upper limit for products considered to be gluten-free). None­ time length of this stage, microorganisms exposed after grinding as well
theless, it is necessary to report its presence (Mancini et al., 2020). as those that survive the 1st drying stage will be eliminated.
The first sifting stage is a CCP for physical hazards such as insect The following CCP is the 2nd sifting stage, in which remnants of
parts, exuvias, stones, and other foreign particles considered to be metal due to equipment wear are eliminated. In this phase, a sieve with a
medium-level risks based on their probability of occurrence and con­ mesh size from 350 to 500 μm will guarantee that these larger particles
sequences to consumers. For this stage, several authors establish a mesh be eliminated, resulting in a safe product for consumers. However, as

8
 H.A. Arévalo Arévalo et al.
Table 4
Critical limits, monitoring system, and corrective actions for production of Tenebrio molitor meal.
Stage Classification Type of Hazard Observations Critical limits Recommendations for monitoring Corrective actions
of hazard
Min Max What How Who

Stage 1. Physical Pieces of metal Metal detector should Not 1 mm Presence of pieces of Pass all products through a Person in charge Equipment maintenance
Reception of be used during this applicable metal metal detector. in the processing and monitoring using a
larvae stage. line metal detector
Assure batch passes through
the 2nd sifting stage.
Stage 3. Fasting Allergens Gluten Through fasting and 24 h 48 h Fasting time assures Record beginning and ending Operator in the Report possible gluten
of larvae washing larvae, gluten reduction of gluten in time of fast. processing line presence on label.
is reduced to less than larvae. Assure additional 24 h of
20 ppm. fasting before processing
batch.
Stage 4. 1st Physical Foreign particles, Mesh size (710 μm) 710 μm 1400 μm Presence of insect parts Pass entire batch through Operator in the Review and monitor wear of
sifting including stones, plastic assures elimination of such as legs and sieves with mesh size processing line sieves.
and insect parts residues. exuviae, stones, and 710–1400 μm and visually Re-sift entire batch using a
other foreign particles evaluate batch for residues. new sieve.
Stage 11. Heat Biological Presence of In this stage, biological 80 ◦ C × 85 ◦ C × 120 Verification of Include a thermocouple in Operator in the Adjust oven temperatures
treatment. Enterobacteriaceae after hazards are reduced. 120 min min temperatures. drying oven, connected to processing line and increase drying time.
(2nd hot air grinding monitoring and recording If temperature exceeds
drying) software. Use alarm to detect upper limit, evaluate
9

excess -temperature. quality of batch to

determine whether to
discard or use it in some
manner.
Stage 12. 2nd Physical Pieces of metal Sieve size (maximum 350 μm 500 μm Presence of pieces of Pass entire batch through 350 Operator in the Review sieves in all stages
sifting 500 μm) assures metal and 500 μm sieves, and processing line and ensure calibration of X-
elimination of larger visually evaluate residues ray equipment in the next
particles. stage.
Stage 13. Physical Foreign particles (e.g. X-ray detector limits 0 ≤1 mm Plastic and other Repeat 2nd sifting. Packaging and Review calibration of X-ray
Packaging plastic) not eliminated hazard. foreign particles not labeling equipment and sieves
and labeling during sifting eliminated during manager carried out during the
sifting previous stage.
Allergens Allergens remaining in Label should alert 0 ppm 20 ppm Presence of allergens Alert consumers to presence Personnel in Assure adequate fasting
final product, including consumers to allergens. of allergens on label. charge of time.
gluten quality-control Assure labels meet
and label design requirements (see Table 1).
Stage 14. Biological Development of This stage is the only 0 Six months Stock rotation Assure adequate product Quality-control Coordinate marketing plan
Storage microorganisms due to one in which this (expiration rotation (first to come, first to personnel with production and stock
prolonged storage hazard can be time) go). rotation. Discard infected
prevented before lots.

Food Control 138 (2022) 109030

product is consumed.

Note: The monitoring system is carried out for each batch by the person in charge of the production line.
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

mentioned above, these CCP must be reinforced by adequate imple­ with a specified result (Codex Alimentarius Commission, 2008; Wallace
mentation of GMP and pre-requisite programs. A proper maintenance & Mortimore, 2016). Thus, producers of Tenebrio molitor meals must
equipment program and use of a metal detector will considerably reduce validate the methods that the company decides to establish in each stage
the risk of physical hazards in Tenebrio molitor meal. of the HACCP plan. With a correct validation process, the control mea­
The packaging and labeling stage is also a CCP because foreign sures are scientifically and technically suitable. It is suggested to give
particles that have managed to bypass the other stages may be effec­ attention to the validation of methodologies that are not common in the
tively controlled through use of an X-ray detector during this stage. food industry and the methods that the processing plant designs or de­
Furthermore, the product label should warn of possible presence of al­ velops as specific to its working conditions.
lergens in the final product. As validation strategies, it is possible to establish the contrast of
Finally, the storage stage is a CCP for microorganisms that develop historical knowledge, scientific publications and regulatory documents
during storage. As no other control point allows for preventing this type against the results obtained in the processing plant. Experimental tests
of hazard before the product reaches the final consumers, this point is (laboratory, processing plant), the use of mathematical models, opera­
crucial for the finished product. tional data (records) and surveys can also be carried out (Codex Ali­
The system for monitoring critical limits for each CCP during pro­ mentarius Commission, 2008). In this sense, Kooh et al. (2020) confirm
duction of Tenebrio molitor meal is similar to those which are typically that the main recommendations to control Tenebrio molitor insect pow­
used in the food industry (Table 4). A monitoring system must contain der safety for human health, for manufacturers and official control and
information about the variables to monitor and involve actions that are surveillance services, are validate the efficiency of the process, and
easy for the industry to carry out on a daily basis. For example, as shown particularly to CCPs, with regards to the selected hazards. This means
in Table 2, metals and other foreign particles are monitored by passing that cooking times, as well as an established treatment for each batch,
the processed meal through a metal detector and an X-ray machine, must be fulfilled as planned in each stage.
while presence of microorganisms is monitored as the flour is exposed to
high temperatures to eliminate them. Likewise, foreign particles that 3.6. Establishment of a verification system for the HACCP plan
have reached the packaging and labeling stage must be monitored, again
passing batches through the 2nd sifting if necessary. Table 5 presents the verification system for the HACCP plan. The
These actions are feasibly carried out by the industry and reveal verification system for CCP in production of Tenebrio molitor meal should
whether the CCP are being properly implemented. This stage allows for be carried out by people other than those who carry out monitoring, and
establishing corrective actions to be implemented if monitoring has the particular strategies used will vary from one processing plant to
detected that critical limits have been surpassed. another (Wallace & Mortimore, 2016). However, verification must
For example, if the monitoring system identifies that foreign particles ensure that each critical point is controlled (Table 5). For example, in
exceed the critical limit of 1.5 mm during the 1st sifting stage, in the 2nd stage 3 (larvae fasting), one possible verification strategy is to send
sifting stage corrective actions should consist of reviewing the sieves larvae samples to a laboratory monthly to determine their gluten level in
used in all stages and ensuring calibration of the X-ray equipment in the order to verify whether the fasting process is effective and whether the
next stage (Table 4). presence of this allergen has been reduced in the larvae, and conse­
In the implementation of the HACCP system, it is necessary that the quently in the Tenebrio molitor meal. Meanwhile, during storage, it is
critical limits, the monitoring methods and the proposed corrective ac­ possible to verify whether or not microorganisms are developing under
tions be validated in the processing plant. Validation is defined as the fixed storage conditions according to a sampling plan consisting of
obtaining evidence that a control measure (or combination of control sending flour samples to a laboratory for analysis of pathogenic micro­
measures), if properly applied, it will be able to controlling the hazard organisms and deterioration of the product (Table 5).

Table 5
Verification proposed for applying the HACCP plan to production of Tenebrio molitor meal.
Stage Classification of Type of Hazard Verification
hazard
What How Frequency Who

Stage 1. Physical Pieces of metal Presence of metal Perform visual and tactile verification of a Weekly Quality-control
Reception of batch sample previously passed through personnel
larvae metal detector. Verify calibration of
equipment according to standards..
Stage 3. Fasting Allergens Gluten Gluten presence greater Carry out laboratory tests to determine Monthly Quality-control
of larvae than 20 ppm gluten (Elisa test) levels. and laboratory
personnel
Stage 4. 1st Physical Foreign particles, including Presence of foreign Randomly select samples of sifting lot, Weekly Quality-control
sifting stones, plastic and insect particles verify with a laboratory sieve, and perform personnel
parts a visual review.
Stage 11. heat Biological Presence of Proper operation of Carry out laboratory analysis of pathogenic Monthly Quality-control
treatment. 1st Enterobacteriaceae after drying oven to eliminate and spoiling microorganisms according to and laboratory
hot air drying grinding microorganisms sampling plan. personnel
Stage 12. 2nd Physical Pieces of metal Presence of metal Select sifted samples to perform visual and Weekly Quality-control
sifting laboratory verification with a standard personnel
sieve.
Stage 13. Physical Plastic and other foreign Presence of foreign Verify calibration of metal detector with Weekly Quality-control
Packaging and particles not eliminated particles standard samples. Carry out visual and personnel
labeling during sifting tactile evaluation of a sample already
passed through X-ray detector.
Allergens Allergens that remain in Gluten presence greater Carry out laboratory tests of larval samples Monthly Quality-control
final product, including than 20 ppm to determine gluten levels. and laboratory
gluten personnel
Stage 14. Storage Biological Development of Compliance with storage Carry out laboratory tests to analyze Monthly Quality-control
microorganisms due to parameters pathogenic and spoiling microorganisms and laboratory
prolonged storage according to sampling plan. personnel

10
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

3.7. Documentation required for operation of the HACCP plan d’Allergologie, 59(Issue 5), 389–393. https://doi.org/10.1016/j.reval.2019.06.001.
ISSN 1877-0320.
Belluco, S., Losasso, C., Maggioletti, M., Alonzi, C. C., Paoletti, M. G., & Ricci, A. (2013).
Principle 7 of the HACCP system refers to the need to generate re­ Edible insects in a food safety and nutritional perspective: A critical review.
cords and other documents to support the HACCP plan. Each company Comprehensive Reviews in Food Science and Food Safety, 12(3), 296–313. https://doi.
may determine its own documentation system. The most important re­ org/10.1111/1541-4337.12014
Bosch, G., Van Der Fels-Klerx, H. J., De Rijk, T. C., & Oonincx, D. G. A. B. (2017).
cords are: I) methods and procedures to be used, including description of Aflatoxin B1 tolerance and accumulation in black soldier fly larvae (hermetia
the monitoring systems selected for CCP; II) corrective actions and im­ illucens) and yellow mealworms (tenebrio molitor). Toxins, 9(6), 1–10. https://doi.
provements that have been planned once the HACCP system is under­ org/10.3390/toxins9060185
Bugsolutely. (2020). Legal status of edible insects. Retrieved from https://www.bugsolute
way (working documents); III) records for monitoring CCP and of ly.com/legal-status-edible-insects/. (Accessed 23 March 2021).
verification and validation of the HACCP plan; and IV) contents and Cámara, H. M., Moreno, P., Daschner, Á., Fandos, E., Gómez, A., Lázaro, D., & Buelga, J.
other information related to staff training programs, as well as evalua­ (2018). Informe del Comité Científico de la Agencia Española de Consumo,
Seguridad Alimentaria y Nutrición (AECOSAN) en relación a los riesgos
tion of effectiveness of staff training, which must be archived (including microbiológicos y alergénicos asociados al consumo de insectos. Revista del Comité
training to carry out monitoring, corrective actions, verification of the Científico de la AESAN, 27, 11–40.
plan HACCP, and improvements made (Wallace & Mortimore, 2016; Codex Alimentarius Commission. (1997). Hazard analysis and critical control point
(HACCP) system and guideline for its application. Annex to CAC/RC 1-1969. Rev. 3.
Kooh et al., 2020). Codex Alimentarius Commission. (2008). Directrices para la validación de medidas de
Key records for monitoring CCP in Tenebrio molitor meal production control de la inocuidad de los alimentos (Vols. 69–2008) p. 16p). CAC/GL.
are those regarding drying times and temperatures, X-ray and metal Colombia. (2013). Resolución 2674. Ministerio de Salud y protección social.
Colombia. (2021). Resolución 810. Ministerio de protección Social Colombia.
detector results for each flour batch, laboratory analysis results, a con­
Colombia. Instituto de Vigilancia de Medicamentos y Alimentos (INVIMA). (2020). Sala
sumer complaints and claims system, and the respective corrective ac­ Especializada de Alimentos y Bebidas. Acta, 4.
tions and improvement plan. All information resulting from Cortes, J., Ruiz, A., Morales, J., Thomas, M., Rojas, M., Tomberlin, J., Yi, L., Han, R.,
implementing the HACCP system may be used as evidence upon carrying Giroud, L., & Jullien, R. (2016). Chapter 6 - insect mass production technologies. In
A. T. Dossey, J. A. Morales-Ramos, & M. G. Rojas (Eds.), Insects as sustainable food
out system audits. ingredients (153-201). Academic Press. https://doi.org/10.1016/B978-0-12-802856-
8.00006-5.
Dalmoro, Y. K., Adams, C. B., Haetinger, V. S., Bairros, L., Yacoubi, N., & Stefanello, C.
4. Conclusions (2021). Energy values of Tenebrio molitor larvae meal and tilapia byproduct meal
for broiler chickens determined using the regression method. Animal Feed Science and
Tenebrio molitor meal has great potential for use as human and ani­ Technology, 272(October 2020), Article 114784. https://doi.org/10.1016/j.
anifeedsci.2020.114784
mal food. However, like all foods of animal origin, it has several po­ De Brauw, A., Van Den Berg, M., Brouwer, I. D., Snoek, H., Vignola, R., Melesse, M.,
tential physicals, chemicals, and biological hazards – as well as allergens Lochetti, G., Van Wagenberg, C., Lundy, M., Maitre D’hotel, E., & Ruben, R. (2019).
that must be controlled through food safety systems such as HACCP. Food system innovations for healthier diets in low and middle-income countries.
International Food Policy Research Institute. https://doi.org/10.2499/
Proper analysis of hazards, establishment of preventive measures, and
p15738coll2.133156
identification of CCP will allow Tenebrio molitor producers to provide a De Gier, S., & Verhoeckx, K. (2018). Insect (food) allergy and allergens. Molecular
meal which does not pose risks to consumer health. Immunology, 100, 82–106. https://doi.org/10.1016/j.molimm.2018.03.015
Most hazards may be identified in stage 1, when the larvae enter Dicke, M. (2017). Ecosystem services of insects. In A. Van Huis (Ed.), Insects as food and
feed: From production to consumption (pp. 60–76). Tomberlin JK: Wageningen
production as a raw material, and are eliminated during the various Academic Publishers. https://doi.org/10.3920/978-90-8686-849-0.
stages of processing the meal. The producer of Tenebrio molitor meal may EFSA European Food Safety Authority. (2015). Risk profile related to production and
considerably reduce these risks by also raising the larvae, being sure to consumption of insects as food and feed. EFSA Journal, 13, 4257–4317. https://
doi:10.2903/j.efsa.2015.4257.
use adequate substrates. However, the company should also carry out EFSA European Food Safety Authority. (2017). Scientific opinion on hazard analysis
preventive maintenance to avoid hazards associated with utensils and approaches for certain small retail establishments in view of the application of their
other equipment, and adequately train personnel to implement pro­ food safety management systems. Panel on Biological Hazards (BIOHAZ), Ricci, A.,
Chemaly, M., Davies, R., Fernandez Escamez, P. S., et al. EFSA Journal, 15(3)
duction practices consistent with the GMP program. https://doi: 10.2903/j.efsa.2017.4697, 1, 4697, 52
Establishment of CCP during production of Tenebrio molitor meal EFSA European Food Safety Authority. (2021). Safety of dried yellow mealworm
allows for monitoring parameters such as drying time and temperature, (Tenebrio molitor larva) as a novel food pursuant to Regulation (EU) 2015/2283.
Panel on Nutrition, Novel Foods and Food Allergens (NDA). Turck, D., Castenmiller,
particle size, fasting time, packaging, and storage. Controlling these J., De Henauw, S., Hirsch-Ernst, K. I., Kearney, J., & Knutsen, H. K EFSA Journal, 19
variables during the appropriate stages ensures that established limits (1), 29pp https://doi:10.2903/j.efsa.2021.6343.
are not exceeded and that meal produced is safe for consumers. Einarsdóttir, H., Emerson, M. J., Clemmensen, L. H., Scherer, K., Willer, K., Bech, M.,
Larsen, R., Ersbøll, B. K., & Pfeiffer, F. (2016). Novelty detection of foreign objects in
food using multi-modal X-ray imaging. Food Control, 67, 39–47. https://doi.org/
Funding 10.1016/j.foodcont.2016.02.023
Errico, S., Spagnoletta, A., Verardi, A., Moliterni, S., Dimatteo, S., & Sangiorgio, P.
(2022). Tenebrio molitor as a source of interesting natural compounds, their
This research did not receive any specific grant from funding recovery processes, biological effects, and safety aspects. Comprehensive Reviews in
agencies in the public, commercial, or not-for-profit sectors. Food Science and Food Safety, 21(1), 148–197. https://doi.org/10.1111/1541-
4337.12863
Fraqueza, M., & Patarata, L. (2017). Constraints of HACCP application on edible insect for
food and feed. Future Foods. London: InTech. https://doi.org/10.5772/
Declaration of competing interest intechopen.69300
Garino, C., Mielke, H., Knüppel, S., Selhorst, T., Broll, H., & Braeuning, A. (2020).
None. Quantitative allergenicity risk assessment of food products containing yellow
mealworm (Tenebrio molitor). Food and Chemical Toxicology, 142, Article 11146.
https://doi.org/10.1016/j.fct.2020.111460
References Global Market Insights Inc. (2019). Easy availability, high protein, and low-fat concentration
characteristics to boost product demand. Retrieved from https://www.gminsights.com/
industry-analysis/edible-insects-market. (Accessed 23 November 2021).
Akhtar, Y., & Isman, M. (2018). 10 - insects as an alternative protein source. In R. Y. Yada
Grau, T., Vilcinskas, A., & Joop, G. (2017). Sustainable farming of the mealworm
(Ed.), Proteins in food processing (2nd ed., pp. 263–288). https://doi.org/10.1016/
Tenebrio molitor for the production of food and feed. Zeitschrift für Naturforschung C,
B978-0-08-100722-8.00011-5 Woodhead Publishing Series in Food Science,
72(9–10), 337–349. https://doi.org/10.1515/znc-2017-0033
Technology and Nutrition.
Hubert, A. (2019). Industrial insect production as an alternative source of animal
Baiano, A. (2020). Edible insects: An overview on nutritional characteristics, safety,
protein. Comptes Rendus Biologies, 342(7–8), 276–277. https://doi.org/10.1016/j.
farming, production technologies, regulatory framework, and socio-economic and
crvi.2019.09.028
ethical implications. Trends in Food Science & Technology, 100, 35–50. https://doi.
IPIFF. International Platform of Insects for Food and Feed. (2019). Guide on good
org/10.1016/j.tifs.2020.03.040
hygiene practices. IPIFF, 1(1), 1–121 https://ipiff.org/wp-content/uploads/2019/
Beaumont, P., Courtois, J., Van der Brempt, X., & Tollenaere, S. (2019). Food-induced
12/IPIFF-Guide-on-Good-Hygiene-Practices.pdf.
anaphylaxis to Tenebrio molitor and allergens implicated. Revue Française

11
H.A. Arévalo Arévalo et al. Food Control 138 (2022) 109030

Kamau, E., Mutungi, C., Kinyuru, J., Imathiu, S., Tanga, C., Affognon, H., Ekesi, S., laying quail (Coturnix japonica) diet. Poultry Science, 100(12), 101487. https://doi.
Nakimbugwe, D., & Fiaboe, K. (2018). Moisture absorption properties and shelf life org/10.1016/j.psj.2021.101487
estimation of dried and pulverized edible house cricket Acheta domesticus (L.) and Selaledi, L., & Mabelebele, M. (2021). The influence of drying methods on the chemical
black soldier fly larvae Hermetia illucens (L.). Food Research International, 106, composition and body color of yellow mealworm (Tenebrio molitor L.). Insects, 12
420–427. https://doi.org/10.1016/j.foodres.2018.01.012 (4), 1–12. https://doi.org/10.3390/insects12040333
Klunder, H., Wolkers - Rooijackers, J., Korpela, J., & Nout, M. (2012). Microbiological Shostak, A. W. (2014). Hymenolepis diminuta infections in tenebrionid beetles as a
aspects of processing and storage of edible insects. Food Control, 26, 628–631. model system for ecological interactions between helminth parasites and terrestrial
https://doi.org/10.1016/j.foodcont.2012.02.013 intermediate hosts: A review and meta-analysis. The Journal of Parasitology, 100(1),
Kooh, P., Jury, V., Laurent, S., Audiat-Perrin, F., Sanaa, M., Tesson, V., Federighi, M., & 46–58. http://www.jstor.org/stable/24624674.
Boué, G. (2020). Control of biological hazards in insect processing: Application of Stoops, J., Crauwels, S., Waud, M., Claes, J., Lievens, B., & Van Campenhout, L. (2016).
HACCP method for yellow mealworm (Tenebrio molitor) powders. Foods, 9(11), 1528. Microbial community assessment of mealworm larvae (Tenebrio molitor) and
https://doi.org/10.3390/foods9111528 grasshoppers (Locusta migratoria migratorioides) sold for human consumption. Food
Liu, C., Masri, J., Perez, V., Maya, C., & Zhao, J. (2020). Growth performance and Microbiology, 53, 122–127. https://doi.org/10.1016/j.fm.2015.09.010
nutrient composition of mealworms (Tenebrio molitor) fed on fresh plant materials- Truzzi, C., Illuminati, S., Girolametti, F., Antonucci, M., Scarponi, G., Ruschioni, S.,
supplmented diets. Foods, 9(151). https://doi.org/10.3390/foods9020151 Riolo, P., & Annibaldi, A. (2019). Influence of feeding substrates on the presence of
Mancini, S., Fratini, F., Tuccinardi, T., Degl’Innocenti, C., & Paci, G. (2020). Tenebrio toxic metals (Cd, pb, ni, as, hg) in larvae of Tenebrio molitor: Risk assessment for
molitor reared on different substrates: Is it gluten free? Food Control, 110, Article human consumption. International Journal of Environmental Research and Public
107014. https://doi.org/10.1016/j.foodcont.2019.107014 Health, 16(23). https://doi.org/10.3390/ijerph16234815
Morales-Ramos, J. A., Rojas, M. G., Kelstrup, H. C., & Emery, V. (2020). Self-selection of van der Spiegel, M., Noordam, M. Y., & van der Fels-Klerx, H. J. (2013). Safety of novel
agricultural by-products and food ingredients by Tenebrio molitor (Coleoptera: protein sources (insects, microalgae, seaweed, duckweed, and rapeseed) and
Tenebrionidae) and impact on food utilization and nutrient intake. Insects, 11(12), legislative aspects for their application in food and feed production. Comprehensive
827. https://doi.org/10.3390/insects11120827 Reviews in Food Science and Food Safety, 12(6), 662–678. https://doi.org/10.1111/
Mota de Carvalho, N., Walton, G., Poveda, C., Silva, S., Amorim, M., Madureira, A., 1541-4337.12032
Pintado, M., Gibson, G., & Jauregi, P. (2019). Study of in-vitro digestion of Tenebrio Varunjikar, M. S., Belghit, I., Gjerde, J., Palmblad, M., Oveland, E., & Rasinger, J. D.
molitor flour for evaluation of its impact on the human gut microbiota. Journal of (2022). Shotgun proteomics approaches for authentication, biological analyses, and
Functional Foods, 59, 101–109. https://doi.org/10.1016/j.jff.2019.05.024 allergen detection in feed and food-grade insect species. Food Control, 137, Article
Poma, G., Cuykx, M., Amato, E., Calaprice, C., Focant, J. F., & Covaci, A. (2017). 108888. https://doi.org/10.1016/j.foodcont.2022.108888
Evaluation of hazardous chemicals in edible insects and insect-based food intended Verhoeckx, K., van Broekhoven, S., den Hartog-Jager, C., Gaspari, M., de Jong, G.,
for human consumption. Food and Chemical Toxicology, 100, 70–79. https://doi.org/ Wichers, H., van Hoffen, E., Houben, G., & Knulst, A. (2014). House dust mite (Der p
10.1016/j.fct.2016.12.006 10) and crustacean allergic patients may react to food containing Yellow mealworm
Purschke, B., Brüggen, H., Scheibelberger, R., & Jäger, H. (2018). Effect of pre-treatment proteins. Food and Chemical Toxicology, 65, 364–373. https://doi.org/10.1016/j.
and drying method on physicochemical properties and dry fractionation behavior of fct.2013.12.049
mealworm larvae (Tenebrio molitor L.). European Food Research and Technology, 244, (Chapter 3) - HACCP. Lelieveld, H., Holah, J. and Gabrić, D Wallace, C. A., &
269–280. https://doi.org/10.1007/s00217-017-2953-8 Mortimore, S. E. (2016). In handbook of hygiene control in the food industry. A volume
Rumbos, C., Karapanagiotidis, I., Mente, E., Psofakis, P., & Athanassiou, C. (2020). in Woodhead Publishing Series in Food Science, Technology and Nutrition (2nd ed.).
Evaluation of various commodities for developing the yellow mealworm, Tenebrio Elsevier Ltd. https://doi.org/10.1016/B978-0-08-100155-4.00003-0.
molitor. Scientific Reports, 10(1), 1–10. https://doi.org/10.1038/s41598-020-67363- Zielińska, E., Karaś, M., & Baraniak, B. (2018). Comparison of functional properties of
1 edible insects and protein preparations thereof. Lebensmittel-Wissenschaft und
Secci, G., Addeo, N. F., Rodriguez, L. F. P., Bovera, F., Moniello, G., & Parisi, G. (2021). In -Technologie- Food Science and Technology, 91, 168–174. https://doi.org/10.1016/j.
vivo performances, ileal digestibility, and physicochemical characterization of raw lwt.2018.01.058
and boiled eggs as affected by Tenebrio molitor larvae meal at low inclusion rate in

12