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2023

A holistic overview of the rearing

Case 11

ABEL BOESCHOTEN (1033596)


ATISH KUMAR (1252429)
JELLE TIMMERMAN (1049421)
MARLEEN HARBERS (1314300)

Insects as Food and Feed: ENT21306


Supervised by Carlotta Savio
27/01/2023
Abstract
This case study evaluates the production of the yellow mealworm, Tenebrio molitor.
Approximately 2100 are edible for humans, but the yellow mealworm has become one of the most
popular insects for food and feed rearing in the last couple of years. This paper provides a holistic
overview of all the aspects to take into consideration when rearing the yellow mealworm. Examples
of fungal, bacterial, and other pathogens found in the mealworm are given, along with contaminants
and abiotic factors that have an influence on the well-being of the mealworm.

For the nutrition of the yellow mealworm to live on, it’s beneficial to use local agricultural / food by-
products. This is not only more cost-effective but also more sustainable due to local waste
management. For high growth performance, the diet should contain the macronutrients between
the following ranges: lipid between 0.10 and 0.03, carbohydrate between 0.75 and 0.65, and protein
between 0.25 and 0.2. Furthermore, for a high-protein yellow mealworm larvae product, a lot of by-
products can be used for the diet, but wheat bran is known to give the highest protein content.

The yellow mealworm can be reared in 65 L x 50 W x 15 H trays. They can be stacked on top of each
other and take less space than other species since the yellow mealworm does not need too much
vertical space, it is not able to jump. The yellow mealworm can be fed with solid, semi-solid, and
liquid feed. To feed the yellow mealworm, serving in time is used to prevent the substrate from
spoiling. The yellow mealworm will take up water from the air. To ensure the safe production of
yellow mealworms for human consumption, a HACCP plan is important. Different microorganisms
that can treat humans are present in the yellow mealworm and to decrease the levels present of
these microbes, it is important to combine process steps that reduce the levels to safe levels of
microorganisms or that keep the levels low. Examples are heating, cooling, drying, etc.

European Commission has already permitted the use of Insects in the form of food and feed under
its laws and regulation. As of now,6 authorizations are granted under EC for accepting insects as
food under regulation (EC) 2283/2015. The amendment of the older regulation( EC)(258/97) was a
necessity in respect of the confusion the European Commission was facing for accepting Whole
insects as an edible part came to an end.

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Table of contents
Abstract.................................................................................................................................................1
1. Introduction...................................................................................................................................3
2. Features of the yellow mealworm.................................................................................................4
3. Diseases.........................................................................................................................................5
3.1. Contaminants........................................................................................................................6
4. Yellow mealworm nutrition...........................................................................................................6
4.1. Influence of nutrition on growth performance......................................................................6
4.2. Influence of nutrition on the nutritional composition...........................................................8
5. Farming techniques.......................................................................................................................9
6. HACCP in insect farming..............................................................................................................11
7. Legislation....................................................................................................................................13
7.1. Amendment of Name..........................................................................................................13
7.2. Insects as food.....................................................................................................................13
7.3. Yellow mealworm as feed....................................................................................................14
7.4. Insect welfare......................................................................................................................14
7.5. Labelling and controls..........................................................................................................14
7.6. Authorization of Insects as a Food in Europe according to regulation EC (2015/2283)......15
7.7. Insect legislation in other countries.....................................................................................15
7.7.1. North America (USA/CANADA)....................................................................................15
7.7.2. Australia and New Zealand..........................................................................................15
7.7.3. Asia..............................................................................................................................16
8. Discussion....................................................................................................................................17
9. Conclusion...................................................................................................................................18
10. References...................................................................................................................................19

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1. Introduction
Out of the almost 2100 insects that are considered edible for humans, there are not many insects
that have gained more popularity recently than the yellow mealworm (Tenebrio Molitor)
(WUR, 2017)
. Considered in the past solely to be a pest for grains (molitor coming from the Latin word for
“miller”) (Moruzzo et al., 2021). The yellow mealworm has gained popularity in Europe over the last
2 years, now that the EFSA (Europe Food Safety Authority) has approved the yellow mealworm for
human food in EU countries (NOS, 2021). However, in other regions of the globe yellow mealworms
have been part of many people’s diets. This report provides a holistic overview of aspects to take
into consideration when rearing the yellow mealworm for human food and animal feed. It will first
provide a quick outline of general features, then delve deeper into the types of food the yellow
mealworm is currently fed on and what effects these foods have on the growth and well-being of the
yellow mealworm.

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2. Features of the yellow mealworm
An important remark is that a yellow mealworm is not a worm in its final stage (like the
Lumbricidae/ common earthworm for example), but the larvae of the darkling beetle. The Tenebrio
molitor is a holometabolous insect, meaning it goes through four different stages of metamorphosis
(egg, larva, pupa and adult stage) (van Huis & Tomberlin, 2017) . After its first stage is finished, the
egg will hatch after about 12 days and a yellow larva comes out. Despite few products on the
European markets containing yellow mealworms (Wang et al., 2022), these insects have been
abundantly used for direct food consumption for humans in Southeast Asian countries like China,
Vietnam and South Korea (Wang et al., 2022), where they are sold as street food on markets like
other insects, either fried, roasted or sometimes even still alive (Wahome, 2022). In Europe
however, yellow mealworms are currently mostly processed for feed for animals like reptiles or
birds. Currently, an increasing number of insect farms related to yellow mealworms are being built,
ranging from small-scale farms to the largest vertical insect farm in the world, Ynsect, located near
Paris, France (Thévenot et al., 2018).

With the increasing number of studies based on the nutrients found in the yellow mealworm,
interest has grown to implement yellow mealworm protein directly into human food and not solely
as livestock or pet food. The yellow mealworm contains many comparable nutrients found in other
animals raised for human consumption. For starters, similar amounts of unsaturated omega-3 and
fatty acids have been found compared to fish (Ravzanaadii et al., 2012). They also contain a high
vitamin content (especially a good source of B12) and mineral content (like phosphorus, zinc and
iron) similar to fish and meat (Gkinali et al., 2022). The main driver for insect farming however is its
potential to be an abundant source of protein. A live yellow mealworm contains on average around
20% of protein, whereas the dried yellow mealworm can reach up to 53% (due to the high-water
content of the insect when unprocessed) (Mariod, 2020). Its amino acid composition is well-
balanced, containing both essential and non-essential components (Wu et al., 2020). The larvae of
the yellow mealworm also contain fibre, which facilitates digestion, and cannot be maintained from
regular livestock (Heidari-Parsa et al., 2018; Ramos-Elorduy et al., 2002).

Because they are relatively easy to raise (for example due to their fast reproduction and high growth
rates and the fact that they produce fewer waste streams and require less feed than other livestock
(Toviho & Bársony, 2022)the yellow mealworm has gained more popularity over the years for insect
farming. Studies have shown that they can be fed on a huge variety of diets (Bordiean et al., 2022).
There are dozens of video examples online in which they eat just about anything, from fruits and
vegetables to bread and meat. One study even showed they can eat Styrofoam as their exclusive
diet without suffering health-wise compared to yellow mealworms fed on a regular diet
(Yang et al., 2015)
. They have shown to be very efficient converters when given an organic waste stream diet,
making them an interesting contributor to a more circular economy (Toviho & Bársony, 2022) .
Another advantage is that they take up much less land (lower LU) than other animals used for
human protein consumption, like cows, pigs or even chickens. As a result of their small size, they can
be stacked up in crates, creating a vertical way of farming, which wouldn’t be possible with regular
livestock. For every hectare of land needed for yellow mealworm production, about triple the
amount of area would be required to produce pork protein, and even more (10 ha) for beef protein
(van Huis et al., 2013).

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Because they are cold-blooded organisms (like all insects are), they adapt to the surrounding
temperature causing them to emit fewer harmful gasses into the atmosphere. It also means they are
much more efficient at converting feed into digestible protein for animal or human consumption
(Toviho & Bársony, 2022). Moreover, the yellow mealworm also contains a lower water footprint
(m3/t) compared to pig and beef meat (Miglietta et al., 2015).

In the next chapters, the challenges of yellow mealworm farming, regarding farming techniques,
insect diseases and legislation are discussed.

3. Diseases
With a dense number of yellow mealworms stacked in crates (up to a density of 300 mg larvae/cm2
(Deruytter et al., 2019)), it is likely for diseases to spread from one individual to the other. Aside
from abiotic environmental factors like food, temperature and population density, there is a number
of pathogens that can inhibit the larvae’s growth. In order to rear yellow mealworms more efficiently
in the future with a higher survival rate, it is essential to understand the mechanisms of yellow
mealworm diseases caused by insect pathogens. This chapter will provide a quick overview of the
most common diseases found in yellow mealworms designed for rearing.

T. molitor can be infected by parasites, entomopathogenic fungi, and viruses


(Vigneron et al., 2019a)
. Strains of the bacterium have been shown to be pathogenic to the T. molitor as well, like the
Aeromonas hydrophila (Noonin et al., 2010). It has also been found that the T. molitor can get
infected by two genera of the Hypocreales (Ascomycota) fungi order (beauveria and metarhizium)
(Maciel-Vergara et al., 2021). Another type of insect pathogen is gregarines (parasite protozoans),
located in the gut of the yellow mealworm. Gregarines are mostly non-lethal; however, they reduce
the insects’ fitness to a significant degree. High numbers of gregarines were found in protozoan
parasites in multiple insects used for human consumption, including the T. molitor. Regarding fungi,
the yellow mealworm has been shown to be infected with the fungus M. anisopliae
(Reeson et al., 1998; Vigneron et al., 2019b)

That being said, not all organisms found in the yellow mealworm have a negative impact on its
survival or well-being. Diet modification (and therefore including the possibility of other species to
emerge) can alter the microbial composition of the digestive system of the larva, leading to possible
higher resistance to infections. The lactic acid and bacterial strain found in the gut called the
Pediococcus pentosaceus is an example of that, showing an increase in growth and endurance of the
larvae of the T. molitor (Lecocq et al., 2021).

It has often been suggested that the substrate that the yellow mealworm is fed on can disturb the
microbiota of the insect (EFSA Scientific Committee, 2015) . Therefore, a logical next step would be to
investigate to what extent a food pathogen in the substrate can be passed on to the yellow
mealworm (and potentially infect animals eating the yellow mealworm, or even pose a health risk
for humans who eat them). Not much is known about the transmission of pathogens located in food
from the substrate to the T. molitor. At least one study looked at the potential of Salmonella sp. to
be transmitted to yellow mealworms when given wheat bran as substrate (which causes diseases in
other livestock like pigs) (Wynants et al., 2019). In this study, they found that yellow mealworms can
remain infected for more than a week once infected with Salmonella. That being said, with the
presence of larvae in the wheat bran they did observe a reduction of Salmonella, with numbers low
enough (2 log cfu/g) so that the larvae would not be contaminated. However, the fact that

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Salmonella is still present in the larvae is a reason for frequent testing when harvesting the yellow
mealworm.

3.1. Contaminants
A study performed in 2021 looked at the hazards of chemical toxins in different substrates
(Meyer et al., 2021)
. Different contaminants were found, including heavy metals, polyaromatic hydrocarbons,
plant toxins and pesticides. These are difficult chemicals to remove during the rearing process. Some
of these contaminants can be degraded by the insect (for example veterinary drugs and mycotoxins),
while others accumulate with heavy metals like lead, mercury cadmium and arsenic. It is unclear to
what extent these contaminants are harmful. Of other contaminants (e.g., polyaromatic
hydrocarbons, dioxins, and plant toxins) it is not clear whether they accumulate or can be degraded
by the yellow mealworm (van Huis et al., 2021). More studies are needed to provide a clearer risk
assessment.

Although total infectious resistance seems inevitable, the Tenebrio molitor does have certain
defences, either more behavioural or more anatomical in order to fight parasitic infections. A study
from 1995 exposed the T. molitor to the tapeworm Hymenolepis diminuta (a parasite found in
rodents that utilize the yellow mealworm beetle as a host) (Pappas et al., 1995). The first defence
mechanism involves simply avoiding contact with parasites and pathogens. The yellow mealworm
beetles get infected by eating the parasitical eggs when they are fed on the contagious rodent
faeces. Despite that, male beetles that were infected have developed a behaviour in which they
avoid the faeces, therefore reducing their likelihood of getting into contact with the tapeworm
(Shea, 2010). On top of that, female individuals have developed resistance to choosing their mates.
The females are capable of evaluating the immunocompetence of the male individuals via
pheromone signalling, consequently choosing a more immunologically qualified male
(Rantala et al., 2002)
. This enables them to choose a partner that is more resistant to pathogens (and therefore
reduces the likelihood of getting contaminated by their mate) and to pass on a more enhanced
immune system to its offspring (Hamilton & Zuk, 1982) .

4. Yellow mealworm nutrition


Insects are considered sustainable in comparison to other animal-derived foods, since insects have
the ability to recycle organic waste, and require only a little space, water and food
(Bessa et al., 2020; DeFoliart, 1975)
. The yellow mealworm, therefore, is also able to live on food and agricultural
by-products, like broilers’ eggshells, banana peels and watermelon rinds. Currently, the nutrition for
the yellow mealworm consists only of wheat bran (Kim et al., 2017). A study by the FAO showed that
of all the food produced worldwide, about one-third goes to waste (FAO, 2011) . However, even
though it is considered ‘waste’, it can still contain high-quality nutrients and active compounds.
Therefore, using these by-products for yellow mealworm production, the by-products become
quality biomass instead of waste. When agricultural by-products come from local producers, the use
of by-products is not only very cost-effective but also very sustainable. Even though a lot of different
food and agricultural by-product can be used for yellow mealworm nutrition, they can have different
effects on the growth rate and nutritional profile of the yellow mealworm (Yan Loh et al., 2018) .

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4.1. Influence of nutrition on growth performance
In the optimization of yellow mealworm production, nutrition has an important role. Yan Loh et al.,
2018, evaluated the growth performance and nutritional profile of the yellow mealworm based on
four different diets (diet 1: rinds of watermelon, diet 2: broilers’ eggshells, diet 3: banana peels, diet
4: a mixture of diets 1, 2 and 3 with a ratio of 1:1:1) and a control diet of commercial white bread.
The growth performance was based on the following criteria: weight and length gain, specific growth
rate and feed conversion ratio and efficiency. The specific growth rate was calculated by the
difference in weight, divided by the total feeding days, times a hundred, the feed conversion ratio
was calculated by the weight of diet divided by the weight of yellow mealworms gained, and the
feed conversion efficiency was calculated by the weight of yellow mealworms gained, divided by the
weight of diet, times a hundred. The study resulted that diet 1 (rinds of watermelon) has the highest
growth rate and the highest feed conversion efficiency in comparison to diets 2, 3 and 4. Diet 1 also
scored better in terms of nutrients, like crude protein, moisture, and crude fibre. Next to
watermelon, also banana peel wastes (diet 3) showed good results. The banana waste resulted to
have the highest survival rate (see figure 1). Therefore, in this study, it is stated that using both
watermelon and banana wastes as a diet for the yellow mealworm enhances growth and nutritional
fortification (Yan Loh et al., 2018) .

Figure 1 Survival rate (%) of the yellow mealworm fed on four different diets (Bordiean et al., 2022)

Another study researched 20 different ingredients in different ratios for the diet of the yellow
mealworm. The ingredients included by-products like potato flour, wheat bran, rice bran, soybean,
cotton, oat and others. They took eight combinations of the ingredients based on the protein, lipid
and carbohydrate content. The lipid intake should be between 0.10 and 0.03, carbohydrate between
0.75 and 0.65 and protein between 0.25 and 0.2. When these ranges of macronutrients are changed,
it resulted in decreased larval growth (Morales-Ramos & Rojas, 2015). The ingredients that resulted
in increased biomass production are potato, cabbage, rice (and defatted rice) bran, wheat bran,
corn, canola meal, and sunflower meal. Other ingredients that have a positive effect on the growth
rate are a diet with rapeseed meal, and rapeseed cake (Bordiean et al., 2022).

Another possibility for yellow mealworm nutrition is the use of waste products from breweries and
distilleries. 85% of the waste from breweries is brewer’s spent grain (Mussatto et al., 2006). This
waste product is high in cellulosic and non-cellulosic polysaccharides. Because of this, these waste
products are already used for animal feed. The other waste product, coming from distilleries, is
distillers dried grain, which contains mainly crude proteins, crude fat, and roughage from fungal
fermentation. Larvae fed with 50% brewer’s spent grain or 50% distillers dried grain, mixed with 50%

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wheat bran have a higher larval and pupal weight, larval survival, and development than larvae fed
with only wheat bran (Kim et al., 2017).

Even though there can be a difference in growth performance and survival rate, a lot of food and
agricultural by-products can be used, as long as the macronutrients in the diet are within the right
ranges. It would be beneficial for insect producers to use local by-products for the production of
insects. In the Netherlands, agricultural waste can come from e.g. potatoes, wheat, onions, sugar
beetle and flower bulbs production, but also waste from breweries and distilleries
(Kim et al., 2017; Yuan, 2019)
. Because these by-products are local, it is not only cost-effective to use these by-
products, but it also improves local waste management.

4.2. Influence of nutrition on the nutritional composition


The nutritional composition of the yellow mealworm is similar to the nutritional composition of
other animal-derived products regarding the high protein levels. Just like other animal-derived
products, the yellow mealworm also has complete proteins. The nutritional composition of the
yellow mealworm varies between different life cycle stages (Toviho & Bársony, 2022) . Dried yellow
mealworm larvae have the following nutritional composition: ±56% protein, ±29% fat, ±6%
carbohydrates, ±5% dietary fibre and an energy value of 2150 kJ/100g dried yellow mealworm
(Turck et al., 2021)
. Not only does the nutritional composition differ between different life cycles but also
rearing conditions and the diet of the yellow mealworm affect the nutritional composition
(Toviho & Bársony, 2022)
.

The study mentioned in chapter 3.1., also investigated the effect of feed on the nutritional profiles
(see table 1). The study showed that yellow mealworms fed on rinds of watermelon gave the highest
crude protein content, in comparison with banana peels, which showed the lowest crude protein
content. However, the difference is very small. This is because the protein content in the yellow
mealworm is not affected by the protein content in the diet (Bordiean et al., 2022). In terms of the
crude fat content of the yellow mealworm, both the yellow mealworms fed with banana peels and
white bread showed the highest content. However, just like the crude protein content, there is only
a slight difference between the different diets (Yan Loh et al., 2018)
. The reason for the slight
difference could be that with lower protein content in the diet, the fat content increases of yellow
mealworms, especially the unsaturated fatty acid content. Unlike protein and fat content, fatty acid
composition can be influenced by nutrition (Bordiean et al., 2022).
Table 1 Nutritional compositions of yellow mealworms (Yan Loh et al., 2018)

Yellow Proximate Compositions (%)


mealworms T. Crude Protein Moisture Ash Crude Fat Crude Fibre Nitrogen-free
molitor Fed on Extract (NFE)
Different Diets
Control diet: 41.51±4.55 8.06±0.55 1.87±0.49 40.13±1.63 6.75±0.6 1.69±4.79
White Bread
Diet 1: 43.38±2.71 9.74±0.23 4.40±0.22 32.84±4.14 6.48±1.40 3.17±5.80
Watermelon
rinds
Diet 2: Broilers’ 42.49±2.28 9.55±0.35 3.44±0.44 33.57±3.69 8.73±0.05 2.23±6.02
eggshells
Diet 3: Banana 38.53±1.43 8.13±0.12 2.48±0.88 40.13±4.66 6.27±0.09 4.46±5.30
peels
Diet 4: Mixture 42.78±1.89 8.48±0.38 3.62±0.24 33.92±2.05 8.18±0.35 3.02±1.07
of diets 1, 2 and
3

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A study by Kim et al. (2017) (see chapter 4.1.) looked at the use of brewer’s spent grain and distillers'
dried grain in comparison to wheat bran. The larvae fed on 100% wheat bran, or 100% distillers dried
grain showed the highest crude protein content, but the amino acid and fatty acid content were very
similar between the different diets (Kim et al., 2017).

Another study also investigated the nutrient composition of yellow mealworm larvae on different
diets. In this study, they also used white wheat bran as a control. The tested diets were barley, oats,
a mixture of barley and oats whole grain (1:1), buckwheat, and a mixture of barley and oat sprouts
(1:1). Next to the nutrient composition, also the mineral content and the fatty acid profile were
determined. The study resulted that wheat bran showed a high protein content in the larvae (71% of
the yellow mealworm powder) and the lowest fat content (7%). However, a linear regression
analysis showed that there is a weak correlation between the diets and the larval protein content
(Jaji et al., 2022) .

Overall, it can be stated that the nutrition of yellow mealworms does not influence the nutritional
composition of the yellow mealworm larvae. Only when a higher fat content is desired, it can be
decided to use a diet that is higher in protein, because this increases the fat content. The studies of
Kim et al. (2017) and Jajić et al. (2022), both show good results for a diet with wheat bran. Larvae
fed on wheat bran are high in protein. Therefore, in terms of nutrition, it is best to use wheat bran
for the nutrition of the yellow mealworm larvae.

5. Farming techniques
Originally, insects were harvested from the wild. In many regions of the world, this is still the case,
especially in the tropics, but the lack of availability of easily harvestable insects from nature is a
problem. Harvesting from nature often harms nature, for example, trees are cut down. Therefore,
industrial farming is a good option. It is easy to domesticate insects. First, they are easy to rear in
small spaces and containers. Secondly, the life cycle of insects is short. The third reason is that they
can eat waste from agriculture. Finally, it is doable to farm in urban as well as rural areas and short-
term financial returns are possible.

The yellow mealworm is able to grow on a lot of different substrates, since not all substrates are the
same, supplements can be added to optimise the substrate further, for example on development
time, larval survival, and efficiency (Morales-Ramos et al., 2011). These could be vegetables which
contain vitamins, essential fatty acids and sterols (van Broekhoven et al., 2015). To increase protein,
which contributes to survival and shortens development time, high protein by-products as
supplements are a good option to keep prices low. Increasing growth rate and pupal can be achieved
by increasing the calorie supply. The other side of this is that it will reduce the survival rate
(van Broekhoven et al., 2015)
.

The yellow mealworm can take up the water it needs from the air, they have the ability to take up
water dissolved in sub saturated air at a relative humidity of 90% (Holmes et al., 2012), but it will be
able to grow at a relative humidity of 75% (Holmes et al., 2012). Extra water supply is not needed
but keeping high humidity in climate rooms can be expensive.

In insect mass rearing, productivity is very important. Production is a balance between


mechanization, automation, labour, investment, and productivity (Cortes Ortiz et al., 2016).
Technology is an important factor as well since it can improve feeding, watering, handling,
harvesting, cleaning, processing, packaging, and storage a lot. For now, mechanisation does not play
such a big role for two reasons: insect products are already overpriced and often can be of low or
widely varying quality.

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In insect rearing it is important to use space efficiently, of course, it depends on the type of insect
and what type of set-up is suitable. If insects can jump and crawl vertically, three-dimensional spaces
like egg crates and cardboard dividers can be used to allow greater density to rear the insects.
Insects like the yellow mealworm will not be able to crawl vertically or jump and so a two-
dimensional flat surface will be sufficient. This is an advantage since it will allow the stacking of more
different layers (Cortes Ortiz et al., 2016). Climate control and air conditioning are very important in
the rooms.

Feed is supplied by serve-in-time if the feed is perishable, for example, high-water content products.
When the feed is not very perishable, i.e., containing low water content, especially the amount
served is important since it should be eaten entirely before it will spoil (Cortes Ortiz et al., 2016).

Specifically for the yellow mealworm T. molitor, it is possible to distinguish between conventional
yellow mealworm production and more modern ways of production. In conventional production
systems, trays are used, with a standard size of about 65 L x 50 W x 15 H cm
(Cortes Ortiz et al., 2016)
, they are deep enough to prevent insects from escaping. They are placed in multilevel racks. In
the conventional farming system, trays are closed, and frass will accumulate, which has the
disadvantage that for example mites can proliferate (Cortes Ortiz et al., 2016)

Figure 2 conventional yellow mealworm tray. A: larvae, B: adults (Cortes Ortiz et al., 2016)

In the modern system, the bottoms are replaced with open screens, like a sieve, which can let frass
particles through so they will not accumulate in the trays. Another advantage is that younger insects
will fall through and so can be separated from the bigger older ones.

Different types of feeds can be used to farm insects. One of the options is the liquid and semisolid
feeds. To be concrete, direct liquid feeds are not directly produced. The liquid feeds consist of
dissolved particles. Some liquid products will be dried, for example, in a spray dryer, mixed and
dissolved later to create a liquid feed. Of course, it is important for the particles used for the liquid
feed they are water-soluble.

In the semisolid feed, the water content is usually above 15%, but a determining factor is water
activity, which ranges between 0.65 and 0.85 (Cortes Ortiz et al., 2016). The water activity is
important for the shelf life of the feed and microbial growth and fungal degradation. The feed is
softer than solid feed, which is an advantage for the insects since they chew and bite on the
fragments.

Finally, there is the solid feed. One way to get a solid feed is by mixing and grinding raw materials to
get a feed mash. Mixing and grinding are done to get the correct proportions of insect nutrition. No
heat treatment or compaction treatments are done and so the energy need is lower when compared
to pellet and extruded feed (Thomas et al., 1997, 1998; Thomas & van der Poel, 1996). Another way
to get a solid feed is by pelleting, which is the most common way. In the pelletizer, raw materials are
dosed by a recipe and shaped pellets are obtained (Thomas et al., 1997, 1998; Thomas & van der Poel, 1996)

10
. A third way is to do it by extrusion, fine grinding is performed in combination with
mixing and preconditioning with for example steam. A large advantage of the treatments in the
extruder is that anti-nutrients can be inactivated and that the feed is sterilized (Guy, 2001). Finally, a
solid feed can be presented in the form of a coacervate. In a coacervate, the outside is solid, and the
inside is a nutritious liquid. The insect can pierce the coacervate and access the nutrients.

6. HACCP in insect farming


To ensure insect rearing is done safely for both insects and humans, HACCP measures should be
taken in the process chain. Generally, a HACCP plan consists of twelve parts. Five Primary tasks and
seven principles. The 12 tasks consist of 1. Assembling the HACCP team. 2. Describe the product. 3.
Identify the intended use. 4. Construct a flow diagram. 5. On-site verification of flow diagram. 6.
Conduct a hazard analysis. 7. Determine Critical Control Points. 8. Establish critical limits for each
CCP. 9. Establish a monitoring system for each CCP. 10. Establish corrective actions. Establish
verification procedures and finally 12. Establish documentation and record keeping.

In the case of the yellow mealworm, the product (task 2) will most probably be the whole insect or a
powder. In task four the flow chart is designed; an example was presented by (Kooh et al., 2020).
Furthermore, the potential hazards were mentioned by (). these are C. botulinum, Cronobacter spp.,
L. monocytogenes, Salmonella spp., B. cereus and C. Perfringens, S. aureus and STEC. To restrict the
microorganisms, it is important to set up Critical Control Point to enforce processing is done carefully
and Good Hygienic Practices are performed.

Below the different bacteria will be outlined.

C. botulinum is known to be heat resistant and to be able to grow anaerobically. It can cause
botulism is not common but could be fatal (WHO, 2018a). In fresh insects, C. botulinum was found in
living insects and may be present in dried insects, although the dry environment will inhibit growth.
Spores may be present too (Norberg et al., 2012; Stoops et al., 2016).

Cronobacter spp. has shown to be very resistant to processing and can survive in dry substances like
infant formula, therefore it is reasonable that it will be able to survive in insect powders too
(Norberg et al., 2012).

Listeria monocytogenes come from the soil and are very resistant (WHO, 2018b). It can grow even at
low temperatures, but slowly. Listeriosis, caused by the bacterium, is a severe foodborne disease.
Listeria is not commonly found in insects (Garofalo et al., 2017).

Salmonella spp. is a gut bacterium and can survive in faecal material (ANSES, 2020a) . Salmonellosis is
not severe, but it could be. The occurrence is large. In processed insects, Salmonella is not found
often, but it is found in I am living insects and since it can survive in substrates, it is a microbe to
consider when setting up a HACCP plan.

Bacillus cereus is a microbe found frequently in edible insects and insect-based products
(Garofalo et al., 2019)
It was found that spores can survive in yellow mealworm powders and that they can
proliferate when rehydrated. The Bacillus cereus comes from the soil and is resistant to processing
and so is a major concern (Fasolato et al., 2018)

Clostridium perfringens originate from water, soil, sewage, dust and the human and animal gut
(ANSES, 2020a) . It produces toxins, which can cause illness. Low levels of C. perfringens are found in
processed insects and so need attention.

11
S. aureus occurs a lot in nature and lives on a human and animal skin. When handled and processed,
insects can be spoiled with S. aureus (Marshall et al., 2016). S. aureus is sensitive to heat, but when
processed, the microbe can produce a toxin which is resistant to heat, and freezing and drying
(Marshall et al., 2016) and is detected in fresh edible insect species, including the yellow mealworm
(Stoops et al., 2016). In dry environments, like insect powders, it will grow as well since it is resistant
to low water activity (Kooh et al., 2020).

Finally, the STEC (Shiga-toxin-producing E. coli) is a hazard in insect processing. It is found in the
intestines of warm-blooded animals (ANSES, 2020b) and can cause foodborne illnesses. At the first
sight, it does not seem to be a hazard, but when E. coli is present in the substrate, it can be taken up
by the insect. This may be the case in ruminant-based feed (Kooh et al., 2020)if it is present in
rearing water or by contamination in the process.

After the determination of the hazards, it is important to decide how the hazard can be controlled,
and how this can be monitored by critical control points. Controlling microbial hazards can be done
in several ways, and in combination, they will be stronger. Some microorganisms are, as described
above, sensitive to heat. In that case, it is important heating is performed during the process, and for
a sufficient time, at a sufficient temperature. Monitoring of temperature during the heating steps is
important because when heated insufficiently, the number of microbes may not be lowered enough
and will be able to grow out fast. How successful the decrease of the microbial load is, depends on
the initial load of microbes present as well.

Table 2 log CFU/g decrease by different processes (Kooh et al., 2020)

As shown in the table above, for some microbes heating is very efficient, but for others it is not.

For species which are resistant to heat, and so will not be killed during heat treatment, it is
important that it is not introduced in the first place. Preventing a microbe is introduced can be done
by monitoring the substrate consumed by the insect, does it contain for example Bacillus cereus or
not, and whether is it in significant amounts. Another way to prevent introduction is by carefully

12
handling the people in the factory. For example, E. coli bacteria are found on human skin and so can
enter the product when touched. If the manufacturers wash their hands, disinfect, wear gloves etc.
introduction of E. coli can be prevented. Product features are important as well to prevent the
growth of microbes. A whole product high in water content will be a good substrate to grow on for
quite some microbes, while a powder will cancel out already some microbes, or at least make it
difficult for them to grow. Another way to inhibit the growth of microorganisms is by cooling the
products.

7. Legislation
The European market can place Novel ingredients (Insects and derived ingredients) in the market by
writing an application to European Commission, the safety regulation by (the European Food Safety
Authority) and the favorable votes given by European member states. The application must be
granted by the following authorities before. So far, dried yellow mealworm (as whole and powder),
frozen, dried, and powder forms of Locusta migratoria, Acheta domesticus and Tenebrio Molitor (in
frozen, dried, and powder forms) have been authorized for human consumption in the EU. The
following products are authorized to be used in the European market: dried yellow mealworm
(whole and powder), freeze-dried and powder form of Locusta Migratoria, Acheta domesticus, and
yellow mealworm (Frozen, dried, and powder form) as a source of human Consumption. According
to IPFF, EU decision-makers have also established restrictions on the feed which may be given to
‘farmed animals’ – i.e. animals that are kept for the production of food, feed, or other derived
products (e.g. wool or hides). These restrictions also apply to insects intended for human
consumption or animal feed use. According to European animal Health Law Regulation, No
(2016/429) on transmissible animal diseases insects are prohibited to be fed on animal-derived
products but may rely on vegetal waste as a source of a substrate (IPIFF, 2020) . But under certain
exceptions, farmed insects can be fed with honey, milk, and blood from non-ruminant animals etc.
IPIFF in the EU legislation also complies with the fact that insect producers must follow the general
rules and regulations for General Food law (Regulation No 178/2002) and the ‘Hygiene Package
(Regulation No 852/2004) and regulation No (183/2005).

7.1. Amendment of Name


The Company BV Insect (Protix Company) had requested the European Commission to be given the
authority to place Tenebrio molitor in the Market as whole and ground yellow mealworms as a Novel
food. Under article 26 of European Legislation 2015/2283, they requested for data protection act on
the application as well. The European Commission under article 10(3), of European Legislation
2015/2283 requested the EFSA to give its opinion on whether the Tenebrio molitor larva in the
ground form and whole form is safe to consume. The target population was counted on General
Population excluding infants and Young Children.

EFSA (European Food Safety and Authority) amended a few changes to the words “whole and
grounded” and included the word “frozen and dried formulation”. The term “mealworm” is generic
and does not exclusively refer to Tenebrio molitor larvae therefore it should be replaced by “Yellow
mealworm”.

7.2. Insects as food


Since 1997 Novel Food regulation insects were falling under the category of “Consisting of or
isolated from plant and food ingredients isolated from animals, except for foods and food
ingredients obtained by traditional propagating and breeding practices and having a history of safe
use”. This old regulation of 258/97 was later modified to 2015/2283 due to interference from the
European Court of Justice, which revealed that whole insects did not fall under the category of

13
258/97 (Delgado et al., 2022). Due to uncertainty in regulatory affairs in the European Union
regarding the rearing or farming of whole insects or production of food containing insects and
import of the insects, updated Novel Food regulation No 2015/2283 was adopted and came into
force on January 1st, 2018 (Delgado et al., 2022).

The new food regulation follows two paths for its authorization procedure.

1. A simplified notification procedure, where the applicant had to show the insect or part of
food follows a “Traditional foods” method, where the diet had been used for at least 25
years in a non-EU country and had a history of safe use. The diet followed a substantial
process and had been accepted by a large number of consumers.
2. The general application procedure is time taking as it requires the safety assessment of the
European Food safety authority.

7.3. Yellow mealworm as feed


The Commission had put a control on the use of PAP (Processed Animal Protein ) according to EU
regulation 893/2017 which is derived from seven insects (among others the Hermetia illucens,
Tenebrio molitor, Alphitobius diapers). Based on the EU regulation (68/2013) and (1009/2009) frozen
and dried whole insects could be used as feed for ruminant animals but using a whole insect as feed
is dependent on national regulations and laws of other European countries (Moruzzo et al., 2021).
The Processed animal protein (PAP) from insects was still put under restriction being used by the EU
due to a major outbreak of Transmissible Spongiform Encephalopathies in 2000 (Reg EC 999/2001).
Rather the use of PAPs (Processed animal protein) was recently extended to be used on Monogastric
animals (poultry, swine ) by European authorities.

7.4. Insect welfare


Insects were not given a place in the European animal welfare directive (98/58/EC) for animal
farming as they were invertebrates. Insects were put out of the regulation on transports (1/2005)
and regulation (1099/2099) on slaughtering as they were invertebrates. The invertebrates are kept
free from all comforts that do not allow them an expression of normal behaviour
. (Lähteenmäki-Uutela & Grmelová, 2016)
As most yellow mealworms have the tendency of cluttering, they require
proper space for expressing their cognitive capacities as well. Insect farmers should not keep the
insect in hunger, injury, disease, fear, or thirst for their profit. The food and Agriculture Organisation
(FAO) also believe that in order to reduce the pain and suffering in insects, they should be killed
under proper techniques, which follow freezing or instantaneous techniques such as shredding.

7.5. Labelling and controls


Insect foods are kept out of specific marketing rules as well. Novel Foods had to follow the general
information requirements laid down in the regulation (1169/2011). The label must carry the specific
name of the insect, the quantity used, any risk of allergic reaction involved, pictorial name, notice,
and label. Special labelling requirements with regulation (EU) No. 2021/882 and 2021/1975 for
authorization of dried Tenebrio molitor larvae and frozen, dried, powder forms of Locusta migratoria
larvae had been used (Delgado et al., 2022). There are few commissions set up in European Union to
regulate the entry of Animal-based food including insects into the European market.

Commission delegated Regulation (EU) No. 2019/625: It contains the only available definition of
insects as food in a legal document, which says insects are foods “food consisting of, isolated from,
or produced from insects or their parts including any life stadia of insects intended for human
consumption which are, when applicable, authorized in accordance with regulation (EU)2015/2283.

14
Commission Implementing Regulation (EU) No.2020/2235: Annex III contains the official certificate
model for the entry of insects proposed for human consumption into the European Union.

Commission Implementing Regulation (EU) No. 2021/405: In Annex XV of this regulation, the list of
third countries authorized to enter the European Union was Considered. The list includes Canada,
Switzerland, South Korea, Vietnam, Thailand, and the UK was added on 31st August 2021. These
Countries were given the authority to bring insects into EU markets that are beneficial for human
consumption.

Commission Implementing Regulation (EU) No. 2021/632: According to this regulation live insects
are included in the list of “animals, products of animal origin, germinal products, animal by-products,
and derived products, composite products and hay and straw that are subject to official controls at
border control pests in accordance with official controls regulation.”

7.6. Authorization of Insects as a Food in Europe according to regulation EC


(2015/2283)
In January 2021, dried Tenebrio Molitor larva had been the approved as the first insect to be used in
European Union, which became valid from June 2021. Following it, dried and frozen Migratory
Locust came into effect into the European market in July 2021. Subsequently, in the year 2022 four
insect Novel foods were given the right to own the market in European Union. Firstly, it goes for
frozen, dried and powder yellow meal worm (Tenebrio Molitor) (28th February,2022), Secondly dried,
ground and frozen house cricket (Acheta domesticus) (2nd March 2022) thirdly partially defatted
house Cricket (May 2022) and finally 6th opinion goes for Frozen and freeze-dried formulation of
lesser mealworm (Alphitobius Diaperinus) (IPIFF, 2021) .

As of now, six authorisations had been approved by the European Commission.

7.7. Insect legislation in other countries


7.7.1. North America (USA/CANADA)
The permission to use insects in the diet was regulated by FDA and came under (Food Drug and
cosmetics act (United States Code, Title 21) The act allows the food to be free from filthy pathogens
and must be produced, stored, and packaged in a safe environment. Insects raised for humans must
follow good manufacturing practices (cGMP,21CFR110. If an insect (in this case the Tenebrio molitor)
could be used as an ingredient in food, it should be recognized by GRAS (Generally Recognised as
Safe) and (FAP) Food additive petition to be used as a parallel process of compliance. FAP is
managed by Company, whereas GRAS is self-affirmed. GRAS must be reviewed by FDA for further
approval. Some Food Companies Consider GRAS to be low-cost and a quick process to enter the
market (Lähteenmäki-Uutela et al., 2021)

According to Canadian regulation, the novel foods must be notified to Health Canada and should be
assessed for nutritional adequacy and safety under the regulation (Canada Gazette part II, Division
28: Novel Foods, October 27, 1999. Novel Food Claims to be not used in history and had never been
in the history of being used in the ongoing diet, nor been notified by Health Canada before as well.
In that context, Cricket has never been considered a novel food in Canada but had been used for a
very long time (Lähteenmäki-Uutela et al., 2021). Only Black soldier larvae are given the authority to
be fed to broiler chickens, poultry, geese, Turkey, and Pitala,.as approved by the Canadian Food
inspection agency. Yellow mealworms, Black soldier fly larvae, and Silkworm pupa had been
approved to be used as Pet foods in Canada.

15
7.7.2. Australia and New Zealand
The insect protein Association of Australia (IPAA) has formulated guidelines for its members who are
involved in insect farming. Insect Food is regulated under Standard 1.5.1 of the Food Standard Code
as a category of Novel Food. Some of the groups of insects have been traditionally used in Australia
for a very long time and do not require the tag of Novel to it. The following insect is as follows.

1. Super Yellow mealworm (Zophobas morio)


2. House Cricket (A. domesticus)
3. Yellow mealworm beetle (T. Molitor)

When a novel Food had to be introduced to the market, it requires a premarket assessment from
FSNAZ (Food Standard Australia and New Zealand). Under any circumstances, if the novel food is not
listed in the Standards, the applicant might write an application to FSNAZ citing the matter. FSNAZ
has the right to permit the applicant to be accepted onto the list, only after the pre-market
assessment. In order to Import novel food to the Australian market, the author must abide by the
‘Food Standards Code’ of the Department of Agriculture, and the novel foods are authorized under
the “Food Control act 1992”, “And Biosecurity act 2015”. Feed Ingredients and additive suppliers in
Australia are represented by Feed Ingredients and Additives Association Australia (FIAAA). This
organization regulates its industry via the Australia New Zealand Code of practice for Animal Feed
Ingredients and Additive Suppliers.

7.7.3. Asia
In Japan, Novel Foods do not come under the pre-market authorization, while novel additives do.
Food safety is governed by the Ministry of Health, safety, and welfare, while for animal feed Ministry
of Agriculture, Forestry, and Fisheries have set the prescribed limits for residues, metal
contaminants, and mycotoxins (Lähteenmäki-Uutela et al., 2021). The ministry had assured the
safety and Quality assurance of the feed to be used. Thailand had set the regulations to be followed
for farms, where insect farming is to be done. Following the regulations, it had set itself as the
world’s biggest Cricket producer. The standard for Cricket farming comes under (Good Agricultural
Practices for cricket farm, Thai Agricultural Standard 8202-2017).

16
8. Discussion
A lot of agricultural / food by-products are suitable for yellow mealworm nutrition, however, not all
the by-products are researched on larval growth performance and nutritional composition. The
products that do show a positive effect on the growth performance are e.g., banana peels and
potatoes, and for nutrient composition, wheat bran. To make insect farming and consumption
cheaper, a more efficient process is needed. For example, in the way of mechanization and further
optimization of the process. More studies assessing the efficiency of the mechanization are needed
in the future for a more profitable and circular insect rearing system.

Regarding insect diseases, to a certain extent these can be prevented by strict regulation of
temperature during the rearing process, however more studies are needed on the prevention of
certain insect pathogens. More information also needs to be provided about the accumulation of
certain contaminants like heavy metals, and to what extent it affects the well-being of the insect. On
the other hand, the question can be asked if it is ethical to rear animals in the way it is done. About
the perception of the yellow mealworm is not too much known, so more research should be done on
this.

Different Countries has their own perspective of accepting insect as a friend or foe. Countries like
China, Japan had been consuming insect for around 2000 years of history, but it took around 1997 to
be approved as a Novel food by European Commission. The regulation and legislation were still
amended in 2015 keeping in mind uncertainty in regulatory affairs and the interference of the
European Court of justice. With the new regulation introduced, the Company applying for license on
Insect food has to wait for approximately one year to be approved by the European Commission and
EFSA (European Food and Safety Authority). Once granted the company would have monopoly in the
product for almost 5 years. European legislation. European delegate Commission had been set up to
keep an control on laws and regulation related to entry of insect foods in the market and import and
export of insect foods in the European Commission .Recently in the year 2021,2022 six insect foods
were given the authority to be used in European market and insect feed could be given as a diet for
monogastric animals like (pig, poultry). The Legislation Covers every aspect of safety and Nutritional
labelling but it still has to put forward laws for the welfare of the insects.

17
9. Conclusion
For insect producers, it is beneficial to use local food and agricultural by-products since it’s cost-
effective and sustainable (waste management). It is important to feed the yellow mealworms a diet
with macronutrients between the ranges of 0.10 and 0.03 for lipids, 0.75 and 0.65 for carbohydrates
and 0.25 and 0.2 for protein, to have high growth performance and a high survival rate.
Furthermore, wheat bran is known to give the highest protein content in yellow mealworm larvae.

Regarding infections, the Tenebrio Molitor can be infected due to abiotic factors (like temperature
and insect rearing density) and biotic factors like parasites, entomopathogenic fungi, and viruses.

The yellow mealworm can be reared in crates. They can be stacked on top of each other and take
less space than for other species. To feed the yellow mealworm, serving in time is used to prevent
the substrate from spoiling. The yellow mealworm will take up water from the air.

As a conclusion about the HACCP of the yellow mealworm it is important to combine process steps
that can reduce the hazards in the yellow mealworm to a safe level. Around 2000 edible insects are
available till now and we are expecting to increase the research development and pre market
authorization for these available insect as well .

18
10. References
ANSES. (2020a). Data sheet on Foodborne Biological Hazards - Salmonella spp.
https://www.anses.fr/en/system/files/MIC2011sa0057FiEN.pdf

ANSES. (2020b, October 22). Data Sheet on Foodborne Biological Hazards - Enterohaemorrhagic E. coli
(EHEC). https://www.anses.fr/fr/system/files/MIC2011sa0058FiEN.pdf

Bessa, L. W., Pieterse, E., Sigge, G., & Hoffman, L. C. (2020). Insects as human food; from farm to fork.
Journal of the Science of Food and Agriculture, 100(14), 5017–5022.
https://doi.org/10.1002/jsfa.8860

Bordiean, A., Krzyżaniak, M., Aljewicz, M., & Stolarski, M. J. (2022). Influence of Different Diets on Growth
and Nutritional Composition of Yellow Mealworm. Foods, 11(19), 3075.
https://doi.org/10.3390/foods11193075

Cortes Ortiz, J. A., Ruiz, A. T., Morales-Ramos, J. A., Thomas, M., Rojas, M. G., Tomberlin, J. K., Yi, L., Han,
R., Giroud, L., & Jullien, R. L. (2016). Insect Mass Production Technologies. In Insects as Sustainable
Food Ingredients (pp. 153–201). Elsevier. https://doi.org/10.1016/B978-0-12-802856-8.00006-5

DeFoliart, G. R. (1975). Insects as a Source of Protein. Bulletin of the Entomological Society of America,
21(3), 161–164. https://doi.org/10.1093/besa/21.3.161

Delgado, L., Garino, C., Moreno, F. J., Zagon, J., & Broll, H. (2022). Sustainable Food Systems: EU
Regulatory Framework and Contribution of Insects to the Farm-To-Fork Strategy. Food Reviews
International, 1–22. https://doi.org/10.1080/87559129.2022.2130354

Deruytter, D., Coudron, C. L., & Teerlinck, S. (2019). Influence of crate size, oviposition time, number of
adults and cannibalism on the reproduction of Tenebrio molitor. Journal of Insects as Food and Feed,
5(4), 247–255. https://doi.org/10.3920/JIFF2019.0018

EFSA Scientific Committee. (2015). Risk profile related to production and consumption of insects as food
and feed. The EFSA Journal, 13, 4256.

FAO. (2011). Global Food Losses and Food Waste - Extent, causes and prevention. In SAVE FOOD: An
Initiative on Food Loss and Waste Reduction . FAO.

Fasolato, L., Cardazzo, B., Carraro, L., Fontana, F., Novelli, E., & Balzan, S. (2018). Edible processed insects
from e-commerce: Food safety with a focus on the Bacillus cereus group. Food Microbiology, 76,
296–303. https://doi.org/10.1016/j.fm.2018.06.008

Garofalo, C., Milanović, V., Cardinali, F., Aquilanti, L., Clementi, F., & Osimani, A. (2019). Current
knowledge on the microbiota of edible insects intended for human consumption: A state-of-the-art
review. Food Research International, 125, 108527. https://doi.org/10.1016/j.foodres.2019.108527

Garofalo, C., Osimani, A., Milanović, V., Taccari, M., Cardinali, F., Aquilanti, L., Riolo, P., Ruschioni, S.,
Isidoro, N., & Clementi, F. (2017). The microbiota of marketed processed edible insects as revealed
by high-throughput sequencing. Food Microbiology, 62, 15–22.
https://doi.org/10.1016/j.fm.2016.09.012

Gkinali, A.-A., Matsakidou, A., Vasileiou, E., & Paraskevopoulou, A. (2022). Potentiality of Tenebrio molitor
larva-based ingredients for the food industry: A review. Trends in Food Science & Technology, 119,
495–507. https://doi.org/10.1016/j.tifs.2021.11.024

19
Guy, R. (2001). Extrusion Cooking: Technologies and Applications. Woodhead Publishing Limited and CRC
Press LLC.

Hamilton, W. D., & Zuk, M. (1982). Heritable True Fitness and Bright Birds: A Role for Parasites? Science,
218(4570), 384–387. https://doi.org/10.1126/science.7123238

Heidari-Parsa, S., Imani, S., Fathipour, Y., Kheiri, F., & Chamani, M. (2018). Determination of yellow
mealworm (Tenebrio molitor) nutritional value as an animal and human food supplementation.
International Academy of Ecology and Environmental Sciences.

Holmes, L. A., Vanlaerhoven, S. L., & Tomberlin, J. K. (2012). Relative Humidity Effects on the Life History
of Hermetia illucens (Diptera: Stratiomyidae). Environmental Entomology, 41(4), 971–978.
https://doi.org/10.1603/EN12054

IPIFF. (2020). Insect farming practices, insects as food and insects as feed. International Platform of Insects
for Food and Feed (IPFF). https://ipiff.org/faqs_2020/

IPIFF. (2021). Insects as novel foods - an overview. International Platform of Insects for Food and Feed
(IPIFF). https://ipiff.org/insects-novel-food-eu-legislation-2/

Jajić, I., Krstović, S., Petrović, M., Urošević, M., Glamočić, D., Samardžić, M., Popović, A., & Guljaš, D.
(2022). Changes in the chemical composition of the yellow mealworm (Tenebrio molitor L.) reared
on different feedstuffs. Journal of Animal and Feed Sciences, 31(2), 191–200.
https://doi.org/10.22358/jafs/147848/2022

Kim, S. Y., Kim, H. G., Yoon, H. J., Lee, K. Y., & Kim, N. J. (2017). Nutritional analysis of alternative feed
ingredients and their effects on the larval growth of Tenebrio molitor (Coleoptera: Tenebrionidae).
Entomological Research, 47(3), 194–202. https://doi.org/10.1111/1748-5967.12236

Kooh, P., Jury, V., Laurent, S., Audiat-Perrin, F., Sanaa, M., Tesson, V., Federighi, M., & Boué, G. (2020).
Control of Biological Hazards in Insect Processing: Application of HACCP Method for Yellow
Mealworm (Tenebrio molitor) Powders. Foods, 9(11), 1528. https://doi.org/10.3390/foods9111528

Lähteenmäki-Uutela, A., & Grmelová, N. (2016). European Law on Insects in Food and Feed. European
Food and Feed Law Review, 11(1), 2–8. https://www.jstor.org/stable/43958606

Lähteenmäki-Uutela, A., Marimuthu, S. B., & Meijer, N. (2021). Regulations on insects as food and feed: a
global comparison. Journal of Insects as Food and Feed, 7(5), 849–856.
https://doi.org/10.3920/JIFF2020.0066

Lecocq, A., Natsopoulou, M. E., Berggreen, I. E., Eilenberg, J., Heckmann, L.-H. L., Nielsen, H. V., Stensvold,
C. R., & Jensen, A. B. (2021). Probiotic properties of an indigenous Pediococcus pentosaceus strain on
Tenebrio molitor larval growth and survival. Journal of Insects as Food and Feed, 7(6), 975–986.
https://doi.org/10.3920/JIFF2020.0156

Maciel-Vergara, G., Jensen, A. B., Lecocq, A., & Eilenberg, J. (2021). Diseases in edible insect rearing
systems. Journal of Insects as Food and Feed, 7(5), 621–638. https://doi.org/10.3920/JIFF2021.0024

Mariod, A. A. (2020). Nutrient Composition of Mealworm (Tenebrio molitor). In African Edible Insects As
Alternative Source of Food, Oil, Protein and Bioactive Components (pp. 275–280). Springer
International Publishing. https://doi.org/10.1007/978-3-030-32952-5_20

20
Marshall, D. L., Dickson, J. S., & Nguyen, N. H. (2016). Ensuring Food Safety in Insect Based Foods:
Mitigating Microbiological and Other Foodborne Hazards. In Insects as Sustainable Food Ingredients
(pp. 223–253). Elsevier. https://doi.org/10.1016/B978-0-12-802856-8.00008-9

Meyer, A. M., Meijer, N., Hoek-van den Hil, E. F., & van der Fels-Klerx, H. J. (2021). Chemical food safety
hazards of insects reared for food and feed. Journal of Insects as Food and Feed, 7(5), 823–831.
https://doi.org/10.3920/JIFF2020.0085

Miglietta, P., de Leo, F., Ruberti, M., & Massari, S. (2015). Mealworms for Food: A Water Footprint
Perspective. Water, 7(11), 6190–6203. https://doi.org/10.3390/w7116190

Morales-Ramos, J. A., & Rojas, M. G. (2015). Effect of Larval Density on Food Utilization Efficiency of
Tenebrio molitor (Coleoptera: Tenebrionidae). Journal of Economic Entomology, 108(5), 2259–2267.
https://doi.org/10.1093/jee/tov208

Morales-Ramos, J. A., Rojas, M. G., Shapiro-Ilan, D. I., & Tedders, W. L. (2011). Self-Selection of Two Diet
Components by Tenebrio molitor (Coleoptera: Tenebrionidae) Larvae and Its Impact on Fitness.
Environmental Entomology, 40(5), 1285–1294. https://doi.org/10.1603/EN10239

Moruzzo, R., Riccioli, F., Espinosa Diaz, S., Secci, C., Poli, G., & Mancini, S. (2021). Mealworm (Tenebrio
molitor): Potential and Challenges to Promote Circular Economy. Animals, 11(9), 2568.
https://doi.org/10.3390/ani11092568

Mussatto, S. I., Dragone, G., & Roberto, I. C. (2006). Brewers’ spent grain: generation, characteristics and
potential applications. Journal of Cereal Science, 43(1), 1–14.
https://doi.org/10.1016/j.jcs.2005.06.001

Noonin, C., Jiravanichpaisal, P., Söderhäll, I., Merino, S., Tomás, J. M., & Söderhäll, K. (2010). Melanization
and Pathogenicity in the Insect, Tenebrio molitor, and the Crustacean, Pacifastacus leniusculus, by
Aeromonas hydrophila AH-3. PLoS ONE, 5(12), e15728.
https://doi.org/10.1371/journal.pone.0015728

Norberg, S., Stanton, C., Ross, R. P., Hill, C., Fitzgerald, G. F., & Cotter, P. D. (2012). Cronobacter spp. in
Powdered Infant Formula. Journal of Food Protection, 75(3), 607–620. https://doi.org/10.4315/0362-
028X.JFP-11-285

NOS. (2021, January 13). EU geeft groen licht voor meelwormcurry en -pasta.
https://nos.nl/artikel/2364258-eu-geeft-groen-licht-voor-meelwormcurry-en-pasta

Pappas, P. W., Marschall, E. A., Morrison, S. E., Durka, G. M., & Daniel, C. S. (1995). Increased coprophagic
activity of the Beetle, Tenebrio molitor, on feces containing eggs of the tapeworm, Hymenolepis
diminuta. International Journal for Parasitology, 25(10), 1179–1184. https://doi.org/10.1016/0020-
7519(95)00051-3

Ramos-Elorduy, J., González, E. A., Hernández, A. R., & Pino, J. M. (2002). Use of <I>Tenebrio
molitor</I> (Coleoptera: Tenebrionidae) to Recycle Organic Wastes and as Feed for Broiler
Chickens. Journal of Economic Entomology, 95(1), 214–220. https://doi.org/10.1603/0022-0493-
95.1.214

Rantala, M. J., Jokinen, I., Kortet, R., Vainikka, A., & Suhonen, J. (2002). Do pheromones reveal male
immunocompetence? Proceedings of the Royal Society of London. Series B: Biological Sciences,
269(1501), 1681–1685. https://doi.org/10.1098/rspb.2002.2056

21
Ravzanaadii, N., Kim, S.-H., Choi, W. H., Hong, S.-J., & Kim, N. J. (2012, September 4). Nutritional Value of
Mealworm, Tenebrio molitor as Food Source. International Journal of Industrial Entomology.

Reeson, A. F., Wilson, K., Gunn, A., Hails, R. S., & Goulson, D. (1998). Baculovirus resistance in the noctuid
Spodoptera exempta is phenotypically plastic and responds to population density. Proceedings of
the Royal Society of London. Series B: Biological Sciences, 265(1407), 1787–1791.
https://doi.org/10.1098/rspb.1998.0503

Shea, J. F. (2010). Do male and female beetles (Tenebrio molitor) respond differently to rat feces
containing eggs from the tapeworm, Hymenolepis diminuta? Natural Science, 02(08), 855–859.
https://doi.org/10.4236/ns.2010.28107

Stoops, J., Crauwels, S., Waud, M., Claes, J., Lievens, B., & van Campenhout, L. (2016). Microbial
community assessment of mealworm larvae ( Tenebrio molitor ) and grasshoppers ( Locusta
migratoria migratorioides ) sold for human consumption. Food Microbiology, 53, 122–127.
https://doi.org/10.1016/j.fm.2015.09.010

Thévenot, A., Rivera, J. L., Wilfart, A., Maillard, F., Hassouna, M., Senga-Kiesse, T., le Féon, S., & Aubin, J.
(2018). Mealworm meal for animal feed: Environmental assessment and sensitivity analysis to guide
future prospects. Journal of Cleaner Production, 170, 1260–1267.
https://doi.org/10.1016/j.jclepro.2017.09.054

Thomas, M., & van der Poel, A. F. B. (1996). Physical quality of pelleted animal feed 1. Criteria for pellet
quality. Animal Feed Science and Technology, 61(1–4), 89–112. https://doi.org/10.1016/0377-
8401(96)00949-2

Thomas, M., van Vliet, T., & van der Poel, A. F. B. (1998). Physical quality of pelleted animal feed 3.
Contribution of feedstuff components. Animal Feed Science and Technology, 70(1–2), 59–78.
https://doi.org/10.1016/S0377-8401(97)00072-2

Thomas, M., van Zuilichem, D. J., & van der Poel, A. F. B. (1997). Physical quality of pelleted animal feed. 2.
contribution of processes and its conditions. Animal Feed Science and Technology, 64(2–4), 173–192.
https://doi.org/10.1016/S0377-8401(96)01058-9

Toviho, O. A., & Bársony, P. (2022). Nutrient Composition and Growth of Yellow Mealworm (Tenebrio
molitor) at Different Ages and Stages of the Life Cycle. Agriculture, 12(11), 1924.
https://doi.org/10.3390/agriculture12111924

Turck, D., Bohn, T., Castenmiller, J., de Henauw, S., Hirsch‐Ernst, K. I., Maciuk, A., Mangelsdorf, I.,
McArdle, H. J., Naska, A., Pelaez, C., Pentieva, K., Siani, A., Thies, F., Tsabouri, S., Vinceti, M.,
Cubadda, F., Frenzel, T., Heinonen, M., Marchelli, R., … Knutsen, H. K. (2021). Safety of frozen and
dried formulations from whole yellow mealworm (Tenebrio molitor larva) as a novel food pursuant
to Regulation (EU) 2015/2283. EFSA Journal, 19(8). https://doi.org/10.2903/j.efsa.2021.6778

van Broekhoven, S., Oonincx, D. G. A. B., van Huis, A., & van Loon, J. J. A. (2015). Growth performance and
feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets
composed of organic by-products. Journal of Insect Physiology, 73, 1–10.
https://doi.org/10.1016/j.jinsphys.2014.12.005

van Huis, A., Rumpold, B. A., van der Fels-Klerx, H. J., & Tomberlin, J. K. (2021). Introducing the special
issue: ‘Advancement of insects as food and feed in a circular economy.’ Journal of Insects as Food
and Feed, 7(5), 495–497. https://doi.org/10.3920/JIFF2021.x004

22
van Huis, A., & Tomberlin, J. K. (2017). Tenebrio molitor Linnaeus, 1758. In Insects as Food and Feed: from
production to consumption . WUR.

van Huis, A., van Itterbeeck, J., Klunder, H., Mertens, E., Halloran, A., Muir, G., & Vantomme, P. (2013).
Edible insects: Future prospects for food and feed security. FAO Forestry Paper.

Vigneron, A., Jehan, C., Rigaud, T., & Moret, Y. (2019a). Immune Defenses of a Beneficial Pest: The
Mealworm Beetle, Tenebrio molitor. Frontiers in Physiology, 10.
https://doi.org/10.3389/fphys.2019.00138

Vigneron, A., Jehan, C., Rigaud, T., & Moret, Y. (2019b). Immune Defenses of a Beneficial Pest: The
Mealworm Beetle, Tenebrio molitor. Frontiers in Physiology, 10.
https://doi.org/10.3389/fphys.2019.00138

Wahome, C. (2022, May 26). What Are The Health Benefits of Mealworms? Nourish.
https://www.webmd.com/diet/health-benefits-mealworms#:~:text=Their%20consumption%20is
%20embraced%20in,%2C%20roasted%2C%20and%20even%20live

Wang, Y., Li, H., Lu, Y., He, W., Wang, C., & Lü, L. (2022). Chemical components in yellow mealworm
(Tenebrio molitor L.) reared with tea powder. Journal of Future Foods, 2(3), 266–269.
https://doi.org/10.1016/j.jfutfo.2022.06.008

WHO. (2018a, January 10). Botulism. https://www.who.int/news-room/fact-sheets/detail/botulism

WHO. (2018b, February 20). Listeriosis. https://www.who.int/news-room/fact-sheets/detail/listeriosis

Wu, R. A., Ding, Q., Yin, L., Chi, X., Sun, N., He, R., Luo, L., Ma, H., & Li, Z. (2020). Comparison of the
nutritional value of mysore thorn borer (Anoplophora chinensis) and mealworm larva (Tenebrio
molitor): Amino acid, fatty acid, and element profiles. Food Chemistry, 323, 126818.
https://doi.org/10.1016/j.foodchem.2020.126818

WUR. (2017, April 1). List of edible insects of the world. https://www.wur.nl/en/research-results/chair-
groups/plant-sciences/laboratory-of-entomology/edible-insects/worldwide-species-list.htm

Wynants, E., Frooninckx, L., van Miert, S., Geeraerd, A., Claes, J., & van Campenhout, L. (2019). Risks
related to the presence of Salmonella sp. during rearing of mealworms (Tenebrio molitor) for food or
feed: Survival in the substrate and transmission to the larvae. Food Control, 100, 227–234.
https://doi.org/10.1016/j.foodcont.2019.01.026

Yan Loh, J., Wei Tan, S., & Song Lai, K. (2018). Effects of Food Wastes on Yellow Mealworm
Tenebriomolitor Larval Nutritional Profiles and Growth Performances. Examines in Marine Biology &
Oceanography, 2(1). https://doi.org/10.31031/EIMBO.2018.02.000530

Yang, Y., Yang, J., Wu, W.-M., Zhao, J., Song, Y., Gao, L., Yang, R., & Jiang, L. (2015). Biodegradation and
Mineralization of Polystyrene by Plastic-Eating Mealworms: Part 1. Chemical and Physical
Characterization and Isotopic Tests. Environmental Science & Technology, 49(20), 12080–12086.
https://doi.org/10.1021/acs.est.5b02661

Yuan, Z. (2019). Agricultural Residues in the Netherlands and Their Role in the Soil Carbon Cycle: Are
Residues Available for Bioenergy?

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