Comp Rev Food Sci Food Safe - 2013 - Spiegel - Safety of Novel Protein Sources Insects Microalgae Seaweed Duckweed and

Safety of Novel Protein Sources (Insects,
Microalgae, Seaweed, Duckweed, and Rapeseed)

and Legislative Aspects for Their Application
in Food and Feed Production
M. van der Spiegel, M.Y. Noordam, and H.J. van der Fels-Klerx
Abstract: Novel protein sources (like insects, algae, duckweed, and rapeseed) are expected to enter the European feed
and food market as replacers for animal-derived proteins. However, food safety aspects of these novel protein sources are
not well-known. The aim of this article is to review the state of the art on the safety of major novel protein sources
for feed and food production, in particular insects, algae (microalgae and seaweed), duckweed, and rapeseed. Potential
hazards for these protein sources are described and EU legislative requirements as regard to food and feed safety are
explained. Potential hazards may include a range of contaminants, like heavy metals, mycotoxins, pesticide residues, as
well as pathogens. Some safety aspects of novel protein sources are intrinsic to the product, but many potential hazards
can also be due to production methods and processing conditions. These aspects should be considered in advance during
product development. European law is unclear on several issues regarding the use of novel protein sources in food and
feed products. For food product applications, the most important question for food producers is whether or not the
product is considered a novel food. One of the major unclarities for feed applications is whether or not products with
insects are considered animal-derived products or not. Due to the unclarities in European law, it is not always clear
which Regulation and maximum levels for contaminants apply. For market introduction, European legislation should be
adjusted and clarified.
Keywords: novel protein sources, food safety, EU legislation, contaminants, pathogens
Introduction consumption, and FAO expects a substantial increase by 2050 if

In response to the Kyoto Protocol on the global climate, the the trend goes on uninterrupted (Boland and others 2013). Sev-
European Union (EU) made agreements on reducing greenhouse eral global developments, such as the increasing demand on animal
gas emissions. Major sources of these gas emissions are cattle breed- products in China and India, necessitates to use animal proteins in
ing and related meat consumption (Steinfeld and others 2006; Van a more responsible manner than currently (Vereijken and Aiking
Beukering and others 2008). 2006).
In the last decades, the global consumption of animal proteins Animal proteins are produced inefficiently. Depending on the
has increased continuously. Between 1950 and 2000, the global animal species and various conditions, 2 to 15 kg plant material is
human population more than doubled from 2.7 to 6 billion peo- needed to produce 1 kg of animal products. Currently, 40% to 50%
ple. Meat production, however, increased by a factor of 5 from of the global grain harvest is used for feed production (Profetas
45 to 233 billion kg per year. For 2050, Food and Agriculture 2008). To reduce the use of area and energy, people should eat less
Organization of the United Nations (FAO) expects a world pop- beef and more pork or chicken, reduce their portions, or change
ulation of 9 billion and meat production of 410 billion kg per the meat portion in the diet by meat substitutes, such as legumes
year (Boland and others 2013; FAO 2006). Animal-derived pro- or eggs (Gerbens-Leenes 2000; Aiking and De Boer 2006). Other
tein accounts currently for almost 40% of humanity’s total protein studies also concluded that reduction of both meat consumption
and production will reduce greenhouse gas emissions (Stehfest and
others 2008; Van Beukering and others 2008).
Novel protein sources (like insects, algae, duckweed, and rape-
MS 20130761 Submitted 6/5/2013, Accepted 7/18/2013. Authors are with RIK-
ILT Wageningen UR, Wageningen Univ. and Research Centre, P.O. Box 230, 6700
seed) are expected to enter the European feed and food market. For
AE Wageningen, the Netherlands. Direct inquiries to author van der Spiegel (E-mail: instance, the Dutch Ministry of Economic Affairs (EZ) supports,
marjolein.vanderspiegel@wur.nl). by the Acceleration agenda “Protein innovations,” various possi-
bilities to make current production and consumption of proteins

C 2013 Institute of Food Technologists®
662 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013 doi: 10.1111/1541-4337.12032
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Safety aspects of novel protein sources . . .
improved by new technologies and valorization of waste streams

dairy, meat, (Stegeman and others 2010; Krijne and Essink 2011).
egg, fish
Another group of protein sources that is currently used for feed
soy, and biofuel products includes rapeseed, algae, grass, duckweed, and
wheat by-products from agricultural processing and waste streams from
legumes, grains, biofuel chains (Stegeman and others 2010). Rapeseed is more or
mushrooms, less ready now for market introduction for food use (Stegeman and
potato, rape seed,
others 2010; Krijne and Essink 2011). The other protein sources
palm
ApplicaƟon
algae, grass,
duckweed,
mentioned are still in early development stages. The same applies
by-products to insect proteins that are now used for petfood and (fish) feed.
insects New processing technologies (such as extraction procedures) and
in vitro meat
valorization of waste streams, in order to apply insect proteins in
feed and food, are being developed (Stegeman and others 2010;
Time to enter market
Krijne and Essink 2011). Processing insect cells opens up new
possibilities for the application of this novel protein source (Verkerk
and others 2007). The major novel protein sources are detailed
Figure 1–Overview of protein sources with respect to time to enter
market and extent of application in food and feed. below.
Insects
more sustainable by modifying the production of animal proteins, Insects consist of many species. Potential insects for applica-
development of new (plant) protein products, and biorefinery and tion in food in the EU are Gryllodus sigillatus and Acheta domesti-
valorization of protein-rich waste streams (Bleker 2012). cus (crickets), Alphitobius diaperinus (lesser mealworm), and Tene-
Currently, research on novel proteins is conducted on the func- brio molitor (yellow mealworm). Potential insects for use in feed
tionality, processing, and industrial application of novel proteins, products in the EU are Hermetia illucens (black soldier fly), lar-
and the valorization of by-products or waste streams obtained in vae of Musca domestica (common housefly), and T. molitor (yellow
other processes. However, food safety aspects of these novel pro- mealworm).
teins are not well-known. Especially the use of waste streams may During the rearing of insects, a metamorphosis occurs from
introduce multiple food safety hazards. The presence of contami- egg via larva and pupa to mature adult. The modification path
nants, antinutritional factors (ANFs), allergens, and accumulation varies depending on the subspecies. Feed used for these insects are,
and modification of substances in protein matrices during process- for example, chicken feed, vegetables, and waste streams. Whole
ing can have effects on public health. insects can be eaten raw, dried, crushed, textured, pulverized, or
The objective of this article is to review the state of the art ground, or they are heated (such as cooked, boiled, fried, roasted,
on the safety of major novel protein sources for feed and food toasted, extruded, and canned) or preserved by freeze-drying or
production, and on EU requirements for their safety. Unclarities to cryovacking after degutting or fasting. Insect proteins can also be
fulfill safety requirements for the introduction of novel proteins on isolated by extraction before use in food products.
the EU market are elucidated. First, novel protein sources will be Most edible insects in non-European countries are harvested
described, as well as the potential hazards for proteins from insects, from the wild (DeFoliart 1995). According to Schabel (2008),
algae (microalgae and seaweed), duckweed, and rapeseed. Second, some insects may be considered as edible in some regions but not
the EU requirements for novel protein sources will be explained in others; some normally safe insects may be unhealthy if they feed
in general and specifically for the selected protein sources. on certain plants or originate from a polluted and pesticide-treated
area; some may be safe for some consumers but less (or not at all)
Novel Proteins for others due to the presence of allergens; and some may require
Major animal protein sources for human consumption include special capture, preparation, storage, or transportation methods to
meat, fish, milk, and eggs. Developments in the production of ani- render and keep them safe (Schabel 2008).
mal protein sources are directed toward the use of cheaper raw ma- The long history of human consumption of insects in non-EU
terials, increased health characteristics, and higher sustainability by countries suggests, with little evidence to the contrary, that insects
using existing and novel protein sources and production methods. harvested for human consumption do not cause any significant
For this purpose, the use of novel protein sources, waste streams of health problems (DeFoliart 1992). Zhou and Han (2006) describe
processing, and by-products of biofuel production are investigated a safety evaluation of silkworm by a series of acute and subacute
(Krijne and Essink 2011). Various novel protein sources can be toxicological tests. Their results indicate that protein of silkworm
used for replacing current animal proteins in feed and food pro- pupae can be generally regarded as safe at a maximum dose of
duction (see Figure 1), but with different estimated time to enter 1.50 g/kg body weight per day in rats (Zhou and Han 2006).
the protein sources on the market. Sirimungkararat and others (2008) reported that consumption of
Current plant protein sources that are widely consumed are processed eri products derived from eri silkmoths was safe in terms
proteins derived from soy, wheat, vegetables, and potatoes. Soy is of the presence of these toxic chemical substances: hydrocyanic
the most important protein source for the production of animal acid, heavy metals (lead, mercury, and cadmium), arsenic, benzoic
proteins. Wheat is the largest group of plant protein sources in acid, and sorbic acid. However, there are no standards for eri foods
the Western diet and is often used for feed products (Krijne and yet, and allowable levels were used that are defined by the Thai
Essink 2011). Community Product Standard (TCPS) for other (nonreported)
Legumes (lupine), grains (rice, maize), mushrooms, and pota- products (Sirimungkararat and others 2008). The U.S. Food and
toes are sources that have already been used in food and feed. Drug Administration (FDA) has prescribed permissible levels of
The availability and functionality of their proteins will be further contamination of food with insect debris (FDA 2011). People are

C 2013 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 663
regularly eating small amounts of insects unconsciously, but no Toxic chemicals are acquired in 2 ways, either by autonomous
serious complications have been observed, with the exception of production of defense chemicals (such as toxins and toxic metabo-
individuals who react allergically (Mitsuhashi 2008). lites) or by sequestering phytochemicals directly from the food
In 2010, the Codex Alimentarius Commission (CAC) reported plant (Duffey 1980; Wirtz 1984; Berenbaum 1993; Blum 1994;
that food safety of edible insects has not been studied extensively, Schabel 2008). Defensive secretions that may be reactive, irritat-
which may be due to the fact that these insects are often treated ing, or toxic include, among many others, carboxylic acids, alco-
as traditional foods of indigenous populations and rarely recog- hols, aldehydes, alkaloids, ketones, esters, lactones, phenols, 1,4-
nized as tradable food items. CAC describes that insects are rich in quinones, hydrocarbons, and steroids. Phytochemicals sequestered
nutrients providing a medium for growth of unwanted microor- by various insects include phenolics, flavin, tannins, terpenoids,
ganisms under certain conditions, especially making uncooked polyacetylenes, alkaloids, cyanogens, glucosinolates, and mimetic
insects susceptible for microbiological hazards unless proper heat amino acids (Wirtz 1984). Some insects may contain chemicals in
treatment or storage conditions are applied. Some people have or concentrations higher than acceptable levels for food consump-
may develop (food) allergies against certain species of insects. Some tion (Yen 2008). For example, arsenic was accumulated in Bogong
insects may require other treatments before they are rendered ed- moth from agricultural sprays, such as the herbicide monosodium
ible (CAC 2010). Insect proteins may display a cross-allergenicity methylarsenate (Green and others 2001), and selenium was ac-
with shrimps and house dust mites (Witteman and others 1994; cumulated in T. molitor (Hogan and Razniak 1991). Food pro-
Leung and others 1996; Reese and others 1999; Houben 2012; cessing can also introduce toxic substances by chemical reactions
Verhoeckx and others 2013). of substrates of insects and other ingredients, such as heterocyclic
Studies on food safety of cultivated European insects are very aromatic amines, acrylamide, chloropropanols, and furans (Dolan
limited. Vijver and others (2003) reported upon the uptake and and others 2010).
accumulation of heavy metals such as cadmium, copper, lead, and Based on these studies on food safety of non-European insects,
zinc from soils by larvae of T. molitor (Vijver and others 2003). food safety issues should be identified and assessed before insects
Zagrobelny and others (2009) described that species of Zygaena can enter the market in Europe. Both chemical and microbiolog-
contained low quantities of cyanogenic glucosides (Zagrobelny ical hazards can be introduced or formed in concentrations that
and others 2009). Goumperis (2012) presented potential hazards may be harmful for public health. Feed for insects (feed, vegetables,
of insects for food and feed application: the presence of pathogens, and waste products) can be contaminated with mycotoxins, natu-
contaminants (such as pesticides, natural toxins, heavy metals, ne- ral toxins, heavy metals, veterinary residues (including antibiotics),
oformed substances due to processing, and veterinary residues), pesticides, and pathogens. Potential hazards of the insects them-
allergenicity, and the introduction of pests, and animal and plant selves can be allergens, pesticides, contaminants, and pathogens.
diseases into the EU (Goumperis 2012). Recently, Belluco and During rearing, insects may be able to convert or accumulate con-
others (2013) published a review on food safety of European and taminants present in their feed, which can result in degradation or
non-European insects, demonstrating the safety of some insects increase of the concentration of substances. The particular safety
with no additional hazards in comparison with usually consumed hazards depend on the insect species, their feed and environment,
animal products. and production methods. Therefore, more attention should be di-
Food safety of non-European insects has been studied more rected toward the effects of these environmental and management
widely (Table 1). Reported food safety hazards of non-European conditions on the safety of insects destined for human or animal
insects include allergens (Baldo and Panzani 1988; Blum 1994; consumption.
Phillips and Burkholder 1995; Vetter 1995; Freye 1996; MacEvilly
2000; Arlian 2002; Lian and Liu 2006; Ji and others 2008; Ji
and others 2009), ANFs (Wirtz 1984; Nishimune and others Algae
2000; Adeduntan 2005; El Hassan and others 2008), mycotoxins Algae belong to a large and diverse group of organisms using
(Simpanya and others 2000; Braide and others 2011), pesticides photosynthesis, which do not belong to the group of terrestrial
(Saeed and others 1993; DeFoliart 1999), heavy metals and al- plants (Cazaux and others 2010). Algae can be distinguished as
kali (Green and others 2001; Handley and others 2007; Zhuang microalgae and seaweed (Kerkvliet 2001; Stegeman and others
and others 2009; Banjo and others 2010), natural toxins (Duffey 2010). Microalgae are single-celled organisms that can grow over
1980; Wirtz 1984; DeFoliart 1992; Berenbaum 1993; Blum a wide range of environmental conditions, whereas seaweeds are
1994; Nishimune and others 2000; Zagrobelny and others 2009), complex multicellular organisms growing in salt water or a marine
and the presence of pathogenic microorganisms (Simpanya and environment (Cazaux and others 2010).
others 2000; Amadi and others 2005; Giaccone 2005; Banjo and About 2% of 4000 varieties of algae can form neurotoxins and
others 2006; Templeton and others 2006; Braide and others 2011; hepatotoxins that can accumulate in shellfish, crustaceans, and
Klunder and others 2012). Examples of bacteria found in insects fish. This may result in diseases such as paralytic shellfish poison-
are species from the genera Staphylococcus and Bacillus (Amadi and ing (PSP) due to saxitoxin, diarrhetic shelfish poisoning (DSP),
others 2005; Banjo and others 2006; Braide and others 2011), neurotoxic shellfish poisoning (NSP) due to brevetoxins, ciguat-
Campylobacter (Templeton and others 2006), Pseudomonas (Banjo era fish poisoning (CFP) due to ciguatoxin/maitotoxin, amnesic
and others 2006), Micrococcus and Acinetobacter (Amadi and others shellfish poisoning (ASP), and microcystin (Roheim and others
2005), Proteus and Escherichia (Braide and others 2011), Enterobac- 1995; Kerkvliet 2001; Vershinin and Orlova 2008; Caron and
teriaceae, and certain sporeforming bacteria (Klunder and others others 2010; Gerssen and others 2010; Van der Fels-Klerx and
2012). Examples of fungi found in insects are Aspergillus, Peni- others 2012a, b).
cillium, Fusarium (Simpanya and others 2000; Braide and others About 30% of the current worldwide algal production is sold
2011), Chaetomium, Mucor, Mucorales, Alternaria, Drechslera, and for animal feeding purposes (Becker 2004). Algae are approved in
Phoma (Simpanya and others 2000). Insects may also contain several countries as chicken feed and do not require new testing
pathogens as a result of improper processing or handling (Banjo or approval for feed use (Becker 1994). With regard to food use,
and others 2006). the marine diatom Odontella aurita by Innovalg (France) has been
664 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013

Table 1–Food safety hazards of non-European insects.
Insect species Country of origin Production method Processing Hazards References

T. molitor (mealworm) and United States – – Allergens (Freye 1996)
Zophobas morio
(superworm)
Silkworm pupa of Bombyx China * * Allergens (sericin) (Lian and Liu 2006)
mori and B. mandarina, and
their silk

Ant, termite, cricket, meal Akure Forest Reserve, Wild: foraging – Antinutritional factors (Adeduntan 2005)
bug, grasshopper, Anaphe Ondo State, Nigeria (tannin, phytate)
venata (silkworm), tree
hopper, winged termite
Anacridium melanorhodon Mayo local market, From market Cleaned, separated, Tannin, phytic acid (El Hassan and others
(tree locust) Khartoum, Sudan milled, defatted, 2008)
then boiled or fried

Acrididae (locust) Kuwait Wild – Chlorinated pesticides, (Saeed and others
organophosphorus 1993)
pesticides (Sumithion
[fenitrothion] and
malathion)
Larvae of Rhynchophorus Markets in Epe, Itokin, From markets and wild Preserved in 70% Nickel, lead, cadmium, zinc, (Banjo and others
phoenicis (beetle), Abigi, Ologbun and alcohol or oven sodium 2010)
Anapleptes trifasciata Ibiade. Wild: Lagos, dried at 60 to 70 ◦ C
(beetle) Ogun, Oyo and
Ondo state, Nigeria
Bogong moths Agrotis infusa Eastern Australia Wild – Arsenic (Green and others
(Lepidoptera: Noctuidae) 2001)
Pupae of Anaphe spp. (A. Suburb of Kampala, Wild Dry pupae: extracted, Thiaminase (Nishimune and
infracta or A. panda) (silk Uganda ground, centrifuged others 2000)
worm)
Caterpillar of the emperor Eastern and Southern Wild from leaves of Degutted, washed, Staphylococcus, Bacillus, (Braide and others
moth Bunaea alcinoe part of Nigeria Cananga odorata spiced, salted, Proteus, Escherichia, 2011)
plant wrapped, roasted, Aspergillus, Penicillium,
sun dried Fusarium, mycotoxins
Larvae of the cabbage tree Niger delta, Nigeria Gmelina tree within – Staphylococcus, Bacillus, (Amadi and others
emperor moth Bunaea the premises of the Micrococcus and 2005)
alcinoe Stoll university Acinetobacter
Larvae of Oryctes monocerus Itokin, Nigeria Wild Culturing Staphylococcus aureus, (Banjo and others
(African Rhinoceros beetle) Pseudomonas aeruginosa, 2006)
and Bacillus cereus
Phane worm (larval stage) of Francistown, Wild – Aspergillus, Penicillium, (Simpanya and others
the emperor moth Imbrasia Botswana Fusarium, Chaetomium, 2000)
belina Westwood Mucor, Mucorales,
Alternaria, Drechslera, and
Phoma, mycotoxins.
Contaminated with fungi
from leaves and soil
Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 665
approved since 9 December 2002 as a novel food (Gouveia and palmata (Kerkvliet 2001; Fahprathanchai and others 2006; Murphy
others 2008). 2007; Akköz and others 2011). Seaweeds can be harvested from
Microalgae. Several microalgae (for example, species from the the sea, but they are also increasingly cultivated (Cazaux and oth-
genera Chlorella, Tetraselmis, Spirulina, Nannochloropsis, Nitzchia, ers 2010). Seaweed products in fresh and dried form are imported
Navicula, Chaetoceros, Scenedesmus, Haematococcus, and Cryptheco- from Japan and France. Laminaria sp. (kelp weed) originating from
dinium) can be used in feed for both terrestrial and aquatic animals the Arctic Ocean, Iceland, and Norway are mainly used in food
(Harel and Clayton 2004). supplements (Kerkvliet 2001). No research has been performed
Microalgae used for human consumption are Arthrospira (spir- on the extraction of proteins of seaweeds for human consumption
ulina, namely, cyanobacteria), Chlorella spp., Dunaliella salina, and (Stegeman and others 2010). Several seaweed species, such as U.
Aphanizomenon flos-aqua (Kerkvliet 2001; Spolaore and others rigida, Ascophyllum, Laminaria, Undaria, Porphyra, Cystoseira barbata,
2006). They originate from several countries: Spirulina from, for and C. glomerata have been evaluated as feed additives in meal to
instance, China, India, Japan, and United States (US) (Spolaore fish diets (Appler and Jauncey 1983; Fahprathanchai and others
and others 2006; Small 2011), chlorella from, for instance, Taiwan, 2006; Kut Güroy and others 2007).
Germany, and Japan, Dunaliella salina from Australia, Israel, US, The use of C. glomerata, M. floccosa, and P. palmata in daily
China, and Aphanizomenon flos-aqua from the US (Spolaore and meals has been safe for humans (Fahprathanchai and others 2006;
others 2006). The green algae (Chlorophycea) Chlorella vulgaris, Mouritsen and others 2013). Several studies show that safety haz-
Haematococcus pluvialis, Dunaliella salina, and the cyanobacteria Spir- ards for seaweed may include iodine, ANFs, heavy metals, radioac-
ulina maxima are widely commercialized and used, mainly as nu- tive isotopes, ammonium, dioxins, and pesticides.
tritional supplements for humans and as animal feed additives In Laminaria, high levels of iodine were found (Van Netten
(Kerkvliet 2001; Gouveia and others 2008; Stegeman and oth- and others 2000; Kerkvliet 2001). A broad diversity of seaweed
ers 2010). species (red, green, and brown) contains ANFs, such as low levels
Several studies show that safety hazards related to algae may of lectins, tannins, and phytic acid, and high levels of trypsin
include allergens, toxins, pathogens, heavy metals, and pesticides. inhibitors and amylase inhibitors (de Oliveira and others 2009).
Allergenicity has been reported for airborne cyanobacteria Seaweeds can accumulate heavy metals depending on the grow-
Phormidium fragile and Nostoc muscorum (Sharma and Rai 2008), ing time in the sea and the levels of heavy metals in the water
and the green algal genus Chlorella (Tiberg and Einarsson 1989). (Ortega-Calvo and others 1993; Murphy 2007; Smith and others
However, a high-lipid product, Whole Algalin Flour, composed 2010). The types and concentration of metals found in seaweed
of dried milled Chlorella protothecoides showed little potential for vary with species, collection time, growth phase, and collection site
food allergy (Szabo and others 2012). (Houa and Yanb 1998; Brown and others 1999; Van Netten and
No toxins have been found in spirulina and chlorella. However, others 2000; Murphy 2007; Smith and others 2010). Reported ac-
in Aphanizomenon flos-aqua, toxic microcystines have been de- cumulation of heavy metals includes arsenic (Van Netten and oth-
tected (Kerkvliet 2001; Heussner and others 2012). Extracts from ers 2000; Kerkvliet 2001; Almela and others 2002; Rose and others
products consisting of Aphanizomenon flos-aquae, Spirulina, and 2007; Besada and others 2009; ), copper (Prasher and others
Chlorella, or mixtures thereof, were cytotoxic (Heussner and others 2004; Murphy 2007; Murphy and others 2007, 2009; Riosmena-
2012). Under favorable conditions, pheophorbides are formed in Rodriguez and others 2010; Akköz and others 2011), cadmium
chlorella, which give rise to photosensibilization in some humans (Prasher and others 2004; Besada and others 2009; de Oliveira and
(Kerkvliet 2001). others 2009; Akköz and others 2011), chromium (Murphy 2007;
Another safety aspect is the presence of pathogenic microorgan- Murphy and others 2008, 2009; de Oliveira and others
isms. Spirulina and chlorella are cultivated in open bassins, which 2009), nickel (Prasher and others 2004; de Oliveira and
may result in microbiological contamination from birds, insects, others 2009; Akköz and others 2011), vanadium (de Oliveira and
and rodents (Kerkvliet 2001). others 2009), iron, magnesium (Riosmena-Rodriguez and others
Algae may accumulate heavy metals. Since algae are at the bot- 2010), mercury (Van Netten and others 2000), lead ( Van Netten
tom of the aquatic food chain pyramid, they are the most important and others 2000; Prasher and others 2004; Akköz and others 2011),
vector for transfer of pollution to upper levels of the trophic chain cesium-137, and radium-226 (Van Netten and others 2000). The
in aquatic environments (Souza and others 2012). Sludge-grown uptake of heavy metals for P. palmata was found to decrease in the
algae contain a rather substantial amount of heavy metals that may order: lead > cadmium > copper > nickel (Prasher and others
impose adverse effects to higher trophic organisms (Hung and 2004). Iron, copper, and magnesium were the most significant
others 1996; Wong and others 1996). Spirulina accumulates more metals found in red and green algae (Riosmena-Rodriguez and
heavy metals than chlorella (Kerkvliet 2001). Other authors found others 2010). In general, brown algae have higher arsenic levels
no exceedance of legal maximum levels of heavy metals as estab- than red or green algae (Almela and others 2002). Other studies
lished in their own jurisprudence (Hsu and others 2001; Kolb and found no harmful quantities of heavy metals (Hwang and others
others 2004; Marles and others 2011). 2010; Smith and others 2010; Dhaneesh and others 2012). Little is
The pesticide fenamiphos and its metabolites can be transformed known about the process of metal bioaccumulation in marine food
and accumulated by Pseudokirchneriella subcapitata and Chlorococcum chains because data on metal concentrations at different trophic
spp. Therefore, contamination of natural environments can have levels and their temporal or spatial variation are sparse (Van Netten
adverse impacts on the food chain and associated biota (Caceres and others 2000; Riosmena-Rodriguez and others 2010; Akköz
and others 2008). and others 2011).
Seaweed. Seaweed species that are used for direct consump- Seaweeds also accumulate ammonium due to a combination
tion include, among others: Ulva rigida, Monostroma sp., Enteromor- of the size of the plant and the spatially and temporally variable
pha sp., Laminaria sp., Undaria pinnatifida, Hizikia fusiforme, Himan- concentration of ammonium in the seawater (Rees 2003).
thalia elongata, Eisenia bicyclis, Ascophyllum nodosum, Fucus vesiculosis, Other contaminants found in seaweeds are dioxins and
Porphyra sp., Cladophora glomerata, Microspora floccosa, and Palmaria pesticides. Seaweeds were contaminated by polychlorinated
dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofu- Derksen and Zwart 2010), chromium (Staves and Knaus 1985;
rans (PCDFs) of industrial origin, such as combustion source Gaur and others 1994; Boonyapookana and others 2002; Chandra
(Hashimoto and Morita 1995). Pesticides that could be present in and Kulshreshtha 2004; Miretzky and others 2004; Derksen and
seaweeds are, for example, azametiphos, diflubenzuron, tefluben- Zwart 2010), nickel (Gaur and others 1994; Axtell and others
zuron, propoxur (Lorenzo and others 2012), and organic mi- 2003; Derksen and Zwart 2010), lead (Gaur and others 1994;
cropollutants (polychlorinated biphenyls (PCBs), chlorinated Gallardo-Williams and others 2002; Axtell and others 2003; Miret-
pesticides, polycyclic aromatic hydrocarbons (PAHs)) (Pavoni and zky and others 2004; Derksen and Zwart 2010; Sobrino and others
others 2003). Further studies regarding the presence of chemother- 2010), zinc (Gaur and others 1994; Miretzky and others 2004;
apeutic agents in seaweeds are required, because of the lack of data Derksen and Zwart 2010; Hoving and others 2011), cobalt (Gaur
on some currently used compounds, and to elucidate the transfor- and others 1994), iron (Jain and others 1989; Chandra and Kul-
mation and biodegradation processes (Lorenzo and others 2012). shreshtha 2004; Miretzky and others 2004; Derksen and Zwart
2010), arsenic (Seth and others 2007; Rahman and others 2008;
Duckweed Hoving and others 2011; Rahman and Hasegawa 2011; Hoving
Duckweed species are small floating aquatic plants. They are and others 2012), uranium (Hogan and others 2010), manganese
monocotyledons of the botanical family Lemnaceae and are higher (Miretzky and others 2004; Derksen and Zwart 2010), aluminum,
plants or macrophytes (Leng and others 1995). Duckweed fam- gold, and strontium (Derksen and Zwart 2010). Duckweed has
ily comprises of 4 genera (Lemna, Spirodela, Wolffia, and Wolfiella) been demonstrated to be a good accumulator of cadmium, sele-
and 34 species (Rahman and Hasegawa 2011). Duckweed species nium, and copper, a moderate accumulator of chromium, and a
are found worldwide; they are adapted to a wide variety of geo- poor accumulator of nickel and lead (Zayed and others 1998). The
graphic areas and climatic zones. They are found in all areas except uptake of metals depends on the chemical form present and on the
waterless deserts and those permanently frozen. They grow best life form of the macrophytes (floating, free floating, well rooted,
in tropical and temperate zones, but many species can survive or rootless) (Chandra and Kulshreshtha 2004).
extreme temperatures (Leng and others 1995). Duckweed species are also capable to uptake and trans-
Duckweeds have been supplemented to feed, especially to com- form phenols (Fujisawa and others 2010) and pesticides, includ-
plement diets and to increase animal growth. Duckweed is used ing organophosphorus pesticides (malathion, demeton-S-methyl,
as feed for fish (for example, carp and tilapia) (Fasakin and others and crufomate) (Gao and others 2000), lipophilic compounds
1999; Leng 1999; Yilmaz and others 2004) and domestic animals, (De Carvalho and others 2007), 3-methyl-4-nitrophenol, 3,5-
including poultry (Haustein and others 1992; Leng 1999; Aham- dichloroaniline, 3-phenoxybenzoic acid (Fujisawa and others
mad and others 2003), ducks (Ikaheimonen and others 1997; Leng 2006), dimethomorph (Olette and others 2008; Dosnon-Olette
1999; Ngamsaeng and others 2004), and pigs (Hang 1998; Leng and others 2010), copper sulphate and flazasulfuron (Olette and
1999; Aguilera-Morales and others 2005). Few studies have been others 2008), and xenobiotics (chlorophenols) (Day and Saunders
performed on duckweed meal as supplement to forages given to 2004).
ruminants. It appears that duckweeds can be used as a mineral Limited work has been done to characterize secondary metabo-
(particularly P) and N source. The combination of crop residues lites in specific species of duckweed. So far, oxalic acid is the only
and fresh duckweeds in a diet for ruminants could give a balance identified compound produced by duckweed that is toxic to ani-
of nutrients. These diets can be potentially applied in cattle, sheep, mals at high levels (Adeduntan 2005).
and goat production systems (Leng and others 1995). Holshof and others (2009) found dioxins in harvested duck-
Besides a component of animal and bird diets, duckweed is weed, probably due to the presence of animal proteins of diving
already a human food resource in traditional/small farmer sys- beetles or snakes (Holshof and others 2009).
tems in South Asia (Leng 1999; Adeduntan 2005; Derksen and Pathogens like Escherichia coli or Clostridium botulinum could con-
Zwart 2010); Wolffia arrhiza has traditionally been eaten as “khai- taminate duckweed (Hoving and others 2011). Islam and oth-
nam,” in Burma, Laos, and northern Thailand. Khai-nam is gen- ers (2004) studied the fecal coliform contamination of duckweed
erally regarded as a poor people’s food and so far has attracted grown on hospital-based wastewater. They found that wastewater-
little attention as a potentially significant source of human food treated duckweed may be safely used as fish feed (Islam and others
(Bhanthumnavin and McGarry 1971). 2004). Moyo and others (2003) concluded that the use of duck-
Safety hazards for duckweed may include the presence of heavy weed for chicken feed was microbiologically safe with respect to
metals, phenols, pesticides, dioxins, and pathogens. E. coli and Salmonella spp. provided that caution is taken during
The accumulation of heavy metals by duckweed poses a po- the processing of duckweed. Chickens may get contaminated, es-
tential danger where heavy metal contamination of water occurs pecially during wet weather due to poor environmental sanitation
(Leng 1999; Chandra and Kulshreshtha 2004). Heavy metals can at the plant (Moyo and others 2003). Duckweed production in
enter the food chain at a number of points, and therefore, these open greenhouse pools would be expected to produce biomass
contaminants have to be monitored during the production of with an associated microflora of bacteria, viruses, fungi, algae, and
duckweed for food/feed purposes (Leng 1999; Hoving and oth- possibly, microscopic invertebrates (Adeduntan 2005).
ers 2011). For instance, crayfish fed with cadmium-containing For using duckweed protein products for food or animal feed,
duckweed were contaminated with cadmium (Arrhenius and oth- methods would need to be developed to insure that heavy metals,
ers 2006). Accumulation of heavy metals from water includes phenols, pesticides, and pathogens would not contaminate the
cadmium (Gaur and others 1994; Boonyapookana and others protein products (Stomp 2005; Hoving and others 2011).
2002; Arrhenius and others 2006; Seth and others 2007; Razinger
and others 2008; Derksen and Zwart 2010), selenium (Zayed Rapeseed
and others 1998), copper (Jain and others 1989; Gaur and oth- Rapeseed (Brassica napus) is a bright yellow flowering member
ers 1994; Chandra and Kulshreshtha 2004; Miretzky and others of the Brassicaceae. In 1986, the definition of canola was intro-
2004; Razinger and others 2007; Kanoun-Boulé and others 2009; duced to refer to B. napus and B. campestris (now Brassica rapa) lines

containing less than 2% erucic acid in the oil and less than 30 seed of Brassica napus L. increased after treatment with sewage water
µmol/g glucosinolates in the air-dried, oil-free meal (OECD (Ahmad and others 2011). Brunetti and others (2011) found that B.
2011). napus was able to accumulate high amount of metals in greenhouse
Rapeseed or canola proteins have been used as feed ingredi- conditions, in the order: chromium > zinc > copper > lead.
ent around the world for many years for a broad range of animal Rapeseed contains allergenic 2S storage proteins (napins) (Mon-
species including poultry, pig, cattle, and fish (including salmon, salve and others 2001; Poikonen and others 2006). These proteins
trout, tilapia, and prawns) (Burel and others 2000; Enami 2011; show a cross-reactivity with related Brassica species (such as mus-
OECD 2011; Nagel and others 2012). For human food, canola tard) (Monsalve and others 1997, 2001; Focke and others 1998),
proteins have been characterized to have interesting functional since these proteins exhibit great sequence similarity with 2S al-
properties that may replace classical ingredients in different food bumins from different seeds. The 2S albumin seed storage proteins
formulations (Aluko and McIntosh 2005; Yoshie-Stark and oth- in mustard seeds share 94% sequence similarity with 2S albu-
ers 2006; Cumby and others 2008; Guo and others 2010; Aider mins from rapeseed (Monsalve and others 2001). Several allergic
and Barbana 2011). However, the application of canola protein reactions in humans have been reported after consumption of
as a human food ingredient has been limited to only a few food mustard and rapeseed products (Meding 1985; Widström and Jo-
products manufactured and marketed on a low scale in Canada, hansson 1986; Monsalve and others 2001; Poikonen and others
Japan, and the US (such as processed meats, cheeses, pizza, and 2006, 2008, 2009; Hafting and others 2012). Currently, mustard is
bagels) due to technological limitations in relation to organoleptic included in the list of 14 allergenic foods that must be declared on
properties and ANFs (Mejia and others 2009). food labels of prepackaged foods in the EU according to Directive
In the US, generally recognized as safe (GRAS) notifications 2006/142/EC.
on canola protein ingredients have been received (ADM 2010; For use of rapeseed protein products for food production, meth-
Keller-and-Heckman 2011). Mejia and others (2009a, b) found, ods would need to be developed to insure that heavy metals would
in specific canola/rapeseed protein isolates, that potential natural not contaminate the protein products. The effects of ANFs and
toxicants such as glucosinolates and erucic acid, as well as potential allergens should also be taken into account.
contaminants such as pesticide residues, solvent residues, heavy
metals, dioxins, aflatoxins, PAHs, and acrylamides, were either Overview of potential hazards in novel protein sources
nondetected or below toxicological and regulatory allowed limits Table 2 shows an overview of the potential hazards in the 5 novel
(Mejia and others 2009). However, in the EU, an application for protein sources considered. Heavy metals and processing contam-
a protein preparation isolated from B. napus and B. rapa was not inants are potential hazards for all 5 protein sources. Pesticides,
accepted as a novel food due to the lack of limit values for relevant pathogens, and allergens can be present in most protein sources.
undesirable compounds, identification of the starting material, and In addition, insects and seaweed have also other potential hazards
studies on allergic reactions (CBG-MEB 2012). like ANFs, mycotoxins, and dioxins.
Several studies showed that safety hazards for rapeseed may in-
clude ANFs, heavy metals, and allergens. Rapeseeds contain sev- Legislation
eral ANFs, such as erucic acid, glucosinolates, phytic acid, phe- Food and feed business operators (FBOs) that wish to put novel
nolics (mainly sinapine and tannins), and a high fiber content food and feed protein products on the market have to comply
(Kozlowska and others 1990; Burel and others 2000; Bonnardeaux with European and national rules for food and feed. For the novel
2007; Mejia and others 2009; Aider and Barbana 2011; OECD products discussed in the previous sections below, some comments
2011). One of the limiting factors for the application of canola will be made on the general legal requirements as regard to market
proteins is that the content of phenolic acids in canola meals is up introduction and food and feed safety legislation.
to 5 times higher than in soybean meals, and in rapeseed/canola
flours 10 to 30 times higher than in flours from other oleaginous General legislation
seeds such as flaxseed (Aider and Barbana 2011). Pig and poultry All FBOs in the EU should comply with the requirements
feed-producing industries are not receptive to using canola meal established in EU and national law. Requirements are set for the
for full protein supplementation because of the ANFs in canola producer (including transporters), the food and feed products, and
meal (Bonnardeaux 2007). However, modern technologies used the presentation of these products. Most of the requirements apply
in processing (such as chemical modifications, microbial and phys- to all FBOs and food and feed products (horizontal law), some only
ical treatments, membrane filtration, as well as a development of to specific products (vertical law).
low-glucosinolate and low-erucic acid rapeseed cultivars) are able The General Food Law (Regulation (EC) 178/2002,1 GFL) sets
to eliminate the majority of the ANFs in canola such as glucosi- the framework for EU legislation on food and feed, and applies to
nolates, phytates, and tannates (Mansour and others 1993; Aider all stages of food and feed production. First of all, this Regulation
and Barbana 2011). gives the definition of what is considered to be food and feed.
Heavy metals from the soil can accumulate in the roots, plant, Both definitions are very broad. Food or foodstuff is defined as
and seeds of rapeseeds. Based on pot experiments, lead and zinc “any substance or product, whether processed, partially processed
from the soil can accumulate in the roots of Brassica napus L., and or unprocessed, intended to be, or reasonably expected to be
small amounts of them move through the conductive system to ingested by humans” (art. 1). Feed or feedingstuff is defined as
the seeds. Cadmium moves relatively easily from root to stem and “any substance or product, including additives, whether processed,
is accumulated in higher concentrations in the top of the plant partially processed or unprocessed, intended to be used for oral
(Angelova and others 2008). Rossi and others (2004) also showed feeding to animals” (art. 2). According to the GFL, the FBO is
that B. napus accumulated zinc and copper and translocated these responsible for compliance of products, processes, and premises
elements in different ways in the harvestable parts of the plants
(Rossi and others 2004). Ahmad and others (2011) found that 1 Thelegal acts quoted in this section refer, where applicable, to the latest
lead, cadmium, and chromium concentrations in soil, forage, and amended version.
Table 2–Overview of potential hazards in 5 novel protein sources (insects, microalgae, seaweed, duckweed, and rapeseed), as based on literature
sources.
Potential hazard Insects Microalgae Seaweed Duckweed Rapeseed

Heavy metals X X X X X
Pesticides X X X X
Pathogens X X X
Allergens X X X
ANFs X X
Toxins X
Natural toxins X
Mycotoxins X
Veterinary residues X
Dioxins X X
Iodine X
Phenols X
Processing contaminants X X X X X
with all requirements of food law (art. 17). Foods (and feeds) are compiled in a register of the EU Commission (Belluco and
should not be placed on the market if they are unsafe (art. 14 and others 2013). For nonprimary producers and transporters, Annex
15) and must be traceable by the FBO (art. 18). Furthermore, in II of Regulation (EC) 852/2004 contains general requirements
case a FBO has reasons to believe that a product is unsafe, it should for premises (like adequate number of lavatories), equipment and
immediately withdraw the product from the market and inform personnel, cleaning and maintenance, rooms where foodstuffs are
the competent authorities (art. 19 and 20). The presentation of handled, for transport, food waste, foodstuffs, and water supply.
the product should not mislead consumers (art. 16). The GFL as For FBOs involved in the production of food of animal origin,
such defines the general rules for FBOs. more elaborate hygiene requirements are laid down in Regulation
(EC) 853/2004. However, the most extensive requirements in this
Food and feed hygiene legislation regulation are only applicable to those animals that are specifically
The Food Hygiene Regulations, Regulation (EC) 852/2003 mentioned in Annex I. For a number of pathogenic microorgan-
and (EC) 853/2004 contain general rules on hygiene of foodstuffs isms in specified foodstuffs, microbiological criteria are laid down
for all manufactures of food, including those involved in primary in Regulation (EC) 2073/2005, for novel food products not in-
production. Only production for private domestic consumption cluded in the categories in this regulation, no microbiological
or handling, and the direct supply of small quantities of primary criteria have been established yet.
products to consumers or local retail establishments are excluded For FBOs producing feed, Regulation (EC) 183/2005 applies.
from the scope of this Regulation. According to the Hygiene reg- Annex I of this regulation contains, among others, hygiene pro-
ulations, the FBO is obliged to notify the competent authorities of visions and the obligation of record keeping for those involved
its existence (art. 6, 852/2004). When FBOs are handling certain in the primary production of feed. For FBOs involved in feed
products of animal origin, they should be approved before start of after the stage of primary production, requirements on facilities
operations (art. 4, 853/2004). Also, FBO involved in feed produc- and equipment, personnel, production, quality control, storage
tion should be either registered or approved (art. 9 and 10, Feed and transport, record-keeping and complaints, and product recall
Hygiene Regulation (EC) 183/2005) by the competent authori- are laid down in Annex II. An obligation for the latter FBOs is
ties of a member state. For registration, a FBO should inform the that they shall monitor for the presence of prohibited and undesir-
competent authority (CA) on the establishment and/or activities. able substances and other contaminants. Furthermore, feed FBOs
For an approval, the CA must visit and give an approval prior to should, like food FBOs, have procedures in place based on hazard
the upstart of the business. analysis and critical control point (HACCP) principles. For assis-
Requirements for FBOs in primary production are laid down tance in the application of HACCP principles, community and
in Annex I, and for FBOs in other stages of production in Annex national guides to good practice have been developed and made
II of Regulation (EC) 852/2004. FBOs in primary production are available (Aider and Barbana 2011).
required to take measures to control contamination of their prod-
ucts (Annex I, Part A. Regulation (EC) 852/2003), such as the Novel food legislation
requirement to use potable or clean water whenever necessary to Novel food and novel food ingredients that were not consumed
prevent contamination, to use biocides, plant protection products, “to a significant degree” in the EU prior to 15 May 1997 have to
veterinary medicinal products, and feed additives correctly, and to be authorized before market introduction according to Regulation
keep records of measures taken to control hazards. Those FBOs (EC) 258/97, the Novel Food Regulation (NFR). At the time of
producing primary products of animal origin should also keep drafting of the NFR, no EU definition of “food” existed in the
records on, among others, the nature and the origin of feed fed to EU (Jones 2012); therefore, 4 categories of novel food and food
animals (Annex I Part A., III 8). FBOs involved in the production, ingredients to which the NFR applies were identified in art. 1 (2)
processing, and distribution of food after the stage of primary pro- c–f (a and b concerning genetically modified organisms were later
duction should have food safety programs and procedures based on moved to separate regulations) (see our italics):
HACCP principles (art. 5 Regulation (EC) 852/2004). National c. Foods and food ingredients with a new or intentionally
and Community guides on good hygiene practices for control modified primary molecular structure.
of hazards, including those in primary production, are (being) d. Foods and food ingredients consisting of or isolated from
developed to help FBOs in this respect. Member states should as- microorganisms, fungi, or algae.
sess these guidances to confirm that they assure compliance with e. Foods and food ingredients consisting of or isolated from plants
hygiene regulations. National guides on good hygiene practice and food ingredients isolated from animals, except for foods

and food ingredients obtained by traditional propagating or the European Commission (DG SANCO) published an “Infor-
breeding practices and having a history of safe food use. mation and Guidance Document on Human Consumption to a
f. Foods and food ingredients to which has been applied a Significant Degree” (Naidu and others 1999). In this document, a
production process not currently used, where the process decision tree is presented and a questionnaire, to be filled in by the
gives rise to significant changes in the composition or structure applicant, on consumption aspects to help applicants to identify
of the foods or food ingredients which affect their nutritional and justify significant consumption. The United Kingdom (UK)
value, metabolism, or level of undesirable substances. and Belgium also provide some advice on how to prove that a food
Most novel protein products mentioned in this publication will is not novel on its Internet site (ANCFP 2005). Examples of proof
fall within category d or e. Although it is not always clear to what of nonnovelty are invoices, legal import documents, lists of prices
category a new food product belongs in reality, this does not make of food products dated before May 15, 1997, literature data, dated
a huge difference in the data that have to be provided by the labels, FAO statistics, certificates or declarations of other member
applicant for the safety assessment (Jones 2012). states on the status of a food, and so on. It is pointed out that the
The producer of a novel food has to notify a member state of the provided evidence should clearly demonstrate oral consumption
EU its intention to place a novel product on its market for the first of the food product by humans in the EU. The “Novel Food Cat-
time. The CA of a member state then checks if the food is a novel alogue” (EC 2013), a searchable database that lists products that
food and if the dossier is complete, and if so, makes a first assessment have already been assessed before, as to being novel or not, could
of the product. This assessment is forwarded to the European also help FBOs to determine the status of a product.
Commission (EC) which forwards the assessment to the CAs in Besides administrative information, extensive data on composi-
all member states. If no objections are made by member states, tion, nutritional value and metabolism, intended use, and intake of
an authorization is granted; if reasonable objections are made, and levels of hazardous substances in the novel food are essential.
then the dossier is forwarded to European Food Safety Authority Furthermore, microbiological and toxicological (including aller-
(EFSA). Based on the EFSA opinion, a decision on authorization genicity) information on the novel food should be provided by the
is taken under the EU committee procedure involving, among applicant. For new products like insect proteins, the data require-
others, the Standing Committee on the Food Chain and Animal ments on composition, like analyses of a number of representative
Health (SCFCAH). An authorization is granted to the applicant batches regarding nutrients, micronutrients, and known and po-
of the novel food, and not to all FBO wishing to put a similar new tential contaminants, might be problematic if only pilot studies
product on the market of the EU. For “substantially equivalent” have been performed with breeding and harvesting of insects. Es-
novel products, however, the applicant can and should notify the pecially for proteins, the allergenic potential should be considered.
EC. In practice, for a substantially equivalent product, a statement For new proteins expressed in genetically modified crops, an EFSA
of the CA of a member state confirming the equivalence should opinion has been published for the assessment allergenicity (EFSA
accompany this notification. The outline of and explanations on 2010a). This opinion could be used as a starting point in the as-
both procedures are given in a recently published decision tree on sessment of non-GM new proteins. Opinions of EFSA on novel
the internet (WageningenUR 2013). protein products like “alfalfa protein concentrate” (EFSA 2009),
The assessment aims to establish whether the novel food, or “sardine peptide product” (EFSA 2010b), and bovine lactoferrin
novel food ingredient, is safe for the consumer, does not mislead (EFSA 2012) further illustrate data requirements for novel proteins.
the consumer, or when it replaces another ingredient, is not nutri-
tionally disadvantageous for the consumer (art. 3.1). For the assess- (Novel) Feed legislation
ment, the applicant has to provide all the necessary data; data re- Feed materials are defined as “products of vegetable or ani-
quirements are further specified in Recommendation 97/618/EC. mal origin, whose principal purpose is to meet animals” nutri-
Since the entering into force of Regulation (EC) 258/97, expe- tional needs, in their state, fresh or preserved, and products de-
rience has revealed that the procedures and requirements are not rived from industrial processing thereof, and organic and inorganic
fully transparent for applicants of novel foods and novel food ingre- substances, whether or not containing feed additives, which are
dients. Main uncertainties concern definitions and data require- intended for use in oral animal-feeding either directly as such, or
ments. The regulation applies to placing on the market any novel after processing, or in the preparation of compound feed, or as
food and food ingredient, in which novel is defined as “which have carrier of premixtures’ (art. 3 (2g) Regulation (EC) 767/2009).
not hitherto been used for human consumption to a significant The term “feed material” is further explained in a Recommenda-
degree within the Community . . . ” “Not hitherto” means before tion (2011/25/EU) that was published with guidelines to clarify
May 15, 1997. Both the date and the borders of the EU were the distinction between feed materials, feed additives, and other
arbitrarily chosen, resulting in some products not being “novel,” feed products. In a quality control system for feed producers, a
while other similar products had to be assessed for safety (Verha- decision tree was developed to guide producers in definitions used
gen and others 2009). CAs from member states interpreted “the in feed legislation (GMPplus 2011). Annex III of Regulation (EC)
Community” as all member states of the EU, irrespective of their 767/2009 lists materials prohibited for feed use.
date of entry. This interpretation was confirmed in the recently There is no premarket authorization procedure for novel feed
published Information and Guidance document (see below). The products. A FBO just has to notify appropriate representatives
expression “used for consumption to a significant degree” is also of the European feed business sectors that the intention is to
not clear, since nowhere in the regulation is explained what is place a novel feed product on the EU market for the first time,
meant by “to a significant degree.” The SCFCAH decided that that is, from 1 September 2010 onwards (art. 26(1) Regulation
presence in food supplements prior to May 15, 1997, would not (EC) 767/2009), and for products that were on the market before
be considered to constitute consumption to a significant degree September 1, 2010, but not listed in the catalogue (see further).
(SCFCAH 2005). An example of use of this guidance is the rul- This notifying FBO has to be registered as a FBO (art. 11, Regu-
ing on chromium picolinate by the SCFCAH (SCFCAH 2011). lation (EC) 183/2005). The representatives should publish the no-
Just recently, the Directorate General for Health & Consumers of tifications on the Internet and update the register of feed materials
with each notified novel feed material (art. 24(6) Regulation (EC) For contaminants, legal maximum levels (MLs) are only set
767/2009). This Feed Materials Register (Feedmaterialsregister for those food products that are contributing to human expo-
2010) was set up solely for information purposes. The safety of sure. Levels are set as low as reasonably achievable (Regulation
the notified novel feed material is not assessed, neither by the (EEC) 315/93). New food products (not on the market yet) do
representatives nor competent authorities. Thus, in the first in- not contribute yet to human exposure. Thus, the regulation on
stance, it is the FBO that is responsible for the safety of the new contaminants in food, Regulation (EC) 1881/2006, does not yet
product. In the register, feed names are not unique, so the same contain MLs for the 5 novel protein foods considered. For oils and
name may be used for feed materials with different characteristics. fats derived from plants and animals, also novel fats and oils, there
However, products mentioned in the Feed Catalogue (Regulation are MLs for lead, and the sum of 3 PAHs, and benzo(a)pyrene.
(EU) 68/2013) are only allowed to be marketed with the name in For oils of marine organisms and vegetable oils and animal fats,
the catalogue, provided they are compliant with the descriptions there are MLs for dioxins, dioxin-like PCBs, and PCBs. Also, for
of the product and labeling requirements to the catalogue. The “food supplements” that may contain new food products, MLs
representatives can make amendments of the catalogue, to include have been set for a limited number of contaminants.
products from the register, on a voluntary basis. Once taken up in For new products used as or in feed, Directive 2002/32/EC
the catalogue, the products with the same name in the register will does contain maximum levels for a rather high, compared to food,
be removed. The fact that a product is mentioned in the register number of undesirable substances. This is because feed products
or catalogue does not imply that it can be used in the feed of all in this directive are not specified in as much detail as in the food
animals. Animal proteins, for instance, are, with some exceptions, contaminants regulation. Most new products will fall in the broad
not allowed to be used in the feed of food-producing animals as a category “feed materials” of this directive. This means that for use
result of the “extended feed ban” (see further under insects). as feed, there are maximum levels for arsenic, cadmium, fluorine,
lead, mercury, nitrite, melamine, aflatoxin B1, several inherent
Legislation on chemical food and feed safety plant toxins, the persistent pesticides aldrin, dieldrin, chlordane,
For certain hazardous chemicals, like pesticides and veterinary DDT, endosulfan, endrin, heptachlor, hexachlorobenzene, hex-
drugs, an application for authorization must be filed with the achlorocyclohexane (alpha, beta, and gamma isomers), dioxins and
competent authorities prior to use. If necessary, legal maximum dioxin-like PCBs, and PCBs for all new products that are used as
limits will be set for residues of these chemicals in foods. Other feed material. Furthermore, harmful botanical impurities (among
chemicals occur naturally, are formed during processing, or are others, several mustards) that should not be present in feed are
present in food and feed due to their presence in the environment. listed in this directive.
For some of these chemicals, maximum limits are also set by law, In the next section, more specific remarks will be made on
and there are limits for “undesirable substances” in feed. This legislation applying to novel proteins derived from animal sources
legislation is listed in Table 3. (insects) and plant sources.
For plant protection products, the maximum residue limits
(MRLs) set apply to the products listed in Annex I of Regula- Specific legislation for novel protein sources
tion (EC) 396/2005 (Regulation (EU) 212/2013), whether they Insects. When farmed insects or products derived from farmed
are used as food or as feed. In general, the products listed in Annex insects are produced to be used as food for humans, or as feed
I are primary agricultural products. It is foreseen that for some pro- for food-producing animals, a FBO has to comply with rather
cessed products, “specific concentration or dilution factors” will complex legal requirements. These requirements are related to the
be laid down in Annex VI of Regulation (EC) 396/2005, but no insects themselves, the feed or substrate fed to the insects, the firm
factors have been established yet. For products not listed in Annex producing the insects, and the ultimate marketing for use as food
I, no EU MRLs for pesticide residues exist. This is also the case or feed.
for the product groups “fish, fish products, shell fish, molluscs In the Netherlands, it is forbidden to keep animals for agri-
and other marine, and fresh water food products” and “crops or cultural production that are not listed in the Dutch Decision on
parts of crops exclusively used for animal feed” in Annex I. For the indication of animals that are allowed to be kept for produc-
the latter groups, MRLs are not applicable until individual prod- tion purposes (Overheid 1997). Several insects, including those
ucts in these groups have been listed, but no individual products proposed to be used in food or feed, are listed in this decision.
have been listed up till now. Seaweeds and “other terrestrial an- The regulation on protection of animals at the time of killing,
imal products” are included in Annex I. Thus, also for food and Regulation (EC) 1099/2009, does not mention insects. Reptiles
feed derived from insects, pesticide MRLs apply, although in most and amphibians are excluded from this regulation, because these
cases, no specific MRLs will have been set and the default MRL “are not animals commonly farmed in the Community,” so maybe
of 10 ppb or limits of quantification will apply. insects will be excluded also in future.
According to the veterinary drug residues legislation (Regu- It is not clear if food products consisting of or derived from
lation (EC) 470/2009), food-producing animals are animals that insects are considered to be “products of animal origin” as defined
are bred, raised, kept, slaughtered, or harvested for the purpose of in the Hygiene Regulations (EC) 852/2004 and (EC) 853/2004.
producing food for humans. The only product of an insect that is No specific requirements are laid down for the production and
included in the list of animal products is honey from bees. In Vol- processing of insects in these regulations. As no requirements for
ume 8, the guidance note for applicants of MRLs for veterinary insects are laid down in Annex III of Regulation (EC) 853/2004,
drugs, the other animal products mentioned are: liver, kidney, fat establishments handling insects do not need approval prior to the
(fat and skin for pigs), and (injection site) muscle from mammals; start of operation (but they should be registered). The breeding of
liver, kidney, fat and skin, and muscle of poultry; and muscle and insects is part of “primary production,” the processing of insects
skin from fish (CVMP 2005). The animal products mentioned are into food is not. Thus, FBOs breeding and converting insects into
the only products of animals for which MRLs are set thus far in food should comply with Annex I and II of Regulation (EC)
the MRL regulation, Regulation (EU) 37/2010. 852/2004.

Table 3–EU legislation on hazardous substances in food and feed products.
EU legislation Substances Food / feed products

Regulation (EC) 396/2005 Residues of plant protection products Primary agricultural products that are used as food
and feed and are listed in Annex I
Regulation (EU) 37/2010 Residues of veterinary medicinal products Muscle meat, liver, kidney, fat (or skin and fat), milk,
egg, and honey used as food
Regulation (EC) 1881/2006 Contaminants (heavy metals, mycotoxins, processing General or specified food products
contaminants, environmental contaminants,
endogenous substances)
Directive 2002/32/EC Contaminants (heavy metals, mycotoxins, General or specified feed products
environmental contaminants, persistent pesticides,
endogenous substances, toxic weeds)
Whether feed, sometimes called substrate, fed to insects that proteins, also from nonmammalian sources, in feeds of all food-
are bred for consumption by humans or food-producing and producing animals (with some minor exceptions). The question is
nonfood-producing animals, should comply with Regulation (EC) thus whether insect-derived proteins are animal proteins. The fact
767/2009 is not clear. A “food-producing animal” in this regu- that insect meal and insects are included in category 9.16.1. in the
lation is defined as “any animal that is fed, bred, or kept for the Catalogue of Feed materials does not imply that these products are
production of food for human consumption, including animals therefore allowed to be used in feed for food-producing animals.
that are not used for human consumption, but that belong to According to an answer given March 25, 2010, by Commissioner
a species that is normally used for human consumption in the Com- Dalli on a question from the European Parliament, insect meal is
munity” (art. 3 (2c)). Insects are “not normally” used for human a “processed animal protein” as referred to in Annex IV of the
consumption in the EU. Annex III of this regulation lists a number Regulation (EC) 999/2001 and is therefore prohibited to be fed
of materials that are prohibited for use as feed, such as feces and to farmed animals. Annex IV of this regulation contains details
“household waste,” materials that could be used to feed insects. concerning the prohibitions (part I) and derogations (part II) on
On the opposite, feed or substrates for insects probably do have to the feeding of animal proteins to categories of food-producing
comply with EU regulations on animal proteins, Regulation (EC) animals, and as such give details for the prohibitions in art. 7.1.
1069/2009 (and the implementing Regulation (EU) 142/2011) (ruminants) and art. 7.2 (other animals). There is neither explicit
as the definition of “farmed animals” in this regulation does not prohibition of, nor derogation for, the use of proteins from terres-
exclude insects: “any animal that is kept, fattened, or bred by hu- trial invertebrates in Annex IV. Contrary to the answer by Dalli in
mans and used for the production of food, wool, fur, feathers, a subsequent communication of the EU Commission, “TSE road
hides, and skins or any other product obtained from animals or map 2” (EC 2010), it is indicated that animal proteins not specifi-
for other farming purposes.” These regulations prohibit the use cally excluded are allowed to be used in feeds of all nonruminants.
of some (animal protein) sources that might be suitable as feed for In the table in this Roadmap, insect proteins are not specifically
insects, like those mentioned under Category 2 materials: manure excluded.
and gut content, dead-in-shell poultry, and fallen stock (art. 9). Regulation (EC) 142/2011 (implementing Regulation (EC)
Also, the use of “catering waste” as feed for farmed animals (apart 1069/2009) gives a definition for “processed animal protein”
from fur animals) is prohibited (art. 11b). Of special concern when (PAP). In this definition, PAP is a product derived from “Cat-
feeding insects are genetically modified (GM) plants with built-in egory 3 material” treated in a certain way. Some specific products
insecticides, like the crops in which insecticidal proteins of the are excluded from the definition, such as milk, eggs, and prod-
microorganism Bacillus thuringiensis (Bt) are expressed. These GM ucts derived thereof. In article 10 of Regulation (EC) 1069/2011,
crops may be detrimental to the growth of insects. All GM crops a description of Category 3 material is given. This category in-
should be labeled according to EU legislation, however; thus, in cludes, among others, all by-products that are the result of the
principle, use of Bt-derived ingredients could be avoided. production of food products derived from animals fit for human
Although insects are already sold as food in the EU, mostly in consumption, but also products from terrestrial invertebrates (not
specialty shops, the discussion as to whether insects and insect- pathogenic to humans and animals, art. 10(l)). Thus, it is here that
derived products are novel foods in the EU is still ongoing. Fur- insect-derived proteins are included in PAP. Proper processing of
thermore, it is not clear if the NFR applies to whole insects used insects to convert them to “processed animal proteins” is a basic
as food, since in the definition only “food ingredients isolated from requirement for use of these proteins in feed. Possible processing
animals” are considered to be novel (Belluco and others 2013). strategies are listed in Annex IV of Regulation (EC) 142/2011.
The Food Standards Agency (FSA) in the UK launched a survey If just grinding and drying of whole insects or insect larvae, part
in August 2011 on the consumption of insects in the UK, to de- of primary production, will be considered as proper processing by
termine if consumption “in a significant degree” before May 15, competent authorities is not clear, although the CA has sometimes
1997, could be substantiated with data. This would obviate the some room to interpret.
need for a market application under the NFR for those insects for Nowadays, new analytical control tools have been developed
which a significant degree of consumption could be proven. The and a relaxation of the ban, allowing proteins from nonruminants
results of this survey are not published yet. to be used in feed again, was recently published. Regulation (EU)
The legislation on the use of insects and insect-derived prod- 56/2013 allows the use of nonruminant proteins in feed for fish
ucts as feed for food-producing animals is complicated. In the past, in aquaculture. As transmission of BSE from nonruminants, also
the use of animal proteins in feed for food-producing animals was nonruminants like insects, to other nonruminants is negligible
banned for safety reasons, for example, the prevention of transmis- (Regulation (EU) 56/2013, recital 6), a lifting of the ban on use
sion of TSE/BSE. The initial ban on use of mammalian proteins of insect proteins in the feed of food-producing pigs and poultry
in feed for ruminants was later extended to the use of all animal should be on the agenda of the Commission in the near future.
Foods consisting of or derived from insects fall under the apply if seaweeds are used for human consumption, not if they are
group “other terrestrial animal products” of the pesticide residue used as feed for animals. For parts of seaweeds or seaweeds used ex-
legislation (Annex I, Regulation (EC) 396/2005). This means that clusively for animal feed, separate MRLs will be set in the future.
either specific MRLs will have been set, or the default MRL or Only for food supplements consisting exclusively, or mainly, of
limits of quantification are applicable. It might be necessary to dried seaweed, and products derived from seaweed, a ML for cad-
treat insects raised for food use for diseases like infestation with mium has been set in Regulation (EC) 1881/2006. Fresh seaweed
other insects, fungi, bacteria, or viruses. Pesticides that are used is explicitly excluded in this regulation as a category of food for
to treat animals, and thus insects fall under the veterinary drugs which the MLs of lead and cadmium are applicable. For seaweed
legislation. A pharmacologically active substance of a veterinary meal and feed materials derived from seaweed, a separate ML for
drug must be listed in Table 1 of the Annex of Regulation (EU) arsenic is set in Directive 2002/32/EC. All other products of sea-
37/2010 and, if necessary, MRL must have been set in food prod- weed used as feed should comply with the other MLs mentioned
ucts before a veterinary drug can be registered in a member state. in Directive 2002/32/EC.
No products derived from insects, apart from honey, are present Duckweed. Common duckweed, Lemna minor, was considered
in this regulation, so there are no MRLs for such products. If sub- to be a novel food when an application was filed under the NFR
stances contained in Table 1 of the Annex are found in the official (Novel Food Catalogue). Also, other subspecies of duckweed are
control in matrices for which no MRLs have been set, member likely to be novel foods and should be authorized prior to market-
states are expected to make a scientific assessment of the risk, and ing as a food. For use in feed, no authorization is required. Duck-
forward this assessment to the Commission. The registration pro- weed is likely to belong to the product group “fish, fish products,
cedure for the use of veterinary drugs on/in insects will probably shell fish, molluscs, and other marine and fresh water food products”
be complicated and of a long duration, as no data requirements in Annex I of pesticide residue Regulation (EC) 396/2005. Like
have been formulated yet. For insects raised solely for feed, the vet- for algae, no MRLs for residues of plant production products have
erinary residue regulations do not apply. But, of course, products been set, as no individual products have been defined yet for this
of animals fed with insects or insect-derived products should com- group. Duckweed products used as feed should comply with all
ply with the veterinary drug residue legislation. Insect products the MLs mentioned in Directive 2002/32/EC.
used as feed should also comply with MLs mentioned in Directive Rapeseed. Oil from rapeseed, or canola, has been used as food
2002/32/EC. for humans for some time now and is thus not a novel food. For
Microalgae. Foods consisting of or derived from algae are in- this oil use, special rapeseed varieties are grown with low levels
cluded in the definition of novel foods in the NFR. Thus, prior of the toxic fatty acid erucic acid (Directive 80/891/EEC) and
to market introduction of novel algae, an application should be glucosinolates. This is different for proteins derived from rapeseed
filed for authorization of the product. Some products of algae seeds. Although leftovers from rapeseed processing have been used
might have been used as food prior to May 15, 1997. The Novel in animal feed, no use of products other than oil is common in
Food Catalogue should provide some insight as to whether an food for humans. For rapeseed proteins, the NFR applies. The
alga is novel or not. Several substances derived from algae are used oilseeds of rapeseed are included in Annex I of Regulation (EC)
as food additive. For food additives, Regulation (EC) 1333/2008 396/2005. Thus, MRLs for plant protection product residues have
applies. In the past, prior to market access, a FBO was obliged been laid down in the other annexes of this regulation. For parts of
to apply for authorization for the use of proteins derived from al- rapeseed other than the seeds, the MRLs are not applicable. For oil
gae in feed under Directive 82/471/EEC. Assessment of safety and from rapeseed, MLs have been set in Regulation (EC) 1881/2006
nutritional value was done according to the guidelines in Directive for the contaminants lead, benzo(a)pyrene, dioxins and dioxin-
83/228/EEC. To assist applicants, EFSA published a “Guidance like PCBs, and PCBs. For the feed material called rapeseed cakes,
for the assessment of biomasses for use in animal nutrition” in a specific ML has been set in 2002/32 for allyliosthiocyanate (an
2011. Regulation (EC) 767/2009 repealed both directives, and indicator of the presence of volatile mustard oil). All other products
to date, no formal authorization and safety assessment is required of rapeseed should comply with the other MLs mentioned in
anymore. But the Guidance of EFSA might still be useful for FBOs Directive 2002/32/EC.
to assess their products.
Algae are likely to belong to the product group “fish, fish prod- Unclarities in EU legislation
ucts, shell fish, molluscs, and other marine and fresh water food prod- Table 4 shows an overview of the unclarities in EU legislation
ucts” in Annex I of Regulation (EC) 396/2005. MRLs for residues for the novel protein sources. Most unclarities in EU legislation
of plant protection products will be set as soon as individual prod- were found for insects as novel protein source. For algae, seeweed,
ucts of this group are defined, which is not the case yet. Algae and duckweed, some MRLs are not yet set. No unclarities were
or their products used as feed should comply with all the MLs found for rapeseed.
mentioned in Directive 2002/32/EC.
Seaweed. Seaweeds are macroalgae, and thus the NFR will ap- Control of Safety Hazards
ply if the seaweed is novel. Whether a certain variety of seaweeds Producers of novel proteins are responsible for the application
is considered to be novel or not can be verified to a certain extent of a novel food dossier or for risk assessment of their new products.
in the Novel Food Catalogue. For instance, the brown seaweed They are obliged to prove that their products are safe. Although
Fucus vesiculosus is not a novel food according to this catalogue, some safety aspects of novel proteins are intrinsic to the product,
but the red seaweed Rhodymenia palmata L (P. palmata) is, as this many potential hazards can be controlled by production methods
seaweed has only been used before in food supplements. For pro- and by production and processing conditions. The selection of a
teins isolated from these algae, however, a novel food application species or a variety of the protein source can affect safety due to
might be necessary (art. 1(2f)). For use in feed no authorization is differences in allergenicity, metabolism, and composition. This has
needed. Seaweeds are mentioned in Annex I of Regulation (EC) already been applied to rapeseed, currently containing less erucic
396/2005. MRLs for residues of plant protection products only acid and glucosinolates than before. As feed of insects may contain

Table 4–Overview of unclarities in EU legislation for the novel protein sources insects, algae, and duckweed.
Protein source Unclarity in EU legislation EU legislation

Insects Are insects and insect derived products Regulation (EC) 258/97
novel foods?
Which feed/substrate can be used for Regulations (EC) 767/2009; (EC)
insects? 1069/2009; (EU) 142/2011
Can food products consisting of /derived Regulations (EC) 852/2004; (EC)
from insects be considered to be “products 853/2004
of animal origin”?
Can insect proteins be used in feed of Regulations (EC) 999/2001; (EC)
food-producing pigs and poultry? 142/2011; (EC) 1069/2009)
Algae and duckweed MRLs for residues of plant protection Regulation (EC) 396/2005; Directive
products are not yet set 2002/32/EC
Seaweed For (parts of) seaweeds used exclusively for Regulation (EC) 396/2005; Directive
animal feed, separate MRLs will be set in 2002/32/EC
future
several contaminants that insects may accumulate and metabo- tion and accumulation of several substances during processing of
lize, the selection of feed is important to prevent contaminants these products, and the transmission of substances to feed and food
in the human and animal diet. For example, the composition of products.
waste streams from industry is variable and can therefore intro-
duce contaminants in the production chain. The same applies for
microalgae, seaweed, duckweed, and rapeseed, all are able to ac- Acknowledgment
cumulate heavy metals from the environment. These plants have The authors acknowledge the Ministry of Economic Affairs
to be produced using controlled conditions. Good Manufacturing (EZ) for financial support of this study (KB-15-007-003).
Practices (GMP)+ requirements can be used to develop a con-
trolled production system. Processing conditions of novel protein Author Contributions
products (as an ingredient or as a product as such) can also affect the M. van der Spiegel drafted the part of novel protein sources as
safety of novel proteins. Heating of products containing novel pro- well as their potential hazards, M.Y. Noordam described the leg-
teins can result in the formation of new components (neoformed islation in general and specific for novel protein sources, and H.J.
components), like acrylamide. Also, the application of solvents for van der Fels-Klerx stated the conclusions and critically reviewed
the extraction of proteins can affect safety of the novel protein the manuscript.
products. During product development, these aspects should be
considered in advance.
Conclusion
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Comp Rev Food Sci Food Safe - 2013 - Spiegel - Safety of Novel Protein Sources Insects Microalgae Seaweed Duckweed and

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Comp Rev Food Sci Food Safe - 2013 - Spiegel - Safety of Novel Protein Sources Insects Microalgae Seaweed Duckweed and

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Safety of Novel Protein Sources (Insects,

Microalgae, Seaweed, Duckweed, and Rapeseed)

Introduction consumption, and FAO expects a substantial increase by 2050 if

improved by new technologies and valorization of waste streams

Insect species Country of origin Production method Processing Hazards References

C 2013 Institute of Food Technologists®

then boiled or fried

Potential hazard Insects Microalgae Seaweed Duckweed Rapeseed

Table 3–EU legislation on hazardous substances in food and feed products.

EU legislation Substances Food / feed products

Protein source Unclarity in EU legislation EU legislation

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