Trends in Food Science & Technology 63 (2017) 80e90

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Trends in Food Science & Technology

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and-technology

Review

Bacteria encountered in raw insect, spider, scorpion, and centipede

taxa including edible species, and their significance from the food
hygiene point of view
Nils Th. Grabowski*, Günter Klein 1
Institute for Food Quality and Food Safety (LMQS), Hannover University of Veterinary Medicine, Bischofsholer Damm 15, 30173 Hannover, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Background: Insects, spiders, scorpions, and centipedes (non-crustacean arthropods; NCA) are consumed
Received 29 December 2015 in most areas of the world. However, Western cultures generally do not practice this food habit (ento-
Received in revised form mophagy) despite its advantages for the present and future of human nutrition. Little is known of the
12 January 2017
microbiological hazards associated with NCA consumption.
Accepted 13 January 2017
Available online 9 March 2017
Scope and approach: The present review summarizes the bacteriological findings on raw arthropod taxa
containing edible species. In a second step, it shows potential of bacteria to impair food hygiene and food
safety for the human consumer by relating the bacteria found to human diseases.
Keywords:
Entomophagy
Key findings and conclusions: Many bacterial species are known to affect invertebrates and humans alike
Food-borne disease (e.g. Bacillus cereus, Staphylococcus aureus, Escherichia coli, and Rickettsiella spp.). Furthermore, insects
Zoonosis can act as carriers for human pathogens if not obtained from a hygienic environment (e.g. salmonellae,
Public health Campylobacter spp., Shigella spp.). As with other foodstuffs of animal origin, exclusion of clinically-
Insect farming diseased specimens, hygienic obtention, washing and thorough heating seem suitable procedures to
Tradition reduce the risk of food-borne diseases by bacteria, following the tradition of most NCA-consuming
communities. Raw consumption of insects should be evaluated thoroughly, even when being tradi-
tional, because environmental changes could affect a previously valid innocuousness.
© 2017 Elsevier Ltd. All rights reserved.

1. Introduction grubs), lepidopteran (butterfly caterpillars and pupae), dipteran (fly

larvae and pupae), and hymenopteran (bee, ant, and wasp larvae
Strictly spoken, entomophagy refers to consuming only insects, and pupae) species (Van Huis et al., 2013).
and the habit of consuming other NCA would be termed “arach- In Europe, the current lack of an EU-wide hygiene legislation
nophagy”, “scorpionophagy”, and “chilopodophagy”. “Anthro- regarding edible insects has been interfering with the establish-
poentomophagy” states the human being as a consumer of insects. ment of major insect production units as they were built in, among
However, “entomophagy” will be used in the following due to others, South-Eastern Asia (Hanboonsong, Jamjanya, & Durst,
reasons of practicability. Recently, FAO recognized (anthropo)en- 2013). In 2014, Belgium and the Netherlands presented legal
tomophagy as one possibility to improve protein supply worldwide interim solutions (Federal Agency for Safety of the Food Chain,
and considered commercial insect production a sustainable 2014; Hoge Gezondheidsraad, 2014; Netherlands Food and
method to ensure this supply. With that, the traditional use of Consumer Product Safety Authority, 2014) to approach a sanitary
edible arthropods (i.e., gathering, cooking and preserving) is control of edible insects. Both documents include a series of bac-
brought to a next level: commercial farming of those species that terial pathogens along with corresponding thresholds which are
have a promising future as ordinary lifestock, typically a series of based on the data for minced meat and seafood. Regarding ento-
orthopteran (grasshoppers and crickets), coleopteran (beetle mophagy legislation in the EU, 2015 was an important year. It saw
the presentation of a scientific opinion on this foodstuff by the EFSA
(2015), as well as a first reading of a legislative resolution regarding
an amendment of the novel food regulation which will include
* Corresponding author.
E-mail address: [email protected] (N.Th. Grabowski). insects (European Parliament, 2015) which was accepted in 2016
1
Deceased author. and will take effect by 2018.

http://dx.doi.org/10.1016/j.tifs.2017.01.007
0924-2244/© 2017 Elsevier Ltd. All rights reserved.
 N.Th. Grabowski, G. Klein / Trends in Food Science & Technology 63 (2017) 80e90 81

Besides prions and viruses, the EFSA statement addresses bac- (Kwong & Moran, 2016; Va squez et al., 2012).
teria, fungi, and parasites, along with a series of non-infectional These interactions were presented in an exemplified manner in
risks. Regarding bacteria and fungi, only traditional food-borne the case of the honeybee (Grabowski & Klein, 2015a) and show that
pathogens were mentioned, claiming that E. coli, Salmonella spp., in the wild, NCA experience a constant uptake and release of mi-
or Aspergillus spp. were encountered in edible insects. However, croorganisms, depending on the environment and even the stage of
and like in other farmed animals, the insect microbiome is complex development. Other expected transmission routes like food transfer
and contains a great variety of different physiological and patho- seems to play a minor role (Kwong & Moran, 2016). This basic
logical microorganisms, i.e. some are vital symbionts for the insect pattern, however, is likely to present itself also while farming NCA
in order to develop properly, while others are powerful entomo- (typically insects), although microorganisms involved may vary
pathogens used, among others, in the biological control of pest greatly. Changes in the microbiome in relation to rearing conditions
insects (Tanada & Kaya, 1993). were observed (e.g. for the silkworm [Bombyx mori; Feng et al.,
While invertebrate pathologists study diseases of these animals 2011]).
and human pathologists usually focus on diseases caused (or
transmitted) by NCA, food hygienists evaluate the role of NCA as a 3. Bacteria isolated from non-crustacean arthropods
source for food-borne diseases. From the latter point of view, it is
less important whether a pathogen actually also causes disease in The publications encountered originated mostly in the field of
the NCA. However, zoonotic pathogens from asymptomatic NCA entomopathology, i.e. they considered the microorganism as found
pose a higher risk for the consumer than those that actually cause in living or dead, raw specimens, either encountered in their nat-
clinical symptoms in the animals, for then there is a good chance ural habitats or subjected to an artificial infection trial. This is
that experienced gatherers and rearers recognize this condition of important to stress and would correspond, from the food hygiene
illness and exclude the affected animals from further processing. point of view, to the findings in raw meat of wild boars or mallards
The present review parts from the EFSA statements and focuses which were hunted for food. For the cross-check of clinical rele-
on the bacteriological findings of raw NCA, evaluating their po- vance, most data was published in medical journals.
tential risk for the human consumer. For that, an internet research According to the type of interaction, several risk classes were
was conducted using NCBI and Google Scholar. All scientific names defined:
of microorganisms were cross-checked using the “List of Prokary-
otic names with Standing in Nomenclature” as available online.
Bacteria which are pathogenic to NCA and humans alike (class I)
So far, almost a million of different insect, about 100,000
Bacteria which are pathogenic only to NCA (class II)
different arachnid and approx. 3000 centipede species have been
Bacteria which are pathogenic only to humans (class III)
described, while the amount of edible NCA is estimated between
Spoilage bacteria transmitted via passive transport (class IV)
2000 and 3000 species. As a reference for the edible insects, the list
by De Jongema (2015) was taken, in the case of other classes, the The authors were cautious with the term “zoonosis” as it refers
corresponding literature. In order to group NCA species, two to a disease that is transmitted naturally from an animal to a human
mechanisms had to be (respectively were) used. On one hand, the being. There is in fact another class of interaction which refers to
data provided in the different publications regarding the identifi- zoonosis in sensu stricto, i.e. pathogens transmitted via active
cation of the NCA was sometimes relatively vague, (e.g. “beetles” or transport as practiced by haematophagous, parasitic, and other
even “insects”). In the following, these generic terms are kept. On arthropods that transmit a variety of human diseases, (e.g.
the other hand, some microorganisms were encountered in trypanosomiasis). However, these insect species are not consumed
different, well-documented NCA species. In this case, the corre- traditionally, which is why they are not considered in this review.
sponding higher taxon (usually family or order) was used, as it Instead the authors rather refer to bacteria which appear in both
seems likely that the pathogen may also interact with species of the NCA and humans, with different levels of pathogenicity, as a direct
same taxon. oral transmission from the arthropod to the human was rarely
documented. This is probably due to the facts that a) the medical
2. Bacterial communities in non-crustacean arthropods implications of traditional entomophagy have been poorly docu-
mented, and b) most NCA are consumed after further processing
Basically, the arthropod flora consists of a taxon-specific, bac- which usually includes heating, inactivating thus the majority of
terial core community and a varying set of other microorganisms pathogenic microorganisms.
capable of reacting towards a series of changes during the lifetime Bacterial diseases in NCA (classes I and II) frequently are char-
of the animal (Tang et al., 2012). In this way, first extensive studies acterized by bacteraemia, septicaemia, and toxaemia. Clinical signs
of the insect gut microbiome revealed that the phyla Proteobacteria in arththropods involve digestive symptomatology, and dead ani-
and Firmicutes were the most prominent taxa, and that the di- mals darken quickly, become soft and acquire a putrid odour. Some
versity of the gut flora was greater in omnivorous than in strictly of these pathogens are responsible for economically important
herbivorous or carnivorous insects. Other factors of influence are production diseases in honeybees and silkworms (e.g. Paenibacillus
the habitat, the season, the feed, the instar, and the phylogeny larvae or Staphylococcus aureus), others were studied because of
(Feng, Wang, Zhou, Liu, & Wan, 2011; Jia et al., 2013; Tang et al., their potential to control pests, especially moths (Bacillus thur-
2012; Yun et al., 2014). Regarding this latter factor, the micro- ingiensis or Enterococcus faecalis). While Table 1 sums up the bac-
biome has been used to clear evolutionary origins of certain insects teria found generically in “insects”, Tables 2e7 detail findings
€ hler, & Brune, 2014]). Bacterial com-
(e.g. of termites [Dietrich, Ko divided into major taxa.
munities also influence oviposition behaviour (Zheng et al., 2013). Most human pathogens may be transmitted by insects that act
Besides, shifts in the gut flora were observed as a response not to as passive vectors without truly affecting them (class III). Data on
environmental changes, but also to pathological conditions, (e.g. by this subject can be gathered by reviewing the role of arthropods in
viruses, fungi, and nematodes [Chaston et al., 2011; Tang et al., modern livestock farming, food storage in general and in human
2012]). In addition and in parallel to other animals, the micro- health facilities. Pathogens are transmitted by means of the me-
biome also includes probiotically-acting bacteria, e.g. Lactobacillus chanical dislodgement from the exoskeleton (by attracting particles
spp. and Bifidobacterium spp., as seen in Apini and Meliponini bees via electrostatic charges and/or adhesion to the body via the sticky
82 N.Th. Grabowski, G. Klein / Trends in Food Science & Technology 63 (2017) 80e90

Table 1
Bacteria affecting insects in general (Broderick et al., 2004; Chaston et al., 2011; Chitty, 2012; Frye, 2012; Greenberg & Klowden, 1972; Inglis, Lawrence, & Davis, 2000; Ishii,
Adachi, Hamamoto, & Sekimizu, 2014; Lù, Hashimoto, Matsumoto, & Maekawa, 1994; Martin & Mundt, 1972; Mead, Kachatourians, & Jones, 1988; Moreira et al., 2005; Park,
Kim, & Kim, 2002; Sr  a
mova  et al., 1992; Tanada & Kaya, 1993; Urban, 1968; Wu, Lei, Yi, Liu, & Gao, 2011; Zhou et al., 2016).

Familia Genus/species classa

Bacillaceae Bacillus thuringiensis sspp. II, III?

Enterobacteriaceae Proteus mirabilis, P. vulgaris, Photorhabdus spp., Providencia rettgeri, Serratia marcescens I
Xenorhabdus spp. II
Enterococcaceae Enterococcus caselliflavus, E. faecium III
Enterococcus faecalis I
Pseudomonaceae Pseudomonas spp., e.g. P. septica, P. chlororaphis, P. chlororaphis ssp. aureofaciens, P. fluorescens, P. putida I, IV
a
I ¼ pathogenic for both NCA and humans, II ¼ pathogenic for NCA only, III ¼ pathogenic for humans only, IV ¼ spoilage microorganism transported passively via vector.

Table 2
Bacteria affecting hemimetabolous insects (Odonata, Blattodea, Isoptera, Orthoptera, Hemiptera; Amadi, Ogbalu, Barimalaa, & Pius, 2005; Broderick et al., 2004; Crippen,
Sheffield, Esquivel, Droleskey, & Esquivel, 2009; Dietrich et al., 2014; Fischer et al., 2004; Fotedar, Banerjee Shriniwas, & Verma, 1991; Fowler, Bueno, Sadatsune, &
Montelli, 1993; Frye, 2012; Graczyk et al., 2001; Greenberg & Klowden, 1972; Inglis et al., 2000; Jones et al., 1991; Kopanic, Sheldon, & Wright, 1994; Mead et al., 1988;
Miller & Miller, 1996; Moreira et al., 2005; Nataraju, Sivaprasad, & Datta, 1999; Pizzi, 2012; Risco Oliva et al., 2010; Rosengaus, Zecher, Schultheis, Brucker, & Bordenstein,
 
2011; Sr amova et al., 1992; Tanada & Kaya, 1993).

Insect group Familia Genus/species classa

dragonflies Mycobacteriaceae Mycobacterium spp. III?

cockroaches Burkholderiaceae Burkholderia cepacia III
Coxiellaceae Rickettsiella spp. I
Enterobacteriaceae Citrobacter koseri, C. freundii, Enterobacter spp., Klebsiella spp., K. oxytoca, K. pneumoniae pneumoniae, III
Pantoea agglomerans, Salmonella Infantis, Oranienburgb, Othmarschen, Thompson, Typhimurium
Enterobacter cloaca, Escherichia coli, Klebsiella mobilis (¼ Enterobacter aerogenes), Proteus spp., I
Serratia marcescens
Flavobacteriaceae Flavobacterium spp.c III, IV
Moraxellaceae Acinetobacter calcoaceticus I
Mycobacteriaceae Mycobacterium spp. III?
Porphyromonada-ceae Dysgonomonas spp. II
Pseudomonaceae Pseudomonas aeruginosa I
Staphylococcaceae Staphylococcus aureus, S. epidermidis I
termites Bacteroidaceae Bacteroides spp. III
Bradyrhizopiaceae Afipia spp. III
Micrococcaceae Arthrobacter spp. III
Porphyromonada-ceae Dysgonomonas spp. II
Sphingomonadaceae Sphingomonas spp. III
Spirochaetaceae Treponema spp. (non-pallidum) II
Streptococcaceae Streptococcus spp. III
orthopterans Coxiellaceae Rickettsiella spp. I
Enterobacteriaceae Serratia spp. I
acridid grasshoppers Enterobacteriaceae Enterobacter spp. III
Enterobacter cloacae, Serratia marcescens I
Serratia liquefaciens II, IV
Enterococcaceae Enterococcus spp. I
Pseudomonaceae Pseudomonas aeruginosa I
true bugs Spiroplasmataceae Spiroplasma spp. II
lygaeid bugs Pseudomonaceae Pseudomonas aeruginosa I
a
I ¼ pathogenic for both NCA and humans, II ¼ pathogenic for NCA only, III ¼ pathogenic for humans only, IV ¼ spoilage microorganism transported passively via vector.
b
Cited as “S. orangenberg” by Jones et al., 1991.
c  
Cited as “Flavobacter” by Sr  et al., 1992.
amova

substances secreted on the most distal leg segment), faecal depo- seem to become infected in a natural way. However, noctuid but-
sition or regurgitation (Graczyk, Knight, Gilman, & Cranfield, 2001). terflies and Drosophila melanogaster fruit flies where infected arti-
Of the class III pathogens, the majority are known to cause oppor- ficially and are in fact used as models to study listeriae pathogeny in
tunistic infections in immunocompromised patients, especially in humans (Mukherjee et al., 2010). The waxmoth Galleria mellonella
hospitals. These noscomial pathogens are very important as some has also become a popular study model for artificial infections (e.g.
of them (e.g. Enterococcus spp. or Acinetobacter spp.) have been for Acinetobacter baumannii, Enterococcus faecalis, several E. coli
becoming increasingly multi-resistant to commonly-used antibi- strains, Proteus vulgaris, Pseudonomas aeruginosa, Serratia marces-
otics. Among the pathogens affecting also immunocomptetent cens, Staphylococcus aureus, and Vibrio anguillarum), while the also
patients, Chlamydia trachomatis, Bacillus anthracis, Citrobacter edible tenebrionid beetle Tribolium castaneum served as a model for
amalonaticus, Enterobacter cloacae, Klebsiella oxytoca, salmonellae, human oral infections (Alghoribi, Gibreel, Dodgson, Beatson, &
shigellae, Yersinia enterocolitica, and Campylobacter jejuni should be Upton, 2014; Milutinovi c, Stolpe, Peub, Armitage, & Kurtz, 2013;
mentioned. Although these microorganisms are known to produce Ramarao, Nielsen-Laroux, & Lereclus, 2012; Sharma-Kuinkel et al.,
disease, a direct infection by consuming NCA has not been 2015; Stahl, Bergmann, Go € ttig, Ebersberger, & Averhoff, 2015).
observed. This is particularly true for Listeria monocytogenes; this Unlike Bifidobacterium spp., some reported human infections also
zoonosis pathogen is considered ubiquitous, but still NCA do not included lactobacilli and lactococci as causative agent (s. Tables 3
 N.Th. Grabowski, G. Klein / Trends in Food Science & Technology 63 (2017) 80e90 83

Table 3
Bacteria affecting bees, wasps, and ants (Hymenoptera; Amadi et al., 2005; Broderick et al., 2004; Fotedar et al., 1991; Fowler et al., 1993; Frye, 2012; Graczyk et al., 2001; Greatti,
2005; Greenberg & Klowden, 1972; Inglis et al., 2000; McFrederick, Mueller, & James, 2014; Mead et al., 1988; Miller & Miller, 1996; Moreira et al., 2005; Nataraju et al., 1999;
 
Peloquin & Greenberg, 2003; Pizzi, 2012; Risco Oliva et al., 2010; Sr amova et al., 1992; Tanada & Kaya, 1993; Vidal-Naquet, 2012).

Insect group Familia Genus/species classa

hymenopterans Bacillaceae Bacillus cereus I

Enterobacteriaceae Citrobacter freundii, Klebsiella pneumoniae ozanae, Pantoea agglomerans III
Enterobacter cloacae, Serratia spp. I
Spiroplasmataceae Spiroplasma spp. II
wasps Moraxellaceae Acinetobacter calcoaceticus I
ants Bacillaceae Bacillus spp. II
Enterobacteriaceae Citrobacter koseri, Enterobacter amnigenus, Hafnia alvei, Klebsiella spp., Klebsiella oxytoca, III
K. pneumoniae pneumoniae, Serratia rubidaea
Klebsiella mobilis (¼ Enterobacter aerogenes) I
Enterococcaceae Enterococcus spp. I
Enterococcus avium III
Moraxellaceae Acinetobacter spp., A. baumanni III
Staphylococcaceae Gemella haemolysans, G. morbillorum, Staphylococcus spp., S. cohnii, S. equorum, III
S. lugdunensis, S. simulans, S. saprophyticus, S. warneri
Staphylococcus aureus I
Lactococcus garvieae III, IV
Streptococcaceae Streptococcus acidominimus III
apid bees Enterococcaceae Melissococcus plutonius II
Lactobacillaceae Lactobacillus spp. II, III?, IV
Nocardiaceae Rhodococcus spp. III
honeybees Alcaligenaceae Achromobacter eurydice II
Bacillaceae Bacillus apisepticus II
Bacillus coagulans I
Mycoplasmataceae Mycoplasma spp. II, III?
Paenibacillaceae Paenibacillus larvae, P. l. pulvefaciens II
Spiroplasmataceae Spiroplasma apis, S. melliferum II
a
I ¼ pathogenic for both NCA and humans, II ¼ pathogenic for NCA only, III ¼ pathogenic for humans only, IV ¼ spoilage microorganism transported passively via vector.

Table 4
Bacteria affecting beetles (Coleoptera; Broderick et al., 2004; Crippen et al., 2009; Crumrine, Foltz, & Harris, 1971; Fischer et al., 2004; Fowler et al., 1993; Frye, 2012; Graczyk
et al., 2001; Greenberg & Klowden, 1972; Hazeleger, Bolder, Beumer, & Jacobs-Reitsma, 2008; Huang, Shend, & Zhang, 2012; Hibberd, Neumann, Rehberger, & Siragusa, 2011;
Jones et al., 1991; Kinde et al., 2005; Kopanic et al., 1994; Mead et al., 1988; Miller & Miller, 1996; Moreira et al., 2005; Noonin et al., 2010; Rojas Jimenez & Hernandez, 2015;
 a
Sr mova  et al., 1992; Tanada & Kaya, 1993; Vidal-Naquet, 2012).

Insect group Familia Genus/species classa

beetles Bacillaceae Bacillus spp. II

Lysinibacillus spp. III?
Coxiellaceae Rickettsiella spp. I
Enterobacteriaceae Enterobacter spp., E. cloacae, Serratia spp. I
Klebsiella spp., Salmonella Infantis, Montevideo, Oranienburg**, Othmarschen, III
Paratyphi B, Thompson, Serratia spp.
Enterococcaceae Enterococcus spp. I
Moraxellaceae Acinetobacter spp. III
Mycobacteriaceae Mycobacterium spp. III?
Rickettsiaceae Wolbachia spp. II
Spiroplasmataceae Spiroplasma spp. II
Staphylococcaceae Staphylococcus haemolyticus, S. hominis III
Xanthomonadaceae Stenotrophomonas spp. III
curculionid beetles Micrococcaceae Micrococcus nigrofaciens II
elaterid beetles Enterobacteriaceae Kluyvera spp. III
Neisseriaceae Chromobacterium spp. III
Tsukamurellaceae Tsukamurella spp. III
passalid beetles Streptomycetaceae Streptomyces spp. III
Xanthomonadaceae Dyella spp. III
scarabeid beetles Bacillaceae Bacillus licheniformis IV
Brucellaceae Ochrobactrum haematophilum III
Enterobacteriaceae Citrobacter spp., C. freundii III
Serratia entomophila II
Microbacteriaceae Microbacterium benotii III
Mycoplasmataceae Mycoplasma spp. II, III?
Paenibacillaceae Paenibacillus lentimorbus I
Paenibacillus popilliae II
Streptomycetaceae Streptomyces spp. III
Xanthomonadaceae Stenotrophomonas maltophilia III
tenebrionid beetles Aeromonadaceae Aeromonas hydrophila I
Campylobacteraceae Campylobacter jejuni III
Clostridiaceae Clostridium perfringens III
Enterobacteriaceae Salmonella serogroups B, C1, C2, D, E, Typhimurium III
Enterobacteriaceae Serratia fonticola III
Moraxellaceae Acinetobacter calcoaceticus I
a
I ¼ pathogenic for both NCA and humans, II ¼ pathogenic for NCA only, III ¼ pathogenic for humans only, IV ¼ spoilage microorganism transported passively via vector.
84 N.Th. Grabowski, G. Klein / Trends in Food Science & Technology 63 (2017) 80e90

Table 5
Bacteria affecting butterflies (Lepidoptera; Amadi et al., 2005; Belda et al., 2011; Broderick et al., 2004; del Campo, Halitschke, Short, Lazzaro, & Kessler, 2013; Feng et al., 2011;
Fotedar et al., 1991; Fowler et al., 1993; Frye, 2012; Graczyk et al., 2001; Greenberg & Klowden, 1972; Inglis et al., 2000; Li, Xia, Zhau, Sendegeya, & Zhu, 2015; Mead et al., 1988;
 a
Miller & Miller, 1996; Moreira et al., 2005; Nataraju et al., 1999; Pizzi, 2012; Risco Oliva et al., 2010; Sr mova
 et al., 1992; Tanada & Kaya, 1993).

Insect group Familia Genus/species classa

butterflies Bacillaceae Bacillus spp. II

Bacillus cereus, B. megaterium I
Coxiellaceae Rickettsiella spp. I
Enterobacteriaceae Citrobacter amalonaticus III
Klebsiella mobilis (¼ Enterobacter aerogenes), Serratia marcescens I
Enterococcaceae Enterococcus spp. I
Micrococcaceae Micrococcus spp. III
Moraxellaceae Acinetobacter calcoaceticus I
Pseudomonaceae Pseudomonas aeruginosa I
Rickettsiaceae Wolbachia spp. II
Staphylococcaceae Staphylococcus aureus I
Xanthomonadaceae Stenotrophomonas spp. III
crambid butterflies Alcaligenaceae Bordetella petrii III
Brucellaceae Brucella abortus, B. melitensis, Ochrobactrum anthropi III
Enterobacteriaceae Citrobacter koseri, Enterobacter spp., E. cancerogenus, Escherichia coli, Klebsiella spp., III
K. pneumoniae, Salmonella enterica
Leuconostocaceae Leuconostoc mesenteroides IV
Sphingobacteriaceae Sphingobacterium spiritovorum III
Staphylococcaceae Staphylococcus spp., S. capitis, S. carnosus, S. epidermidis, S. haemolyticus, S. hominis, III
S. lugdunensis, S. saprophyticus, S. warneri
Streptococcaceae Streptococcus pyogenes III
Xanthomonadaceae Stenotrophomonas maltophila III
lasiocampid butterflies Clostridiaceae Clostridium brevifaciens, C. malacosomae II
saturniid butterflies Moraxellaceae Acinetobacter spp. III
Staphylococcaceae Staphylococcus spp. III
silkworms Corynebacteriaceae Corynebacterium spp. III
Enterobacteriaceae Klebsiella spp. III
Staphylococcaceae Staphylococcus epidermidis I
a
I ¼ pathogenic for both NCA and humans, II ¼ pathogenic for NCA only, III ¼ pathogenic for humans only, IV ¼ spoilage microorganism transported passively via vector.

Table 6
Bacteria affecting flies (Diptera; Amadi et al., 2005; Broderick et al., 2004; Crippen et al., 2009; Fotedar et al., 1991; Fowler et al., 1993; Frye, 2012; Graczyk et al., 2001;
Greenberg & Klowden, 1972; Hazeleger et al., 2008; Inglis et al., 2000; Jones et al., 1991; Kinde et al., 2005; Kopanic et al., 1994; Martin & Mundt, 1972; Mead et al., 1988;
 a
Moreira et al., 2005; Pelli et al., 2007; Pizzi, 2012; Risco Oliva et al., 2010; Skov et al., 2008; Sr mova
 et al., 1992; Tanada & Kaya, 1993; Vidal-Naquet, 2012).

Insect Familia Genus/species classa

group

Flies Burkholderiaceae Burkholderia cepacia III

Coxiellaceae Rickettsiella spp. I
Enterobacteriaceae Citrobacter freundii, Hafnia alvei, Klebsiella pneumoniae pneumoniae, Morganella morganii, Pantoea agglomerans, Proteus inconstans, III
Salmonella spp., Enteriditis, Infantis, Oranienburgb, Othmarschen, Paratyphi B, Thompson, Typhi, Typhimurium, Shigella
dysenteriae, S. flexneri
Enterobacter cloacae, Escherichia coli, Klebsiella mobilis (¼ Enterobacter aerogenes), Serratia spp., S. marcescens I
Enterococcaceae Enterococcus spp. I
Micrococcaceae Micrococcus luteus III, IV
Moraxellaceae Acinetobacter calcoaceticus I
Mycoplasmataceae Mycoplasma spp. II, III?
Paenibacillaceae Brevibacillus laterosporus II
Pseudomonaceae Pseudomonas aeruginosa I
Rickettsiaceae Wolbachia spp. II
Spiroplasmataceae Spiroplasma spp. II
Staphylococcaceae Staphylococcus aureus I
Staphylococcus haemolyticus, S. hominis III
muscoid Bacillaceae Bacillus moritai II
flies
house flies Bacillaceae Bacillus spp. II
Campylobacteraceae Campylobacter spp. III
Chlamydiaceae Chlamydia trachomatis III
Enterobacteriaceae Enterobacter spp., Klebsiella spp., Salmonella serogroups B, C1, C2, D, E, Shigella spp., Yersinia enterocolitica III
Moraxellaceae Acinetobacter spp. III
psychodid Nocardiaceae Nocardia cyriacigeorgica III
flies
a
I ¼ pathogenic for both NCA and humans, II ¼ pathogenic for NCA only, III ¼ pathogenic for humans only, IV ¼ spoilage microorganism transported passively via vector.
b
Cited as “S. orangenberg” by Jones et al., 1991.

and 7). However, it should be stressed that the major role of these Some bacterium families are predominantly entomopathogenic
bacteria is that of probiotics (Kwong & Moran, 2016; V
asquez et al., (e.g. Bacillaceae, Paenibacillaceae, and Clostridiaceae). Compared to
2012), also in the human being. the amount of pathogenic bacteria affecting NCA, those posing a
 N.Th. Grabowski, G. Klein / Trends in Food Science & Technology 63 (2017) 80e90 85

Table 7
Bacteria affecting arachnids and centipedes (Arachnida, Chilopoda; Amadi et al., 2005; Chitty, 2012; Fotedar et al., 1991; Frye, 2012; Graczyk et al., 2001; Greenberg & Klowden,
 a
1972; Inglis et al., 2000; Mead et al., 1988; Moreira et al., 2005; Nataraju et al., 1999; Pizzi, 2012; Risco Oliva et al., 2010; Sr mov
a et al., 1992; Tanada & Kaya, 1993).

Arthropod group Familia Genus/species classa

centipedes Pseudomonaceae Pseudomonas spp., P. septica, P. chlororaphis, P. c. aureofaciens, P. fluorescens, P. putida I, IV

scorpions Bacillaceae Bacillus spp. II
Bacillus megaterium I
Caulobacteraceae Brevundimonas diminuta II
Coxiellaceae Rickettsiella spp. I
Enterobacteriaceae Escherichia coli, Proteus vulgaris, Serratia marcescens I
Lactobacillaceae Lactobacillus spp. II, III?, IV
Moraxellaceae Acinetobacter calcoaceticus, Moraxella spp. I
Staphylococcaceae Staphylococcus aureus I
spiders Enterobacteriaceae Citrobacter freundii III
Klebsiella mobilis (¼ Enterobacter aerogenes), Proteus spp. I
Morganella morganii III
theraphosid spiders Bacillaceae Bacillus spp. II
Bacillus cereus I
a
I ¼ pathogenic for both NCA and humans, II ¼ pathogenic for NCA only, III ¼ pathogenic for humans only, IV ¼ spoilage microorganism transported passively via vector.

health risk also to humans are relatively few (e.g. Bacillus cereus, includes the de-novo formation on the digestive tract. However,
Paenibacillus lentimorbus, Staphylococcus aureus, Enterobacter imagos may reinfect themselves by ingesting contaminated feeds
cloacae, Escherichia coli, Klebsiella mobilis [also known as Entero- and foods (Graczyk et al., 2001). The presence of some pathogens
bacter aerogenes], Proteus vulgaris, Aeromonas caviae, Rickettsiella (e.g.) enterococci, also depends on the season (Martin & Mundt,
spp., and Pseudomonas aeroginosa). Some organisms, like Bacillus 1972).
cereus, Pseudomonas aeruginosa, Staphylococcus aureus, and others The infectivity of a given pathogen varies greatly with the spe-
are typically involved in food-borne diseases. cies it is encountered in and, in the case of enteric bacteria, on the
As can be seen from Tables 1e7, categorization of NCA bacteria is composition of the gut flora which in turn varies with the foraging
complex, as one and the same genus (or even species) may even- habits. It was seen that multiplication of salmonellae in flies
tually be grouped into several categories (e.g. as a pathogen and a depended significantly on the presence and amount of Proteus spp.
food spoiler). Besides that, many unsolved questions remain. To which acts as an inhibitor. Then, the site where the NCA were
give an example, the role of many different subspecies of Bacillus collected is also important as is the kind of potential human host;
thuringiensis as potential human pathogens is not yet clear. mealworms in a bakery shop may be disgusting, but cockroaches or
Experimentally, some strains cause death to mice and rats, while ants carrying salmonellae or Staphylococcus aureus in a human
some strains only affect vertebrate tumour cells. When combined hospital may pose an even greater threat to immuno-compromized
with Acinetobacter calcoaceticus var. anitratus, Bacillus thuringiensis patients, particularly if the nosocomial strains are multi-resistant to
ssp. israelensis was reported to produce discoloration and other several antibiotics. Finally, many infections were performed under
cutaneous symptoms when inoculated accidentally into the finger. in-vitro conditions, and doses were applied which were higher that
Separately, neither bacteria type produced any disorder (Tanada & would be expected under natural conditions (Broderick, Raffa,
Kaya, 1993). Still, some Bacillus spp. and Paenibacillus sp. are Goodman, & Handelsman, 2004; Greenberg & Klowden, 1972;
capable of producing HBL enterotoxins which are usually associated Moreira, de Morais, Vieira da Motta, Campos Farinha, & Tonhasca,
with B. cereus, i.e. B. coagulans, B. megaterium, and B. thuringiensis 2005; Tanada & Kaya, 1993).
(Jay, Loessner, & Golden, 2005). The bacterial species presented so far were encountered in
Another important issue is the method used to determine bac- (respectively on) living or recently dead NCA. Few data exists on
teria. Classical culturing expectedly yields less data than micro- NCA prepared as a foodstuff. The microbiological properties of
biome analysis based on molecular biology techniques. To provide Botswanan saturniid caterpillars (“phane”) were studied exten-
an example, the results published by Belda et al. (2011) on the sively by Mpuchane et al. (2000). Total bacterial count (TBC) varied
microbiome of the European corn borer (Crambidae: Ostrinia from 1  102e2  103 CFU/g for laboratory-processed phane to
nubilalis; Table 5) mention a series of pathogens not encountered so 1  104e2  108 CFU/g for phane sampled while processing or sold
far in other insects (e.g. Brucella abortus, B. melitensis, and Strepto- on the market. Drying the caterpillars on plain ground enhanced
coccus pyogenes). On one hand and unlike other insect guts, the Bacillus spp. Pathogenic and opportunistic taxa were isolated, i.e.
lepidopteran one has an alcalinic pH. On the other hand, data is Arthrobacter spp., Bacillus cereus, B. licheniformis, B. megaterium,
based on predicted genes only. B. mycoides, B. pumilus, B. subtilis, Paenibacillus circulans, Spor-
Special attention must be laid upon Rickettsiella spp. which was osarcina pasteurii, Flavobacterium spp., Pseudomonas spp., and
identified as infecting invertebrates and vertebrates likewise. Xanthomonas spp. Bacillus brevis and Geobacillus stearothermophilus
Experimentally, infection with R. grylli occurs is the respiratory are known to be entomopathogenic and apathogenic, respectively,
tract, leading to chronical bronchopneumonia. Initially an infection while B. licheniformis and B. badius act as spoilage bacteria.
per os was excluded (Ignoffo, 1973), but then it was seen that Own microbiological analyses (Grabowski & Klein, 2010;
symptoms developed by both intranasal and oral challenge 
Grabowski, Jansen, & Klein, 2014; Grabowski, Ramírez Alvarez, &
(Delmas & Timon-David, 1984). Klein, 2011) were carried out with dried insects introduced into
Data presented in Tables 1e7 only refers to the bacteria Germany and edible insects sold as pet food. A sample of caterpil-
encountered in NCA in a very basic way. To evaluate an individual lars of the West African saturniid Cirina forda yielded a TBC of
risk, much more information is necessary, as some pathogens are 5.7  107 CFU/g and contained high amounts of Bacillus spp. (non-
only present in certain instars and absent in others. Many patho- B. cereus). Mexican grasshoppers (Acrididae: Sphenarium spp.) dis-
gens ingested by larvae are eliminated once the final meta- played a TBC of 5.7  103 containing E. coli and other coliforms,
morphosis towards the imago instar is completed because this step enterococci, Bacillus cereus, and clostridia.
86 N.Th. Grabowski, G. Klein / Trends in Food Science & Technology 63 (2017) 80e90

4. Human health implications and consumption by one and the same person to a coordinated
market for entire countries:
4.1. Arthropod hosts

Level 1: NCA are caught and consumed by the same individuals, or
The information contained in Tables 1e7 shows that, depending shared with some companions. NCA comprise insects, spiders,
on the pathogenic taxon, some microorganisms are known to be scorpions and centipedes. This is typical for many hunter-
associated with certain species (e.g. silkworms or honeybees), a gatherer or forager societies, but also for some agricultural so-
certain family (scarabeid beetles), order (hymenopterans) or even cieties that improve their diet with NCA (e.g. indigenous
class (insects), i.e. they reportedly may affect only one, a few or a Australian, Papuan, Indonesian or Amazonian peoples). Knowl-
great variety of arthropod species. Additionally, each taxon yields edge on which species may be consumed under which condi-
an individual combination of bacteria encountered. This reflects the tions is passed on via (oral) tradition. NCA consumption may
categorization into a bacterial core community on one hand and the also be mediated culturally (e.g. partial taboos, magic, and
supplementary community on the other hand (Tang et al., 2012) myths).
which can be extrapolated from species to family and order levels.
Level 2: NCA are caught, eventually processed and sold in public by
However and as mentioned before, information on infected NCA the same individuals, usually on local markets. NCA species are
species at present is selective (hospital hygiene, pest control etc.) mostly insects. People involved in this trade usually have an
and far from complete, and many more interactions are expected to agricultural background. In Mexico, edible pentatomid bugs are
be revaled in the future. This is the reason why this review chose to caught and sold alive, while Sphenarium spp. grasshoppers are
present the data on arthropod family level and beyond. caught, allowed to starve one day, killed, roasted and sold. In
These differences were expected as they also occur in more Western Africa, saturniid caterpillars are gathered, squeezed out
common lifestock species. However, bacterial infections use to be and cooked, then dried or smoked, and then sold.
less host-specific than viral ones, and in this way, salmonellae can
Level 3: NCA trade involves two or more distinct groups of persons:
also affect a series of vertebrates. gatherers and/or rearers, and traders and/or processors that may
also act as vendors. NCA species are recruited from many different
4.2. Class of pathogen taxa. The product they offer usually is of the ready-to-consume
type (e.g. insects offered as street food in the larger cities in
While microorganisms categorised in group I may pose a risk for Thailand). These insects are bought from Thai or Cambodian
NCA consumers, those contained in group II only affect the in- gatherers or rearers, stored as frozen, and thawed and processed
vertebrates and would not represent a direct threat to the con- on a daily basis. The insect species traded here would also
sumers' health. However, NCA affected or killed by class II include silkworm pupae from industrial silk production.
pathogens affect the quality including taste of the animals, partic-
Level 4: NCA trade refers to similar players as in level 3. Unlike the
ularly if the dead animals had entered a state of putrefaction before latter, this level involves a higher degree of industrialization leading
processing. This is why it is recommended to separate living edible to preserved NCA products, mostly insects and scorpions. Examples
insects from the dead ones before (Grabowski & Klein, 2015b). are canned saturniid caterpillars in South Africa, dried Sphena-
Pathogens classified in group III can affect any human being, rium spp. grasshoppers in Mexico, sold in sealed plastic con-
regardless of his or her consumption habits (considering however tainers, or butterfly caterpillars (“gusano del maguey”; several
the immune status). From the food hygiene point of view, the lepidopteran families) and scorpions contained in Mexican
importance of NCA as passive transmitters of microorganisms is far mescal, a spirit (Hanboonsong et al., 2013; Menzel & D'Alusio,
more important as their role of vectors for several infectious dis- 1998).
eases; immune-suppressed and immune-competent patients alike
can be affected by a series of typical food-borne pathogens. Finally, These levels can also occur in traditionally-non-
the section of transmitted spoilage agents appears small, but this entomophageous (TNE) societies in which only few persons
area is possibly not well-studied, and corresponding future studies consume NCA, although some modifications are observed starting
are prone to reveal a major relevance. with the amount of persons involved in entomophagy:
The present review contains all the pathogens cited in the sci-
entific EFSA opinion on edible insects (done on genus level only, i.e.
Level 1: Due to species protection legislation and awareness of
Acinetobacter, Bacillus, Campylobacter, Escherichia, Micrococcus, environmental pollution, gathering native NCA in TNE societies
Proteus, Pseudomonas, Salmonella, Staphylocccus, and Streptococcus) is uncommon. One rare exception are those whishing to adopt
and a series of additional genera. However, the EFSA list is based on survival skills as a sport, which eventually would also include
(scarce) data found on farmed insects only. It however shows that gathering and consuming NCA under very simple conditions.
many pathogens known from wild-rearing, raw insects made their Besides, some pet keepers breed their own NCA for feeding and/
way into the existing production systems, probably belonging to or display reasons, and they might also consume NCA them-
the core community, and since some of those mentioned in the selves. Finally, a soup based on adult cockchafer (Scarabeidae:
present review may not grow readily on rountine media, their non- Melolontha spp.) beetles was consumed in Alsace-Lorraine (now
viability under farming conditions remains to be investigated more belonging to Germany and France), and some children in
intensively. Yet, farming insects does not seem to broaden the Northern Italy still collect certain zygaeniid caterpillars in order
spectrum of pathogens so far, suggesting that similar mechanisms to consume the low-toxic but very sweet ingluvies (crops).
of microbial development occur in wild and farmed insects, and
Level 2: Artificially-reared insects sold on-line to NCA con-
that NCA are as prone to become carriers of bacteria from the sumers would be the European equivalent. Typical species are
environment as other livestock. Locusta migratoria and Schistocerca gregaria locusts, Acheta
domesticus und Gryllus spp. crickets, and Tenebrio molitor,
4.3. Level of technification Alphitobius spp., and Zophobas atratus larvae.

Level 3: “Public” consumption is limited to specialized restau-
On a global scale, traditional entomophagy (TE) is practised on rants, cooking classes, and extraordinary events (e.g. trading
different levels of technification, ranging from simple gathering fares, scientific studies and television shows). Besides that, any
 N.Th. Grabowski, G. Klein / Trends in Food Science & Technology 63 (2017) 80e90 87

pet shop selling food insects (see level 2) or NCA usually household.
destined for keeping and display to NCA consumers would also Levels 3 and 4 are characterized by the inclusion of a series of
enter this category. intermediates between producer and consumer, extending the time

Level 4: This level is developing focally also in TNE societies, between killing and consuming even more. This also implies effi-
exemplarily by selling processed foodstuffs containing NCA, e.g. cient means to extend shelf life, stressing the need to avoid the
candies with entire animals, cookies and nuggets made with a growth of food spoilers. So, the array of microorganisms, especially
certain percentage of mealworm meal (Grabowski & Klein, bacteria, is thought to shift from zoonotic to spoilage. In either way,
2015b, 2016a; Van Huis et al., 2013). NCA are traditionally submitted to heat treatment, eventually
including drying (when a longer storage is intended) to reduce the
Law issues also interfere with these categories in a much more bacterial counts and eliminate pathogens.
pronounced way that in TE societies where many NCA have a status
comparable to the United States' concept of GRAS (“generally 4.4. Tradition and recommendations
regarded as safe”).
The exposure risk is expected to change in relation to the degree In this way, traditional NCA consumption includes, in many
of technification and the role of the person involved. cases, animals to be caught, killed (usually by heat), eventually
eviscerated (caterpillars and grubs), washed, and heated (Menzel &

Class I pathogens may pose a risk to primary producers D'Alusio, 1998). In order to extend shelf life, drying may take place.
(including hunters and gatherers) and everyone else before the Considering the microbiological risks exposed in section 3, this a
animals are processed, particularly when the disease is sub- sensible procedure which is reinforced by many authors of NCA
clinical in the animal, cooking books for TNE countries (Fritzsche & Gitsaga, 2002;

Class II pathogens are not expected to affect humans, but are Gordon, 1998). In his book on survival training in the field,
prone to impair the food quality if diseased animals are pro- Sackmann (2011) also claims that washing and thorough heating
cessed along with healthy ones, and in insect farming, ento- are mandatory to feed on invertebrates. Washing of course implies
mopathogens may infect entire charges, meaning economical clean water, and while this step is strongly recommended under
loss, normal conditions, clean water may a limiting factor in the wild.

Class III pathogens may be a risk for all actors engaged in the Ramos Elorduy and Menzel (1998) however recommend not
production and consumption chain until animals are processed washing insects before preparation in order to improve the taste, as
in a way to eliminate these pathogens, and certain pheromones are prone to add to it. Besides, they claim that

Class IV may become more important with the increasing pro- surface antibiotics would prevent the insects from being carriers of
duction chain, i.e. rotten animals will be excluded from gath- major pathogens. A chemical skin protection is known in many
ering, but with increasing amounts, control may become more living beings, but as Tables 1e7 show, many pathogens are able to
difficult, and spoilage bacteria can take over if storage is penetrate this defence mechanism. The role of potential edible NCA
inadequate. as pathogen carriers has also been stressed, so that it is recom-
mended to wash the animals before further preparation, in spite of
In this way, a shift from pathogens toward food spoilers occurs the fact that this preparation usually includes heating. Further in-
with an increasing food chain length and complexity. Level 1 fo- vestigations will be necessary to justify the omission of this hy-
cuses on a very short food chain, characterized by the fact that the gienic procedure.
one who obtains the NCA is basically the same person to consume Ramos Elorduy and Menzel (1998) also recommend not freezing
them, and by a short span of time from obtention to consumption. the animals because of a reduced taste. While this may be feasible
This level occurs in both TE and TNE countries resp. societies. Level on consumption levels 1 and 2, in the more technified TNE coun-
1 comsumers are expected to be exposed to a greater variety of tries with longer trading routes, freezing is one effective way to
pathogens than consumers at the end of longer food chains. Food extend shelf life before and after acquisition by the consumer.
control can only take place by the actors themselves, relying on Freezing is also practiced by sellers of deep-fried insects as street-
their knowledge and experience. They are unlikely to include ani- food in Thailand. In order to ensure a constant supply in Bangkok,
mals found dead in an unknown state of putrifaction. They are they buy the dead animals at the Thai-Cambodian border and
certain to exclude those specimens suggestedly associated with a freeze them. Besides that, freezing is one humane method of killing
zoonotic disease (“odd-looking”) and know the procedures to invertebrates accepted by animal welfare specialists.2 So, freezing
eliminate potential hazards (e.g. squeezing out, cooking, and sun- may reduce flavour, but as with raw milk consumption, food safety
drying). TE country dwellers will doubtlessly have a deeper and should be rated higher than some flavour experience.
broader knowledge than a person producing and consuming NCA Raw arthropod consumption is also part of the entomophagous
for his own need in a TNE country who might be eventually only tradition worldwide (Chung, 2010; Costa Neto & Ramos Elorduy,
experienced in the species he rears (Menzel & D'Alusio, 1998). 2006; Van Huis, 2003; Yen, 2010). However, this seems to be
In level 2, NCA are consumed by persons that did neither catch limited to insects, since other NCA are toxic, and heating is neces-
nor rear the animals. Unless they are sold alive, there is an extended sary to inactivate the toxins (Yen & Ro, 2013). Comby (1994) was
time between killing and consuming, providing the opportunity for one of the first recent authors to promote insect consumption in
food spoilers to grow. So, either the span is short enough and/or the Europe. Although he admits the possibility to heat them, he rec-
preparation at the household is efficient enough to avoid major ommends eating them raw, or even alive. While the latter, despite
risks, or the seller prepared the animals himself to ensure a more an existing tradition in Africa (Van Huis, 2003), to cite only one
extended shelf life (e.g. by drying). As in level 1, a sufficient example, has to be discouraged from the ethical point of view,
knowledge on preparing and ensuring food safety must be ex- consumption of raw insects can still be discussed controversely.
pected in TE households (Menzel & D'Alusio, 1998). In TNE societies, On one hand, there are many examples of insects eaten raw. This
consuming this kind of foodstuff is but sporadical. However it may
be expected that the few households engaged regularly in this food
habit may have a comparable knowledge to that of TNE households. 2
Prof. Hansjoachim Hackbarth, Hannover University of Veterinary Medicine,
Problems may arise when the NCA are newly introduced into a Foundation, personal communication.
88 N.Th. Grabowski, G. Klein / Trends in Food Science & Technology 63 (2017) 80e90

consumption may occur in the field, when an edible insect is place only on level 2. People who reared their own insects, having
encountered. Also, some insects are sold alive, bearing the potential complete control of the entire production cycle, and dealing with
of consuming them raw at home (Chung, 2010). Animals may be species that are not toxic in their raw state, could consume them
eaten as entire animals or mashed resp. ground with spices unheated. Raw animals could only be sold frozen or alive in order to
(Adeoye, Alebiosu, Akinyemi, & Adeniran, 2014; Costa Neto & reach more consumers. This would resemble the trade with raw
Ramos Elorduy, 2006). In this way, raw insect consumption may milk practiced in some countries, like in Germany. There, to ensure
typically take place in TE countries and on the consumption levels 1 a maximum of food safety, this so-called “attested milk” has to be
to 3. produced observing strict hygiene standards, and production is
On the other hand, not all insects are traditionally eaten raw. The monitored closely by the authorities. Currently, this procedure does
question on which insects may be consumed raw can be answered not exist in TNE countries, of which only some consider insects in
only on a specific culture level, since the degree varies with the their food law at all (Halloran, Vantomme, Hanboonsong, & Ekesi,
ethnic group and their cultural idiosyncrasies. In their survey 2015).
conducted in northeastern Thailand, Hanboonsong, Rattanapan,
Waikakul, and Liwvanich (2001) found that 93% of questionnaire 5. Conclusion
respondents consumed raw insects. However, in Thailand in gen-
eral, insects are typically eaten after heating rather than raw Although NCA do not form part of the current food habits in
(Hanboonsong, 2010). A Nigerian study revealed 30% of raw insect Europe or other “Western” countries to a major extent, the means
consumers (Adeoye et al., 2014). In Borneo, only those insects with to ensure food safety from the microbiological point of view do not
soft bodies like hymenopteran and lepidopteran larvae or pupae are differ from those adapted for other, more common foodstuffs: hy-
likely eaten raw (Chung, 2010). On Kiriwina Island belonging to gienic obtention, washing and heating are principles which are
Papua New Guinea, raw insect consumption depends on the size of practiced daily in every household, and there is no reason to change
the animals, as small to medium-sized insects are eaten raw, while this when preparing non-crustacean arthropods. Raw consumption
the larger ones are submitted to heating. On the mailand, raw insect as practiced in many TE countries may be safe within a very
consumption depends on the indigenous group (Meyer-Rochow, narrowly-defined, traditional frame. Environment changes how-
1973; Schiefenho € vel & Blum, 2007). In Japan, insects are typically ever may affect this tradition, particularly in TE countries. For TNE
boiled in soy sauce and sugar (“tsukudani”). There are several other countries, eating raw NCA is discouraged until more information
preparation ways, but raw consumption is not traditional there proving the opposite will be available.
(Mitsuhashi, 1997; Nonaka, 2010). Insects are always served heated
in Northern Benin (Riggi, Veronesi, Verspoor, & MacFarlane, 2013)
Acknowledgements
just as caterpillars are in Mexico (Ramos Elorduy et al., 2011).
The practice of eating raw insects should be evaluated thor-
The authors whish to express their gratitude to Dr. Wiebke
oughly. This review shows the microbiological risks associated with
Jansen, formerly at the Institute for Food Quality and Food Safety
raw insect consumption. The reason why eating raw insects has
(LMQS), Hannover University of Veterinary Medicine, for proof-
continued from ancient times on in TE countries the first place,
reading the article.
despite having dominated the fire, remains speculative. However, a
practical point of view would be because the advantages out-
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