POTENTIAL HEALTH AND SAFETY ISSUES IN THE SMALL-SCALE PRODUCTION OF FLY LARVAE FOR ANIMAL FEED-A REVIEW

Abstract

Fly larvae from Musca domestica and Hermetia illucens, are increasingly considered for animal feed worldwide because they represent a viable and sustainable alternative protein source. However , the use of fly larvae as animal feed also raises concerns regarding health and safety for the fed animal, the consumer and the producer. Studies are presently being carried out in the framework of large production systems, but the use of fly larvae is also commonly advised in small-scale, rural systems, which may raise different safety concerns. The review the potential health and safety issues associated to the small-scale production of fly larvae on farm, with particular focus on Africa. Three categories of health and safety hazards are considered: those affecting the animal, the consumer and the producer. The most likely effects on animal health are through contamination of the rearing substrates or inadequate processing and storing conditions. Many chemical and biological contaminants also have the ability to pass through the food chain and reach the consumer, although studies on the safety of meat and fish produced with fly larvae are clearly lacking. Similarly , the potential effect of rearing fly larvae on the producers' health in small-scale production systems have not yet been considered in any study. Flies can potentially affect producers mainly through allergies as well as disease transmission by adult flies and substrate manipulation. The production of insects for animal feed does not pose more health and safety issues than the production of other animal protein sources but more research is clearly needed. The review provides recommendations for further research.

Full text

Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
POTENTIAL HEALTH AND SAFETY ISSUES IN THE
SMALL-SCALE PRODUCTION OF FLY LARVAE
FOR ANIMAL FEED-A REVIEW
Nkegbe1, E. K., Adu-Aboagye1, G., Affedzie1, O. S., Nacambo2, S.,
Boafo3, A. B., Kenis2, M., and Wallace1, P.
1CSIR-Animal Research Institute
2CABI, 2800 Delemont, Switzerland
3CABI-West Africa, Accra
ABSTRACT
Fly larvae from Musca domestica and Hermetia illucens, are increasingly considered for animal
feed worldwide because they represent a viable and sustainable alternative protein source. Howev-
er, the use of fly larvae as animal feed also raises concerns regarding health and safety for the fed
animal, the consumer and the producer. Studies are presently being carried out in the framework
of large production systems, but the use of fly larvae is also commonly advised in small-scale, rural
systems, which may raise different safety concerns. The review the potential health and safety is-
sues associated to the small-scale production of fly larvae on farm, with particular focus on Africa.
Three categories of health and safety hazards are considered: those affecting the animal, the con-
sumer and the producer. The most likely effects on animal health are through contamination of
the rearing substrates or inadequate processing and storing conditions. Many chemical and biolog-
ical contaminants also have the ability to pass through the food chain and reach the consumer,
although studies on the safety of meat and fish produced with fly larvae are clearly lacking. Simi-
larly, the potential effect of rearing fly larvae on the producers’ health in small-scale production
systems have not yet been considered in any study. Flies can potentially affect producers mainly
through allergies as well as disease transmission by adult flies and substrate manipulation. The
production of insects for animal feed does not pose more health and safety issues than the produc-
tion of other animal protein sources but more research is clearly needed. The review provides rec-
ommendations for further research.
Keywords: biological, chemical, larvae, feed, substrates, processing
INTRODUCTION
The use of insects to feed livestock has a long
tradition in Africa (Kenis et al., 2014). However,
the increasing prices of the few conventional
protein sources for animal feed as well as the
need to improve the performances of traditional
animal farming has in recent times led to the
exploration and development of many new initi-
atives aimed at enhancing the use of insects as
animal feed. Fly larvae are particularly suited for
the production of protein for animal feed be-
cause they can be produced rapidly and at rela-
tively lower cost using waste organic material
such as manures, domestic or market waste
among others. Furthermore, fly larvae are suita-
ble for large livestock production and smallhold-
er farms (Charlton et al., 2015). Two fly species
namely the black soldier fly (Hermetia illucens)
and the house fly (Musca domestica) are pres-
ently being promoted for feed production world-
wide (Park et al., 2015). In Africa, M. domestica
larvae are occasionally used to feed animals. For
example, in Benin about 6% of smallholder
farmers use them at least occasionally for poul-
Ghanaian Journal of Animal Science, Vol. 9 No.1, 2018 1

Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
try feeding (Pomalegni et al., 2016).
In order to increase the efficiency of available
production methods, new rearing techniques are
presently being developed (Maciel, 2014; Koné
et al., 2016). In contrast, H. illucens, an exotic
species established in Africa, has no tradition in
the continent. Production techniques for H. illu-
cens were first developed in North America,
from where the fly originates (Newton et al.,
1977, Bondari and Sheppard, 1987) but its use
for feed or waste reduction is increasingly pro-
moted elsewhere (Diener et al. 2011; Caruso et
al., 2013; Drew and Pieterse 2015; Maurer et
al., 2016). The two species reportedly can be
produced either by rearing the adults in captivity
and placing eggs on substrates, or by exposing
substrates for natural oviposition (Kenis et al.,
2014). Production could take place in large fac-
tories which aim at commercializing dry larvae
or larvae extracts for the animal feed market
(Drew and Pieterse, 2015). There are also sys-
tems that can be directly associated to farms,
from large livestock producers to smallholder
farmers which feed their own animals (Caruso et
al., 2013; Koné et al., 2016; Zhao et al., 2016).
Various issues have been reported to be associat-
ed with the use of fly larvae as animal feed.
Health and safety concerns have been empha-
sized to be neglected (van der Spiegel 2013;
Charlton et al., 2015). The risks related to the
use of insects as food and feed are increasingly
being addressed by national and regional organi-
sations (EFSA, 2015 and ANSES, 2015), but
these usually rather refer to large production
units, mostly in developed countries. In this re-
view, attention is specifically focused on the
potential health and safety issues associated with
the small-scale production of fly larvae, M. do-
mestica and H. illucens. Though the review fo-
cuses on the situation in Africa it is expected
that conclusions and recommendations drawn,
be valid for other regions where similar systems
are used. Generally three categories of health
and safety hazards would form the basis of the
review and these include those affecting animal,
consumer and producer.
ANIMAL HEALTH AND SAFETY
The most likely health issue posed by the use of
insect as feed is the direct effect on animal
health. Fly larvae themselves can potentially
induce allergies but, it is widely recognized that
healthy fly larvae have positive effect on growth
performance of animals (Kenis et al., 2014;
Makkar et al., 2014). In all these studies almost
none reported any abnormal mortalities when fly
larvae were used as feed for animals. The most
likely chemical or biological contamination
pathway is through a contaminated rearing sub-
strate or inadequate processing and storing con-
ditions (van Der et al., 2013; EFSA, 2015).
DIRECT EFFECT OF FLY LARVAE ON
ANIMAL HEALTH
Allergy risks are known to occur both in humans
and animals as animals can develop allergies
with similar symptoms to humans and that in-
cludes cutaneous erythema, scratching diarrhea,
vascular congestion of ears, nose, etc. However,
there is little information regarding natural food
allergy in farm animals and fish (Boyce et al.,
2010). So far, no observation of any sign of al-
lergy or detrimental effect of fly larvae ingestion
in animal has been documented. An exception
for this general view is an experiment carried out
by Bouafou et al. (2011) on rats, which showed
that ingestion of 10% dried maggot meal caused
them histological and pathological damages.
Contrary to the above findings, Li et al. (2011)
concluded that there is no embryonic and terato-
genic toxicity for M. domestica larvae powder
on mice. Furthermore, Lei et al. (1998) showed
that Kunning mice exhibited increased functions
in immunity as well as increase in humoral and
macrophage phagocytosis when fed on different
doses of fly larvae active powder. This powder
reportedly could also resist radiation, protects
the liver from CCI4 and delay senility.
In broilers, Téguia et al. (2002) detected an in-
crease in liver and gizzard mass when the level
of maggot meal in the diet increased from 50 to
100% substitution of fishmeal, which suggested
a potential toxic effect. However, in a more
complete study, Pretorius (2011) evaluated M.
domestica pupae and larvae meal in terms of
possible toxicities, organ stress and immune
suppression in broilers. The results showed that
neither the use of M. domestica larvae, pupae
meal nor the temperature of drying of larvae
meal (45 – 85ºC) induced gizzard erosion; a sa-
fety index was further shown that use of the M.
domestica larvae meal did not have any detri-
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Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
mental effect in any of the gastrointestinal and
organ parameters assessed.
Other studies tend to show that fly larvae in feed
have positive effect on animal health. For exam-
ple, it was noted in a Chinese study that the he-
moglobin levels of experimental animals im-
proved (Zhang and Yao, 1998). Hou (2008) not-
ed that M. domestica maggot meals reduced
production duration to 20-30 days and upgraded
survival rate and immunity in shrimps and tur-
tles. This was confirmed in hens by Lang et al.,
(2004) who discovered that fresh housefly larvae
fed to hens improved their immunity.
Generally, fly larvae, particularly M. domestica
are well known for their antibacterial and antiox-
idant effects (Wang et al., 2004, 2005; Cao et al.,
2006). Similarly, Choi et al. (2012) demonstrat-
ed that methanol extracts of H. illucens larvae
not only had antibacterial activity but also pos-
sess unique properties, which effectively
blocked viability of the bacteria. Extracts of H.
illucens larvae also showed antibacterial activi-
ty against plant pathogens (Park et al., 2015).
INDIRECT EFFECTS THROUGH
PRODUCTION CONDITIONS
Negative effects on animal health are likely to be
caused by the use of contaminated substrates. In
particular, manure can contain a lot of animal
and human pathogens (Strauch 1991; EPA,
2013; Chen and Jiang, 2014). Pathogens found
in insect rearing substrates can be found in the
insect itself (Erickson et al., 2004; Belluco et al.,
2013; Lalander et al., 2013).
Substrates, reportedly can also contain many
chemical contaminants Petersen et al., 2007 Hal-
ling-Sørensen et al.,(1998) and these can enter
into the food chain (Belluco et al., 2013; Charl-
ton et al., 2015; Diener et al., 2015). For exam-
ple, Zhuang et al. (2009) observed the accumula-
tion and transfer of trace and heavy metal (Pb,
Zn, Cu, and Cd) along a soil-plant-insect chick-
en food chain at contaminated sites. Diener et al.
(2015) fed H. illucens larvae in chicken feed
spiked with heavy metals (Cd, Pb and Zn). Lar-
vae and pre-pupae accumulated Cd, yet the in-
corporation of Pb and Zn was suppressed as con-
centrations found in the body were lower than in
the food. None of the three heavy metal had sig-
nificant effects on the life cycle determinants
(prepupal weight, development time and sex
ratio).
Charlton et al. (2015) worked extensively on
contaminants in house fly and Black soldier fly
larvae meal from Europe, Asia and Africa. They
analyzed veterinary medicine, pesticides, heavy
metals, dioxins, polychlorinated biphenyls and
polyaromatic hydrocarbons and mycotoxins. In
most cases, contaminants, when found, were
below recommended maximum concentrations
suggested by bodies such as European Commis-
sion, World Health Organisation and Codex Ali-
mentarius. The main concern was the presence
of the toxic heavy metal, Cadmium that was
found in all samples. In three M. domestica sam-
ples, the level was slightly above the lowest EU
limit for cadmium in animal feed (500 μg/kg).
In addition, nicarbazin, a coccidiostat (4, 4-
dinitrocarbanilide) was detected in M. domesti-
ca, but the observation needed further assess-
ment in order to determine its concentration and
compare it to National Standards for poultry
feed. An insecticide, Chlorpyrifos, was found in
M. domestica larvae at 800 µg/kg. At this level,
it does not pose significant safety threat com-
pared to the 5000 µg/kg threshold for this organ-
ophosphate in EU regulations. However the
presence of pesticides in fly larvae needs further
consideration. Similarly polychlorinated biphen-
yls were present but at lower concentration than
the threshold fixed by EU for animal feed (10
µg/kg).
Polyaromatic hydrocarbons were also detected
as well as several naturally occurring mycotox-
ins and these included beauvericin and enniatin.
Aflatoxin was however absent. In a Chinese
study, proteins extracted from housefly larvae
powder contained lower heavy metals (Pb, As
and Hg) than the minimum levels expected in
the natural food standards and also contained no
pathogens (Zhang et al., 2009). In some cases,
infections can also come from inadequate pro-
cessing and storing conditions. Awoniyi et al.
(2004) showed that improperly stored samples of
maggot meal was prone to deterioration by fungi
and bacteria particular when moisture content
was too high. They recommended drying the
larvae to 4–5% moisture content and then further
prevention of moisture absorption by adopting
appropriate packaging and storage systems.
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Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
Artisanal fly larvae production systems are
prone to contaminations by way of substrates
and other production conditions unlike in indus-
trial procedures, where heat treatments, proper
storage systems, protein extractions, etc. are
likely to reduce risks of contamination, especial-
ly those of biological origin. In contrast, in sys-
tems where larvae are not treated but given fresh
or sun- dried to animals, pathogens are more
likely to be passed from the substrate to the fed
animal, in particular when larvae have been
reared on manure from the same animal species.
For example, Salmonella spp. and many other
pathogenic bacteria and viruses are commonly
found in manure (Strauch, 1991; EPA, 2013;
Chen and Jiang, 2014). In such cases, rearing
flies on manure produced in the same produc-
tion unit is preferable to importing manure from
another producer. The storage conditions of ma-
nure before being used to rear larvae is also im-
portant, for example, pathogens do not survive
very long in stored manure because of the tem-
peratures and biological and biochemical activi-
ties prevailing in the middens, in contrast to slur-
ry, in which the temperature does not rise as
much and biochemical activity is lower (Strauch,
1991).
Interestingly, Lalander et al. (2015) showed that
the conversion of human and pig manure mixed
with organic waste by H. illucens resulted in a
drastic reduction of Salmonella spp. and viruses
in the treatment residue. In a previous study,
Lalander et al. (2013) had examined the effect of
H. illucens larvae on the concentration of patho-
genic microorganisms in human faeces and
found an increased reduction in Salmonella spp.
after eight days. In prepupae, Salmonella spp.
was reduced to an undetectable level. In con-
trast, ascaris eggs and enterococcus were not
inactivated/destroyed. Erickson et al. (2004)
observed a similar reduction of E. coli and S.
enterica serovar enteritidis in chicken manure
treated with H. illucens.
In addition, a house fly production system based
on natural oviposition may enhance fly densities
on site. Considering the ability of M. domestica
adults to transmit diseases, such rearing could
locally affect not only human health, but also
animals if the animals are kept in close vicinity
of the fly larvae production unit. For example, it
has been shown that flies in poultry houses may
be vectors of Salmonella enterica serovar enter-
itidis (Holt et al., 2007) and Campylobacter
(Nelson and Harris, 2006).
CONSUMER’S HEALTH AND SAFETY
Transmission of contaminants to consumers
There are hardly any studies having analyzed
potential contaminants in meat or eggs resulting
from animals fed with insects. However, many
contaminants that are found in the larvae may
potentially pass through the meat, fish or egg
and affect human health (Van Der et al., 2013).
For example, when flies transmit Salmonella
enterica to the poultry (Holt et al., 2007), the
bacteria can easily be transmitted to the consum-
er if the meat or eggs are not properly treated.
Similarly, chemical contaminants such as heavy
metals or dioxins accumulate along the food
chain to the final consumer (Belluco et al.,
2013). Further work on the biosafety of eggs,
milk, fish and meat is necessary to ascertain the
bioaccumulation of chemical and microbiologi-
cal contaminants (Charlton et al., 2015). On the
positive side, EFSA (2015) states that mammali-
an prions cannot replicate in insects. However, it
should be investigated to ascertain whether fly
larvae could still potentially be mechanical vec-
tors of prions from substrates to human or rumi-
nant. Insects fed on substrates of non-human and
non-ruminant origin should be safer.
Product quality for human consumption
Some studies conducted have highlighted and
evaluated the quality of meat or eggs from ani-
mals fed with fly larvae. Aniebo et al. (2011)
tested the substitution of fishmeal with maggot
meal in catfish regimen and its impact on fla-
vour, juiciness and texture/mouth feel and
showed no negative effects on the quality and
acceptability of the final products. Akpodiete et
al., (1998) showed that maggot meal could nu-
tritionally and productively replace fishmeal in a
layer diet without adverse consequences on per-
formance and egg quality characteristics. Egg
yolk cholesterol and calcium concentration were
significantly reduced in the lots fed with fly lar-
vae. A consumer preference study revealed no
difference in taste between chicken fed with
fishmeal and fly larvae (Awoniyi, 2007).
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Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
PRODUCER’S HEALTH AND SAFETY
To our knowledge, the potential effect of fly
larvae on the health of fly larvae producers and
their workers has not yet been considered in any
specific study. Flies can affect workers mainly in
two ways. Firstly, as in all insect rearing, fly
production systems may cause allergies. Second-
ly, adults, and larvae in their substrates, can
transmit diseases.
Human Allergies
Van Huis et al., (2013) cited allergies as a major
health and safety issue to be addressed when
rearing insects as food and feed because many
insects are known to induce inhalant and contact
allergic reactions in man, particularly in rearing
facilities (Wirtz, 1980, 1984; Bellas, 1990,
Lopata et al., 2005). Sources of allergy in insects
are linked to dried exuviates, hairs, metabolic
products, faeces, silk, etc. Brinchmann et al.
(2011) also cited chitin as a possible allergen.
Flies are not particularly known for being aller-
genic although some isolated cases of nasal dis-
charge and ocular itch caused by M. domestica
have been reported (Tee et al., 1985; Wahl and
Fraedrich, 1997; Focke et al., 2003). M. domes-
tica tropomyosin showed cross-reactivity with
sera from patients with allergy to various house-
hold arthropods (Martínez et al., 1997).
Romero et al. (2016) studied the larvae of four
fly species including M . domestica and H. illu-
cens and focused on the homology of tropomyo-
sin, arginine kinase and myosin light chain with
the crustacean orthologous proteins and other
known allergenic proteins. It was found that the
three proteins share homology with known aller-
gens and therefore it was likely that individuals
allergic to crustaceans would also be allergic to
fly larvae. Ingestion would not be necessary
since people who are allergic to food by inges-
tion can react to the same allergen by inhalation
or smelling (Ramirez and Bahna, 2009).
Allergies related to the substrates used for rear-
ing flies cannot be discounted. For instance the
proliferation of fungal spores or mites could
induce allergenic response. However, no such
incidence has been reported in literature.
Diseases transmission
Adult M. domestica and other flies are known to
transport and transmit many pathogens including
bacteria, protozoa, virus, rickettsia, fungi and
helminths (Greenberg, 1973; Scott et al., 2014;
Phoku et al., 2014). Classical examples of dis-
eases transmitted by flies include salmonello-
sis,ophthalmia, shigellosis, typhoid fever and
infantile diarrhea. Of all these, M. domestica is
considered as a worldwide pest that is common-
ly the target of management programmes. Adults
in cages or other closed environments are proba-
bly much cleaner than the free range flies, espe-
cially when they are not in direct contact with
the rearing substrate. In contrast, systems based
on natural oviposition on exposed substrate may
locally increase fly populations and, subsequent-
ly, increase the danger of infection for the breed-
ers and other people in the immediate vicinity of
the fly larvae production facility. Although ob-
servations suggest that the exposure of substrates
on-farm to attract flies does not increase house
fly populations around the farm homestead
(Kenis et al., 2014). However, this needs to be
ascertained through rigorous investigations. Fur-
thermore, it would be important to verify if fly
rearing does not increase the potential for vec-
toring human pathogenic micro-organisms.
Production systems of H. illucens cause much
less concern in this matter since adults do not
feed and, thus, are less likely to transmit patho-
gens.
The pathogenic potential of fly larvae originates
from the substrate in which they are grown and,
thus, strongly depends on the substrate used.
Some substrates are known for carrying human
diseases, in particular animal manure, e.g. Esch-
erichia coli, Campylobacter, Salmonella, Cryp-
tosporidium parvum, and Giardia lamblia (EPA,
2013) or animal offal, e.g. brucellosis, toxoplas-
mosis and leptospirosis (Swai and Schoonman,
2012). The precautions when handling such sub-
strates should be the same as those taken in ani-
mal husbandry.
CONCLUSIONS AND RECOMMENDA-
TIONS
Recent studies and reviews suggest that the use
of insects as animal feed does not pose more
health and safety issues than other animal pro-
tein sources but that chemical accumulation is
still largely unknown. Substrate used to feed the
insects serve as the key entrance point for bio-
logical and chemical contaminations. However,
Ghanaian Journal of Animal Science, Vol. 9 No.1, 2018 5

Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
fly larvae are typically produced on substrates
that are generally considered as potential con-
taminants, such as animal manure, offal and post
-consumer food wastes. Thus studies on the po-
tential bioaccumulation of metals in insects and
in particular cadmium. Assessment of the poten-
tial bioaccumulation of metals in insects and in
particular cadmium should be of paramount con-
cern to larvae producers after.
Their potential levels in poultry and animal
product insect larval meal need to be ascertained
per locality in order to determine their source
and possible relation to the food chain. Small-
scale fly larvae production systems provide more
opportunities for biological and chemical con-
taminations to animals, consumers and produc-
ers than industrial systems. Flies are often given
fresh or dried at low temperatures and, thus,
maintain viable biological contaminants as
feedstuff or feed to animals. Production and stor-
age conditions are more favorable to the devel-
opment of contaminants such as mycotoxins.
More so rearing substrates are not sterilized nor
controlled in order to reduce contaminants.
Generally, quality assessments are reported not
to be carried out. Adult flies are often not con-
fined to rearing cages but fly naturally, and are
therefore, prone to carry biological contami-
nants. Fly larvae are increasingly being assessed
for their safety as animal feed, but it is likely
that most studies only focus on industrial pro-
duction systems. Therefore, it is essential to car-
ry out specific health and safety studies related
to small-scale rearing production systems in
Africa and elsewhere.
Hematology and serum biochemistry of live-
stock suggest the physiological disposition of the
animals to their nutrition. To totally accept the
larvae meal as alternative to soya and fishmeal,
analyses of these hematological and biochemical
parameters need be assessed during trials.
These should include non protein nitrogen, urea,
uric acid, creatine, plasma albumin, plasma
globulin, hemoglobin, fatty acids, cholesterol,
bilirubin, magnesium of serum, calcium, potassi-
um, sodium, chlorides as sodium chloride, total
phosphorus, etc. Safety assessments on the final
food products (meat, egg and fish) need to be
thoroughly studied, in particular for biological
safety, dioxins, heavy metals and pesticides.
Health issues for the producer and other people
exposed to flies have been poorly investigated.
In particular, prior to promote the use of M. do-
mestica production systems based on natural
oviposition, it would be important to further
assess whether this system does not increase the
amount of flies in the vicinity of the production
unit and whether it does not increase the poten-
tial of flies for vectoring human pathogenic mi-
croorganisms.
ACKNOWLEDGEMENT
The authors would want to thank everyone in-
volved in the review of this manuscript for their
useful comments. This study was carried out as
part of the project IFWA - Sustainable use of
insects to improve livestock production and food
security in smallholder farms in West Africa,
funded by the Swiss Agency for Development
and Cooperation and Swiss National Science
Foundation, in the framework of the Swiss Pro-
gramme for Research on Global Issues for De-
velopment (R4D). The financial contribution of
all these is acknowledged with gratitude.
REFERENCE
Akpodiete, O.J., Ologhobo, A.D., and Onwade,
A.A. (1998). Maggot meal as a substitute
for fish meal in laying chicken diet. Journal
of Agricultural Science, 31: 137-142.
Aniebo, A., Odukwe, C., Ebenebe, C., Ajuogu,
P., Owen, O. and Onu, P. (2011). Effect of
housefly. larvae (Musca domestica) meal on
the carcass and sensory qualities of the mud
catfish, (Clarias gariepinus). Advances in
Food and Energy Security. 1: 24-28
ANSES (2015). Opinion on the use of insects as
food and feed and the review of scientific
knowledge on the health risks related to the
consumption of insects. ANSES, Maisons-
Alfort, France. Available at: http://tinyurl.
com/oru9ly9 .
Awoniyi, T.A., Adetuyi, F.C. and Akinyosoye,
F.A. (2004). Microbiological investigation
of maggot meal, stored for use as livestock
feed component. Journal of Food, Agricul-
ture and Environment, 2: 104-106
Awoniyi, T.A.M. (2007). Health, nutritional and
consumers’ acceptability assurance of mag-
got meal inclusion in livestock diet: a re-
Ghanaian Journal of Animal Science, Vol. 9 No.1, 2018
6

Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
view. International Journal of Tropical
Medicine, 2:52-56.
Bellas, T. E. (1990). Occupational inhalant aller-
gy to arthropods. Clinical Reviews and Al-
lergy.8: 15–29.
Belluco, S., Losasso, M., Alonzi, C.C., Paoletti,
M.G. and Ricchi, A. (2013). Edible insects
in a food safety and nutritional perspective:
A critical review. Comprehensive Reviews
in Food Science and Food Safety, 296-313.
Bondari, K. and Sheppard, D.C. (1987). Soldier
fly, Hermetia illucens L., larvae as feed for
channel catfish, Ictalurus punctatus
(Rafinesque), and blue tilapia, Oreochromis
aureus (Steindachner). Aquatic Fish Man-
agement, 18: 209-220.
Bouafou, K.G.M., Doukouré, B., Konan, B.A.,
Amonkan, K.A. and Katy-Coulibally, S.
(2011). Incorporation of a dried maggots'
meal in growing rats’ diet: pathological
risks? International Journal of Bioscience,
1: 65-70.
Boyce, J.A., Assa'ad, A., Burks, A.W., Jones,
S.M., Sampson, H.A., Wood, R.A., Plaut,
M., S.F., Fenton, M.J., Arshad, S.H., Bahna,
S.L., Beck, L.A., Byrd-Bredbenner, C., Ca-
margo, Cooper, C.A., Eichenfield, L., Fu-
ruta, G.T., Hanifin, J.M., Jones, C., Kraft,
M., Levy, B.D., Lieberman, P., Luccioli, S.,
McCall, K.M., Schneider, L.C., Simon,
R.A., Simons, F.E., Teach, S.J., Yawn, B.P.
and Schwaninger, J.M. (2010). Guidelines
for the diagnosis and management of food
allergy in the United States: report of the
NIAID-sponsored expert panel. Journal of
Allergy and Clinical Immunology, 126:1-
58.
Brinchmann, B.C., Bayat, M., Brogger, T.,
Muttuvelu, D.V., Tjonneland, A. and
Sigsgaard, T. (2011). A possible role of
chitin in the pathogenesis of asthma allergy.
Annuals of Agriculture and Environmental
Medicine, 18: 7–12
Cao, X.H., Yan, Z.L. and Wang, C.L. (2006).
Activity study on antibacterial protein iso-
lated from Musca domestica during larvae
pupae metamorphosis. China Biotechnolo-
gy, 26: 33-37.
Caruso, D., Devic, E., Subamia, I.W., Talamond,
P. and Baras, E. (2013). Technical hand-
book of domestication and production of
Diptera Black Soldier Fly (BSF) Hermetia
illucens, Stratiomyidae. IRD Edition, Mar-
seille
Charlton, A.J., Dickinson, M., Wakefield, M.E.,
Fitches, E., Kenis, M., Han, R., Zhu, F.,
Kone, N. M., Devic, E., Bruggeman, G.,
Prior, R. and Smith, R. (2015). Exploring
the chemical safety of fly larvae as a source
of protein for animal feed. Journal of Insects
as Food and Feed, 1: 7-16.
Chen, Z. and Jiang, X. (2014). Microbiological
safety of chicken litter or chicken litter-
based organic fertilizers: A review. Agricul-
ture, 4: 1-29.
Choi, W.H., Yun J.H., Chu, J.P., Chu, K.B.,
(2012). Antibacterial effect of extracts of
Hermetia illucens (Diptera: Stratiomyidae)
larvae against Gram-negative bacteria. En-
tomological Research, 42:219–226.
Diener, S., Studt, Solano, N.M., Roa Gutiérrez,
F., Zurbrugg, C. and Tockner, K. (2011).
Biological treatment of municipal organic
waste using black soldier fly larvae. Waste
and Biomass Valorisation, 2 :357-363.
Diener, S., Zurbrügg, C. and Tockner, K. (2015).
Bioaccumulation of heavy metals in the
black soldier fly, Hermetia illucens and
effects on its life cycle. Journal of Insects as
feed and food 1: 261-270.
Drew, D. J. W. and Pieterse, E. (2015). Markets,
money and maggots. Journal of Insects as
feed and Food, 1, 227-231 EFSA (2015).
Scientific opinion on a risk profile related to
production and consumption of insects as
food and feed. EFSA Journal,13: 4257.
EPA (2013). Literature Review of Contaminants
in Livestock and Poultry Manure and Impli-
cations for Water Quality, Office of Water
(4304T) EPA 820-R-13-002, July 2013
Erickson, M.C., Islam, M., Sheppard, C., Liao, J.
and Doyle, M.P. (2004). Reduction of Esch-
erichia coli O157:H7 and Salmonella enter-
ica serovar enteritidis in chicken manure by
larvae of the black soldier fly. Journal of
Food. Prot., 67:685–690.
Ghanaian Journal of Animal Science, Vol. 9 No.1, 2018 7

Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
Focke, M., Hemmer, W., Wöhrl, S., Götz, M.,
Jarisch, R. and Kofler, H. (2003). Specific
sensitization to the common housefly
(Musca domestica) not related to insect
allergy. Allergy, 58: 448-451.
Greenberg, B. (1973). Flies and diseases, Prince-
ton, Princeton University Press
Halling-Sørensen, B., Nielsen, S. N., Lanzky, P.
F., Ingerslev, F., Lützhøft, H. H. and
Jørgensen, S. E. (1998). Occurrence, fate
and effects of pharmaceutical substances in
the environment-A review. Chemosphere,
36: 357-393.
Holt, P.S., Geden, C.J., Moore, R.W. and Gast,
R.K. (2007). Isolation of Salmonella enter-
ica serovar enteritidis from Houseflies. Ap-
plied and Environmental Microbiolo-
gy,6030-6035.
Hou, W.G. (2008). Rearing shrimps and turtles
with housefly maggots. Patent CN 101138-
395 A.
Kenis, M., Koné, N., Chrysostome, C.A.A.M.,
Devic, E., Koko, G.K.D., Clottey, V.A.,
Nacambo, S. and Mensah, G.A. (2014).
Insects used for animal feed in West Africa.
Entomologia, 2: 107–114. doi: 10.4081/
entomologia.2014.218
Kone, N., Sylla, M. and Kenis, M. (2016). Per-
formances of a house fly production system
for animal feed in Mali. Journal of Insects
as Feed and Food. In Press.
Lalander, C., Diener, S., Magri, M.E., Zurbrügg,
C., Lindström, A. and Vinnerås, B. (2013).
Faecal sludge management with the larvae
of the black soldier fly (Hermetia illucens)
—from a hygiene aspect. Science of the
Total Environment, 458:312–318.
Lalander, C. H., Fidjeland, J., Diener, S.,
Eriksson, S. and Vinnerås, B. (2015). High
waste-to-biomass conversion and efficient
Salmonella spp. reduction using black
soldier fly for waste recycling. Agronomy
and Sustainable Development, 35: 261-271.
Lang, S.Y., Guo, G., Hong, M., Wang, H. and
Wu, J.W. (2004). A study on the change of
the hen’s immune response after fed with
fresh housefly larvae. Journal of Guiyang
Medical College, 29: 287-289.
Lei, C.L., Zhong, C.Z., Zong, L.B., Niu, C.Y.,
Jiang, Y. and Song. (1998). Evaluation of
the health function of fly-maggot nourishing
active powder. Journal of Guiyang Medical
College, 29:287-289.
Li, Y.X., Zhu, J.Y., Lin, C.Q., Jin, X.B., Zeng,
A.H. and Chu, F.J. (2011). Study on the
preclinical teratogenicity of Musca domesti-
ca larvae powder. Laboratory Medicine
Clinic, 1:1709-1712.
Lopata, A.L., Fenemore, B., Jeebhay, M.F. and
Potter, P.C. (2005). Occupational allergy in
laboratory workers caused by the African
migratory grasshopper Locusta migratoria.
Allergy, 60: 200–205.
Maciel, and Vergara, G. (2014). Improvement of
a house fly maggot production system for
animal feed in Ghana. MSc thesis, Universi-
ty of Catania, Italy, and University of Co-
penhagen, Denmark.
Martinez, A., Martinez, J., Palacios, R. and Pan-
zani, R.C. (1997). Importance of tropomyo-
sin in the allergy to household arthropods.
Cross-reactivity with other invertebrate ex-
tracts Allergy and Immunology, 25:118-
126.
Makkar, H. P., Tran, G., Heuzé, V. and Ankers,
P. (2014). State-of-the-art on use of insects
as animal feed. Annals of Food Science and
Technology, 197: 1-33.
Maurer, V., Holinger M., Amsler., Früh, B.,
Wohlfahrt, J., Stamer, A. and Leiber, F.
(2016). Replacement of soybean cake by
Hermetia illucens meal in diets for layers.
Journals of Insects as Feed. Online First:
DOI: http://dx.doi.org/10.3920/JIFF2015.
0071
Nelson, W. and Harris, B. (2006). Flies, fingers,
fomites, and food. Campylobacteriosis in
New Zealand food-associated rather than
food-borne. New Zealand Medical Journal,
119:1–7.
Newton, G.L., Booram, C.V., Barker, R.W. and
Hale, O.M. (1977). Dried Hermetia illucens
larvae meal as supplement for swine. Jour-
nal of Animal Science, 44:395-400.
Ghanaian Journal of Animal Science, Vol. 9 No.1, 2018
8

Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
Park, K. H., Kwak, K. W., Nam, S. H., Choi, J.
Y., Hyun, S., Lee, H. G. K. and Kim, S. H.
(2015). Antibacterial activity of larval ex-
tract from the black soldier fly Hermetia
illucens (Diptera:Stratiomyidae) against
plant pathogens. Journal of Epidemiology
and Zoology Studies, 3(5):176-179.
Petersen, S.O., Sommer, S.G., Béline, F., Bur-
ton, C., Dach, J., Dourmad, J.Y., Leip, A.,
Misselbrook, T., Nicholson, F., Poulsen,
H.D., Provolo, G., Sorensen, P., Vinneras,
B., Weiske, A., Bernal, M.P., Böhm, R.,
Juhasz, C. and Mihelic, R. (2007). Recy-
cling of livestock manure in a whole-farm
perspective. Livestock science, 112: 180-
191.
Phoku, J. Z., Barnard, T. G., Potgieter, N. and
Dutton, M. F. (2014). Fungi in housefly
(Musca domestica L.) as a disease risk indi-
cator—A case study in South Africa. A cta
Tropica, 140: 158-165.
Pomalégni S.C.B., Gbemavo D.S.J.C., Kpadé
C.P., Babatoundé S., Chrysostome
C.A.A.M., Koudandé O.D., Kenis M., Glèlè
Kakaï R.L. and Mensah G.A. (2016). Per-
ceptions et facteurs determinant l'utilisation
des asticots dans l'alimentation des poulets
locaux (Gallus gallus) au Bénin. Journal of
Applied Bio-science, 98: 9330 – 9343.
Pretorius Q. (2011). The evaluation of larvae of
Musca domestica (common house fly) as
protein source for broiler production. - The-
sis dissertation. University of Stellenbosch,
South Africa.
Ramirez, D.A. Jr. and Bahna, S.L. (2009). Food
hypersensitivity by inhalation. Clinical
Molecullar Allergy,7: 4.
Romero, M. R., Claydon, A. J., Fitches, E. C.,
Wakefield, M. E. and Charlton, A. J.
(2016). Sequence homology of the fly pro-
teins tropomyosin, arginine kinase and myo-
sin light chain with known allergens in in-
vertebrates. Journal of Insects as Food and
Feed, 2: 69-81
Scott, J. G., Warren, W.C., Beukeboom, L.W.,
Bopp, D., Clark, A.G., Giers, S.D., Hediger,
M., Jones, A.K., Kasai, S., Leichter, C.A.,
Li, M., Meisel, R.P., Minx, P., Murphy,
T.D., Nelson, D.R., Reid, W.R., Rinkevich,
F.D., Robertson, H.M., Sackton, T.B., Sat-
telle, D.B., Nissen, F.T., Tomlinson, C., van
de Zande, L., Walden, K.K., Wilson, R.K.
and Liu, N. (2014). Genome of the house
fly, Musca domestica L., a global vector of
diseases with adaptations to a septic envi-
ronment. Genome Biolology, 15:466.
Strauch, D. (1991). Survival of pathogenic micro
-organisms and parasites in excreta, manure
and sewage sludge. Revue Science Tech-
nogyde l'OIE, 10:813-846.
Swai, E. and Schoonman, L. (2012). A survey of
zoonotic diseases in trade cattle slaughtered
at Tanga city abattoir: a cause of public
health concern. A sia Pacific Journal of
Tropical Biochemistry, 2:55–60.
Tee, R.D., Gordon, D.J., Lacey, J., Nunn, A.J.,
Brown, M. and Newman Taylor, A.J.
(1985). Occupational allergy to the common
house fly (Musca domestica): Use of immu-
nologic response to identify atmospheric
allergen. Journal of Allergy and Clinical
Immunology, 76: 826–831.
Teguia, A., Mpoame, M. and Mba, J.A.O.
(2002). The production performance of
broiler birds as affected by the replacement
of fish meal by maggot meal in the starter
and finisher diets. Tropiculture, 20: 187-
192.
Van der Spiegel, M., Noordam, M.Y. and Van
der Fels-Klerx, H.J. (2013). Safety of novel
protein sources (insects, microalgae,
seaweed, duckweed, and rapeseed) and
legislative aspects for their application in
food and feed production. Comprehensive
Reviews in Food Science and Food
Safety,12:662-678.
Van Huis A., Van Itterbeeck J., Klunder H.,
Mertens E., Halloran, A., Muir G. and Van-
tomme P. (2013). Edible insects future pro-
spects for food and feed security. FAO For-
estry Paper 171.
Wahl, R. and Fraedrich, J. (1997). Occupational
allergy to the housefly (Musca domestica).
Allergy, 52: 236–238.
Wang, F.R., Huang, W., Wang, Y.L. and Lei,
C.L. (2005). Proteins isolated from the larva
of the housefly and their activities on
Ghanaian Journal of Animal Science, Vol. 9 No.1, 2018 9

Potential health and safety issues in the small-scale production of fly larvae... Nkegbe et al.
scavenging the hydroxyl radical proteins
isolated from the larva of the housefly and
their activities. Chinese Bulletin of Entomo-
logy, 42:546-549.
Wang, M.F., Tong, Y.F. and Xue, W.Q. (2004).
Prospects for the Flies Resources and Utili-
zation. Resources Science, 26, 153-159.
Wirtz, R.A. (1980). Occupational allergies to
arthropods--documentation and prevention.
Bulletin of Entomological Society America,
26:356-60.
Wirtz, R. A. (1984). Health and safety in arthro-
pod rearing, In: King, E.G., Leppla,N.C.,
(eds.), Advances and challenges in insect
rearing. USDA/ARS, New Orleans, LA,
USA.pp. 263-268.
Zhang, A.J., Wu, Y.J., Chen, C., Qin, Q.L.,
Zhang, H. and Li. (2009). Extraction of
edible protein from the housefly larvae.
China Bulletin of Entomology, 46: 627-
631.
Zhang, Z.S. and Yao, G.X. (1998). Nutritional
evaluations of the house fly in traditional
health food "Bazhengao". Science and
Technology of Food Industry, 2:12-14.
Zhao, G.Y., Chen, J.H., Su, H.Y., Bruggeman,
G., Fitches, E., Kenis, M. and Han, R.C.
(2016). Influence of house fly Musca do-
mestica larvae as a feed supplement on the
performance immune activation of Huxu
Breeders. Journal of Industrial Science. In
Press.
Zhuang, P., Zou, H., Shu, W., (2009). Biotrans-
fer of heavy metals along a soil-plant-insect
-chicken food chain: Field study. Journal of
Environmental Science, 21: 849–853.
Ghanaian Journal of Animal Science, Vol. 9 No.1, 2018
10