Evaluation of Supplementation of Defatted Black Soldier Fly (Hermetia illucens) Larvae Meal in Beagle Dogs

Abstract

The objective of this experiment was to test the effects of supplementation of defatted black soldier fly (Hermetia illucens) larvae (BSFL) meal in beagle dogs. A total of nine healthy female beagles (initial body weight 12.1 ± 1.76 kg) were fed grain-based diets with three levels of BSFL meal (0, 1% or 2%) in a 42-day feeding trial. At the end of week 6 of the experiment, all dogs were intraperitoneally challenged with Escherichia coli lipopolysaccharide (LPS) at 100 μg/kg of body weight. Albumin concentration was linearly increased with increasing BSFL meal level (P<0.05). A linear increase (P<0.05) in calcium concentration was observed when increasing dietary BSFL meal. Although dietary treatments did not affect the digestibility of ether extract, the digestibility of dry matter and crude protein were linearly increased with increasing the level of BSFL meal. The concentration of tumor necrosis factor-α was linearly decreased but glutathione peroxidase (GPx) concentration was linearly increased when increasing the level of BSFL meal at 6 h after challenge (P<0.05). In addition, there were quadratic increases in concentrations of GPx and superoxide dismutase with increasing dietary BSFL meal level at 3 h after challenge (P<0.05). These findings from the present study demonstrate that BSFL meal can be supplemented in the diet to convert beneficial effects to beagle dogs, indicated as improved digestibility of dry matter and crude protein and anti-inflammatory and anti-oxidative capacity.

Full text

Ann. Anim. Sci., Vol. 19, No. 3 (2019) 767–777 DOI: 10.2478/aoas-2019-0021
EVALUATION OF SUPPLEMENTATION OF DEFATTED BLACK
SOLDIER FLY (HERMETIA ILLUCENS) LARVAE MEAL IN BEAGLE
DOGS
X.J. Lei1,2, T.H. Kim3, J.H. Park2, I.H. Kim2♦
1College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, People’s
Republic of China
2Department of Animal Resource and Science, Dankook University, Cheonan, 31116,
Republic of Korea
3Foodyworm Inc., Chopyeong-Myeon, Jincheon-Gun 27858, Republic of Korea
♦Corresponding author: inhokim@dankook.ac.kr
Abstract
The objective of this experiment was to test the effects of supplementation of defatted black soldier
y (Hermetia illucens) larvae (BSFL) meal in beagle dogs. A total of nine healthy female beagles
(initial body weight 12.1 ± 1.76 kg) were fed grain-based diets with three levels of BSFL meal
(0, 1% or 2%) in a 42-day feeding trial. At the end of week 6 of the experiment, all dogs were
intraperitoneally challenged with Escherichia coli lipopolysaccharide (LPS) at 100 μg/kg of body
weight. Albumin concentration was linearly increased with increasing BSFL meal level (P<0.05).
A linear increase (P<0.05) in calcium concentration was observed when increasing dietary BSFL
meal. Although dietary treatments did not affect the digestibility of ether extract, the digestibility
of dry matter and crude protein were linearly increased with increasing the level of BSFL meal.
The concentration of tumor necrosis factor-α was linearly decreased but glutathione peroxidase
(GPx) concentration was linearly increased when increasing the level of BSFL meal at 6 h after
challenge (P<0.05). In addition, there were quadratic increases in concentrations of GPx and su-
peroxide dismutase with increasing dietary BSFL meal level at 3 h after challenge (P<0.05). These
ndings from the present study demonstrate that BSFL meal can be supplemented in the diet to
convert benecial effects to beagle dogs, indicated as improved digestibility of dry matter and
crude protein and anti-inammatory and anti-oxidative capacity.
Key words: blood prole, digestibility, dogs, Hermetia illucens
Insects have been proposed as a promising, high quality, and efcient alternative
protein feedstuff for animal feeds (Charlton et al., 2015). Insects are such an alterna-
tive protein source because they can sustainably by reared on organic side streams

X.J. Lei et al.
768
and they have a favorable feed conversion efciency (Veldkamp et al., 2012). The
production of insects specically with the intention of being fed to livestock has been
the subject of evaluations for several decades (Veldkamp and Bosch, 2015; Cullere
et al., 2016; Khan et al., 2016).
The black soldier y (Hermetia illucens) can grow on a wide range of decompos-
ing organic materials, such as fruits, vegetables to kitchen wastes, and livestock ma-
nure (Martínez-Sánchez et al., 2011). Therefore, being potentially interesting in re-
ducing environmental criticisms by transforming waste into valuable biomass, black
soldier y is a high-quality animal protein feedstuff (Nguyen et al., 2015). Previous
studies have suggested that black soldier y larvae (BSFL) could be used as feed
ingredient for pigs (Józeak et al., 2016), poultry (Marono et al., 2017; Mwaniki
et al., 2018; Secci et al., 2018), and sh species (St-Hilaire et al., 2007; Renna et
al., 2017). Apart from the growing farm animals population, the population of pet
animals (dogs and cats) is also large and growing, therefore, the availability of high
quality and sustainable protein sources for pet food production is increasing in im-
portance (McCusker et al., 2014; Bosch et al., 2016; Leriche et al., 2017). Bosch et
al. (2014; 2016) indicated that the use of insects as protein sources in dog food is
drawing attention. Kröger et al. (2017) and Kierończyk et al. (2018) studied the ap-
plication of BSFL meal in dogs. To our best knowledge, however, the study of the
inclusion of BSFL meal into dog diet is still limited. Therefore, the aim of the present
experiment was to determine the effects of inclusion of 0, 1%, and 2% BSFL meal
in beagle dogs.
Material and methods
All the animal procedures were reviewed and approved by the Animal Care and
Use Committee of Dankook University (DK-1-1712).
Source of BSFL meal
The defatted BSFL meal used in the present study was provided by Foodyworm
Inc. (Seoul, Republic of Korea). The nutrient contents of BSFL meal is presented in
Tables 1 and 2.
Table 1. Chemical composition and amino acid concentration of black soldier y larvae meal
Item %
1 2
Moisture 7.93
Crude protein 53.64
Crude fat 13.43
Crude ash 11.02
Amino acids
aspartic acid 4.85
threonine 2.15

Black soldier y larvae in dogs 769
Table 1 – contd.
1 2
serine 2.35
glutamic acid 6.11
proline 2.89
glycine 2.69
alanine 3.62
valine 3.68
isoleucine 2.06
leucine 3.61
tyrosine 3.08
phenylalanine 2.19
histidine 1.60
lysine 3.42
arginine 2.73
cysteine 0.70
methionine 1.33
tryptophan 0.65
Table 2. Fatty acid components of black soldier y larvae meal
Item %
Saturated fatty acid
C8:0 0.01
C10:0 1.19
C12:0 29.61
C14:0 5.57
C15:0 0.12
C16:0 15.14
C17:0 0.26
C18:0 3.96
C20:0 0.06
Unsaturated fatty acid
C14:1 0.20
C15:1 0.15
C16:1 3.42
C17:1 0.19
C18:1 20.49
C18:2n6 13.07
C18:3n6 0.06
C18:3n3 2.43
C18:4n3 0.16
C20:1n9 0.61

X.J. Lei et al.
770
Experimental design, animals, and housing
A total of 9 female beagle dogs, in good general health, aged 15–18 months, with
initial body weight (BW) of 12.1 ± 1.76 kg were randomly allotted to one of three
dietary treatments with three replications per treatment and one beagle dog per rep-
lication (cage), according to initial BW. The dietary treatments included commercial
basal diets with 0, 1%, or 2% of BSFL meal. One month before the experiment,
all the dogs were fed the same commercial pelleted diet as the basal diet used in
the present study for the adaption. The commercial basal diet was formulated to
meet nutrient requirements in accordance with the Association of American Feed
Control Ofcials (AAFCO, 2009) nutrient guide for dogs. The nutrient level of the
basal diet is shown in Table 3. Experimental dogs were individually fed twice daily
(08:00 h and 16:00 h). Beagles were housed in cages (100 cm × 210 cm) that were
equipped with a feeder, a water bucket, and slatted plastic ooring in an environ-
mentally controlled room. Dogs were allowed free access to drinking water through-
out the experiment. Room temperature and relative humidity were maintained at
20 ± 3°C and 50 ± 10%, respectively. At the end of week 6 of the experiment, all
dogs were intraperitoneally injected with Escherichia coli lipopolysaccharide (LPS,
E. coli serotype 055: B5) at 100 μg/kg of BW.
Table 3. The analyzed nutrient level of basal diet (as-fed basis)
Item %
Dry matter 90.59
Crude protein 32.01
Crude fat 19.97
Crude ber 2.20
Crude ash 8.79
Calcium 1.96
Total phosphorus 1.26
Sampling and measurements
The apparent total tract digestibility (ATTD) was performed using the
total collection method (AAFCO, 2009). To estimate the ATTD of crude protein
(CP), dry matter (DM), and ether extract (EE), during the last 3 days of the
experiment, feces were collected at least two times daily and weighed. Fecal samples
from the same dog were pooled and mixed, after which fecal samples were
kept at –20°C until required for analysis. For chemical analysis, fecal samples
were oven-dried at 55°C for 72 h and ground to pass through a 1.0-mm screen (Lei
and Kim, 2018; Liu et al., 2018). Dietary and fecal samples were analyzed
for DM (method 930.15), CP (method 984.13), and EE (method 920.39) using
the AOAC (2007) method. The ATTD of DM, EE, and CP was calculated as fol-
lows:
ATTD of nutrient (%) = [(nutrient intake, g – nutrient excretion, g)/ nutrient intake, g]
× 100

Black soldier y larvae in dogs 771
At the end of week 6, blood samples were collected via jugular vein from each
dog in non-heparinized tubes. Blood samples were centrifuged at 1,500 × g for
20 minutes to get serum and then frozen at –20°C until further analysis (Kruger
et al., 2016). The concentrations of alanine transaminase (ALT), albumin, aspartate
transaminase (AST), bilirubin, blood urea nitrogen (BUN), globulin, glucose, and
protein were analyzed using commercially specic available enzyme-linked im-
munosorbent assay (ELISA) kits (Quantikine, R&D Systems, Minneapolis, MN,
USA). Serum high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein
cholesterol (LDL-C), total cholesterol (TC), and triglyceride (TG) concentrations in
serum were determined enzymatically using reagent kits (Wako Pure Chemical In-
dustries Ltd., Tokyo, Japan). The amounts of calcium (Ca), chlorine (Cl), magnesium
(Mg), phosphorus (P), potassium (K), and sodium (Na) in serum were determined
by ame atomic absorption spectrophotometry (AA-6300, Shimadzu Corp., Tokyo,
Japan).
Before challenge and 3 and 6 h after challenge, blood was collected via jugular
vein from each dog into non-heparinized tubes. Then, blood samples were centri-
fuged at 1,500 × g for 20 minutes to get serum and then frozen at –20°C until analysis
(Kruger et al., 2016). The serum tumor necrosis factor-α (TNF-α) and interleukin-6
(IL-6) concentrations were assessed using specic commercially available ELISA
kits (Quantikine, R&D Systems, Minneapolis, MN, USA) according to the manu-
facturer’s instructions. The concentrations of superoxide dismutase (SOD) and glu-
tathione peroxidase (GPx) in serum were determined using commercial kits (Cell
Biolabs, Inc. San Diego, CA, USA) following the instructions.
Statistical analysis
All data were analyzed as a randomized complete block design using the general
linear model procedures of SAS (version 9.2, Institute Inc., Cary, NC, USA). The
individual beagle was considered as the experimental unit. Both linear and quadratic
polynomial contrasts were performed to determine the effects of a different level (0,
1%, and 2%) of BSFL in the diet. Variability in data was expressed as the pooled
standard error of the mean and a probability less than 0.05 was considered statisti-
cally signicant.
Results
The protein, glucose, globulin, BUN, bilirubin, AST, and ALT concentrations in
serum were not affected by dietary treatments (P>0.05; Table 4). However, albumin
concentration was linearly increased with increasing BSFL meal level (P<0.05). No
differences in blood cholesterol, triglyceride, HDL-C, and LDL-C were observed
among treatments (P>0.05; Table 5). The concentrations of tested minerals in blood
did not differ among dietary treatments with the exception of calcium (P>0.05; Table
6). With the increasing level of BSFL meal, a linear increase (P<0.05) in calcium
concentration was observed. Although the digestibility of EE was not inuenced by
dietary treatments, increasing the level of BSFL meal linearly increased the ATTD

X.J. Lei et al.
772
of DM and CP (Table 7). Before the challenge, the IL-6, TNF-α, SOD, and GPx
concentrations in serum did not differ among treatments (P>0.05; Table 8). How-
ever, the concentration of TNF-α was linearly decreased while GPx concentration
was linearly increased when increasing the level of BSFL meal at 6 h after challenge
(P<0.05). In addition, there were quadratic increases in concentrations of GPx and
SOD with increasing dietary BSFL meal level at 3 h after challenge (P<0.05).
Table 4. Effects of black soldier y larvae (BSFL) meal on selected serum parameters in beagle dogs
Item BSFL meal (%) SEM1P-value
0 1 2 linear quadratic
Protein (mg/mL) 64.84 63.42 62.21 0.102 0.270 0.664
Albumin (mg/mL) 28.11 32.12 36.8 0.134 0.017 0.609
Glucose (mg/mL) 0.83 0.80 0.77 0.023 0.456 0.933
Globulin (mg/mL) 35.01 31.32 25.94 0.191 0.062 0.867
Blood urea nitrogen (mg/dL) 0.06 0.06 0.08 0.007 0.290 0.496
Bilirubin (μg/mL) 0.98 1.02 0.97 0.091 0.898 0.876
Aspartate transaminase (U/mL) 0.03 0.03 0.03 0.002 0.336 0.464
Alanine transaminase (U/mL) 0.03 0.06 0.03 0.008 0.801 0.187
1SEM, standard error of the mean.
Table 5. Effects of black soldier y larvae (BSFL) meal on blood lipid proles in beagle dogs
tem (mg/mL) BSFL meal (%) SEM1P-value
0 1 2 linear quadratic
Cholesterol 1.79 1.54 1.84 0.079 0.828 0.176
Triglyceride 0.69 0.71 0.76 0.069 0.792 0.954
High-density lipoprotein cholesterol 1.32 1.26 1.31 0.134 0.871 0.583
Low-density lipoprotein cholesterol 0.17 0.12 0.13 0.017 0.415 0.475
1SEM, standard error of the mean.
Table 6. Effects of black soldier y larvae (BSFL) meal on mineral proles in beagle dogs
Item BSFL meal (%) SEM1P-value
0 1 2 linear quadratic
Calcium (mg/mL) 0.09 0.12 0.14 0.001 0.020 0.660
Phosphorus (mg/mL) 0.04 0.04 0.05 0.002 0.055 1.000
Sodium (mmol/mL) 0.15 0.15 0.15 0.001 0.070 0.656
Potassium (μmol/mL) 5.21 4.89 5.22 0.072 0.622 0.071
Chloride (mmol/mL) 0.11 0.11 0.11 0.001 0.386 0.151
Magnesium (mg/mL) 0.02 0.02 0.02 0.001 0.108 0.809
1SEM, standard error of the mean.

Black soldier y larvae in dogs 773
Table 7. Effects of black soldier y larvae (BSFL) meal on nutrient digestibility in beagle dogs
Item (%) BSFL meal (%) SEM1P-value
0 1 2 linear quadratic
Dry matter 71.97 74.55 75.21 2.964 0.017 0.992
Nitrogen 73.16 77.06 78.51 2.640 0.039 0.825
Ether extract 78.80 78.97 79.22 3.523 0.934 0.994
1SEM, standard error of the mean.
Table 8. Effects of black soldier y larvae (BSFL) meal on blood prole in beagle dogs challenged
with lipopolysaccharide
Item BSFL meal (%) SEM1P-value
0 1 2 linear quadratic
Interleukin-6 (pg/mL)
before injection 15.72 17.84 15.20 2.264 0.091 0.290
after 3 h 66.35 67.09 63.94 7.351 0.314 0.312
after 6 h 65.60 67.21 55.94 6.422 0.213 0.291
Tumor necrosis factor-α (pg/mL)
before injection 4.55 5.53 5.65 1.412 0.563 0.550
after 3 h 17.77 18.47 18.47 2.974 0.342 0.537
after 6 h 13.64 12.63 7.48 3.025 0.038 0.779
Superoxide dismutase (U/mL)
before injection 1.78 1.94 2.32 0.781 0.239 0.692
after 3 h 1.06 3.61 2.81 1.124 0.441 0.036
after 6 h 1.05 1.67 0.89 0.390 0.798 0.196
Glutathione peroxidase (nmol/min/mL)
before injection 58.96 54.76 55.01 5.261 0.849 0.894
after 3 h 3.11 6.72 3.64 0.754 0.989 0.034
after 6 h 42.12 50.94 53.05 4.642 0.014 0.371
Discussion
Black soldier y represents one of the most promising insect species that can be
used as a protein source for livestock and sh (Biancarosa et al., 2018). This study
evaluated the application of BSFL meal in beagle dogs. In this study, the protein, glu-
cose, globulin, BUN, bilirubin, AST, and ALT concentrations in serum were not in-
uenced by treatments, whereas albumin concentration was linearly increased when
increasing BSFL meal level. The increased concentration of albumin in the serum of
the dogs fed higher level of BSFL meal might have resulted from the increased ow
of protein to the intestine (Min et al., 2003). The blood lipid proles (concentrations
of cholesterol, HDL-C, LDL-C, and triglyceride) were not inuenced by treatments

X.J. Lei et al.
774
indicating that inclusion of BSFL meal had no harmful effects on lipid metabolism in
beagle dogs. Similarly, in sh and broilers, Li et al. (2016) and Dabbou et al. (2018)
observed that inclusion of BSFL oil did not inuence serum cholesterol, triglyceride,
HDL-C, and LDL-C contents in serum. In this study, the concentrations of phospho-
rus, sodium, potassium, chloride, and magnesium in blood were not inuenced by
treatments, whereas a linear increase in calcium concentration was observed when
increasing the dietary BSFL meal. Dabbou et al. (2018) indicated that inclusion of
defatted BSFL meal increased phosphorus content in serum of broilers, but the con-
centrations of calcium, magnesium, and iron did not differ from dietary treatments.
Schiavone et al. (2017) suggested that BSFL oil had no effects on serum phosphorus,
magnesium, and iron concentrations.
In this experiment, increasing the level of BSFL meal linearly increased the di-
gestibility of DM and N, but the digestibility of EE was not affected by treatments.
This indicates that providing BSFL meal has a positive effect on DM and CP digest-
ibility. However, Cutrignelli et al. (2018) completely replaced soybean meal with
BSFL meal and found that laying hens fed diet with BSFL meal showed lower appar-
ent ileal digestibility of DM and CP compared with hens offered diet without BSFL
meal, but lipid digestibility was not affected by treatment. The authors suggested
that the reductions in DM and CP digestibility were related to the chitin in the BSFL
meal which could negatively affect the nutrient digestibility (Longvah et al., 2011).
In broiler quails, Cullere et al. (2016) found that the digestibility of DM, and CP
were not affected by the inclusion of BSFL meal, whereas the digestibility of EE was
reduced by supplementation of BSFL meal. In addition, in weaned pigs, Spranghers
et al. (2018) observed that inclusion of 4% or 8% BSFL meal had no effects on ap-
parent ileal and total tract digestibility of DM and CP. Further studies are warranted
to test higher levels of BSFL meal on nutrient digestibility in beagle dogs.
Cytokines play an important role in the immune and inammatory response.
Previous studies have indicated that over-production of TNF-α (pro-inammatory
cytokine) has negative effects on intestinal integrity and epithelial function (Waititu
et al., 2016; Yu et al., 2017; Xu et al., 2018 a, b). In the present study, the concentra-
tion of TNF-α was linearly decreased when increasing the level of BSFL meal at
6 h after challenge. The down-regulation of TNF-α may indicate that inamma-
tion induced by LPS was alleviated. The concentration of GPx was linearly in-
creased when increasing the level of BSFL meal at 6 h after challenge. In addition,
there were quadratic increases in concentrations of GPx and SOD with increasing
dietary BSFL meal level at 3 h after challenge. The GPx and SOD are major an-
ti-oxidative enzymes in serum (Štukelj et al., 2013). The increased concentrations
of GPx and SOD may suggest that BSFL meal improved the anti-oxidative
capacity. Li et al. (2016) suggested that the improved anti-oxidative property in-
dicated as increased catalase activity in serum from sh by the inclusion of BSFL
meal could be attributed to the chitin and its derivatives in BSFL meal. In the pres-
ent study, the improved anti-oxidative capacity may be caused by the chitin and
its derivatives in BSFL meal, although the chitin in BSFL meal and experimental
diets was not specically analyzed (Khoushab and Yamabhai, 2010; Ngo and Kim,
2014).

Black soldier y larvae in dogs 775
In conclusion, these ndings from this study demonstrate that BSFL meal can
be supplemented in the diet to convert benecial effects to beagle dogs indicated as
improved ATTD of DM and CP and anti-inammatory and anti-oxidative capacity.
Acknowledgement
This work was supported by Korea Institute of Planning and Evaluation for Tech-
nology in Food, Agriculture, Forestry and Fisheries (IPET) through Agri-Bio Indus-
try Technology Development Program, funded by Ministry of Agriculture, Food and
Rural Affairs (MAFRA)(116151-2).
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Received: 19 XI 2018
Accepted: 4 III 2019