Received: 31 July 2019 | Revised: 16 October 2019 | Accepted: 2 November 2019

DOI: 10.1111/jpn.13265

SPECIAL ISSUE ARTICLE

Growth performance, carcass characteristics, meat quality and

serum profile of broiler chicks fed on housefly maggot meal as
a replacement of soybean meal

Usman Elahi | You-biao Ma | Shu-geng Wu | Jing Wang | Hai-jun Zhang |

Guang-hai Qi

Key Laboratory of Feed Biotechnology,

Ministry of Agriculture and Rural Affairs,
National Engineering Research Center of
Biological Feed, Feed Research Institute,
Chinese Academy of Agricultural Sciences,
Beijing, P. R. China
Correspondence
Hai-jun Zhang and Guang-hai Qi, Key
Laboratory of Feed Biotechnology, Ministry
of Agriculture and Rural Affairs, National
Engineering Research Center of Biological
Feed, Feed Research Institute, Chinese
Academy of Agricultural Sciences, Beijing
100081, P. R. China.
Emails: zhanghaijun@caas.cn (H.-j. Z.);
qiguanghai@caas.cn (G.-h. Q.)
Funding information
Beijing Innovation Consortium of Agriculture
Research System, Grant/Award Number:
BAIC04-2019; Agricultural Science and
Technology Innovation Program (ASTIP) and
National Key R&D Program of China, Grant/
Award Number: 2018YFD0500403-4
Summary
A study was conducted to invesstigate the housefly maggot meal (HMM) as an alter-
native protein source to replace the soybean meal in broiler chick's diet. A total of
720 1-day-old male broiler chicks were divided into three groups and fed diets for-
mulated with HMM to replace soybean meal at the rate of 0%, 4% and 8%. The study
lasted for 42 days in two phases. Results showed that HMM addition did not mark-
edly affect body weight, average daily body weight gain and average daily feed intake
of the broiler chicks. Feed conversion ratio increased linearly (1–21 days) in starter or
quadratically (22–42 days) in the grower phase. HMM non-significantly increased the
feed intake and body weight during the grower phase. Slight changes were observed
for decrease of blood biochemical indices in the platelets (day 21), and alkaline phos-
phatase and lysozyme (day 42), and increase for red blood cells, packed cell volume,
total protein and uric acid on day 42; however, the fluctuations were within the physi-
ological range. Non-significant effects were observed for carcass composition and
meat quality, except that HMM numerically reduced the shear force of breast muscle
(linear, p = .058). These results are the strong evidence that HMM can be used as an
alternative protein source at 8% in broiler chick's diet without any adverse effect on
chick's performance.

KEYWORDS

broiler, housefly maggot, insect meal, meat quality, musca domestica

1 | I NTRO D U C TI O N immense pressure on the poultry feed industry to enhance produc-

Demand for food supply is continuously increasing with the rapid
growth of the world population. Poultry products (meat and eggs)
play an important contribution to the global food supply. Poultry
meat growth will increase up to 121%, and there will be an esti-
mated 65% increase in egg production by 2050 (Mottet & Tempio,
2017). As the resources are shrinking and the population and prices
of feed ingredients are increasing, this situation will undoubtedly put
tion efficiency. Soybean meal has been the primary protein source in
the poultry feed; however, soybean is facing intermittent supply due
to limited availability, high prices, trade wars and politics. A possible
solution to reduce poultry feed cost is to find efficient and inexpen-
sive alternative feed sources.
Use of insect meal in poultry diets could be a potential solution
to improve sustainability as insects fed on vegetable waste, and in-
sects are then directly consumed by the poultry. Ants, aphids, bees,

J Anim Physiol Anim Nutr. 2019;00:1–10. wileyonlinelibrary.com/journal/jpn © 2019 Blackwell Verlag GmbH | 1
2 |
beetles, caterpillars, cicadas, cockroaches, fleas, flies, grasshoppers,
lice, locusts, psyllids, scale insects, stink bugs, termites and wasps
have been used in poultry diets (Ravindran & Blair, 1993). Black sol-
dier fly, house fly, orthoptera meal, mealworm and silkworm have
been used in poultry diets and been under further investigation.
So far, literature regarding the insect meal is scarce, and there is no
complete database available on all insect species.
Insects are being used as medicine and food in China for centu-
ries. In China, there is no specific rules and regulations for insect pro-
duction; however, feed materials should be authorised for hygienic
standard from Agricultural Administrative Department of the State
Council (Lähteenmäki-Uutela et al., 2017). Housefly maggot meal
(Musca domestica) common fly can be found in all countries and in
any climate. It is commonly associated with animal faeces and can
be seen feeding on animal manure and food wastes. House flies are
recognised as the carrier of diseases. There are opinions that using
maggot meal in poultry diets can increase the risk of disease trans-
mission (Makkar, Tran, Heuzé, & Ankers, 2014). Maggot itself does
not contain any disease-causing agent. Maggot therapy has been
used for decades for the treatment of rotten injuries of patients
(Infectious Diseases Society of America, n.d.; Kittson & Diaz, 2019).
Housefly larvae flourish in manure and organic waste, produce an-
timicrobial compounds to protect themselves from microbial infec-
tions, and additionally, these compounds could also be functional in
chicks (Veldkamp & Bosch, 2015).
Housefly maggot contains about 38%–76% crude protein (CP)
in dry matter (DM). The recently reported values for CP are 48.4%
(Mbiba, Etchu, & Ndamukong, 2019a), 40.12% (DM basis) (Dillak et
al., 2019), 54.36% (DM basis) (Radulović et al., 2018), 50% (Khan,
Chand, Khan, Khan, & Sultan, 2018b), 53.3% (Hall et al., 2018),
60.51% (DM basis) (Fitches et al., 2018) and 55.6% (Khan et al.,
2016). The variation in the nutritional profile of the insects largely
depends on age, species, rearing medium, environment and process-
ing method (sun or oven drying).
In the recent studies, (Hall et al., 2018; Khan, Chand, Chand,
Khan, Khan, & Sultan, 2018a; Radulović et al., 2018) reported a sig-
nificant difference in growth performance and nutrient digestibility
in broiler chicks fed on HMM. Insect meal in poultry diets also con-
tributes to the meat quality. Broiler chicks fed on the insect meal
have better meat quality and blood traits due to the presence of es-
sential amino acids and minerals in the insect (Dabbou et al., 2018;
Khan et al., 2016). Meat from broiler chicks fed on the HMM had
significant higher acceptability as well as higher scores for flavour,
colour, tenderness, juiciness, aroma and desirability (Jiya et al., 2014;
Khan et al., 2016; Radulović et al., 2018). Moreover, (Hwangbo et al.,
2009; Mbiba, Etchu, & Ndamukong, 2019b) observed improved car-
cass quality, meat quality and stable haematological parameters in
broiler chicks fed on the HMM. Black soldier fly meal fed to barbary
partridges and laying hens resulted in higher level of globulin and
lower level of creatinine and albumin to globulin ratio (Loponte et
al., 2017; Marono et al., 2017). In another study, (Zang, Bing, Zhang,
Sheng, & Shu, 2018) reported broiler chicks fed on earthworm meal
diet had increased antioxidant. These studies demonstrated that
ELAHI et al.
insect meal may have the potential to positively affect the broiler
meat quality.
The high content of protein and fat, exemplary amino acid com-
position and low levels of fibre makes insect meal as an ideal protein
source for poultry feed and also comparable to the conventional
protein sources (Pretorius, 2011). As an alternative protein source,
HMM could be used in poultry diets due to its abundant protein and
energy content and possibly beneficial modulation on growth exhi-
bition and meat quality in broiler chicks. Thus, the current study is
conducted to investigate the growth performance, blood biochemi-
cal indices, carcass characteristics and meat quality of broiler chicks
fed on the diet containing housefly maggot meal as a replacement of
soybean meal.
2 | M ATE R I A L S A N D M E TH O DS
All the experimental protocols for this study were approved by the
Animal Care and Use Committee of the Feed Research Institute of
the Chinese Academy of Agricultural Sciences.
A total of 720 one-day-old Ross 308 male broiler chicks obtained
from local hatchery were raised in wire floor battery cages under an
environmentally controlled house. The temperature in the chicken
house was 33°C for the first week and then decreased by 3°C per
week until it reached 24°C. Diet and water were supplied ad libitum.
Each treatment was divided into 12 replicates containing 20 broiler
chicks each. Three diets were formulated with HMM to replace soy-
bean meal at the rate of 0%, 4% and 8% (Table 1). Body weight (BW)
and feed intake documented during the starter phase (1–21 days)
and grower phase (22–42 days). Average daily gain (ADG), average
daily feed intake (ADFI) and feed conversion ratio (FCR) were calcu-
lated from the documented data.
At 21 and 42 days of age, one chick was randomly selected from
each replicate for blood. A 3 ml of blood was sampled from wing vein
and kept in heparin lithium-treated tubes. The blood was then cen-
trifuged at 1,800 rpm for 10 min, and the plasma was stored in 1.5 ml
Eppendorf tube at −30°C until analysis. Immunoglobulin (Ig) G, IgM
and IgA serum concentrations were analysed by ELISA quantitation
kits. Alanine aminotransferase (ALT), aspartate amino transferase
(AST), alkaline phosphate (ALP), total protein (TP), albumin (ALB),
uric acid (UA), total bilirubin (TBIL), blood urea nitrogen (BUN) and
glucose (GLU) were determined by Nanjing kit (Nanjing Jiancheng
Bioengineering Institute, Nanjing, China) with a biochemical anal-
yser (ERBA CHEM-5, Beijing biochemical instrument company,
Beijing, P.R. China). The assessment of lysozyme (LZM) activity was
conducted by immunoturbidimetry (ITM) method, and Micrococcus
Lysodeikticusis is used as a substrate.
On 21 and 42 days, one broiler chick from each cage was slaugh-
tered, and breast meat yield (% of carcass), leg meat yield (% of car-
cass), leg weight and abdominal fat were documented. Meat quality
parameters including muscle pH, colour and shear force were deter-
mined by slaughtering one broiler chick from each replicate. Muscle
pH was determined by an electronic pH meter at 45 min and 24 hr of
ELAHI et al. | 3

TA B L E 1 Feed formula and nutritional

Housefly Maggot Meal (HMM) inclusion
profile of the diets
Starter phase Grower phase

Ingredients 0% 4% 8% 0% 4% 8%

Corn 58.64 61.15 63.60 63.30 65.70 68.31

HMM 0 4.00 8.00 0 4.00 8.00
Soybean meal 34.79 29.11 23.45 30.40 24.74 18.95
Soybean oil 2.08 1.28 0.51 2.75 1.98 1.15
CaHPO 4 1.98 2.02 2.07 1.55 1.77 1.82
Limestone 1.22 1.20 1.19 1.10 0.96 0.93
NaCl 0.14 0.14 0.14 0.14 0.14 0.14
NaHCO3 0.19 0.19 0.19 0.19 0.18 0.19
DL-methionine 0.32 0.31 0.30 0.19 0.19 0.18
L-lysine HCl 0.31 0.27 0.22 0.05 0.01 0
a
Vitamin premix 0.02 0.02 0.02 0.02 0.02 0.02
Mineral premixb 0.20 0.20 0.20 0.20 0.20 0.20
Choline chloride (50%) 0.10 0.10 0.10 0.10 0.10 0.10
Phytase 0.01 0.01 0.01 0.01 0.01 0.01
CP% 22.00 22.00 22.00 20.15 20.15 20.15
AME kcal/kg 2,950 2,950 2,950 3,050 3,050 3,050
Ca % 1.00 1.00 1.00 0.90 0.90 0.90
Available P % 0.45 0.45 0.45 0.40 0.40 0.4
Lysine % 1.15 1.15 1.15 1.05 1.05 1.0
Methionine % 0.50 0.50 0.50 0.40 0.40 0.40
Met + Cys % 0.88 0.88 0.88 0.75 0.75 0.75
Threonine % 0.75 0.75 0.75 0.69 0.69 0.69
Tryptophan % 0.24 0.22 0.22 0.20 0.20 0.20
a
Premix is provided for each kilogram of feed: vitamin A 12,500 IU and vitamin D3 2,500 IU; the
following is mg: vitamin E 18.75, vitamin K3 2.65, vitamin B1 2, vitamin B2 6, vitamin B12 0.025,
biotin 0.0325, folic acid 1.25, pantothenic acid 12, nicotinic acid 50, Cu 8, Zn 75, Fe 80, Mn 100, Se
0.15 and I 0.35.
b
Calculated according to China Feed Database (2014).

post-mortem. Meat colour was determined in duplicate by a Chroma
meter and described in CIE-Lab trichromatic system as lightness (L*),
redness (a*) and yellowness (b*) at 24 hr of slaughtering. Shear force
was determined at 96 hr of post-mortem by water bathing 20 g mus-
cle sample in a zip-sealed plastic bag at 85°C for 20 min, and on cool-
ing down, shear force values was calculated in triplet as described by
(Froning & Uijttenboogaart, 1988).
Data regarding growth performance, carcass characteristics and
meat quality and serum biochemistry were analysed using SPSS
software (Version, 20). Linear and quadratic effects were assessed
to compare treatment means using regression analysis. All the data
expressed as mean and pooled SEM assuming the following regres-
sion model:
( )
Yij = 𝛼 + 𝛽1 Xi + 𝜀ij Linear Regression
( )
Yij = 𝛼 + 𝛽1 Xi + 𝛽2 Xi2 + 𝜀ij Quadratic Regression
where, Yij = Response Variable; α = Intercept; β1 and β2 = Regression
Coefficient; Xi = Main effect inclusion of HMM (i = 0%, 4%, 8%);
εij = Residual Error Term.
3 | R E S U LT S
The analysed chemical composition of HMM is shown in Table 2.
HMM contains high amount of protein (crude protein 62.98%) and
amino acids. Growth performance results during the trial are pre-
sented in Table 3. A total of 39 mortalities were recorded during
the trial. Supplementation with HMM in diets linearly decreased the
21 day BW (p < .001), and ADG (p < .001) and FCR (p < .001) in-
creased linearly during the starter phase. Meanwhile, 42 day BW,
ADG and ADFI (p = .081) during the grower phase showed no lin-
ear or quadratic effect of HMM; however, FCR in the grower phase
showed a quadratic effect of HMM. The overall (1–42 days) growth
4 | ELAHI et al.

TA B L E 2 Chemical Composition and nutritional value of yield, breast muscle percentage, leg muscle percentage, spleen per-
Housefly Maggot Meal centage, bursa percentage and lowered abdominal fat and thymus
Dry matter (%) 93.22 percentage for 21 day with no statistical difference.
Crude Protein (%) 62.98 Meat quality parameters are shown in Table 6. Dietary supple-
Crude Fat (%) 5.58 mentation of HMM decreased the shear force (p = .058) with no

Ash (%) 8.15 statistical effect. Broiler chicks fed on 8% HMM diet had reduced
redness, yellowness, lightness in colour and higher pH at 1 hr
Crude Fibre (%) 9.64
post-mortem; however, reduced redness, yellowness, pH and in-
Gross Energy (Kcal/kg) 4,658
creased lightness were observed after 24 hr of post-mortem with no
Amino acids (% Protein)
difference of statistical significance.
Aspartic Acid 4.59
Leucine 5.03
Threonine 2.57 4 | D I S CU S S I O N
Tyrosine 1.77
Serine 4.97 Cage system is popular in the broiler chick farming because of no
Phenylalanine 2.86 litter requirement, increased chick density, minimum labour cost,
Glutamic acid 7.23 lower disease and parasites, better hygienic conditions and ef-
Histidine 0.81 ficient space utilisation (Al-Bahouh, Al-Nasser, Abdullah, Ragheb,
Proline 4.59 & Mashaly, 2012; Santos, Santos, Oviedo-Ron, & Ferket, 2012;

Lysine 4.88
Glycine 4.21
Arginine 3.79
Alanine 2.98
Cysteine 1.29
Valine 3.83
Methionine 1.04
Isoleucine 2.57
Tryptophan 0.48
performance showed both linear and quadratic effect of diet on FCR
(p = .004). ADG and ADFI were not affected linearly or quadratically
by HMM.
Haematological characteristics of broiler chicks fed on HMM
diet are shown in Table 4. HMM in diets linearly decreased the
21 day platelets (p = .023); however, 42 day red blood cells (RBCs)
(p = .018) and packed cell volume (PCV) (p = .015) increased qua-
dratically with the increasing level of HMM. There is no linear
or quadratic effect of HMM on white blood cells (WBCs), RBCs
(21 days), haemoglobin, PCV (d21) and platelets (d42). HMM sup-
plementation had both linear and quadratic effect on TP, ALP, UA
and LZM on 42 day. Results show UA (p < .001) and LZM (p = .017)
linearly increased on 21 day; however, ALT (p = .004) decreased
linearly on d42. Dietary HMM had a quadratic effect on TP, ALB
and ALP on 21d; however, TP, IgA and AST showed the quadratic
effect on 42 days.
Effect of HMM diet on carcass characteristics is shown in
Table 5. Broiler chicks fed on the diet containing HMM have no lin-
ear or quadratic effect on eviscerated weight, eviscerated yield, ab-
dominal fat, dressing percentage, breast muscle, leg muscle, thymus,
spleen, bursa, thigh, shanks, wings and pectoral. Broiler chicks fed
on a diet containing 8% HMM have numerically higher eviscerated
Wang et al., 2015). Numerous studies supported higher growth
rate, feed efficiency and better survival rate of commercial broiler
chicks reared under cage system (Al-Bahouh et al., 2012; Bahreiny,
Dadvar, Mororvat, & Bujarpoor, 2013; Thanga, Thiagarajan, Ramesh,
Gnanaraj, & Sivakumar, 2001). However, contradictory studies also
reported reduced weight gain, breast yield, ash percentage of tibia
and femur in broiler chicks when reared under cage system (Darwish,
El-Sayiad, El-Maghawry, & Mahrose, 2017; Fouad, Razek, & Badawy,
2008; Özhan, Şimşek, & Özçelik, 2016). Furthermore, inconsist-
ent findings also revealed no significant difference in growth per-
formance, feed efficiency and tibia strength of commercial broiler
chicks reared either in cage or floor (Bahreiny et al., 2013; Wang
et al., 2015). In the current study, wire floor cage system, a typical
broiler raising system in China, was used in the grow-out feeding
experiment. The purpose of the current study was to investigate
the possibility of housefly maggot meal as a replacement of soybean
meal in caged broiler chicken.
Among the alternative protein feed sources for poultry, insect
meal is the perfect choice because it has high protein, fat and ideal
amino acid profile. Insects are a good source of protein, energy and
lipids, and poor in fibre and anti-nutritional factors (Tran, Heuzé, &
Makkar, 2015). Insects have high reproductive capacity, nutritional
quality and feed conversion efficiency (Oonincx, 2015). Nutritional
composition of the HMM is comparable to soybean meal. The re-
sults in our study also support the concept that HMM is rich in crude
protein (62.98%). Similar proximate composition of housefly maggot
larvae with slight variations were also reported by (Đorđević et al.,
2008; Fitches et al., 2018; Hwangbo et al., 2009). The variations in
the composition could be due to the natural or induced conditions
involved in the production process of the HMM. The amino acids
composition data indicate that HMM had higher lysine and methi-
onine content than soybean meal.
In the current study, linearly reduced BW and ADG during the
starter phase were observed. However, BW on 42 day and ADG for
ELAHI et al. | 5

TA B L E 3 Effect of Housefly Maggot

Housefly Maggot Meal (HMM)
Meal inclusion on growth performance of
inclusion p-value
broiler chicks
Itemsa 0% 4% 8% SEM Linearb Quadraticb

21 day
BW (g) 886.35 857.27 839.04 6.25 .001 .632
ADG (g) 39.96 37.98 36.92 0.33 <.001 .392
ADFI (g) 56.59 56.35 56.54 0.37 .960 .793
FCR 1.42 1.48 1.53 0.01 <.001 .380
42 day
BW (g) 2,771.24 2,736.24 2,805.51 32.35 .676 .464
ADG (g) 87.54 86.78 93.17 1.45 .113 .240
ADFI (g) 146.51 149.18 155.30 2.03 .081 .684
FCR 1.68 1.72 1.67 0.01 .669 .010
1−42d
ADG (g) 62.01 60.43 63.11 0.67 .507 .143
ADFI (g) 98.28 99.07 102.55 1.06 .106 .548
FCR 1.59 1.64 1.63 0.01 .004 .004
a
BW, body weight; ADG, average daily gain; ADFI, average daily feed intake; FCR, feed conversion
ratio (feed: gain, g:g).
b
Linear and quadratic effects of housefly maggot meal supplementation were evaluated using
regression analysis.

the grower phase were numerically increased. It could be because
of the feed colour. Chicks are sensitive to colour (Olsson, Wilby, &
Kelber, 2016; Riber, 2015). Diet containing HMM was darker in co-
lour, so the broiler chicks showed their sensitivity to the feed colour
in the starter phase and accustomed to it in the grower phase. In the
grower phase, the numerically increased ADFI partly supports the
judgement. Broiler chicks fed on the HMM diet showed the poor
FCR in relation to the control group. The disturbance in the FCR
could be because of the lower body weight in the starter phase, and
broiler chicks consumed more feed to compensate their weight in
the grower phase.
Haematological characteristics of the broiler chicks fed on HMM
diets are within physiological range (Sturkie's avian physiology,
2000). The TP in the blood is the indicator of the health condition
of the broiler chick. TP is significantly increased in the grower phase,
which is in agreement with (Zang et al., 2018) who reported a sig-
nificantly higher level of TP in broiler chicks fed on a diet containing
earthworm meal. In contrast, no effects of dietary mealworm meal
on broiler chick's blood TP (Biasato et al., 2017, 2018) and dietary
black soldier fly meal on laying hen's blood TP (Marono et al., 2017)
were reported. The TP level in our study could be attributed to the
excellent amino acid profile of HMM. ALP and ALT significantly al-
tered in the grower phase, which is inconsistent with the findings
of (Biasato et al., 2017, 2018; Marono et al., 2017; Zang et al., 2018)
who reported no effect in laying hens and broiler chicks fed on black
soldier fly meal, mealworm meal and earthworm meal. The IgG, IgM
and IgA showed no linear or quadratic effect of HMM except IgA ef-
fected quadratically in the grower phase, which is inconsistent with
the findings of (Islam & Yang, 2017). Our results show that broiler
chicks are in normal healthy immune status and HMM was safe to
broiler chicks. UA is the final and main nitrogenous waste product
in poultry. In the current study, UA significantly increased with the
increasing inclusion level of HMM. However, (Loponte et al., 2017)
reported significantly lower levels of UA in barbary partridges fed
on black soldier fly meal and mealworm meal. In contrast, no ef-
fect for UA in broiler chicks fed on mealworm meal (Biasato et al.,
2017, 2018) or black soldier fly meal (Dabbou et al., 2018) diet. UA
is associated with high dietary nitrogen intake (Donsbough, Powell,
Waguespack, Bidner, & Southern, 2010). High levels of UA could be
because of dietary nitrogen in HMM. LZM is a natural antimicrobial
protein having bacteriostatic and bactericidal properties involved in
the immune process (Liu, Guo, Wang, & Yuan, 2010; Torki, Schokker,
Duijster-Lensing, & Krimpen, 2018). The increased level of LZM
could be because of its presence in the HMM. LZM is present in
the gut of insects to digest microorganisms (Gong, 2014). Dietary
HMM did not significantly influence the WBCs, RBCs, haemoglo-
bin, PCV, ALB, IgG, IgM, IgA, AST, BUN, GLU and TBIL. Similar find-
ings were reported for laying hens (Marono et al., 2017) and broiler
chicks (Dabbou et al., 2018) fed on black soldier fly meal, barbary
partridges fed on mealworm meal and black soldier fly meal (Loponte
et al., 2017). Our results demonstrated that the addition of HMM in
the diet of broiler chicks did not result in any adverse effect on the
haematological response.
Carcass characteristics are associated with the economics of
broiler production. In our study, the unchanged breast and thigh
percentage is in line with early reports in broiler chicks and free-
range chicks fed on diet containing black soldier fly fat, black sol-
dier fly meal and mealworm meal (Biasato et al., 2018; Dabbou et
6 | ELAHI et al.

TA B L E 4 Effect of Housefly Maggot

Housefly Maggot Meal inclusion p-value
Meal inclusion on Haematological
Items 0% 4% 8% SEM Lineara Quadratica characteristics of broiler chicks

21 day
WBCs (106/µl) 5.25 5.83 5.59 2.21 .543 .406
RBCs (Per 100 WBCs) 1.77 1.69 1.72 0.03 .434 .309
Haemoglobin (g/dL) 0.75 0.73 0.76 1.40 .818 .416
PCV (%) 23.30 22.35 22.33 0.28 .174 .439
3
Platelet (M/mm ) 4.00 2.50 1.17 0.51 .023 .933
TP (g/L) 25.25 23.32 24.94 0.33 .649 .009
ALB (g/L) 15.80 14.55 16.36 0.25 .208 .001
IgG (g/L) 4.37 4.44 4.38 0.05 .913 .565
IgM (g/L) 1.62 1.62 1.56 0.02 .188 .438
IgA (g/L) 2.42 2.42 2.42 0.01 .995 .822
ALT (µ/L) 9.58 9.54 10.08 0.17 .252 .602
AST (µ/L) 127.91 137.46 125.71 2.86 .748 .087
ALP (µ/L) 144.23 158.72 149.57 2.00 .158 .002
BUN (mmol/L) 0.50 0.51 0.44 0.02 .287 .470
UA (µmol/L) 238.25 262.39 301.46 6.93 <.001 .265
GLU (µmol/L) 10.27 9.92 11.25 0.35 .257 .267
TBIL (µmol/L) 11.95 11.28 10.73 0.26 .064 .901
LZM (U/ml) 96.50 101.07 104.76 1.44 .017 .872
42 day
WBCs (106/µl) 4.65 5.11 4.11 1.88 .221 .065
RBCs (Per 100 WBCs) 1.81 2.04 1.87 0.04 .516 .018
Haemoglobin (g/dL) 0.77 0.78 0.77 1.66 .970 .810
PCV (%) 24.22 27.13 24.80 0.52 .605 .015
Platelet (M/mm3) 1.50 2.33 1.17 0.49 .789 .361
TP (g/L) 25.81 25.37 27.68 0.33 .006 .017
ALB (g/L) 17.64 16.78 17.52 0.23 .829 .119
IgG (g/L) 4.33 4.43 4.38 0.05 .660 .484
IgM (g/L) 1.60 1.58 1.57 0.01 .362 .778
IgA (g/L) 2.41 2.47 2.42 0.01 .610 .025
ALT (µ/L) 10.08 9.91 8.91 0.18 .004 .173
AST (µ/L) 165.23 179.14 164.78 2.61 .933 .008
ALP (µ/L) 247.22 279.33 201.79 7.80 .000 .000
BUN (mmol/L) 0.52 0.52 0.48 0.04 .648 .823
UA (µmol/L) 198.47 228.22 218.49 3.28 <.001 <.001
GLU (µmol/L) 10.13 10.50 10.35 0.29 .778 .690
TBIL (µmol/L) 14.90 14.23 14.57 0.25 .596 .355
LZM (U/ml) 109.40 95.38 97.58 1.74 <.001 .001
a
Linear and quadratic effect of housefly maggot meal supplementation were evaluated using
regression analysis.

al., 2019; Kareem et al., 2018; Mohammed, 2017; Pieterse, Erasmus,
& Hoffman, 2018; Schiavone et al., 2017, 2018, 2019). However,
(Hwangbo et al., 2009) reported a significant effect of HMM diet
fed to broiler chicks. In the current study, broiler chicks fed on HMM
diet have numerically lower abdominal fat on 42 day compared con-
trols. Broiler chicks fed on 4% HMM have decreased abdominal fat
proportion followed by broiler chicks fed on 8% HMM, although no
statistical differences exist. Different from our results, decreased
abdominal fat in broiler chicks fed increasing level of HMM (Téguia,
Mpoame, & Okourou Mba, 2002) and higher abdominal fat in broiler
chicks fed black soldier fly meal diet (Schiavone et al., 2019) were re-
ported. Carcass characteristics extremely depend on the nutritional
ELAHI et al. | 7

TA B L E 5 Effect of Housefly Maggot

Housefly maggot meal inclusion p-value
Meal inclusion on carcass quality of
broiler chicks Items 0% 4% 8% SEM Lineara Quadratica

21 day
Eviscerated 651.20 624.40 626.17 6.11 .094 .262
weight (g)
Eviscerated yield 73.48 73.34 74.18 0.31 .367 .465
(g)
Abdominal fat % 1.41 1.44 1.37 0.08 .810 .752
Breast muscle % 24.05 23.97 24.69 0.26 .343 .481
Leg muscle % 19.49 19.16 19.61 0.27 .866 .513
Thymus % 2.46 2.69 2.41 0.17 .915 .492
Spleen % 0.90 1.01 1.03 0.06 .372 .692
Bursa % 1.55 1.66 1.75 0.07 .284 .943
42 day
Live weight (g) 2,793.80 2,718.90 2,826.20 38.82 .739 .284
Eviscerated 2,432.25 2,299.63 2,466.38 49.67 .781 .169
weight (g)
Dressing % 84.59 67.73 77.42 5.34 .632 .245
Eviscerated yield 69.00 68.78 69.04 0.98 .988 .910
(g)
Abdominal fat % 2.29 2.19 2.21 0.09 .708 .754
Spleen % 0.99 0.90 0.88 0.21 .279 .671
Thymus % 2.25 1.99 2.08 0.08 .369 .316
Bursa % 1.43 1.52 1.58 0.09 .511 .928
Thigh % 16.88 17.98 16.34 0.39 .569 .101
Shank % 13.69 13.95 14.26 0.25 .359 .960
Wing % 10.52 10.42 10.28 0.22 .676 .968
Pectoral % 29.88 28.31 27.07 0.74 .127 .915
a
Linear and quadratic effects of housefly maggot meal supplementation were evaluated using
regression analysis.

value and chemical composition of the diet (Zuidhof et al., 2003).
Thus, diverse results in carcass characteristics among the broiler
chicks fed on different dietary HMM level may be due to the feed
utilisation efficiency, which depends on the amino acids profile of
the diet (Hwangbo et al., 2009).
It the current study, meat quality was not significantly af-
fected by HMM. Broiler chicks fed on HMM had reduced shear
force (p = .059) in breast muscle; however, there is no statistical
effect. Shear force determines the tenderness of the meat, which
is an important factor of meat quality (Rajkumar et al., 2016). Our
study resulted that shear force numerically decreased with in-
creasing inclusion level of HMM. Normally, broiler chick's meat
has L* value range 52–56, a* value range 7–15, b* value range 8–16
(Karunanayaka, Jayasena, & Jo, 2016) and pH 5.3–6.5 (Hertanto,
Nurmalasari, Nuhriawangsa, Cahyadi, & Kartikasari, 2018). Results
of our study show that L* values for 1 hr post-mortem are lower
than the range; however, L* values for 24 hr post-mortem are within
the range. Higher L* values are the indicator of poor meat quality
(Pieterse et al., 2018). The lower L* values in our study express ac-
ceptable meat quality. Meat colour a* resulted in lower than the
range, however, b* values are within the range for both 1 and 24 hr
post-mortem. Our study is in agreement with (Cullere, Schiavone,
Dabbou, Gasco, & Zotte, 2019; Dabbou et al., 2019; Kareem et al.,
2018; Pieterse et al., 2018; Schiavone et al., 2017) who reported
no significant effect of black soldier fly and mealworm meal on
meat colour of broiler chicks, broiler quails and free-range chicks.
In contrary, (Pieterse, Pretorius, Hoffman, & Drew, 2014) reported
significant lower breast muscle L* value of broiler chicks fed on
HMM diet. pH values for 1 and 24 h to post-mortem values are
within range. Meat colour may change with variation in pH value
due to the ante-mortem stress experienced by broiler chicks during
the handling and slaughtering procedure (Hertanto et al., 2018;
Pieterse et al., 2014). Our studies showed no statistical effect on
the meat quality; however, it is acceptable as it numerically reduced
the shear force, which directly enhances the meat quality. The
overall results demonstrated that HMM did not negatively affect
meat quality.
In conclusion, our study confirmed that HMM could be alterna-
tive protein source as a replacement of soybean meal without any
detrimental effect on chick's performance, haematological profile
8 | ELAHI et al.

TA B L E 6 Effect of Housefly Maggot

Housefly Maggot Meal (% intake) p-value
Meal inclusion on meat quality of broiler
Itemsa 0 4 8 SEM Linearb Quadraticb chicks

Shear force (N) 28.27 27.10 22.95 1.17 .058 .542

1 hr PM
a* 4.04 3.74 3.94 0.24 .866 .646
b* 10.77 11.35 10.43 0.26 .577 .200
L* 46.42 48.12 45.53 0.60 .526 .112
pH 6.11 6.08 6.09 0.03 .320 .396
24 hr PM
a* 5.93 5.64 5.76 0.30 .822 .771
b* 11.96 11.69 10.86 0.31 .146 .674
L* 53.58 54.01 54.47 0.57 .543 .989
pH 5.87 5.92 5.89 0.03 .797 .504
a
p.m., post-mortem; a*, redness; b*, yellowness; L*, lightness.
b
Linear and quadratic effects of housefly maggot meal supplementation were evaluated using
regression analysis.

and meat quality. Further research is needed to determine the HMM
optimal level for broiler chick's diets and its effect on haematological
characters and meat quality.
AC K N OW L E D G M E N T S
This work was financially supported by Beijing Innovation
Consortium of Agriculture Research System (BAIC04-2019), the
Agricultural Science and Technology Innovation Program (ASTIP)
and National Key R&D Program of China (2018YFD0500403-4). The
authors declare that they have no conflict of interests.
E T H I C A L S TAT E M E N T
All experimental procedures were reviewed and approved by the
Animal Care and Use Committee of the Feed Research Institute of
the Chinese Academy of Agricultural Sciences (FRI-CAAS20181112).
ORCID
Usman Elahi https://orcid.org/0000-0003-0033-4337
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How to cite this article: Elahi U, Ma Y-b, Wu S-g, Wang J,
Zhang H-j, Qi G-h. Growth performance, carcass
characteristics, meat quality and serum profile of broiler
chicks fed on housefly maggot meal as a replacement of
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https​://doi.org/10.1111/jpn.13265​