Aquaculture Reports 24 (2022) 101183

Contents lists available at ScienceDirect

Aquaculture Reports
journal homepage: www.elsevier.com/locate/aqrep

Effect of dietary chicken gut meal levels on growth performance, plasma

biochemical parameters, digestive ability and fillet quality of
Cyprinus carpio
Zuxiang Peng a, b, Lin Yan a, b, Libo Wei a, b, Xin Gao a, b, Lidong Shi a, b, Tongjun Ren a, b, c,
Wei Wang a, b, c, Yuzhe Han a, b, c, *
a
College of Fisheries and Life Sciences, Dalian Ocean University, Dalian 116023, China
b
Laboratory of Aquatic Animal Nutrition and Feed, Dalian Ocean Universiteny, Dalian 116023, China
c
Key Laboratory of Applied Biology and Aquaculture of Northern Fishes in Liaoning Province, Dalian Ocean Universiteny, Dalian 116023, China

A R T I C L E I N F O A B S T R A C T

Keywords: An eight-week feeding trial was conducted to investigate the effects of chicken gut meal (CGM) in experimental
Chicken gut meal diet on growth performance, plasma biochemical parameters, digestive enzymes activity, intestinal morphologic,
Growth performance muscle composition, and fillet quality of common carp (Cyprinus carpio) (initial body weight: 57.34 ± 0.13 g).
Plasma biochemical parameters
Experimental fish were fed with experimental diets containing CGM at 0% (CGM 0 group), 5% (CGM 5% group),
Digestive activity
10% (CGM 10% group), 15% (CGM 15% group), and 100% (CGM 100% group) levels, respectively. The results
Fillet Quality
Common carp (Cyprinus carpio) revealed that CGM significantly improved final body weight (FBW), weight gain rate (WGR), specific growth rate
(SGR), and feed conversion ratio (FCR) (P < 0.05) of experimental fish. Plasma GH and IGF-I concentrations in
the CGM 15% group were substantially higher than in the other groups (P < 0.05). CGM 15% group showed the
highest FBW, WG, SGR, and lowest FCR (P < 0.05) of all treatments. Except for plasma total protein (TP), al­
bumin (ALB), and globulin (GLB) contents, the plasma biochemical parameters were significantly improved (P <
0.05). Pepsin (PEP), amylase (AMS), and lipase (LPS) activities were significantly higher in CGM 10%, CGM 15%,
and CGM 100% groups compared to the control group and reached a maximum in the CGM 15% group (P <
0.05). Diet supplementation with CGM significantly increased midgut villi height (VH), villi width (VW), and
muscle layer thickness (MT) in common carp. The inclusion of dietary CGM to the diet could improve the crude
protein and crude lipid content of common carp muscle, as well as influence fillet quality by increasing chew­
iness. In conclusion, the optimum inclusion of CGM to the diet is 15%, which can considerably improve growth
performance, plasma biochemical parameters, digestive activity, and fillet quality of common carp.

1. Introduction and high price of fishmeal resources have led to the instability of fish­
meal resources, which to a certain extent limits the sustainable devel­
Over decades, global aquaculture production has been increasing opment of the aquaculture industry. Nowadays, there is an urgent need
and it is expected to exceed capture production by 2025 (Freitas et al., to develop a new feed protein source with high protein content, low
2020; Ottinger et al., 2016). Feed represents one of the most significant price, easy access, and stable supply to meet the needs of the aquafeed
operational expenses in aquaculture, and reducing feed costs is critical industry.
to profitability as the expansion of aquaculture occurs. Protein is always Although high quantities of plant protein in aquatic animal diets may
dominant and most costly as a primary ingredient necessary for the reduce feed costs, the anti-nutritional factors and amino acid imbalances
maintenance and growth of animals in fish and shrimp diets (Galkan­ may also harm fish intestine and hinder growth (Fontinha et al., 2021;
da-Arachchige et al., 2020; Shiau, 1998). Fishmeal serves as a Oliva-Teles, 2012). Animal by-products are considered a high-quality
high-quality animal protein with reasonable amino acid composition protein that is less costly than fishmeal and devoid of anti-nutrients as
and is widely used by the aquafeed industry. In recent years, the scarcity compared to plant protein sources (Fuertes et al., 2013; Moutinho et al.,

* Corresponding author at: College of Fisheries and Life Sciences, Dalian Ocean University, Dalian 116023, China.
E-mail address: hyz@dlou.edu.cn (Y. Han).

https://doi.org/10.1016/j.aqrep.2022.101183
Received 21 April 2022; Received in revised form 18 May 2022; Accepted 18 May 2022
Available online 26 May 2022
2352-5134/© 2022 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Z. Peng et al. Aquaculture Reports 24 (2022) 101183

2017; Randazzo et al., 2021; Wuraola, 2019). Among animal committee of Dalian Ocean University. The use and care of animals tally
by-products, poultry by-product meal (PBM) offered one of the best with China’s animal protection law.Table 1.
nutritional values and amino acid balances (Dawood et al., 2020a;
Fontinha et al., 2021). Previous studies revealed positive results on the
2.2. Experimental diets
utilization of PBM to substitute fish meal in aquatic feed for grass carp
(Ctenopharyngodon idella) (Tabinda and Butt, 2012), catfish (Clarias
Five experimental diets were formulated as clarified in Table 2.
batrachus) (Giri et al., 2010), humpback grouper (Cromileptes altivelis)
Anshan Yufeng Feed Co. Ltd. (Anshan city, China) offered CGM (crude
(Shapawi et al., 2007), and juvenile cobia (Rachycentron canadum)
protein 65.47%, crude lipid 14.80%). The experimental diets were
(Zhou et al., 2011). However, PBM is made up of a diverse range of raw
formulated to contain 0, 5, 10, 15, 100% CGM (CGM 0, CGM 5%, CGM
materials, including necks, feet, undeveloped eggs, and intestines. Thus,
10%, CGM 15%, CGM 100% diets). Group CGM 0 was set up as a control
the quality of PBM is determined by both the quality of the ingredients
group and Group CGM 100% as a negative control group. As additional
used in the meal and how the ingredients are processed and vary from
supplements, FM, soybean meal, and other plant protein blends were
batch to batch, and among supplier companies, and may lack certain
used, soybean oil was added to the experimental diets to balance lipid
functional components (Hill et al., 2019； Chaklader et al., 2020；
levels. All ingredients were fully mixed before being fabricated into a
Chaklader et al., 2019). Chicken gut meal (CGM) is a kind of PBM that is
single pellet size (3.5 mm) using a press machine (JLA-125; Pinzheng
a new form of high-quality feed protein source manufactured from the
Equipment Co. Ltd.). Pellets were dried in a ventilated oven (DK-s26;
fresh chicken gut as a single raw material and processed by rinsing,
Shanghai Samsung Laboratory Instrument Co. Ltd.) to a moisture con­
steaming, spray drying, and crushing procedures, resulting in a more
tent of approximately 10%. All diets were packaged and stored at − 20
consistent quality. The crude protein and crude lipid level of CGM are
℃ until used.
similar to that of fish meal, and some of the amino acid content is even
greater, making CGM a high-quality animal protein with some promises
based on nutritional and amino acid analyses (Tabinda and Butt, 2012). 2.3. Experimental procedures
Only few studies reported the utilization of CGM in aquatic species
(Tabinda and Butt, 2012). The study of Tabinda and Butt (2012) Common carps were obtained from a private farm located in Dan­
revealed that 100% of FM can be replaced by CGM without addition of dong City, China, temporarily reared at the Key Laboratory of Fish
amino acids and compromising growth and feed conversion ratio in Applied Biology and Aquaculture in North China (Dalian, China) for two
grass carp fry diet. weeks and fed with the CGM 0 diet.The experiment was conducted using
Common carp (Cyprinus carpio) is an omnivore fish that is a major cages in a concrete pond (4.5 m × 3.5 m×1.4 m) with a circulation and
freshwater aquaculture species in China, accounting for a significant filtration system, and similar-sized individuals (57.30 ± 0.10 g) were
percentage of aquaculture (Luo et al., 2020). The yield of common carp randomly distributed into 15 polycarbonate cages (1.3 m × 0.8 m×0.7
in 2020 reached 2896,700 tonnes, an increase of 11,400 tonnes or m) at a density of ten fish per cage. Fish were fed to apparent satiety
0.92% compared to 2019 (Fisheries and Fisheries Administration, twice a day (08:00 and 16:00) for 56 days. Water temperature, dissolved
2021). The objective of this study was to analyze the effects of dietary oxygen and pH in this trial were 26 ± 1 ◦ C, 6 ± 0.5 mg/L and 7.9 ± 0.3,
CGM on growth performance, plasma biochemical parameters, digestive respectively.
ability and fillet quality of common carp to provide scientific evidence
for their application in aquaculture. Table 2
Composition and nutrient levels of experimental feed (dry matter).
2. Materials and methods Ingredients (g/kg) CGM 0 CGM CGM CGM CGM
5% 10% 15% 100%
2.1. Ethical statement Chicken gut meal 0 50 100 150 1000
Fishmeal 40 40 40 40 0
The study protocol and procedures were approved by the ethics Corn protein meal 50 50 50 50 0
Soybean 315 312 309 306 0
Casein 140 105 70 35 0
Rapeseed meal 60 60 60 60 0
Table 1 Wheat flour 323.1 320.1 317.1 314.1 0
Nutritional levels and amino acid composition of chicken gut meal and fish meal. Soybean oil 41 35 29 23 0
Sodium chloride 3 3 3 3 0
Items Chicken gut meal Peru fish meal
Calcium bis 20 20 20 20 0
Crude protein 65.47% 65.04% 50% Choline 1.5 1.5 1.5 1.5 0
Crude lipid 14.80% 10.21% chloride
Ash 6.12% 8.17% Vitamin C 0.4 0.4 0.4 0.4 0
Amino acids Vitamin mixture1 1 1 1 1 0
Asp 5.30% 5.81% Mineral mixture2 5 5 5 5 0
Thr 2.71% 2.71% Proximate
Ser 2.59% 2.47% composition
Glu 8.58% 8.40% Dry matter, % 89.97 89.92 89.85 89.83 89.91
Gly 3.62% 3.91% Crude protein, % 31.23 31.48 31.73 31.98 65.47
Ala 3.59% 4.08% DM
Val 3.31% 3.13% Crude lipid, %DM 5.49 5.61 5.72 5.84 14.80
Ile 2.73% 2.61% Ash, %DM 6.67 6.68 6.70 6.99 6.12
Leu 4.74% 4.75%
Tyr 2.23% 2.00%
1Vitamin mixture (per kg of premix): vitamin A, 1000,000 IU; vitamin D3,
Phe 2.58% 2.66% 300,000 IU; vitamin E, 4000 IU; vitamin K3, 1000 mg; vitamin B1, 2000 mg;
His 1.29% 1.92% vitamin B2, 1500 mg; vitamin B6, 1000 mg; vitamin B12, 5 mg; nicotinic acid,
Lys 3.98% 5.14% 1000 mg; vitamin C, 5000 mg; Ca pantothenate, 5000 mg; folic acid, 100 mg;
Arg 3.64% 3.61% inositol, 10,000 mg; carrier glucose; H2O ≤ 100 g/kg. 2Mineral mixture (0.025
Pro 2.73% 2.54% mg/g of premix): NaCl, 107.79; MgSO4⋅7 H2O, 380.02; NaHPO4⋅2 H2O, 241.91;
Cys 0.80% 0.66% KH2PO4, 665.20; Ca(H2PO4)⋅2 H2O, 376.70; Fe citrate, 82.38; Ca lactate,
Met 1.04% 1.76%
907.10; Al(OH)3, 0.52; ZnSO4⋅7 H2O, 9.90; CuSO4, 0.28; MnSO4⋅7 H2O, 2.22; Ca
TAA 54.42% 58.16%
(IO3)2, 0.42; CoSO4⋅H2O, 2.77.

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2.4. Sample collection Table 3

Effects of dietary CGM levels on growth performances of common carp (Cyprinus
At the end of the trial, all fish were starved for 24 h before the carpio).
sampling. Then the fish were anesthetized with 50 mg/L MS222 Parameters Groups
(ScanVac, Sigma Aldrich Shanghai Trading Co., Ltd, Shanghai, China) CGM 0 CGM 5% CGM 10% CGM 15% CGM
and weighted to calculate growth performance refer to Wang et al. 100%
(2020). The livers, anterior midguts, and dorsal muscles of six fish from
IBW/g 57.34 ± 57.24 ± 57.20 ± 57.32 ± 57.32 ±
each parallel were promptly removed, then the samples were combined FBW/g 0.13 0.11 0.05 0.18 0.15
into the same group and kept at − 80 ◦ C for testing. To produce sections 131.77 ± 137.70 ± 151.65 ± 165.01 ± 138.36 ±
of intestinal tissue, a 1 cm piece of midgut was fixed in Boone’s solution. 5.13a 0.15a 2.14b 1.32c 1.35a
Blood was collected intravenously from 4 fish in each parallel using WGR/% 129.81 ± 140.56 ± 165.13 ± 187.87 ± 141.39 ±
7.43a 0.33a 2.72b 2.10c 3.36a
heparinized (1600 U/ml; Nakalai Tesque) syringes and centrifuged at SGR/(%/d) 1.41 ± 1.53 ± 1.70 ± 1.92 ± 1.53 ±
5000 r/min for 10 min. The supernatant was stored at − 80 ◦ C and used 0.01a 0.04a 0.04b 0.01c 0.08a
for the analysis of plasma biochemical parameters. CF/(g/ 1.44 ± 1.49 ± 1.43 ± 1.46 ± 1.46 ±
cm3) 0.06 0.05 0.04 0.01 0.03
VSI/% 7.18 ± 6.64 ± 6.88 ± 6.45 ± 6.92 ±
2.5. Biochemical analysis
HSI/% 0.23 0.20 0.52 0.50 0.31
1.60 ± 1.77 ± 1.61 ± 1.62 ± 1.62 ±
Plasma growth hormone (GH) and insulin-like growth factor (IGF-1) 0.04 0.06 0.12 0.14 0.10
levels were measured by kits from Jiancheng Bioengineering Institute ISI/% 2.30 ± 2.42 ± 2.48 ± 2.53 ± 2.60 ±
(Nanjing, China). FCR 0.12 0.09 0.18 0.04 0.03
FI/g 1.51 ± 1.49 ± 1.42 ± 1.25 ± 1.23 ±
Plasma biochemical parameters were measured by 7600–110 auto­ SR/% 0.01a 0.01a 0.01b 0.02c 0.05c
matic biochemical analyzer (Hitachi, Japan), including total protein 112.35 ± 120.15 ± 133.80 ± 134.25 ± 99.86 ±
(TP), albumin (ALB), globulin (GLB), total cholesterol (TC), triglyceride 6.01ab 0.55bc 1.85c 1.64c 8.91a
(TG), alanine aminotransferase (ALT), aspartate aminotransferase 100 100 100 100 100
(AST). Note: IBW: Initial body weight. FBW: Final body weight. WGR: weight gain rate.
The activities of digestive enzymes including lipase (LPS), amylase CF: condition factor.SGR: specific growth rates. FCR: feed conversion ratio. VSI:
(AMS), and pepsin (PEP) were measured by kits from Jiancheng viscerosomatic index. HSI: hepatosomatic index. ISI: Intestinesomatic index. FI:
Bioengineering Institute (Nanjing, China). feed intake. SR: Survival rate. Values represent means ± SEM (n = 3), and values
Histology of midgut was performed according to Zeng et al. (2021). in the same row with different letters were significantly different (P < 0.05).
The intestinal sample was fixed using 10% formalin for 24 h and
dehydrated using a series of graded ethanol concentrations. Then to those in the control group (P < 0.05). However, there was no significant
prepare the slices for hematoxylin-eosin (HE), standard paraffin difference in the FI between the CGM 100% group and the control group
embedding methods were utilized. Measurement using S-viewer soft­ (P > 0.05). Figs. 1 and 2 depicted the impact of a dietary CGM on the
ware and observation with a light microscope equipped with an image plasma GH and IGF-I contents of common carp. The plasma GH and IGF-
analyzer. To assess muscle layer thickness (MT), villus height (VH), and I concentrations in the CGM 15% group were substantially greater than
villus width (VW), at least 10 intact villi were chosen and averaged for in the other groups (P < 0.05).Figs. 3 and 4.
each sample.
AOAC standard method (AOAC, 1990) was used for proximate 3.2. Plasma biochemistry
analysis of diet and dorsal muscles.
The fillet quality analysis was conducted using samples from three In Table 4, the plasma biochemical parameters of Cyprinus carpio fed
fish per cage. For the texture analyser, 2.0 cm × 2.0 cm× 1.0 cm sized of the experimental diets for 56 days were shown. Dietary CGM adminis­
white muscle taken from the highest point matching to the dorsal fin. tration did not affect plasma total protein (TP), albumin (ALB), or
Texture analysis parameters were set refer to Yu et al. (2020). globulin (GLO) levels among groups (P > 0.05). CGM 15% group
showed the lowest total cholesterol (TC) content and triglyceride (TG)
2.6. Statistical analysis content while the CGM 100% group showed the highest cholesterol (TC)
content and triglyceride (TG) content (P < 0.05). A similar result was
The experimental data were analyzed using one-way ANOVA with also found in plasma transaminase activity, the CGM 15% group showed
the software SPSS 25.0 (SPSS, Chicago, Illinois), while data were the lowest aspartate aminotransferase (AST) and alanine aminotrans­
expressed as mean values ± standard error of mean (SEM). Data from ferase (ALT) activities while the CGM 100% group showed the highest
each group were compared by the Duncan test and a significant differ­ AST and ALT activities (P < 0.05).
ence was set at P < 0.05.
3.3. Digestive enzyme activity
3. Results
Intestinal PEP, AMS, and LPS activities in groups CGM 10%, CGM
3.1. Growth performances 15%, and CGM 100% were significantly higher than in groups CGM
0 and CGM 5% (P < 0.05) while no significant variations were observed
As presented in Table 3, There was no significant difference in the
condition factor (CF), viscerosomatic index (VSI), hepatosomatic index
(HSI) and survival rates (SR) among groups (P > 0.05). The group of fish
fed CGM 15% and CGM 10% diets showed significantly higher FBW,
WGR, and SGR than those fed the CGM 0, CGM 5%, and CGM 100% diets
(P < 0.05). Significantly lower FCR was observed in CGM 100%, CGM
15%, and CGM 10% groups and FCR in a dose-dependent manner (P <
0.05). CGM 15% group showed the highest FBW, WGR, and SGR while
CGM 100% group showed the lowest FCR (P < 0.05). FI of common carp
in the CGM 10% and CGM 15% groups was significantly higher than Fig. 1. The sampling site of fish for fillet quality.

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3.4. Intestinal morphologic

Dietary CGM levels had a significant impact on the histomorpho­

metric characteristics of the midgut (P < 0.05) (Table 6). Muscular layer
thickness (MT) was significantly impacted by dietary amounts of CGM in
the D4 group, which had the greatest MT compared to the other groups
(P < 0.05). Villus height (VH) in groups CGM 10% and CGM 15% were
significantly higher than in groups CGM 0, CGM 5%, and CGM 10%
(P < 0.05) meanwhile no significant variations were observed in groups
CGM 0, CGM 5%, and CGM 100% (P > 0.05). The CGM 15% group had
the highest villus width (VW) (P < 0.05), and there were no significant
differences in the other groups (P > 0.05).

3.5. Muscle proximate analysis

The proximate analysis of the muscle of Cyprinus carpio fed with

experimental diets for 56 days are shown in Table 7. The contents of
crude protein and crude lipid in groups CGM 10% and CGM 15% were
substantially higher than in the CGM 0 group. The highest contents of
crude protein and crude lipid were observed in the CGM 15% group
(P < 0.05). The crude protein and crude lipid contents in groups CGM
5%, CGM 10%, CGM 15%, and CGM 100% were all higher than in group
CGM 0 (P > 0.05). There were no considerable differences were
observed in the contents of ash and moisture among groups (P > 0.05).

Fig. 2. Effects of dietary CGM on serum GH content of Cyprinus carpio. Note:

3.6. Fillet quality parameters
Different lowercase letters at the top of the bar chart indicate significant dif­
ferences between groups (P < 0.05).
The texture parameters of Cyprinus carpio fed the experimental diets
for 56 days are shown in Table 8. In comparison to fish fed a basic diet,
dietary chicken gut meal generated a higher muscle hardness, springi­
ness, cohesiveness, gumminess, and chewiness in muscle. Dietary in­
clusion of CGM had a significant effect on the chewiness of the fillet
(P < 0.05), while there were no significant variations in hardness,
cohesiveness, springiness, and gumminess (P > 0.05). The CGM 15%
group exhibited the highest values for chewiness and chewiness in
groups CGM 5%, CGM 10%, CGM 15%, and CGM 100%, which were
significantly higher than CGM 0 group (P < 0.05).

4. Discussion

4.1. Growth performances

PBM as an excellent quality animal protein feed ingredient in

aquaculture has been proven can impact growth parameters in aquatic
animals including Nile tilapia (Oreochromis niloticus) (Dawood et al.,
2020b), totoaba juveniles (Totoaba macdonaldi) (Zapata et al., 2016),
Japanese sea bass, (Lateolabrax japonicas) (Y. Wang et al., 2015), sun­
shine bass (Morone chrysops ×M. saxatilis) (Rawles et al., 2011), black
sea bass (Centropristis striata) (Dawson et al., 2018), gilthead seabream
(Sparus aurata) (Sabbagh et al., 2019), barramundi (Lates calcarifer)
(Chaklader et al., 2019), and juvenile crayfish (Pacifastacus leniusculus
Dana, Astacidae) (Fuertes et al., 2013). In this study, the dietary CGM
had a significant impact on FBW WGR, SGR, and FCR of common carp.
WGR, SGR, and FCR in CGM 10%, CGM 15%, and CGM 100% groups
Fig. 3. Effects of dietary CGM on serum IGF-I content of Cyprinus carpio. Note: improved substantially and the CGM 15% group exhibited the highest
Different lowercase letters at the top of the bar chart indicate significant dif­ values for FBW, WGR, and SGR. Similar results were also declared in
ferences between groups (P < 0.05). common carp and Nile tilapia with fermented PBM inclusion of 20%
enhancing growth performance and feed utilization dramatically
in groups CGM 0 and CGM 5% (P > 0.05) ( Table 5). CGM 15% group (Dawood, et al., 2020a, 2020b). The maximum growth performance of
showed the highest PEP, AMS, and LPS activities while CGM 0group grass carp was observed at 22.5% CGM in the diet, according to Tabinda
showed the lowest (P < 0.05). While no significant effect was observed and Butt (2012). The promoted growth performance of common carp fed
in groups CGM 0 and CGM 5%, the PEP, AMS, and LPS activities of CGM high levels of fermented PBM might be attributed to an increase in
5% were higher than in CGM 0. digestive enzyme activity, according to Dawood et al. (Dawood et al.,
2020a). Similar to the former, The present study found that the inclusion
of CGM increased the intestinal digestive enzyme activities of common
carp in each test group, and the activities of PEP, AMS, and LPS in the

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Fig. 4. midgut morphology of common carp fed the experimental diets for 8 weeks (×40).

Table 4 Table 6
Effects of dietary CGM levels on plasma biochemical parameters of common carp Effect of dietary CGM levels on the intestinal (midgut) morphology of common
(Cyprinus carpio). carp (Cyprinus carpio).
Parameters Groups Parameters Groups

CGM 0 CGM 5% CGM 10% CGM 15% CGM CGM 0 CGM 5% CGM 10% CGM CGM
100% 15% 100%

TP/(g /L) 22.65 23.08 23.25 23.44 23.29 MT (μm) 17.76 19.85 23.47 28.41 20.15
± 0.32 ± 0.58 ± 0.26 ± 0.69 ± 0.36 ± 2.32a ± 3.33a ± 0.25ab ± 0.25b ± 0.05a
ALB/(g /L) 10.22 10.03 10.12 11.13 11.28 VH (μm) 98.69 134.18 153.85 155.06 136.86
± 0.15 ± 0.17 ± 0.19 ± 0.32 ± 0.13 ± 15.76a ± 20.63ab ± 5.42b ± 1.55b ± 4.37ab
GLO/(g /L) 12.43 13.05 13.13 12.31 12.41 VW (μm) 22.30 25.98 25.00 28.87 24.93
± 0.28 ± 0.46 ± 0.19 ± 0.45 ± 0.21 ± 1.23a ± 0.99ab ± 1.37ab ± 1.63b ± 1.09ab
TC/(mmol/ 2.60 2.59 2.58 2.55 3.31
L) ± 0.02b ± 0.03ab ± 0.05ab ± 0.03a ± 0.01c Values represent means ± SEM (n = 3), and values in the same row with
TG/(mmol/ 1.77 1.76 1.76 1.73 1.92 different letters were significantly different (P < 0.05).
L) ± 0.03c ± 0.02b ± 0.01b ± 0.01a ± 0.02d
AST/(U/L) 116.33 115.67 112.33 106.33 137.00
ALT/(U/ ± 0.67b ± 1.76b ± 0.88b ± 1.76a ± 2.65c Table 7
L) 14.67 13.67 12.67 9.67 24.33 Muscle proximate composition of common carp (Cyprinus carpio) fed with test
± 0.67c ± 0.33bc ± 0.33b ± 0.33a ± 0.67d diets for 56 days (dry matter).
Values represent means ± SEM (n = 3), and values in the same row with Parameters Groups
different letters were significantly different (P < 0.05).
CGM 0 CGM 5% CGM 10% CGM CGM
15% 100%

Table 5 Crude 55.90 56.43 60.67 63.70 61.35

Effects of dietary CGM levels on digestive enzyme activity of common carp protein % ± 0.04a ± 0.30a ± 0.16b ± 0.21c ± 0.29b
Crude lipid 14.42 15.42 15.74 16.92 14.77
(Cyprinus carpio).
% ± 0.32a ± 0.42ab ± 0.63bc ± 0.21c ± 0.24ab
Parameters Groups Ash % 2.44 2.35 2.53 2.56 2.58
± 0.15 ± 0.02 ± 0.15 ± 0.10 ± 0.08
CGM 0 CGM 5% CGM 10% CGM 15% CGM
Moisture % 77.21 77.25 77.24 77.34 77.27
100%
± 0.59 ± 0.71 ± 0.83 ± 0.23 ± 1.01
PEP (U /mg 5.87 6.58 9.36 16.85 14.39
prot) ± 0.07a ± 0.29a ± 0.23b ± 1.07d ± 0.27c Values represent means ± SEM (n = 3), and values in the same row with
AMS (U/mg 0.93 0.99 1.84 1.89 1.44 different letters were significantly different (P < 0.05).
prot) ± 0.03a ± 0.11a ± 0.06c ± 0.06c ± 0.02b
LPS (U/g 4.99 5.32 8.10 15.41 11.59 CGM 10%, CGM 15%, and CGM 100% groups were significantly higher
prot) ± 0.12a ± 0.33a ± 0.06b ± 0.29d ± 0.63c
than those in the CGM 0 group. In part, the excellent growth perfor­
Values represent means ± SEM (n = 3), and values in the same row with mance under the treatment conditions can be attributed to the
different letters were significantly different (P < 0.05). enhancement of these digestive enzyme activities, which promoted the

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Table 8 tends to perform better in fish diets (Farmanesh et al., 2019; Dozier
Effects of dietary CGM levels on fillets texture profiles of common carp (Cyprinus et al., 2003; Hoehler, 2003; Tabinda and Butt, 2012). According to the
carpio). evidence presented above, a diet supplemented with a suitable CGM
Parameters Groups may increase growth performance by promoting the expression of
CGM 0 CGM 5% CGM 10% CGM 15% CGM
growth-related genes.
100%
4.2. Plasma biochemical parameters
Hardness/(gf) 702.75 773.53 790.67 923.24 800.39
± 33.42 ± 17.75 ± 22.77 ± 67.49 ± 30.28
Cohesiveness 0.16 0.18 0.20 0.21 0.18 Plasma biochemical indicators are crucial for determining whether
± 0.13 ± 0.03 ± 0.01 ± 0.03 ± 0.01 or not the fish are healthy, and plasma indicators are extremely
Springiness/ 0.74 0.76 0.77 0.84 0.90
vulnerable to the impact of feed nutrition (Sankian et al., 2018). plasma
(mm) ± 0.02 ± 0.01 ± 0.02 ± 0.08 ± 0.06
Gumminess/ 110.32 139.24 158.13 193.88 144.07
TP, which is the plasma of ALB and GLO, is synthesized in the liver and
(gf) ± 6.17 ± 4.21 ± 6.22 ± 9.72 ± 5.19 reflects the body’s protein metabolism and the liver’s functional con­
Chewiness/ 83.11 105.13 121.35 161.77 122.16 dition; a rise in TP and ALB content shows that the liver’s capacity to
(mJ) ± 6.32a ± 3.20b ± 5.10c ± 4.49d ± 7.94c synthesis protein is increased (Tan et al., 2017). TC and TG indicate the
Values represent means ± SEM (n = 3), and values in the same row with status of the body’s fat metabolism, with lipid transport blockage
different letters were significantly different (P < 0.05). leading to a rise in total plasma cholesterol levels (S. Li et al., 2017;
Sankian et al., 2018). In the current research, the amount of CGM added
absorption of nutrients. In this study, FI of common carp in the CGM to the feed had no significant effect on plasma TP, ALB, or GLO of
10% and CGM 15% groups was significantly higher than those in the common carp, but did show an increasing trend, indicating that adding
control group. We speculated that the increased feed intake also CGM to the feed had no effect on normal protein metabolism and was
contributed to the growth of common carp to some extent. HSI is highly beneficial to protein synthesis. The plasma TG and TC levels decreased
sensitive to the nutritional status of the fish, and excessive nutrient and then increased with the addition of CGM in this experiment, indi­
intake may lead to an increase in HSI (Brusle and Anadon, 2017). The cating that an appropriate amount of CGM in the feed could improve fat
reasons why the four groups (CGM 0, CGM 5%, CGM 10%, and CGM metabolism of common carp, whereas an excessive amount of CGM
15%) and the CGM 100% group did not show significant changes in HSI could lead to fat metabolism disorder. AST and ALT are transaminases
in this study might be different. On the one hand, increasing the amount involved in amino acid metabolism in the liver. Under normal circum­
of CGM in the feed boosted the levels of growth hormone and insulin stances, the activity of these two aminotransferases in the plasma is
growth factor, stimulating growth, while on the other hand, the common minimal, and they are only released into the plasma when the liver is
carp themselves are in a rapid growth phase, consuming a range of damaged, increasing activity (Tan et al., 2016). The current research on
nutrients (Stallings et al., 2010). This also prevented a large number of the influence of PBM on plasma biochemical parameters in aquatic an­
nutrients from being converted into fat deposited in the liver, and imals is mostly focused on feed protein source replacement. High
therefore the HSI did not increase significantly. Therefore these four amounts of PBM replacing fish meal in aquatic species such as hybrid
groups (CGM 0, CGM 5%, CGM 10%, and CGM 15%) did not show an grouper (Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀) (Wang
increase in HSI. The crude lipid content of the CGM 100% diet is 14.8%, et al., 2020), juvenile gilthead seabream (Karapanagiotidis et al., 2019),
which is already a high-fat diet for common carp (Abasubong et al., and tench (Panicz et al., 2017) had no negative impact on plasma
2018). Previous studies have shown that high-fat diets reduce feed biochemical parameters or protein and lipid metabolism, according to
intake, limit lipid absorption and inhibit growth in aquatic animals research. In the present study, AST and ALT activities exhibited a trend
(Zhou et al., 2019; Yin et al., 2021). As shown in Table 2, the high fat of decreasing and then increased with increasing CGM addition levels.
diet had a negative effect to some extent on both growth performance Plasma TG content, AST, and ALT activities in CGM 15% group were the
and feed intake in the CGM 100% group. We speculated that the lowest and considerably lower than other groups. Plasma triglyceride
reduction in feed intake prevented the common carp in the CGM 100% content, AST, and ALT activities in group CGM 100% were the highest
group from depositing large amounts of fat in the liver and increasing and substantially higher than other groups. Hence, the results of this
the HSI within a short period of time. Therefore CGM 100% group did study suggested that the addition of CGM to the diet can improve the
not show an increase in HSI. plasma biochemical parameters of common carp, but the addition of
Growth in vertebrates, including fish, is controlled mainly by the 100% may cause abnormalities in the liver metabolism of common carp.
GH–IGF system (Sheridan, 2011; Blanco, 2020; Kaneko et al., 2019). In
the current research, with increasing amounts of CGM in the diet, 4.3. Digestive enzymes activity
plasma GH and IGF-I levels rose and then declined, peaking in the D4
group, which also corresponded to common carp growth. The above Considering digestive enzymes activity in the fish intestine is regu­
results indicate that the addition of appropriate levels of CGM to feed lated by the protein source in the diet and can promote feed utilization in
can promote the secretion of GH and IGF-I to improve growth perfor­ the fish intestine, they are commonly used to assess digestive capacity in
mance. Sardines fed the PBM-based diet showed decreased IGF-I fish (Moutinho et al., 2017; Karapanagiotidis et al., 2019; Magalhães
expression in the liver and muscle, but no growth retardation, accord­ et al., 2015). Previous studies on the effect of PBM on the activities of the
ing to Hatlen et al. (2015). Except for the spleen, Panicz (2016) found digestive enzymes of aquatic animals have primarily focused on the
that there were no suppressions of the amount of GH gene expression in substitution of feed protein sources. The results of studies on the sub­
most tissues after complete replacement of fish meal by PBM in tench stitution of PBM for fish meal in Nile tilapia (Dawood et al., 2020b),
(Tinca tinca) diets. However, Karapanagiotidis et al. (2019) reported that juvenile sobaity sea bream (Sparidentex hasta) (Hekmatpour et al.,
the liver gene expression of the GH/IGF axis was decreased by high 2019), and gilthead seabream (Karapanagiotidis et al., 2019) have
dietary doses of PBM and suppress growth in gilthead seabream. Kar­ shown that the substitution of fish meal with appropriate amounts of
apanagiotidis et al. (2019) and Kumar et al. (2017) believed that the PBM can enhance the intestinal digestive enzymes activity of aquatic
downregulation of GH/IGF gene expression in PBM-fed fish might be species. Correspondingly, Dawood et al. (2020a) demonstrated that
due to changes in dietary amino acid composition. The amino acid supplementing the diets of common carp with 15% and 20% fermented
composition of PBM can be affected by the raw material composition PBM increased the activity of digestive enzymes in the intestine
and processing of PMB, in contrast to the consistent quality CGM, which considerably. In the current investigation, these results revealed that the
inclusion of CGM to the diet had a massive effect on the intestinal PEP,

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Z. Peng et al. Aquaculture Reports 24 (2022) 101183

AMS, and LPS activities of common carp, with maximal intestinal the muscle crude lipid content of the CGM 100% group was not signif­
digestive enzyme activity occurring when the CGM was supplemented at icantly different from that of the control group, which could well be
15%. attributed to the negative effects of the high-fat diet. The high-fat diet
reduced feed intake and inhibited lipid absorption, which is likely to
4.4. Intestinal morphologic account for the lower muscle fat content of common carp in the CGM
100% group.Thus, these results demonstrated that supplementing 10%
Fish feed ingredients have a considerable influence on intestine ar­ or 15% CGM to the diet considerably enhanced the muscle crude protein
chitecture and general health. Intestine morphology, which is primarily and crude lipid content of common carp.
assessed by measuring the muscle thickness and villi, is a significant
method for assessing the health and function of the gut (Li et al., 2019;
Wang et al., 2020). Higher villus height or breadth is considered to show 4.6. Fillet quality parameters
increased surface area for nutrient absorption, and increased muscle
thickness can boost intestine digestion and absorption capabilities (Tan The quality of aquatic animal flesh can impact the sale of aquatic
et al., 2018; Wei et al., 2019; Wang et al., 2016). The source of protein in animals to some extent and is one of the most important variables
the diet also has a massive effect on the intestinal morphology as well as influencing customer purchases (Cheng et al., 2014; Gatlin et al., 2007).
the digestive and absorption capacity of fish. Previous research has Fillet quality is an essential indication for assessing the quality of fish
shown that high levels of plant protein sources in feed have a detri­ products, and texture parameters such as hardness, springiness, chewi­
mental influence on fish gut health (Pham et al., 2020; Wang et al., ness, cohesiveness, and resilience are commonly employed to assess fish
2020; Couto et al., 2014; Hossain et al., 2018; Zhu et al., 2021). Ma et al. flesh quality (Yang et al., 2019; Ceppa et al., 2018; Hafezparast-Moadab
(2019) and Zhu et al. (2021) believed that the detrimental effects of et al., 2018; Yu et al., 2020). Fish muscle composition and fillet quality
plant protein on the gut are primarily attributable to anti-nutritional are heavily influenced by the protein in their diet (Yu et al., 2020; Song
factors. When compared to plant protein sources, PBM is regarded as a et al., 2014). Higher amounts of plant proteins in the diet enhanced
low-cost, high-quality protein that is free of anti-nutrients (Dawood muscle hardness, gumminess, and chewiness in grass carp, according to
et al., 2020a; Fontinha et al., 2021). In the present study, MT, VH, and Hu et al. (2019). Similarly, after replacing fishmeal with greater quan­
VW in the midgut of common carp did not diminish remarkably with the tities of plant protein in the diet, Liu et al. (2014) observed a substantial
addition of CGM from 0% to 100%, and morphologic parameters of the increase in muscle hardness, gumminess, and chewiness of turbot. The
intestine in the CGM 15% group were the highest indicating that the inclusion of moderate amounts of animal protein in the diet had been
suitable addition of CGM to the feed can improve the intestinal structure proven in some trials to improve the fillet quality of red porgy (Pagrus
and absorption capacity, which also corresponded to the growth per­ pagrus) (García-Romero et al., 2014), Atlantic salmon (Salmo salar L.)
formance of common carp. Similarly, Dawood et al. (2020a) revealed (Morkore et al., 2020), and Pacú (Piaractus mesopotamicus) (Pavón et al.,
that supplementing the diet with 15% and 20% fermented PBM 2018). The inclusion of CGM into the diet can enhance fillet quality by
considerably enhanced the morphologic of common carp intestinal vil­ improving hardness, springiness, cohesiveness, and chewiness, accord­
lus. As a consequence, these results implied that the addition of 15% ing to our results.
CGM to the diets can improve the intestinal structure and enhances
digestive nutrient absorption. Furthermore, in the findings of this study, 5. Conclusions
increasing the amount of CGM in the diet improved the intestinesomatic
index, suggesting that CGM can aid in the growth of the carp intestinal In summary, this study indicated that the inclusion of CGM in diet
tract and therefore improve nutrient absorption. can induce positively affect growth performance, plasma biochemical
parameters, digestive ability, and fillet quality of the common carp.
4.5. Muscle proximate analysis Growth performance, plasma biochemical parameters, digestive ability,
and fillet quality were significantly improved in common carp fed the
The muscle nutrient composition of aquatic species is affected by the diet supplemented with 15% CGM.
living environment, the kind and composition of feed, and the culture
cycle, and is not only related to the growth, age, and tissue structure of CRediT authorship contribution statement
the fish, but also the fillet quality of the fish (Fauconneau et al., 1995;
Pavasovic et al., 2007; Cai et al., 2018; Kłobukowski et al., 2018). Pre­ Zuxiang Peng: Conceptualization, Investigation, Formal analysis,
vious researches on the effect of PBM on the whole body and muscle Data curation, Writing – original draft. Lin Yan: Conceptualization,
composition of aquatic species have primarily focused on feed protein Investigation, Formal analysis, Data curation. Libo Wei: Conceptuali­
replacement. According to some research, substituting fishmeal in the zation, Investigation, Project administration. Xin Gao: Conceptualiza­
diet with varying levels of PBM had no substantial influence on the tion, Methodology, Data curation. Lidong Shi: Investigation, Project
whole body and muscle composition of tilapia (AMM, 2015), tiger administration. Tongjun Ren: Investigation, Project administration.
grouper (Epinephelus fuscoguttatus) (Gunben et al., 2014), blunt snout Wei Wang: Investigation, Project administration. Yuzhe Han:
bream (Megalobrama amblycephala) (Cai et al., 2018), black sea bass Conceptualization, Writing – review & editing.
(Dawson et al., 2018), and juvenile tench (González-Rodríguez et al.,
2016). Dawson et al. (2018) concluded that PBM did not interfere with
fish absorption and fish absorbed protein from both poultry by-product Declaration of Competing Interest
meal and fish meal equally well. Fauconneau et al. (1995) considered
that a reasonable increase in crude protein and crude lipid contents in The authors declare that they have no known competing financial
fish contributes to the appearance and taste of flesh. In this study, with interests or personal relationships that could have appeared to influence
increasing doses of the CGM, the crude protein and crude lipid content of the work reported in this paper.
each treatment group rose, reaching a maximum in the CGM 15% group.
In the four groups (CGM 0, CGM 5%, CGM 10%, and CGM 15%), the Acknowledgments
intestinal digestion and absorption capacity of common carp gradually
increased as the amount of CGM added to the diet increased, and the This work was supported by Project for Dalian Youth Star of Science
CGM was better absorbed and utilized. This also promoted the deposi­ and Technology, China (grant no. 2019RQ137) and Blue Talents Project
tion of protein and fat in the muscles of the fish. It is worth noting that of Dalian Ocean University, China.

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Z. Peng et al. Aquaculture Reports 24 (2022) 101183

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