Effects of Dietary Fishmeal Replacement with Soybean Meal on Growth Performance, Digestion, Hepatic Metabolism, Antioxidant Capacity, and Innate Immunity of Juvenile Large Yellow Croaker (<i>Larimichthys crocea</i>)

Wang, Yuntao; Wang, Zhen; Zhang, Zhou; Tang, Yuhang; He, Yuliang; Mai, Kangsen; Ai, Qinghui

doi:https://doi.org/10.1155/2023/8842781

Aquaculture Research

On this page

Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 8842781 | https://doi.org/10.1155/2023/8842781

Effects of Dietary Fishmeal Replacement with Soybean Meal on Growth Performance, Digestion, Hepatic Metabolism, Antioxidant Capacity, and Innate Immunity of Juvenile Large Yellow Croaker (Larimichthys crocea)

Yuntao Wang,¹Zhen Wang,¹Zhou Zhang,¹Yuhang Tang,¹Yuliang He,¹Kangsen Mai,^1,2and Qinghui Ai^1,2

Academic Editor: Zhitao Qi

Received06 Feb 2023

Revised06 Apr 2023

Accepted04 Nov 2023

Published28 Nov 2023

Abstract

A 70-day feeding trial was conducted to determine the effects of the replacement of fishmeal (FM) by soybean meal (SM) in diets on growth performance, digestion, hepatic metabolism, antioxidant capacity, and innate immunity of juvenile large yellow croaker (Larimichthys crocea). Four iso-lipidic and iso-nitrogenous diets replacing 0, 15, 30, and 45 FM protein by SM protein were formulated, named FM, SM15, SM30, and SM45, respectively. Results indicated that the specific growth rate (FM = 1.55, SM15 = 1.50, SM30 = 1.48, and SM45 = 1.34%) of fish showed a significant linear trend (). With increasing dietary SM, the activity of trypsin (262.02, 179.34, 144.41, and 123.92 U/mg·prot) significantly decreased (linear trend, ). The content of high-density lipoprotein cholesterol showed a significant linear trend and quadratic trend, and the maximum was observed in fish fed the diet with 45% protein from SM (). The mRNA expression of the mechanistic target of rapamycin (m-tor) and ribosomal protein S6 (rps6) showed a significant linear trend (). The content of malondialdehyde (81.82, 92.91, 79.64, and 126.45 nmol/mg·prot) showed a significant linear trend and quadratic trend; the minimum was observed in fish fed the diet with 30% protein from SM (). The activity of acid phosphatase (328.45, 300.08, 254.03, and 223.51 U/mg·prot) significantly decreased with increasing dietary SM substitution levels (linear trend, ). A significant quadratic trend was observed in the mRNA expression of interferon-γ and interleukin-1β, while the maximum was observed in fish fed the diet with 45% protein from SM (). In conclusion, this study demonstrated that the replacement of FM by SM in diets can decrease the growth performance, digestion, antioxidant capacity, and innate immunity and affect the hepatic metabolism of juvenile large yellow croaker. The minimum negative effect was obtained when 30% of FM was replaced by SM.

1. Introduction

Fishmeal (FM) is the traditional protein source of aquatic feed, which has the advantage of sufficient essential amino acids, easy availability, and high digestibility [1]. However, due to overfishing, environmental pollution, and extreme weather, FM production has declined year by year [2]. Especially with the development of aquaculture, FM resources are becoming increasingly scarce, which has led to the soaring price of FM [3]. Therefore, the search for high-quality alternative protein sources of FM has become a research hotspot [1, 3]. At present, vegetable protein is the best alternative to fish meal [4–6].

In recent years, due to the low price and large supply of plant protein sources, many researches about replacing FM with plant protein sources has been carried out [3, 7]. Among the protein sources (peanut, sweet potato, and melon seed meal), soybean meal (SM) is the most widely used in the production and application of feed. Compared with other protein sources, SM has the advantages of more affordable price, easier digestion and absorption, and better amino acid composition. It becomes the first choice of FM replacement with protein sources [4–6]. However, many factors restrict the replacement of FM by SM, such as unbalanced amino acid composition and antinutritional factors [8–10]. Therefore, the development and utilization of SM still need to be further studied. At present, there are already some studies on FM replacement with SM, fermented SM, and soybean protein concentrate, including Chinese sucker [11], grouper [7], rainbow trout [12], tilapia [13], and so on. However, as far as we know, there are no reports about dietary FM replacement with SM without additional additives in the treatment group on juvenile large yellow croaker.

As the most cultured marine fish in China, the large yellow croaker is popular with consumers because of its delicious meat, rich nutrition, and affordable price [14–16]. However, the high price of FM seriously restricted the further development of the artificial formula feed industry [17, 18]. Therefore, the purpose of this feeding trial is to assess the effect of FM replacement with SM on growth performance, digestion, hepatic metabolism, antioxidant capacity, and innate immunity of juvenile large yellow croaker, which will provide a theoretical basis for the application of FM replacement with SM in artificial formula feed.

2. Materials and Methods

2.1. Feed Ingredients

On the basis of previous experimental diets of Yi et al. [19], four iso-nitrogenous (42.03% crude protein) and iso-lipidic (12.07% crude lipid) trail diets were formulated with 0%, 15%, 30%, and 45% of FM replacement with SM, named FM, SM15, SM30, and SM45, respectively (Table 1). This feeding trial was in strict accordance with the Management Rule of Laboratory Animals (Chinese Order No. 676 of the State Council, revised March 1, 2017).

2.2. Feeding Procedure

All of the large yellow croaker were obtained from NingdeFufa Fishery Co., Ltd (Fujian, China). First, the large yellow croaker was acclimated in a big sea cage and fed with commercial feed for 14 days. Then, after 1-day starvation, 720 fish (11.78 ± 0.03 g) were randomly distributed into 12 sea cages (1 × 1 × 2 m). Four kinds of diets were randomly allocated to triplicate cages. During the feeding trial, fish were fed at 05:00 and 17:00 daily; the salinity was maintained between 25.4 and 29.8‰, the dissolved oxygen was maintained between 6.1 and 7.1 mg/L, and the water temperature was maintained between 19.4 and 22.8°C.

2.3. Sample Collection

Before the trial, the initial body length and weight of a large yellow croaker were measured by rulers and balances. After the trial, the surviving large yellow croaker in each cage was counted for the calculation of the survival rate (SR). After 24 hr of starvation to empty the intestine, the remaining large yellow croaker was anesthetized with eugenol (1 : 10,000) to sample. The final body weight (FBW) and final body length (FBL) of the large yellow croaker were measured by rulers and balances. Five juvenile large yellow croakers in each cage were collected and frozen for body composition analysis. The 1 mL syringes were used to collect the blood of the juvenile large yellow croaker. The blood was coagulated at 4°C for 4 hr, then centrifuged (4,500 rpm, 10 min) to obtain serum for subsequent analysis. Then, the remaining juvenile large yellow croakers were dissected and separated the head kidney, liver, and intestine on ice. The head kidney, liver, and intestine were put into liquid nitrogen for preservation rapidly, then stored at −80°C until use. Ten livers of juvenile large yellow croaker were soaked in 4% paraformaldehyde for 1 day for hematoxylin–eosin staining.

2.4. Analytical Methods

2.4.1. Fish Body and Diets Composition Analysis

The moisture, crude protein, and crude lipid of juvenile large yellow croaker and diets were analyzed by the standard method of AOAC (2003). All samples were laid inside an oven at 110°C for over 1 day until a constant weight for the calculation of moisture. All samples were measured by the Kjeldahl method (Kjeltec^TM 8400, FOSS) for the calculation of crude protein content and measured by Automatic Soxhlet Extractor (Soxtec 2050, FOSS) for the calculation of crude lipid content.

2.4.2. The Intestinal Digestive Enzyme Activities

The α-amylase (no. C016-1-1), lipase (no. A054-2-1), and intestinal trypsin (no. A080-2-2) activities of juvenile large yellow croaker were detected by kits purchased from Nanjing Jiancheng Bioengineering Institute Co., Ltd. The detailed operations refer to the instructions of kits.

2.4.3. The Serum Innates Immune and Antioxidant Activities

The serum catalase (CAT, no. A007-1-1), superoxide dismutase (SOD, no. A001-3-2), acid phosphatase (ACP, no. A060-2-1), alkaline phosphatase (AKP, no. A059-2-1) activities, total antioxidant capacity (T-AOC, no. A015-2-1), and malondialdehyde (MDA, no. A003-1-2) of juvenile large yellow croaker were detected by kits purchased from Nanjing Jiancheng Bioengineering Institute Co., Ltd. The detailed operations refer to the instructions of kits.

2.4.4. The Serum Lipid Profiles and Transaminases

The serum aspartate aminotransferase (AST, no. C010-2-1), alanine aminotransferase (ALT, no. C009-2-1) activities, the content of low-density lipoprotein cholesterol (LDL-C, no. A113-1-1), high-density lipoprotein cholesterol (HDL-C, no. A112-1-1), total cholesterol (TCHO, no. A111-1-1), and total triglyceride (TG, no. A110-1-1) of large yellow croaker were detected by kits purchased from Nanjing Jiancheng Bioengineering Institute Co., Ltd. The detailed operations refer to the instructions of kits.

2.4.5. Liver Morphology Analysis

According to the method of published paper by Mai et al. [22], the livers of fish were washed, dehydrated, embedded, sectioned, stained, and finally observed under a microscope.

2.5. RNA Extraction and RT-qPCR

The total RNA extraction from the liver and head kidney of a large yellow croaker was carried out according to the instructions of the TRIzol Reagent kit (Takara, Japan). The RNA integrity was detected by 1.2% denaturing agarose gel under the manufacturer’s protocol. The RNA concentration was measured by Nanodrop®2000 (Thermo Fisher Scientific, USA). The cDNA synthesis was carried out in strict accordance with the instructions of the PrimeScript-RT reagent kit (Takara, Japan). Then, the CFX96TM Real-Time System (BIO-RAD, USA) was used for RT-qPCR. In this study, the β-actin was regarded as a reference gene. Based on GenBank and a previous study by Wang et al. [23], primer sequences were designed by Megalign software (Table 2). The threshold of primer amplification efficiencies ranged between 0.95 and 1.05. The 20 μL RT-qPCR amplification system included 7 μL RNase-free water, 10 μL SYBR-Premix Ex TaqII (Takara, Japan), 0.5 μL upstream primers, 0.5 μL downstream primers and 2 μL cDNA. The program of qPCR was as follows: 95°C for 2 min, followed by 39 cycles of 95°C for 10 s, 59°C for 10 s, and 72°C for 20 s. Melting curve analysis was carried out to confirm that a single PCR product was present. The mRNA expression levels were calculated with the 2^−ΔΔCT methods. [24].

2.6. Calculations and Statistical Analysis

SR (%) = (N1)/(N2) × 100; Specific growth rate (SGR, %/day) = 100 (Ln (W1) – Ln (W2)) × 100/D; Viscerosomatic index (VSI, %) = 100 × (final viscera weight)/(W1); Hepatosomatic index (HSI, %) = 100 × (final liver weight)/(W1).

Where N1 is final fish number, N2 is initial fish number, W1 is final fish weight, W2 is initial fish weight, and D is the experimental duration.

Results in this study were expressed as means ± S.E.M. All data were analyzed by SPSS Statistics 19.0 with orthogonal polynomial contrasts to assess if the pattern (or trend) was linear or quadratic. The significant level was set as .

3. Results

3.1. Survival, Growth Performance, and Body Composition

With increasing dietary SM, the FBW () and SGR () of large yellow croaker showed a significant linear trend and the minimum was observed in fish fed the diet with 45% protein from SM (Table 3). However, no significant linear or quadratic trend was observed in the FBL, VSI, HSI, and SR (). For the body composition of the large yellow croaker, no significant linear or quadratic trend was observed in the moisture, crude protein, and crude lipid with increasing dietary SM replacement levels () (Table 4).

3.2. Digestive Enzyme Activities

With increasing dietary SM replacement levels, the activity of trypsin in a large yellow croaker significantly decreased (linear trend, , Table 5). The activity of α-amylase in large yellow croaker showed a significant linear trend and quadratic trend, and the minimum was observed in fish fed the diet with 45% protein from SM (). At the same time, a significant linear trend was observed in the activity of lipase with the increase of FM replacement with SM, and the maximum was observed in fish fed the diet with 45% protein from SM ().

3.3. Lipid Profiles, Transaminases, and Liver Histology

With the SM substitution increasing from 0% to 45%, a significant linear trend was observed in the content of TG, and the maximum was observed in fish fed the diet with SM30 (, Table 6). The content of HDL-C in large yellow croaker showed a significant linear trend and quadratic trend, and the maximum was observed in fish fed the diet with 45% protein from SM (). However, there was no significant linear or quadratic trend in the content of TCHO and LDL-C (). For the transaminases of large yellow croaker, both the activities of ALT and AST showed a significant quadratic trend with the increase of FM replacement with SM; the maximum was observed in fish fed the diet with SM15 (). Meanwhile, the activity of AST also showed a significant linear trend (). When SM replacement level reached to 15% or 45%, the vacuolation of cells in the liver of a large yellow croaker was more serious than the control, which indicated the degree of liver injury became more serious than the control (Figure 1).

3.4. The Genes Expression of Protein Metabolism-Related

For the protein synthesis genes, the mRNA expression of m-tor and rps6 showed a significant linear trend with the increase of FM replacement with SM (, Figure 2). In regard to protein catabolic metabolism genes, no significant linear or quadratic trend was observed in the mRNA expression of eif4ebp1 among different dietary treatments ().

3.5. Antioxidant and Innate Immunity Capacity

As dietary SM replacement levels increased, the content of MDA in large yellow croaker showed a significant linear trend and quadratic trend, and the minimum was observed in fish fed the diet with SM30 (, Figure 3). However, there was no significant linear or quadratic trend in the activities of SOD, CAT, and T-AOC (, Figure 3(a)–3(c)). For the phosphatase of large yellow croaker, the activity of ACP significantly decreased with the SM substitution increasing from 0% to 45% (linear trend, , Figure 3(d)). No significant linear or quadratic trend was observed in the activity of AKP among different dietary treatments (, Figure 3(f)). For the pro-inflammatory cytokines, the mRNA expression of tnf-α and interferon-γ (ifn-γ) showed a significant linear trend with the increase of FM replacement with SM (, Figure 4). Meanwhile, a significant quadratic trend was observed in the mRNA expression of ifn-γ and interleukin-1β (il-1β), while the maximum was observed in fish fed the diet with 45% protein from SM (). However, there was no significant linear trend or quadratic trend in the mRNA expression of il-8 (). For the anti-inflammatory cytokines, no significant linear trend or quadratic trend was observed in the mRNA expression of il-10 ().

(a)

(b)

(c)

(d)

(e)

(f)

4. Discussion

Growth performance is a crucial index to measure the applicability of protein alternative feed [25]. The SR of the large yellow croaker was unaffected by the replacement of SM in this study. A similar result also can be found in the data of Chinese sucker [11]. Meanwhile, 45% protein from SM could decrease the FBW and SGR of fish, while 15% protein from SM could decrease the FBL of fish. Similarly, this result was also reported in the study of tilapia [25] and Atlantic salmon [26, 27] treated with different replacement levels of FM by SM. Overall, the replacement of FM by SM in diets could inhibit the growth performance of fish.

Digestive enzymes mainly exist in the intestine tract, affecting the digestion of fish and ultimately affecting the growth performance [28]. This study showed that 30% and 45% protein from SM could decrease the activity of trypsin in the intestine, which reflects the decrease of protein digestibility of large yellow croaker [29]. Meanwhile, 45% protein from SM could decrease the activity of α-amylase, which was consistent with the previous research on Atlantic salmon [30], catfish [31], and several aquatic animals [25]. However, the intestinal activity of lipase was increased by 45% protein from SM. This may be due to its lower activity of trypsin and α-amylase, which made the large yellow croaker fed the diet with 45% protein from SM have to obtain more energy from fat. In general, improper replacement of FM by SM could reduce the digestive enzyme activities of fish.

Based on some previous studies, the replacement of plant protein for FM will lead to changes in physiological state and blood biochemical indexes [32, 33]. The result indicated that 15% protein from SM could increase the content of serum LDL-C, 30% protein from SM could increase the content of serum TG, while 45% protein from SM could increase the content of serum HDL-C and LDL-C. These data suggested that the replacement of FM by SM in diets could increase the serum lipids level, which was not consistent with the research results of other fish, such as cyprinus carpio-haematopterus [33], Chinese sturgeon [32], and Tiger puffer [34]. This difference may be caused by the different fish species and experimental breeding environment. When the liver is damaged, AST will enter the blood and increase the activity of AST in serum [35]. The result indicated that the AST activity could be increased by 15% protein from SM, which was similar to the research result in starry flounder [36]. Furthermore, this result was also consistent with the results of liver morphology. Combined the result of liver morphology and the result of transaminases in serum, this study demonstrated that inappropriate replacement of FM by SM could lead to liver damage of fish.

Liver protein metabolism of fish could be affected by liver injury [37]. According to previous researches, the replacement of FM by SM in diets can impact the protein composition of several aquatic animals, including juvenile Japanese flounder [32] and Rhynchocypris lagowskii Dybowski [38]. For protein synthesis, 15% and 45% protein from SM could decrease the mRNA expression of m-tor and rps6, which indicated that the replacement of FM by SM might reduce the hepatic metabolic capacity of large yellow croaker.

The severe oxidative stress and severe inflammatory reaction of fish will affect the health [39]. Some studies have proved the replacement of FM by SM decreased the antioxidant and innate immunity capacity of different kinds of fish [40, 41]. The result indicated that 45% protein from SM could decrease the T-AOC of juvenile large yellow croaker, and the content of MDA of large yellow croaker could be increased by 45% protein from SM correspondingly. This result showed that a high proportion replacement of FM by SM could reduce the antioxidant capacity of fish, which was in accordance with the research of Schizothorax prenanti [42] and red seabream [43]. Innate immunity can rapidly respond to various invading pathogens and maintain the health of fish [44]. The serum ACP activity could be decreased by 45% protein from SM in the present study, which indicated a decrease in serum immune ability. Previous studies also proved severe inflammatory response could lead to nonspecific immunity reduction, ultimately leading to the reduction of SR [45]. The data showed that 15% protein from SM could increase the mRNA expression of il-1β, il-8, and tnf-α, while 45% protein from SM could increase the mRNA expression of ifn-γ and il-1β, indicating the inappropriate replacement of FM by SM might induce inflammatory response. Similar results could be found in turbot [46], Atlantic salmon [47], and zebrafish larvae [48]. Overall, the replacement of FM by SM might induce oxidative stress and inflammation, which might affect the health of large yellow croaker.

5. Conclusion

In conclusion, this study assesses the effects of the replacement of FM by SM in diets on growth performance, digestion, hepatic metabolism, antioxidant capacity, and innate immunity of juvenile large yellow croaker. Results indicated improper replacement of FM by SM could decrease the growth performance, digestive enzyme activity, antioxidant, and innate immunity capacity, resulted in morphological changes of the liver and affected hepatic metabolism of juvenile large yellow croaker. The minimum negative effect was obtained when 30% of FM was replaced by SM.

Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare that there are no conflicts of interest.

Acknowledgments

This study was supported by the China Agriculture Research System of MOF and MARA (CARS-47) and the Leading Talent of Technological Innovation of Ten-Thousands Talents Program (grant no. 2018-29).

References

W. Takeshi, “Strategies for further development of aquatic feeds,” Fisheries Science, vol. 68, no. 2, pp. 242–252, 2002.
View at: Publisher Site | Google Scholar
G. Merino, M. Barange, C. Mullon, and L. Rodwell, “Impacts of global environmental change and aquaculture expansion on marine ecosystems,” Global Environmental Change, vol. 20, no. 4, pp. 586–596, 2010.
View at: Publisher Site | Google Scholar
A. G. J. Tacon, Trends in Aquaculture Production, with Particular Reference to Low-Income Food-Deficit Countries 1984–1993, FAO Aquaculture Newsletter, 1996.
C. Burel, T. Boujard, S. J. Kaushik et al., “Potential of plant-protein sources as fish meal substitutes in diets for turbot (Psetta maxima): growth, nutrient utilisation and thyroid status,” Aquaculture, vol. 188, no. 3-4, pp. 363–382, 2000.
View at: Publisher Site | Google Scholar
Q. C. Zhou, K. S. Mai, Y. J. Liu, and B. P. Tan, “Advances in animal and plant protein sources in place of fish meal,” Journal of Fisheries of China, vol. 29, pp. 404–410, 2005.
View at: Google Scholar
J. Li, L. Zhang, K. Mai et al., “Potential of several protein sources as fish meal substitutes in diets for large yellow croaker, Pseudosciaena crocea R,” Journal of the World Aquaculture Society, vol. 41, no. s2, pp. 278–283, 2010.
View at: Publisher Site | Google Scholar
Z. Luo, Y.-J. Liu, K.-S. Mai, L.-X. Tian, D.-H. Liu, and X. Y. Tan, “Partial replacement of fish meal by soybean protein in diets for grouper Epinephelus coioides juveniles,” Journal of Fisheries of China, vol. 28, pp. 175–181, 2004.
View at: Google Scholar
C. Burrells, P. D. Williams, P. J. Southgate, and V. O. Crampton, “Growth, physiological and immunological responses of rainbow trout to different inclusion levels of dehulled lupin (Lupinus angustifolius) in the diet as fish meal replacements,” Veterinary Immunology and Immunopathology, vol. 72, pp. 277–288, 1999.
View at: Google Scholar
B.-M. Krogdahl and B. RØed, “Feeding Atlantic salmon Salmo salar L. soybean products: effects on disease resistance (furunculosis), and lysozyme and IgM levels in the intestinal mucosa,” Aquaculture Nutrition, vol. 6, no. 2, pp. 77–84, 2000.
View at: Publisher Site | Google Scholar
R. L. Chou, B. Y. Her, M. S. Su, G. Hwang, Y. H. Wu, and H. Y. Chen, “Substituting fish meal with soybean meal in diets of juvenile cobia Rachycentron canadum,” Aquaculture, vol. 229, no. 1–4, pp. 325–333, 2004.
View at: Publisher Site | Google Scholar
D.-H. Yu, S.-Y. Gong, Y.-C. Yuan, Z. Luo, Y.-C. Lin, and Q. Li, “Effect of partial replacement of fish meal with soybean meal and feeding frequency on growth, feed utilization and body composition of juvenile Chinese sucker, Myxocyprinus asiaticus (Bleeker),” Aquaculture Research, vol. 44, no. 3, pp. 388–394, 2013.
View at: Publisher Site | Google Scholar
S. A. Collins, A. R. Desai, G. S. Mansfield, J. E. Hill, A. G. Van Kessel, and M. D. Drew, “The effect of increasing inclusion rates of soybean, pea and canola meals and their protein concentrates on the growth of rainbow trout: concepts in diet formulation and experimental design for ingredient evaluation,” Aquaculture, vol. 344–349, pp. 90–99, 2012.
View at: Publisher Site | Google Scholar
D. M. S. D. El-Saidy and M. M. A. Gaber, “Complete replacement of fish meal by soybean meal with dietary L-lysine supplementation for Nile tilapia Oreochromis niloticus (L.) fingerlings,” Journal of the World Aquaculture Society, vol. 33, no. 3, pp. 297–306, 2002.
View at: Publisher Site | Google Scholar
S. Li, Ó. Monroig, T. Wang et al., “Functional characterization and differential nutritional regulation of putative Elovl5 and Elovl4 elongases in large yellow croaker (Larimichthys crocea),” Scientific Reports, vol. 7, no. 1, Article ID 2303, 2017.
View at: Publisher Site | Google Scholar
X. Li, K. Cui, W. Fang et al., “High level of dietary olive oil decreased growth, increased liver lipid deposition and induced inflammation by activating the p38 MAPK and JNK pathways in large yellow croaker (Larimichthys crocea),” Fish & Shellfish Immunology, vol. 94, pp. 157–165, 2019.
View at: Publisher Site | Google Scholar
M. Wu, Q. Li, K. Mai, and Q. Ai, “Regulation of free fatty acid receptor 4 on inflammatory gene induced by LPS in large yellow croaker (Larimichthys crocea),” Frontiers in Immunology, vol. 12, Article ID 703914, 2021.
View at: Publisher Site | Google Scholar
C. J. Thiele, M. D. Hudson, A. E. Russell, M. Saluveer, and G. Sidaoui-Haddad, “Microplastics in fish and fishmeal: an emerging environmental challenge?” Scientific Reports, vol. 11, no. 1, Article ID 2045, 2021.
View at: Publisher Site | Google Scholar
B. Huang, S. Zhang, X. Dong et al., “Effects of fishmeal replacement by black soldier fly on growth performance, digestive enzyme activity, intestine morphology, intestinal flora and immune response of pearl gentian grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂),” Fish & Shellfish Immunology, vol. 120, pp. 497–506, 2022.
View at: Publisher Site | Google Scholar
X. Yi, Z. Fan, X. Wei, J. Li, and K. Mai, “Effects of dietary lipid content on growth, body composition and pigmentation of large yellow croaker Larimichthys croceus,” Aquaculture, vol. 434, pp. 355–361, 2014.
View at: Publisher Site | Google Scholar
C. Yao, W. Huang, Y. Liu et al., “Effects of dietary silymarin (SM) supplementation on growth performance, digestive enzyme activities, antioxidant capacity and lipid metabolism gene expression in large yellow croaker (Larimichthys crocea) larvae,” Aquaculture Nutrition, vol. 26, no. 6, pp. 2225–2234, 2020.
View at: Publisher Site | Google Scholar
Y. Liu, Y. Miao, N. Xu et al., “Effects of dietary Astragalus polysaccharides (APS) on survival, growth performance, activities of digestive enzyme, antioxidant responses and intestinal development of large yellow croaker (Larimichthys crocea) larvae,” Aquaculture, vol. 517, Article ID 734752, 2020.
View at: Publisher Site | Google Scholar
K. Mai, H. Yu, H. Ma et al., “A histological study on the development of the digestive system of Pseudosciaena crocea larvae and juveniles,” Journal of Fish Biology, vol. 67, no. 4, pp. 1094–1106, 2005.
View at: Publisher Site | Google Scholar
Y. Wang, W. Xu, J. Zhang et al., “Effects of glycyrrhizin (GL) supplementation on survival, growth performance, expression of feeding-related genes, activities of digestive enzymes, antioxidant capacity, and expression of inflammatory factors in large yellow croaker (Larimichthys crocea) larvae,” Aquaculture Nutrition, vol. 2022, Article ID 5508120, 11 pages, 2022.
View at: Publisher Site | Google Scholar
K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2^−ΔΔCt method,” Methods, vol. 25, no. 4, pp. 402–408, 2001.
View at: Publisher Site | Google Scholar
Y. Liu, X. Leng, X. Li, and A. Liu, “Effects of replacing fish meal with soybean meal on growth, digestibility and immunity of tilapia (Oreochromis niloticus × O.aureus),” Journal of the Chinese Cereals and Oils Association, vol. 24, pp. 95–100, 2009.
View at: Google Scholar
J. J. Olli, Å. Krogdahl, T. S. G. A. van den Ingh, S. Bratt, and L. E. Brattås, “Nutritive value of four soybean products in diets for Atlantic salmon (Salmo salar, L.),” Acta Agriculturae Scandinavica, Section A—Animal Science, vol. 44, no. 1, pp. 50–60, 1994.
View at: Publisher Site | Google Scholar
J. J. Olli, Å. Krogdahl, and A. Våbenø, “Dehulled solvent-extracted soybean meal as a protein source in diets for Atlantic salmon, Salmo salar L.,” Aquaculture Research, vol. 26, no. 3, pp. 167–174, 1995.
View at: Publisher Site | Google Scholar
D. Castro-Ruiz, K. B. Andree, E. Blondeau-Bidet et al., “Isolation, identification, and gene expression analysis of the main digestive enzymes during ontogeny of the Neotropical catfish Pseudoplatystoma punctifer (Castelnau, 1855),” Aquaculture, vol. 543, Article ID 737031, 2021.
View at: Publisher Site | Google Scholar
M. Grabner, “An in vitro method for measuring protein digestibility of fish feed components,” Aquaculture, vol. 48, no. 2, pp. 97–110, 1985.
View at: Publisher Site | Google Scholar
A. M. Bakke-McKellep, C. M. Press, G. Baeverfjord, Å. Krogdahl, and T. Landsverk, “Changes in immune and enzyme histochemical phenotypes of cells in the intestinal mucosa of Atlantic salmon, Salmo salar L., with soybean meal-induced enteritis,” Journal of Fish Diseases, vol. 23, no. 2, pp. 115–127, 2000.
View at: Publisher Site | Google Scholar
H. Li, F. Huang, B. Hu, Y. Zhou, and L. Zhang, “Effects of replacement of fish meal with fermented soybean in the diet for channel catfish (Ictalurus punctatus) on growth performance and apparent digestibility of feed,” Freshwater Fisheries, vol. 37, pp. 41–44, 2007.
View at: Google Scholar
W. Liu, H. Wen, M. Jiang et al., “Effects of soy protein concentration on growth performance, plasma lipids and carcass composition of juvenile Chinese sturgeon (Acipenser sinensis),” Freshwater Fisheries, vol. 40, pp. 27–32, 2010.
View at: Google Scholar
H. Yin, J. Huang, X. Li, and X. Zheng, “Effect of replacing fish meal with fermented and unfermented soybean meal on growth performance, serum antioxidant capacity and digestive enzymes of juvenile Cyprinus Carpio-haematopterus,” Feed Industry, vol. 40, pp. 46–52, 2019.
View at: Google Scholar
S.-J. Lim, S.-S. Kim, G.-Y. Ko et al., “Fish meal replacement by soybean meal in diets for tiger puffer, Takifugu rubripes,” Aquaculture, vol. 313, no. 1–4, pp. 165–170, 2011.
View at: Publisher Site | Google Scholar
P. T. Giboney, “Mildly elevated liver transaminase levels in the asymptomatic patient,” American Family Physician, vol. 71, no. 6, pp. 1105–1110, 2005.
View at: Google Scholar
Z. Song, H. Li, J. Wang, P. Li, Y. Sun, and L. Zhang, “Effects of fishmeal replacement with soy protein hydrolysates on growth performance, blood biochemistry, gastrointestinal digestion and muscle composition of juvenile starry flounder (Platichthys stellatus),” Aquaculture, vol. 426–427, pp. 96–104, 2014.
View at: Publisher Site | Google Scholar
A. M. Madden and M. Y. Morgan, “Resting energy expenditure should be measured in patients with cirrhosis, not predicted,” Hepatology, vol. 30, no. 3, pp. 655–664, 1999.
View at: Publisher Site | Google Scholar
L. Wu, K. Zhou, L. Yan et al., “Effects of fermented soybean meal replacement of fishmeal on main biochemical parameters, protease activity and protein metabolism of Rhynchocypris lagowskii Dybowski,” Journal of Jilin Agricultural University, vol. 42, pp. 90–95, 2020.
View at: Google Scholar
H. Zhang, L. Yi, R. Sun et al., “Effects of dietary citric acid on growth performance, mineral status and intestinal digestive enzyme activities of large yellow croaker Larimichthys crocea (Richardson, 1846) fed high plant protein diets,” Aquaculture, vol. 453, pp. 147–153, 2016.
View at: Publisher Site | Google Scholar
J.-H. Kim, K. K. Su, and Y. B. Hur, “Toxic effects of waterborne nitrite exposure on antioxidant responses, acetylcholinesterase inhibition, and immune responses in olive flounders, Paralichthys olivaceus, reared in bio-floc and seawater,” Fish & Shellfish Immunology, vol. 97, pp. 581–586, 2020.
View at: Publisher Site | Google Scholar
A. Akbari, G. R. Mobini, S. Agah et al., “Coenzyme Q10 supplementation and oxidative stress parameters: a systematic review and meta-analysis of clinical trials,” European Journal of Clinical Pharmacology, vol. 76, no. 11, pp. 1483–1499, 2020.
View at: Publisher Site | Google Scholar
X. Xiang, X.-H. Zhou, J. Chen, D.-J. Li, W.-J. Wang, and X.-Q. Zhou, “Effect of dietary replacement of fish meal protein with soybean meal protein on the growth, body composition and hematology indices of Schizothorax prenanti,” Journal of Fisheries of China, vol. 36, no. 5, pp. 723–731, 2012.
View at: Google Scholar
S. Dossou, S. Koshio, M. Ishikawa et al., “Growth performance, blood health, antioxidant status and immune response in red sea bream (Pagrus major) fed Aspergillus oryzae fermented rapeseed meal (RM-Koji),” Fish and Shellfish Immunology, vol. 75, pp. 253–262, 2018.
View at: Publisher Site | Google Scholar
S. Bindu, S. Dandapat, R. Manikandan et al., “Prophylactic and therapeutic insights into trained immunity: a renewed concept of innate immune memory,” Human Vaccines & Immunotherapeutics, vol. 18, no. 1, Article ID 2040238, 2022.
View at: Publisher Site | Google Scholar
R. Ungaro, S. Mehandru, P. B. Allen, L. Peyrin-Biroulet, and J.-F. Colombel, “Ulcerative colitis,” The Lancet, vol. 389, no. 10080, pp. 1756–1770, 2017.
View at: Publisher Site | Google Scholar
M. Gu, N. Bai, Y. Zhang, and Å. Krogdahl, “Soybean meal induces enteritis in turbot Scophthalmus maximus at high supplementation levels,” Aquaculture, vol. 464, pp. 286–295, 2016.
View at: Publisher Site | Google Scholar
S. M. Inderjit, M. C. Elvis, C. V. Elin, K. Åshild, and M. B. Anne, “Transcriptional regulation of IL-17A and other inflammatory markers during the development of soybean meal-induced enteropathy in the distal intestine of Atlantic salmon (Salmo salar L.),” Cytokine, vol. 60, no. 1, pp. 186–196, 2012.
View at: Publisher Site | Google Scholar
M. I. Hedrera, J. A. Galdames, M. F. Jimenez-Reyes et al., “Soybean meal induces intestinal inflammation in zebrafish larvae,” PLOS ONE, vol. 8, no. 7, Article ID e69983, 2013.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2023 Yuntao Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies