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. 2021 Feb 20;11(3):133. doi: 10.1007/s13205-021-02684-0

Modulation of the growth performance and innate immunity of loaches (Paramisgurnus dabryanus) upon dietary mannan oligosaccharides

Bing Xu 1,2,3,4, Shengjun Wu 1,2,3,4,✉, Qi Han 1,2,3,4
PMCID: PMC7897336  PMID: 33680698

Abstract

Different levels of mannan oligosaccharides (MOs) (100, 300 and 500 mg kg−1) were incorporated into a basal diet to formulate three diets, which were used to test the growth performance and innate immunity of loaches. The basal diet without any MOs served as the control. Loaches fed with MO-containing diets for 70 days showed a higher specific growth rate, condition factor, survival rate, intestine weight index, intestine length index, intestine Lactobacillus population, intestine Bifidobacterium population, phenoloxidase activity, superoxide dismutase activity, glutathione peroxidase activity, acid phosphatase activity, alkaline phosphatase activity, lysozyme level, complement 3 and resistance to Aeromonas hydrophila than the loaches in the control group. The feed conversion ratio, intestine Escherichia coli population, malondialdehyde level, aspartate aminotransferase level and alanine aminotransferase level showed an opposite trend. The optimal dose of dietary MOs required for the maximum growth of loaches was 300 mg kg−1. Results indicated that dietary MOs promoted the growth performance and innate immunity of loaches and could be used as a dietary supplement for loaches.

Keywords: Loach, Growth performance, Innate immunity

Introduction

Mannan oligosaccharides (MOs) are a new class of antigenic active substances extracted from the cell wall of yeast cultures, and they are widely present in konjac flour, guar gum, sessin gum and various microbial cell walls (Dimitroglou et al. 2010). MOs derived from different sources have various structures. Konjac MOs are made up of glucose and mannose residues with a molecular ratio of 1:1.5 connected by β-1,4 glycoside bonds, and their side chain is connected by β-1,3 glycoside bonds. Konjac MOs primarily consist of five to eight sugar units and do not break down in animals. MOs derived from microbial cell walls are mainly connected by α-1,6 glycoside bonds to form the main chain and have highly branched pyranose residues; their side chain is connected by α-1,2 and α-1,3 glycoside bonds. The polymerisation degree of MOs derived from microbial cell walls is relatively low (two to four sugars), and these MOs are easy to hydrolyse. At present, the MOs used for feed are derived from the enzymatic hydrolysates of konjac flour and yeast cell wall extract (Meng et al. 2019).

MOs have many biological activities; they promote nutrient absorption (Fritts and Waldroup 2003; Savage et al. 1997; Torrecillas and Makol 2011; White et al. 2002), optimise the intestinal microflora, eliminate pathogenic microorganisms (Freter 1996; Fuller et al. 1981; Jankowski et al. 2005; Mathew et al. 1997; Ofek et al. 1997) and improve the non-specific immune function in animal body (Fernandez et al. 2002; Helland et al. 2008; Newman et al. 1993; Sandi and Mühlbach 2001). In recent years, MOs have been used to improve the growth performance of gilthead sea bream (Sparus aurata) (Dimitroglou et al. 2010), juvenile abalone (Haliotis discus hannai Ino) (Meng et al. 2019), turkeys (Fritts and Waldroup 2003), weanling pigs (Mathew et al. 1997; White et al. 2002), Holstein calves (Newman et al. 1993), Atlantic salmon (Salmo salar) (Helland et al. 2008; Refstie et al. 1998), sea cucumber (Apostichopus japonicas) (Gu et al. 2011), juvenile Pacific white shrimp (Litopenaeus vannamei) (Zhang et al. 2012), fattening pigs (Giannenas et al. 2016), juvenile narrow clawed crayfish (Astacus leptodactylus) (Eschscholtz, 1823) (Safari et al. 2014), and Caspian trout (Salmo trutta caspius) (Kessler, 1877) (Jami et al. 2019). However, the effects of MOs on the growth performance and innate immunity of loaches (Paramisgurnus dabryanus) remain unclear. This study aims to explore whether the administration of dietary MOs to loaches could improve the growth performance, innate immunity and resistance against Aeromonas hydrophila of loaches.

Materials and methods

Materials

The MO product (Bio-Mos) used in this study was purchased from Alltech Inc., USA. This product is derived from the cell wall of Saccharomyces cerevisiae and contains 30% protein, 13% crude fibre and 1.4% crude fat. The microelisa stripplate provided in this kit had been pre-coated with an antibody specific to the target enzyme. All other chemicals used in this study were of reagent grade.

Diet preparation

MOs were added to the basal diet at three levels (100, 300 and 500 mg kg−1 dry diets). The ingredients of the basal diet for loaches are presented in Table 1. All feed ingredients were fully mixed with an appropriate amount of tap water, coldly extruded using an extruder (Polylab, Thermo Fisher Scientific Company, USA), cut into pellets, air dried at 45 °C and stored at − 18 °C until use.

Table 1.

Composition of basal diet for loaches

Ingredient Content (g kg−1)
Fish meal 210
Soybean meal 360
Wheat flour 100
wheat bran 70
Rapeseed meal 40
Peanut oil 20
Corn flour 170
Ca(H2PO4)2 15
Sodium methylcellulose 10
NaCl 3
Vitamin mixturea 1.2
Mineralb 0.8
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aVitamin mixture provided per kg of diet: VA 12,500,000 IU; VD 2,000,000 IU; VE 7000 IU; VK 2000 mg; VB1 800 mg; VB2 2,500 mg; VB6800 mg; VB1210 mg; niacin 3000 mg; pantothenic acid 10, 000 mg; folic acid 300 mg; biotin 20 g; VC 20,000 mg

bMineral provided per kg of diet: Mn 19 mg; Mg 230 mg; Co 0.1 mg; I 0.25 mg; Fe 140 mg; Cu 2.5 mg; Zn 65 mg; Se 0.2 mg

Loach culture

Loaches with an average body weight of 3.16 ± 0.02 g were purchased from an aquaculture farm in Haizhou, China. Prior to the feeding trial, the loaches were subjected to acclimation for 2 weeks in a semi-intensive culture pond and fed with a basal diet twice a day (08:00 and 18:00).

The aquaculture equipment were 100 L PVC tanks containing aerated dechlorinated freshwater. For the feeding trial, 720 loaches were randomly assigned to 4 groups, i.e. 1 control group (received diet without MO addition) and 3 MO-containing groups (received diets containing 100, 300 and 500 mg kg−1 of MOs). The loaches were randomly assigned to 12 tanks. Three tanks were assigned to each group, and 60 loaches were cultured in each tank.

The feeding ration was initially set to 5–7% of the body weight twice daily at 08:00 and 18:00 and adjusted thereafter in accordance with the feeding response of the loaches in each tank. The following culture conditions were maintained: water temperature, 25 °C ± 1 °C; dissolved oxygen, 6.0–6.8 mg L−1; pH, 7.1 ± 0.2; total ammonia nitrogen, below 0.06 mg L−1; and nitrite, below 0.02 mg L−1. The culture water was renewed daily with a volume of 30% fresh water.

Growth performance

After the 70-day breeding test, six loaches in each tank were randomly selected. They were bulk-weighed after being starved for 24 h, and their body length was measured to calculate the specific growth rate (SGR), feed conversion ratio (FCR), condition factor (CF) and survival rate using the following equations:

FCR (%) = 100 × total dry feed consumption/net weight gain;

SGR (% day−1) = 100 × [Ln (final mean body weight) − Ln (initial mean body weight)]/time (days);

CF (%) = final body weight/body long;

Survival rate (%) = 100 × (final number of loaches/initial number of loaches).

Intestine weight index and intestine length index

After the 70-day breeding test, six loaches in each tank were randomly selected, sacrificed by using MS222 (Sigma-Aldrich) and bulk-weighed after starved for 24 h. The body length and bowel length of loaches were measured. The peritoneal cavity was aseptically opened using a sterile scalpel, and part of the intestine between the pyloric caeca and approximately 1 cm anterior to the anus was excised and weighed to calculate the intestine weight index (IWI) and intestine length index (ILI) by using the following equations:

IWI = 100 × intestine weight/body weight;

ILI = 100 × bowel length/body length.

Intestinal microflora

At the end of the 70-day feeding trial, six loaches were randomly selected and sacrificed by using MS222 (Sigma-Aldrich). The surface of the loaches was sterilised using 70% ethanol. The peritoneal cavity was aseptically opened with a sterile scalpel, and the part of the intestine between the pyloric caeca and approximately 1 cm anterior to the anus was excised. The intestinal wall was washed with sterile saline, and intestinal contents with mucus were stripped off using sterile forceps.

Escherichia coli was cultured in EMB medium, Lactobacillus was cultured in MRS medium and Bifidobacterium was cultured in MRS + X-gal medium. The intestinal contents of the fish were placed in a triangular flask with glass beads, weighed and added with sterile normal saline at a ratio of 1:10. The mixture was shaken at 250 r/min for 10 min and diluted with a gradient of 10 times to select the appropriate dilution degree. E. coli, Lactobacillus and Bifidobacterium were inoculated with sterilised saline and diluted to 10−1, 10−2, 10−3, 10−4, 10−5 and 10−6. Diluents with a volume of 0.02 mL were obtained from high to low dilution using a micro-sampler and added to each selected medium. Three dilutions (10−3, 10−4 and 10−5 for E. coli; 10−4, 10−5 and 10−6 for Lactobacillus; and 10−4, 10−5 and 10−6 for Bifidobacterium) were applied to each sample, and three repetitions were made for each dilution. E. coli was aerobically cultured for 24 h, and Lactobacillus and Bifidobacterium were anaerobically cultured for 72 h. The E. coli, Lactobacillus and Bifidobacterium counts were expressed as log10 CFU/g intestinal contents.

Blood biochemical assays

Six fishes were randomly selected from each tank after the 70-day breeding test, and blood was collected from their tail vein. Blood samples were centrifuged at 3,000×g for 10 min to obtain serum, which was collected and stored in a refrigerator at − 45 °C for biochemical parameter analysis.

The biochemical parameters, namely, the activities of superoxide dismutase (SOD), phenoloxidase (PO), glutathione peroxidase (GPx), aspartate aminotransferase (AST), alanine aminotransferase (ALT), acid phosphatase (ACP), alkaline phosphatase (AKP) and lysozyme (LYZ) and the level of complement 3 (C3), were analysed using ELISA kits following the methods described by Gao et al. (2017). A unit of enzyme activity was defined as the amount of enzyme that decreased the absorbance by 0.001 min−1. Malondialdehyde (MDA) was assayed using kits (Solarbio, Beijing, China) in accordance with the manufacturer’s instructions.

Resistance of loaches to A. hydrophila

After the 70-day breeding test, 30 loaches were selected from each of the 4 groups, raised in tanks, acclimated for 5 days and intraperitoneally injected with 0.2 mL of 3.0 × 109 CFU/mL A. hydrophila. Meanwhile, the loaches in the control group were intraperitoneally injected with an equal volume of saline. A challenge test was performed for 15 days. The feeding conditions were in accordance with those of the aforementioned feeding trials. During the challenge experiment, the behaviour and feeding of the loaches were observed, and the accumulative mortality was recorded.

Statistical analysis

All tests were performed in triplicate, and the data were presented as means ± standard deviation. The data were processed and statistically analysed using SPSS 13.0 software. If significant differences existed between groups, Duncan’s multiple comparison was performed, and P < 0.05 indicated a significant difference.

Results

The effects of dietary MO supplementation on the growth performance of loaches are presented in Table 2. Dietary MO supplementation increased SGR, CF and survival rate but decreased FCR (P < 0.05). However, the group supplemented with a high level of dietary MO (500 mg kg−1) exhibited decreased SGR and CF but increased FCR compared with the group supplemented with a moderate level of dietary MO (300 mg kg−1, P < 0.05).

Table 2.

Growth performance and survival rate of loaches feeding different diets after 70 days of feeding different diets

Parameters Control MOs (mg kg−1)
100 300 500
Initial weight (g) 3.17 ± 0.02a 3.16 ± 0.02a 3.15 ± 0.02a 3.16 ± 0.02a
Final weight (g) 6.62 ± 0.03a 6.82 ± 0.03b 7.35 ± 0.04c 6.84 ± 0.03b
SGR (%) 0.95 ± 0.03a 1.10 ± 0.04b 1.36 ± 0.06c 1.12 ± 0.04b
FCR (%) 1.91 ± 0.21a 1.67 ± 0.16b 1.53 ± 0.13c 1.68 ± 0.17b
CF (%) 4.27 ± 0.46a 5.11 ± 0.46b 5.96 ± 0.61c 5.12 ± 0.48b
Survival rate (%) 89.24 ± 1.16a 94.52 ± 1.28b 95.06 ± 1.32b 95.47 ± 1.34b
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Different superscript letters indicate significant differences between the same row (p < 0.05). Values are the mean ± SD (n = 3)

The changes in IWI, ILI and intestinal microflora of loaches after 70 days of feeding with different diets are shown in Table 3. The experimental groups showed increased IWI, ILI and intestinal Lactobacillus and Bifidobacterium populations but decreased E. coli populations compared with the control group (P < 0.05). However, a high level of dietary MO supplementation (500 mg kg−1) exhibited reduced efficiency compared with the moderate level of dietary MO supplementation (300 mg kg−1, P < 0.05).

Table 3.

Effect of dietary mannan oligosaccharides (MOs) level on intestine weight index (IWI), intestine length index (ILI) and intestinal microflora of loaches after 70 days of feeding different diets

Parameters Control MOs (mg kg−1)
100 300 500
IWI (%) 1.29 ± 0.08a 1.36 ± 0.06b 1.42 ± 0.07c 1.35 ± 0.05b
ILI (%) 41.16 ± 1.18a 44.08 ± 1.57b 48.14 ± 1.79c 44.31 ± 1.53b
Escherichia coli [(log10 CFU) g−1)] 6.31 ± 0.38a 6.02 ± 0.14b 5.63 ± 0.17c 5.97 ± 0.13b
Lactobacillu [(log10 CFU) g−1)] 6.85 ± 0.11a 7.32 ± 0.16b 7.71 ± 0.14c 7.27 ± 0.15b
Bifidobacterium [(log10 CFU) g−1)] 7.91 ± 0.13a 8.24 ± 0.14b 8.65 ± 0.12c 8.29 ± 0.16b
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Different superscript letters indicate significant differences between the same row (p < 0.05). Values are the mean ± SD (n = 3)

The changes in the activities of PO, SOD and GPx and MDA levels in the loaches are shown in Table 4. Dietary MO supplementation increased the activities of PO, SOD and GPx but decreased MDA levels compared with the control group (P < 0.05). However, a high level of dietary MO supplementation (500 mg kg−1) did not further increase the efficiency compared with a moderate level of dietary MO supplement (300 mg kg−1, P < 0.05).

Table 4.

Phenoloxidase (PO) activity, superoxide dismutase (SOD) activity, glutathione peroxidase (GPx) activity and malondialdehvde (MDA) level of loaches after 70 days of feeding different diets

Parameters Control MOs (mg kg−1)
100 300 500
PO activity (O.D. 490 nm) 0.41 ± 0.04a 0.63 ± 0.07b 0.86 ± 0.11c 0.88 ± 0.05c
SOD activity (U g protein−1) 31.71 ± 4.03a 35.37 ± 5.27b 39.91 ± 6.18c 40.12 ± 4.85c
GPx (U g protein−1) 94.17 ± 17.63a 105.55 ± 0.06b 116.67 ± 0.09c 117.08 ± 0.11c
MDA (ng/ml) 159.81 ± 15.14a 142.74 ± 10.75b 127.05 ± 8.7c 125.51 ± 8.56c
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Different superscript letters indicate significant differences between the same row (p < 0.05). Values are the mean ± SD (n = 3)

Table 5 presents the levels of serum immune molecules in the loaches fed with MO-containing diets and the basal diet for 70 days. Dietary MO supplementation increased the ACP, AKP and LYZ activities and C3 levels but decreased AST and ALT activities compared with the control (P < 0.05). However, the differences in efficiency between high and moderate levels of dietary MO supplementation were not significant.

Table 5.

Effects of dietary mannan oligosaccharides (MOs) on the levels of serum immune molecules in loaches after 70 days of feeding different diets

Parameters Control MOs (mg kg-1)
100 300 500
AST (U/l) 0.39 ± 0.06a 0.31 ± 0.04b 0.24 ± 0.03c 0.23 ± 0.04c
ALT (U/l) 14.64 ± 0.14a 12.26 ± 0.12b 10.85 ± 0.09c 10.51 ± 0.07c
ACP (U/ml) 113.29 ± 13.52a 164.68 ±1 0.18b 273.54 ± 13.82c 281.71 ± 17.74c
AKP (U/ml) 186.92 ± 9.26a 256.83 ± 13.63b 361.66 ± 15.94c 369.68 ± 17.72c
LYZ (μg/ml) 151.19±8.37a 217.61 ± 13.64b 349.27 ± 18.75c 352.73 ± 15.68c
C3 (g/l) 0.13±0.02a 0.21±0.03b 0.38±0.06c 0.39±0.04c
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Different superscript letters indicate significant differences between the same row (p < 0.05). Values are the mean ± SD (n = 3)

AST aspartate aminotransferase; ALT alanine aminotransferase; ACP acid phosphatase; AKP alkaline phosphatase; LYZ Lysozyme; C3 complement 3

The effects of dietary MO supplementation on the resistance of loaches to A. hydrophila are presented in Table 6. Dietary MO supplementation decreased accumulative mortalities compared with the control group (P < 0.05). However, the differences in accumulative mortalities between high and moderate levels of dietary MO supplementation were not significant.

Table 6.

Accumulative mortality (%) of loaches fed with mannan oligosaccharides (MOs) diets, after being challenged by Aeromonas hydrophila

Parameters Control MOs (g kg−1)
100 300 500
Accumulative mortality (%, 5 day) 5.83 ± 0.26a 0 0 0
Accumulative mortality (%, 10 day) 31.48 ± 1.83a 18.61 ± 0.86b 14.27 ± 0.79c 13.91 ± 0.61c
Accumulative mortality (%, 15 day) 51.74 ± 2.72a 30.67 ± 1.92b 16.39 ± 1.17c 16.08 ± 1.12c
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Different superscript letters indicate significant differences between the same row (p < 0.05). Values are the mean ± SD (n = 3)

Discussion

Although native compounds, such as β-1,3-glucan (Zhu and Wu, 2018), vitamin C (Zhao et al. 2017), Se-chitosan (Victor et al. 2019), fulvic acid (Gao et al. 2017) and chitosan (Chen and Chen 2019), have been used to improve the growth performance of loaches, data on the effects of MOs on the growth performance and innate immunity of loaches are limited. In the present study, the SGR, FC and survival rates of the loaches fed with MO-containing diets were higher than those in the control group, whereas FCR exhibited an opposite trend. MOS can improve intestinal morphology (Merrifield et al. 2009; Torrecillas and Makol 2011), promote nutrient absorption and therefore improve the growth performance of loaches (Fritts and Waldroup 2003; Savage et al. 1997; Torrecillas and Makol 2011; White et al. 2002). However, in the present study, a high level of dietary MO supplementation (500 mg kg−1) decreased SGR and FC values but increased FCR compared with a moderate level of MOs (300 mg kg−1). The high levels of MO presumably exhibited mainly hypolipidaemic activity (Yan et al. 2019).

The intestine is the main site for digestion and absorption in loaches, and the growth status is closely related to the functional status of the intestine. IWI and ILI reflect the health status of the intestine. Dietary MO supplementation increased the IWI and ILI of loaches; this result can be ascribed to the ability of MOs to improve intestinal morphology (Merrifield et al. 2009; Torrecillas and Makol 2011). Animal intestinal flora is closely related to host health, and an intact and healthy intestinal mucosal structure is related to intestinal micro-ecological balance. When animals are in a sub-healthy or diseased status, E. coli multiply in large numbers, gain an absolute advantage, disrupt the balance of the digestive tract flora, affect the normal environment of the digestive tract and reduce the disease resistance of animals. In this study, the group given with dietary MO supplementation showed increased intestinal Lactobacillus and Bifidobacterium populations and decreased E. coli populations compared with the control group. This result indicates that MOs can optimise the intestinal flora of loaches, maintain the ecological balance of digestive tract microorganisms and promote the normal function of the digestive tract. Similarly, Torrecillas and Makol (2011) reported that MOs can significantly reduce the number of E. coli and A. hydrophila in the hindgut and increase the number of Bifidobacterium and Lactobacillus.

Innate immune function plays an important role in the defence of fish and has a considerable effect on fish growth and disease resistance. A system with antioxidant capacity can scavenge excess free radicals and protect itself from oxidative damage. PO, SOD and CAT are the most important parameters for evaluating antioxidant capacities in animals (Rahman et al. 2006). MDA is a highly toxic metabolite derived from lipid peroxides and causes body damage (Munoz and Cedenq 2000). The current results indicated that the serum PO, SOD and CAT activities of loaches fed with MO-containing diets increased, whereas the serum MDA level showed an opposite trend. Hence, dietary MO supplementation improved the antioxidant capacity of loaches. AST and ALT are important indicators of liver health status. The permeability of the hepatocyte membrane increases when the liver is damaged; afterwards, large quantities of AST and ALT transfer to the blood, thus decreasing the functions of AST and ALT in the liver (Yang et al. 2014). The current results indicated that dietary MO supplementation decreased the activities of AST and ALT in the serum of loaches; this result can be attributed to the antioxidant and immunomodulatory activities of MOs (Meng et al. 2019). ACP and AKP are essential metabolic regulatory enzymes in organisms and play important roles in the transfer reaction of phosphoric groups and metabolism of phosphorus. They also play a vital role in the nutrient utilisation of aquatic animals and improve their disease resistance (Zhang et al. 2011). The current results indicated that dietary MO supplementation improved the nutrient utilisation of loaches, increased protein biosynthesis and promoted loach growth. The antibacterial activity of LYZ is closely related to the innate immunity and health status of fish (Holland and Lambris 2002). In the current study, the LYZ activities in the serum of loaches increased compared with that of the control group. The complements in fish can lyse and opsonise foreign cells (Holland and Lambris 2002), and C3 plays an important role in the activation reaction of the complement system (Kuroda et al. 2000). The serum C3 levels in the current study increased significantly when the MO doses increased to up to 300 mg kg−1, but higher MO doses did not further increase the serum C3 levels. The results indicated that dietary MO supplementation increased the innate immunity of loaches.

With regard to the challenge test against A. hydrophila, the loaches that received MO-containing diets exhibited less susceptibility to A. hydrophila than those in the control group. This phenomenon could be ascribed to the ability of MOs to eliminate pathogenic microorganisms (Freter 1996; Fuller et al. 1981; Jankowski et al. 2005; Mathew et al. 1997; Ofek et al. 1997) and improve the non-specific immune function in the animal body (Fernandez et al. 2002; Helland et al. 2008; Newman et al. 1993; Sandi and Mühlbach 2001).

In conclusion, dietary MO supplementation increased the growth performance and innate immunity of loaches. However, a high level of MOs (> 300 mg kg−1) did not further improve the efficiency. We found that 300 mg kg−1 was the appropriate level of MOs for dietary supplementation. Overall, the results indicated that MOs can be used as a dietary supplement for improving the growth performance and innate immunity of loaches.

Acknowledgements

This research was supported by A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Compliance with ethical standards

Conflict of interest

The authors have declared that no competing interests exist.

Ethics statement

This study was approved by the ethics committee of Jiangsu Ocean University, China. All procedures were conducted in compliance with relevant laws and institutional guidelines.

References

  1. Chen J, Chen L. Effects of chitosan-supplemented diets on the growth performance, nonspecific immunity and health of loach fish (Misgurnusanguillicadatus) Carbohydr Polym. 2019;225:115227. doi: 10.1016/j.carbpol.2019.115227. [DOI] [PubMed] [Google Scholar]
  2. Dimitroglou A, Merrifield DL, Spring P, et al. Effects of mannan oligosaccharide (MOS) supplementation on growth performance, feed utilisation, intestinal histology and gut microbiota of gilthead sea bream (Sparus aurata) Aquaculture. 2010;300:82–188. doi: 10.1016/j.aquaculture.2010.01.015. [DOI] [Google Scholar]
  3. Fritts CA, Waldroup PW. Evaluation of Bio-Mos Mannan Oligosaccharide as repleacement for growth promoting antibiotics in diets for Tukeys. Int J Poult Sci. 2003;2:19–22. [Google Scholar]
  4. Fernandez F, Hinton M, Vaugils GB. Dietary mannanoligosacclla rides and their effect on chicken caecal microflora in relation to Salmonella Entcritidis colonization. Avian Pathol. 2002;31:49–58. doi: 10.1080/03079450120106000. [DOI] [PubMed] [Google Scholar]
  5. Freter R (1996) Studies of the mechanism of action of intestinal antibudy in experimental cholera.Tex Rep Bio-Med 27:299
  6. Fuller R, Houghton SB, Brooker BE. Attachment of streptococcus faecium to the duodenal epithelium of the chicken and its importance in colonization of the small intestine. Appl Environ Microbiol. 1981;41:1433–1441. doi: 10.1128/AEM.41.6.1433-1441.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gao Y, He J, He ZL, et al. Effects of fulvic acid on growth performance and intestinal health of juvenile loach Paramisgurnus dabryanus (Sauvage) Fish Shellfish Immunol. 2017;62:47–56. doi: 10.1016/j.fsi.2017.01.008. [DOI] [PubMed] [Google Scholar]
  8. Giannenas I, Doukas D, Karamoutsios A, et al. Effects of Enterococcus faecium, mannan oligosaccharide, benzoic acid and their mixture on growth performance, intestinal microbiota, intestinal morphology and blood lymphocyte subpopulations of fattening pigs. Anim Feed Sci Technol. 2016;220:159–167. doi: 10.1016/j.anifeedsci.2016.08.003. [DOI] [Google Scholar]
  9. Gu M, Ma HM, Mai KS, et al. Effects of dietary β-glucan, mannan oligosaccharide and their combinations on growth performance, immunity and resistance against Vibrio splendidus of sea cucumber, Apostichopus japonicas. Fish Shellfish Immunol. 2011;31:303–309. doi: 10.1016/j.fsi.2011.05.018. [DOI] [PubMed] [Google Scholar]
  10. Helland BG, Stale J, Delbert M. The effects of dietary supplementation with mannan oligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar) Aquaculture. 2008;283:163–167. doi: 10.1016/j.aquaculture.2008.07.012. [DOI] [Google Scholar]
  11. Holland MC, Lambris JD. The complement system in teleosts. Fish Shellfish Immunol. 2002;12:399–420. doi: 10.1006/fsim.2001.0408. [DOI] [PubMed] [Google Scholar]
  12. Jankowski J, Zduńczyk Z, Juśkiewicz J, et al. Indices of response of young turkeys to diet containing mannan oligosaccharide or inulin. Veterinarija Ir Zootechnika. 2005;31:98–101. [Google Scholar]
  13. Jami MJ, Kenari AA, Paknejad H, et al. Effects of dietary β-glucan, mannan oligosaccharide, Lactobacillus plantarum and their combinations on growth performance, immunity and immune related gene expression of Caspian trout, Salmo trutta caspius (Kessler, 1877) Fish Shellfish Immunol. 2019;91:202–208. doi: 10.1016/j.fsi.2019.05.024. [DOI] [PubMed] [Google Scholar]
  14. Kuroda N, Naruse K, Shima A, et al. Molecular cloning and linkage analysis of complement C3 and C4 genes of the Japanese medaka fish. Immunogenetics. 2000;51:117–128. doi: 10.1007/s002510050020. [DOI] [PubMed] [Google Scholar]
  15. Meng XX, Yang XY, Lin G, et al. Mannan oligosaccharide increases the growth performance, immunity and resistance capability against Vibro Parahemolyticus in juvenile abalone Haliotis discus hannaiIno. Fish Shellfish Immunol. 2019;94:654–660. doi: 10.1016/j.fsi.2019.09.058. [DOI] [PubMed] [Google Scholar]
  16. Merrifield DL, Moate R, Davies SJ, et al. Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhy nchus mykiss. J Anim Sci. 2009;87:3226–3234. doi: 10.2527/jas.2008-1428. [DOI] [PubMed] [Google Scholar]
  17. Munoz M, Cedenq R. Measurement of reactive oxygen intermediate production in haemocytes of the penaeid shrimp, Penaeusvannamei. Aquaculture. 2000;191:89–107. doi: 10.1016/S0044-8486(00)00420-8. [DOI] [Google Scholar]
  18. Mathew AG, Robbins CM, Chattin SE, et al. Influence of galactosy lactose on energy and protein digestibility, enteric microflora and performance of weanling pigs. J Anim Sci. 1997;75:1009–1016. doi: 10.2527/1997.7541009x. [DOI] [PubMed] [Google Scholar]
  19. Newman KE, Jacquea K, Buede R. Effect of mannan oligosaccharide supplementation on performance and fecal bacteria of Holstein calves. Anim Sci. 1993;7:271. [Google Scholar]
  20. Ofek I, Mirelman D, Sharon N. Adherence of Escherichiacoli to human mucosal cells mediated by mannose receptors. Nature (London) 1997;265:623–625. doi: 10.1038/265623a0. [DOI] [PubMed] [Google Scholar]
  21. Rahman MM, Escobedo-Bonilla CM, Corteel M, et al. Effect of high water temperature (33 °C) on the clinical and virological outcome of experimental infections with white spot syndrome virus (WSSV) in specific pathogenfree (SPF) Litopenaeus vannamei. Aquaculture. 2006;261:842–849. doi: 10.1016/j.aquaculture.2006.09.007. [DOI] [Google Scholar]
  22. Refstie S, Storebakken T, Roem AJ. Feed consumption and convers in Atlantic salmon (Salmo salar) fed diets with fish meal extracted soybean meal or soybean meal with reduced content of oligosaccharide trypsin inhibitors lectins and soya antigens. Aquaculture. 1998;162:301–312. doi: 10.1016/S0044-8486(98)00222-1. [DOI] [Google Scholar]
  23. Safari O, Shahsavani D, Paolucci M, et al. Single or combined effects of fructo- and mannan oligosaccharide supplements on the growth performance, nutrient digestibility, immune responses and stress resistance of juvenile narrow clawed crayfish, Astacus leptodactylus leptodactylus Eschscholtz, 1823. Aquaculture. 2014;17:192–203. doi: 10.1016/j.aquaculture.2014.05.012. [DOI] [Google Scholar]
  24. Sandi D, Mühlbach PRF. Performance of Holstein bull calves weaned at 28 or 56 days of age with or without additive based on mannan oligosaccharides. Cienc Rural. 2001;31:487–490. doi: 10.1590/S0103-84782001000300021. [DOI] [Google Scholar]
  25. Savage TF, Zakrzewska EI, Andreasen JR. The effects of feeding mannan oligosaccharide supplemented diets to poults on performance and morphology of the small intestine. Poul Sci. 1997;76:139. [Google Scholar]
  26. Torrecillas S, Makol A. Reduced gut bacterial translocation in European sea bass (Dicen trarchus labrax) fed mannan oligosaccharides (MOS) Fish Shellfish Immunol. 2011;30:674–681. doi: 10.1016/j.fsi.2010.12.020. [DOI] [PubMed] [Google Scholar]
  27. Victor H, Zhao B, Mu Y, et al. Effects of Se-chitosan on the growth performance and intestinal health of the loach Paramisgurnus dabryanus (Sauvage) Aquaculture. 2019;498:263–270. doi: 10.1016/j.aquaculture.2018.08.067. [DOI] [Google Scholar]
  28. White LA, Newman MC, Cromwell GL, et al. Brewers dried yeast as a source of mannan oligosaccharides for weanling pigs. J Anim Sci. 2002;80:2619–2628. doi: 10.2527/2002.80102619x. [DOI] [PubMed] [Google Scholar]
  29. Yan SK, Shi RJ, Li L, et al. Mannan Oligosaccharide Suppresses Lipid Accumulation and Appetite in Western-Diet-Induced Obese Mice Via Reshaping Gut Microbiome and Enhancing Short-Chain Fatty Acids Production. MolNutr Food Res. 2019;63:e1900521. doi: 10.1002/mnfr.201900521. [DOI] [PubMed] [Google Scholar]
  30. Yang WW, Liu WB, Shen MF, et al. Effects of Selenium on Antioxidant Enzymes and Transaminases of Liver in Cadmium Chronic Toxic Tilapia nilotica. Chinese Vet Sci. 2014;29:40–44. [Google Scholar]
  31. Zhu M, Wu SJ. The growth performance and nonspecific immunity of loach Paramisgurnus dabryanus as affected by dietary β-1,3-glucan. Fish & Shellfish Immunology. Fish Shellfish Immunol. 2018;83:368–372. doi: 10.1016/j.fsi.2018.09.049. [DOI] [PubMed] [Google Scholar]
  32. Zhao Y, Zhao J, Zhang Y, et al. Effects of different dietary vitamin C supplementations on growth performance, mucus immune responses and antioxidant status of loach (Misgurnus anguillicaudatus Cantor) juveniles. Aquac Res. 2017;48:4112–4123. doi: 10.1111/are.13231. [DOI] [Google Scholar]
  33. Zhang J, Liu YJ, Tian LX, et al. Effects of dietary mannan oligosaccharide on growth performance, gut morphology and stress tolerance of juvenile Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol. 2012;33:1027–1032. doi: 10.1016/j.fsi.2012.05.001. [DOI] [PubMed] [Google Scholar]
  34. Zhang HJ, Li ZJ, Zhang JS, et al. Changes in non-specific immune parameters and water quality in Pacific white leg shrimp Litopenaeus vannamei culture ponds. J Dalian Ocean Univ. 2011;26:356–361. [Google Scholar]

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