Effects of Dietary Mannan Oligosaccharides on Growth, Nonspecific Immunity and Tolerance to Salinity Stress and <i>Streptococcus iniae</i> Challenge in Golden Pompano, <i>Trachinotus ovatus</i>

Do-Huu, Hoang; Nguyen, Hue Thi Nguyet; Vo, Hai Thi

doi:https://doi.org/10.1155/2023/9973909

Aquaculture Nutrition

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

Research Article | Open Access

Volume 2023 | Article ID 9973909 | https://doi.org/10.1155/2023/9973909

Effects of Dietary Mannan Oligosaccharides on Growth, Nonspecific Immunity and Tolerance to Salinity Stress and Streptococcus iniae Challenge in Golden Pompano, Trachinotus ovatus

Hoang Do-Huu,^1,2Hue Thi Nguyet Nguyen,¹and Hai Thi Vo¹

Academic Editor: Yanjiao Zhang

Received13 Sept 2023

Revised18 Oct 2023

Accepted02 Nov 2023

Published25 Nov 2023

Abstract

The effects of dietary supplementation with mannan oligosaccharide (MOS) on growth performance, haematological parameters, abundance of intestinal Vibrio spp., immune response, and tolerance to low salinity stress and Streptococcus iniae challenge were evaluated in pompano (Trachinotus ovatus). Pompano (3.24 ± 0.45 g) were fed six diets including a basal diet as control, and the basal diets supplemented with 0.1%, 0.2%, 0.4%, 0.6%, or 0.8% MOSs for 8 weeks. The results showed that pompano fed 0.1%–0.4% MOS had significantly improved specific growth rates (). Dietary MOS did not affect the survival rate of pompano (). WBC count was significantly higher in fish fed diets containing 0.1%–0.6% MOS. Dietary MOS increased lymphocytes count () and reduced monocytes and basophils counts (); however, no effects were found on neutrophils and eosinophil numbers (). Intestinal Vibrio spp. counts reduced in fish fed diets containing 0.1%–0.4% MOS (). The phagocytic ratio significantly increased in pompano fed diets containing 0.1%–0.6% MOS (), while the phagocytic index and serum lysozyme activity in fish fed 0.1%–0.4% MOS were significantly higher than the control (). There were significant positive correlations between MOS levels and fish growth on days 14, 28, 42, and 56 (). In addition, dietary MOS levels were highly correlated with blood parameters, abundance of intestinal Vibrio spp., and immune responses. Optimal dietary MOS requirements for maximal growth were estimated to be 0.440% on day 21 (R² = 0.861), 0.385% on day 28 (R² = 0.877), 0.371% on day 42 (R² = 0.891), and 0.365% on day 56 (R² = 0.750), showing decreasing tendency in MOS requirement as fish size increased. Furthermore, the optimal MOS concentration for maximal immunity based on lysozyme activity was estimated to be 0.431% (R² = 0.817) on day 56. In addition, fish fed 0.1%–0.4% MOS showed better resistance to low salinity stress and Streptococcus iniae challenges (). In conclusion, MOS supplementation effectively reduced the prevalence of intestinal Vibrio spp. and enhanced the growth, immune responses, and tolerance to low salinity stress and Streptococcus iniae in juvenile pompano.

1. Introduction

Aquaculture has played a crucial role in meeting the increasing demand for animal protein by humans over the past decades. In 2020, total global aquaculture production reached 122.6 million metric tonnes, with a value of USD 281.5 billion. This accounts for almost 56% of the world’s seafood production in 2020 and is expected to rise to 59% by 2030 [1].

Pompano, Trachinotus ovatus (Carangidae), is an important commercial species distributed in China, Japan, Australia, Vietnam, and other countries [2]. Pompano is a highly valued aquaculture species due to its rapid growth rate and high-quality delicious meat. Aquaculture of this species has recently expanded quickly in Asia, and it is now one of the most prevalent marine cultured species in Vietnam [2, 3]. The expansion of intensive aquaculture, which has resulted in the release of more harmful organic and inorganic wastes, has caused outbreaks of infectious diseases, damage to the natural environment, particularly eutrophication, and loss of biodiversity [4]. Genus Streptococcus are Gram-positive bacteria. Streptococcosis refers to severe diseases caused by Streptococcus that affect humans, terrestrial animals, and fish [5]. Streptococcosis is one of the most prevalent fish pathogens in both freshwater and marine aquaculture, particularly in tropical regions in fish, which is mostly caused by S. agalactiae and S. dysgalactiae. Streptococcus iniae [6]. Streptococcus has caused $150 millions of dollars in economic loss in the aquaculture industry globally each year [7] and about 500,000 human deaths yearly [8].

Antibiotics are commonly used to treat bacterial infections in aquaculture [9]. However, the use of antibiotics in aquaculture has been associated with a number of major issues, including the presence of residual antibiotics in commercially cultured products, the appearance of drug-resistant bacteria, and concerns about food safety and public health [10]. Research estimates that at least 10 million cases will be at risk annually by the year 2050 due to the rise of infections caused by antimicrobial-resistant strains [11]. Evidence of antibiotic resistance in aquaculture has also increased [12, 13]. Moreover, increasing studies have proven the risk of antibiotics to the environment and human health [10]; therefore, more research is needed to introduce novel antibiotic replacements [14]. Research has shown that a potential solution is to use dietary supplements such as pre- and pro-biotics [15, 16].

Prebiotics are indigestible dietary components that can enhance the health of the host by selectively promoting the development and/or stimulating the metabolic processes of beneficial microbes in the intestinal tract [17]. MOS as a prebiotic has been reported to be ecofriendly and possibly an antibiotic alternative that is safe for fish and the environment [18]. Some of the effects of prebiotics include protecting the host against pathogens, modulating the immune system, facilitating the minerals intake, bowel function, metabolic effects, and safety [19]. Mannan oligosaccharides (MOSs) are recognized as beneficial prebiotics for their role in enhancing immunological and intestinal functions [20, 21]. MOS would adhere pathogenic bacteria and prevents them from colonizing in the intestine, and migrating from the lumen into other parts of the body [22]. Mannose-containing compounds induce intracellular signaling related to proinflammatory cytokine production, which may enhance the immunity and health of aquatic animals [23].

The beneficial effects of dietary MOSs have been reported in many aquaculture species, including improved growth performance of Asian Catfish (Clarias batrachus) [24], grass carp (Ctenopharyngodon Idella) [25], while significantly effect was found in tilapia (Oreochromis niloticus × O. aureus) [26], Gulf sturgeon Acipenser oxyrinchus desotoi [27], and gilthead sea bream (Sparus aurata) [28]. In addition, dietary MOS supplementation could boost immune responses in milkfish (Chanos chanos) [29] and hybrid grouper (Epinephelus lanceolatus♂ × Epinephelus fuscoguttatus♀) [30], while MOS did not affect immune response. Moreover, intestinal microorganisms improve in Nile tilapia (Oreochromis niloticus) fed MOS diet [17]. Furthermore, MOS supplemented diet could enhance resilience to stressors in grass carp (Ctenopharyngodon idella) challenged with Aeromonas hydrophila [25]. According to Xue et al. [31], the effect of MOS on fish growth depends on species and developmental stage. In addition, as suggested by Akhter et al. [32], the optimal dosage of feed additives, such as MOS and β-glucan, for the highest growth of pompano is highly variable and requires determination of the optimal level, as improper dose supplementation (insufficient or overdose) would inhibit the growth of aquaculture species [33]. Because no previous study has defined the dietary MOS requirement for pompano, it is essential to conduct an experiment to determine the dietary MOS requirement for pompano.

MOS has demonstrated its effectiveness in several aquaculture species; however, its impact on juvenile pompano is still unknown. In addition, few studies have investigated fish growth and immune in relation to MOS levels. This is critical because inappropriate feed additive doses can harm fish [33–35]. Therefore, this study examined the effects of MOS on growth, haematological parameters, intestinal Vibrio spp., immunity, MOS demand, and stress tolerance of juvenile pompano Trachinotus ovatus. Owing to the importance of dietary MOS and pompano, this topic is worthy of investigation.

2. Materials and Methods

2.1. Ethical Statement

This study was conducted according to the ethical principles and guidelines of the animal use protocol approved by the Institute of Oceanography, Viet Nam Academy of Science and Technology.

2.2. Experimental Fish and Culture Systems

Pompano, Trachinotus ovatus (3.24 g ± 0.45, mean weight ± SD) obtained from a local hatchery. Healthy fish were selected and transported to a laboratory at the Institute of Oceanography, Nha Trang, and acclimated for 3 weeks in a 2-m³ tank prior to the experiment. During acclimation, fish were fed a commercial diet (INVE, Protein > 55%, Lipid > 9%) at a rate of 5% of their body weight per day. A single recirculation system was installed in each of the experimental tanks with a volume of 300 L (50 cm × 80 cm × 80 cm) for a total of 36 tanks. There were six replicate tanks for each dietary treatment, and 20 fish were stocked randomly in each tank. After the acclimation period, the fish were weighed, and the treatment diets were fed as the experiment started (day 0). Water chemistry was measured every second day, and temperature was measured daily. The mean water temperature was 28.5°C; salinity: 33–34 ppt; dissolved oxygen: 6.1 ± 0.5 mg L⁻¹; pH: 8.1–8.3, NH₄⁺: 0.05 mg L⁻¹, NO₂⁻: <0.01 mg L⁻¹. Throughout the experiment, the fish were maintained under a natural photoperiod.

2.3. Experimental Diets and Feeding

MOS (Active-MOS® provided by Biorigin) was added to the base diet (control), as shown in Table 1. This diet formulation has been used previously and has demonstrated favorable growth and survival in pompano [33]. Mannan oligosaccharides (Active-MOS® provided by Biorigin® Ltd., Vietnam) contain 23.4% MOSs extracted from cell yeast wall. Dry ingredients were mixed in a Panasonic mixer (HMB-6383, China) for 15 min, then MOS was added, followed by adding the fish oil and mixed for a another 10 min. Water (350 mL) was then added to 1,000 g of ingredients and stirred to make an a dough before extrusion twice by an extruder (THL-03 Thang Long Electric Machinery. Ltd., Vietnam). The feeds were air-dried overnight and stored at 4°C until use.

Six diets were produced: a control basal diet without MOS (MOS0.0) and five concentrations of Active-MOS®, including 0.10% (MOS0.1), 0.20% (MOS0.2), 0.4% (MOS0.4), 0.6% (MOS0.6), and 0.8% (MOS0.8), supplemented to the basal diet. During the feeding trial, the fish were fed twice a day (7 : 00 and 17 : 00). Pompanos were provided feed in slight excess of satiety. The amount of uneaten feed was monitored daily, and the feed was adjusted daily to attain satiety. The fish status was monitored in the morning, and uneaten pellets and waste were removed before the morning feed. In this experiment, we did not calculate the feed consumption, feed utilization, so feed uneaten feed was not collected and weighed.

2.4. Sampling and Data Collection

The weight and length of all fish in each tank were measured initially (day 0) and at every 2 weeks. The fish were starved for 24 hr before weighing or sampling. The fish were weighed using a balance with an accuracy of 0.01 g. At day 56 (end), 12 fish per treatment were randomly sampled and sacrificed for blood samples and tissues (head-kidney, liver, and intestine). Prior to dissection, the fish were anaesthetized with 100 mg L⁻¹ tricaine methanesulfonate (MS-222, Sigma, USA) for 2–5 min. The fish were washed with 2% sterile saline water prior to dissection.

2.5. Haematological Assays

Blood samples from four pools of three fish (4 pools/treatment × 3 fish/pool = 12 fish/treatment) were used. Pooling was chosen because of the small size of the fish and their low blood volume is low (0.1–0.3 mL/ind). Also, pool samples could minimize variation among individuals. The volume of blood from each fish was recorded to calculate dilution. A haemocytometer was used to count the white blood cells (WBCs) and red blood cells (RBCs) [36]. In order to obtain differential leukocyte counts, including monocytes, lymphocytes, neutrophils, and eosinophils, fish blood was smeared, air-dried before fixing in methanol, and stained with Diff-Quick®. Leukocytes were classified based on their morphology and counted at ×1,000 magnification using a microscope.

2.6. Abundance of Vibrio Spp. in Intestine

The fish were sampled and cleaned with sterile saline (2%). The midgut was hand-ground using ceramic mortar and pestle. Subsequently, the ground tissue was mixed with 0.85% saltwater (1 : 10), and an examination for the presence of Vibrio spp. was carried out using Thiosulfate Citrate Bile Salt Sucrose (TCBS Agar) as a conventional medium recommended to isolate pathogenic Vibrio on fish following the APHA standard method. After incubation at 37°C for 24 hr, the total colony-forming units (CFU) were counted and calculated per unit of fish tissue (g).

2.7. Head-Kidney Macrophage Isolation

Macrophage isolation was performed using a technique developed by Secombes [37]. Head kidneys from four pools of three fish (4 pools/treatment × 3 fish/pool = 12 fish/treatment) were used for macrophage isolation. Pooling was chosen because of the small size of the fish and their head kidneys, while also aiming to minimize heterogeneity among individual samples. The collected head-kidney was cut into small pieces, and 10 mL of RPMI-1640 culture medium was added and subsequently supplemented with 100 IU mL⁻¹ streptomycin, 100 IU mL⁻¹ penicillin, 10 IU mL⁻¹ heparin, and 2% neonatal calf serum (FCS). To obtain leukocytes (HKLs), the head-kidney pieces were ground through a 100-µm mesh. Then, 5 mL of 51% Percoll and 5 mL of 34% Percoll were added to a 15-mL Falcon tube to make a 34%/51% Percoll solution. Next, the head-kidney cell suspension was mixed with 34%/51% Percoll and centrifuged at 400 g for 35 min at 4°C. Subsequently, the leukocyte cell interface was collected and centrifuged at 200 × g for 10 min after washing with phosphate-buffered saline (PBS) (2 : 1) for 10 min. Afterward, the cell pellet was resuspended in 5 mL L-15 medium. The viable cell was stained with 1% trypan blue and counted using a haemocytometer.

2.8. Nonspecific Immune Responses

2.8.1. Phagocyte Activity

The head kidney leukocyte phagocytosis index assay was conducted according to the method described by Siwicki [38]. The head kidney leukocytes were adjusted to a density of 1 × 10⁸ cells mL⁻¹ using 0.1 M phosphate citrate buffer (PBS) at pH 5.8. Fifty microlitres of head kidney leukocytes (1 × 10⁸ cells mL⁻¹) were mixed with 500 μL Congo-red stain yeast zymosan (Sigma) (1 × 10⁷ cells mL⁻¹) in an eppendorf tube and incubated for 2 hr at 22°C. After this, they were washed three times with PBS to remove noningested cells. Then, approximately 50 µL of the mixture was smeared on a microscope slide, and the slides were left to dry for 2 hr at room temperature. Approximately 100 phagocytes were counted on each slide using a microscope at 1,000x magnification. To determine phagocytic activity, both the phagocytic index (PI) and phagocyte ratio (PR, %) were calculated as follows: PR = no. phagocytes engulfed with zymosan/no. of phagocytes; PI = no. of engulfed zymosan/no. of phagocyte cells [39].

2.8.2. Lysozyme Activity

For lysozyme analysis, the collected blood from four pools of three fish was left at room temperature for 30 min to clot and then centrifuged at 1,500 g for 15 min at 4°C to obtain serum. Next, 25 µL of serum samples (three replicates) were added to a 96-well microplate. For standard, 25 µL hen egg-white lysozyme (Sigma) with a serial dilution of 0–20 µg mL⁻¹ in PBS was used. Blank wells, which served as controls, were filled with the same volume of PBS alone. Next, 175 µL of Micrococcus lysodeikticus suspension (0.75 mg mL⁻¹ in PBS) was added to each well, and the microplate was mixed thoroughly. There were three replicates for each serum sample or dilution of hen egg-white lysozyme. Afterward, a microplate reader was used to measure turbidity at 440 nm and 20°C after 15 and 30 min, respectively [3, 40]. The lysozyme activity (μg mL⁻¹) for each sample was determined in comparison with the standard, which was obtained from hen egg-white lysozyme.

2.9. Predicting MOS Requirements for Maximal Growth and Maximal Immune Response in Pompano

The Pearson’s correlation (r) was used to evaluate the relationships between MOS concentrations in the diets, growth rate of fish, intestinal microbiota, and haematological parameters. The present study indicated that specific growth rate (SGR) and serum lysozyme activity in pompano had the strongest significant correlations with dietary MOS levels, so they were used to estimate the MOS level necessary to gain maximum growth and health in pompano. MOS level requirements were analyzed using six regression models in Microsoft Excel 2007, including exponential, linear, logarithmic, quadratic polynomial, power, and moving average. The input parameters in each case included the concentrations of MOS as independent variables and growth rate data and serum lysozyme activity as dependent variables. The model chosen for prediction analysis was based on a higher correlation coefficient (R²). The results indicated that the quadratic polynomial model had a higher R² value; thus, this model was used for the analysis of growth and immune responses. The quadratic polynomial model is shown as the following equation: y = ax² + bx + c; where y is the SGR over time or serum lysozyme of pompano at day 56; x is dietary MOS concentrations; a, b are coefficients; and c is a constant of the equation.

2.10. Challenge Trial

2.10.1. Salinity Stress Test

At the end of the feeding trial, the fish were exposed to low salinity stress. Eighteen fish from each treatment group were randomly captured and transferred to three 400 L tanks as replicates. Each tank contained water with salinity of 1 ppt. The low salinity level and the exposure time were based on previous research on pompano [33]. Death was recorded every 30 min for a total of four hours. When the gill operculum stopped moving, the fish was recorded as dead.

2.10.2. Pathogen Challenge Test

At the end of the feeding trial, 18 fish from each diet treatment were randomly collected and injected with Streptococcus iniae (obtained from Nha Trang University). Each fish received an intraperitoneal injection of a 100 µL suspension of Streptococcus (1.5 × 10⁴ CFU fish⁻¹) in phosphate-buffered saline (PBS) using a 0.3 mL insulin syringe. Fish from each diet treatment were kept in three 400 L tanks as replicates. The injection dose of Streptococcus and time were based on lethal dose (LD50) determined in our previous study on pompano [41]. The fish in each dietary treatment group maintained the same diet throughout the challenge test, with adjustments required for satiation performed via observation. Fish mortality was observed twice daily for 10 days. It was assumed that the longer a fish survived, the greater its resistance to Streptococcus iniae infection.

2.11. Data Calculation and Statistical Analysis

Specific growth rate (SGR % day⁻¹), survival rate, and relative percent survival (RPS) was calculated as follows: SGR = 100 × (Ln(W_t)–Ln(W_o))/days; S = 100 × (N_t/N_o); RPS = 100 × (1−M_d /M_o) [42]; where W_t and W_o are the weight of the fish at time t and at the commencement, S is the survival rate (%), N_t and N_o are the number of the fish at time t and at the commencement, and M_d and M_o are the percentage mortalities of pompano fed MOS diets and control diets, respectively.

Data are displayed as treatment means and standard errors (SE). ANOVA F-tests were used to compare data among treatments. Before the data were analyzed, they were checked to see if they were normally distributed, and if not, they were transformed. If the results of the F-test were significant, differences between treatment means were compared using the least significant difference method. The nonparametric Kruskal–Wallis ANOVA test was used to analyze the survival data. Pearson’s correlation coefficient (r) was used to examine the correlations between dietary MOS concentrations, growth performance, haematological indices, intestinal microbes, and immune responses. When comparing the data, if , the difference was considered significant. SPSS version 18 (IBM, Chicago, IL, USA) was used for all statistical analyses.

3. Results

3.1. Growth Performance

At the end of the experiment (day 56), the group of fish given 0.2% MOS showed the largest weight increment (4.83 times higher compared to the weight of fish fed the control), followed by fish fed diets containing 0.1% and 0.4% MOS (4.61 and 4.41 times higher than the weight of fish fed the control, respectively). The lowest weight gain was observed in the group fed with the control diet (3.44 times) (Figure 1).

Significant variations in the SGR of pompano were observed between diet treatments on days 14, 28, 42, and 56 (Figure 2). After 14 days, the SGRs of pompanos fed diets containing 0.1%–0.6% MOS were significantly higher than those of pompanos fed the control diet (). On days 28 and 42, there were significant differences among the SGRs of pompanos fed diets containing 0.1%–0.4% MOS () compared with the SGR of pompano fish fed the control (MOS0.0). After 56 days of feeding, SGRs of pompanos fed diets with 0.1%–0.2% MOS were significantly higher than SGR of pompanos fed the basal diet () (Figure 2).

3.2. Survival Rate and Relative Survival Rate

At the end of the investigation (day 56), the survival rates of pompano fed various MOS diets ranged from 92% to 98% (Figure 3). The fish that were fed diets with 0.1%–0.6% MOS had the greatest survival rate, which ranged from 97.5% to 98%. The relative percentage survival (RPS) was highest in the group of pompanos fed the diet supplemented with 0.2% MOS, followed by pompanos fed the diets supplemented with 0.1% and 0.4% MOS (both RPS were 72.5%).

3.3. Haematological Parameters

RBCs of pompano fed MOS0.1, MOS0.2, and MOS0.4 diets were higher than that of the control (). Pompano fed 0.1%–0.6% MOS had a higher WBC than the pompano fed control diet () (Table 2).

Pompano fed MOS containing diets had higher proportion of lymphocytes (), whereas monocytes and basophils were significantly decreased in fish fed MOS enriched diets (). In addition, dietary MOS did not significantly influence the number of neutrophils or eosinophils () (Table 2, Figure 4).

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3.4. Intestinal Abundance of Vibrio Spp.

The Vibrio spp. counts in the gut of fish fed 0.1%–0.4% MOS in diet were significantly lower than fish fed the control diet () (Figure 5).

3.5. Immune Response

3.5.1. Phagocytic Ratio (PR) and Phagocytic Index (PI)

Pompano fed diets supplemented with 0.1%–0.6% MOS had significantly greater phagocytic ratios (PRs) than those fed the control diet () (Figure 6). The PI values in pompano fed 0.1%–0.4% MOS increased significantly compared with the PI value in fish fed the control diet (MOS0.0) (). In addition, the PR values were not significantly different between fish fed any level of MOS () (Figure 7).

3.6. Serum Lysozyme Activity

The lysozyme activity of pompano increased significantly () after 56 days of feeding on diets supplemented with MOS. The highest lysozyme activity was observed in fish fed diets containing 0.2% and 0.4% MOS (1.25 times and 1.24 times higher than the lysozyme of the pompano fed control), followed by the pompano fed diets containing 0.1 and 0.6% MOS (Figure 8).

3.7. Relationship between MOS Concentrations and the Growth of Pompano over Time

Pearson correlation analyses showed significant positive relationships between MOS levels and fish growth rate at days 14, 28, 42, and 56 (). Among the growth performance parameters, MOS levels showed the strongest correlation with SGR at all time points (Table 3). On day 14, MOS concentration in the diet had a significant positive correlation with SGR (r = 0.471, ). The correlation values (r) between SGR and MOS levels were 0.494 and 0.483 on days 28 and 42, respectively, with a significance level (P) less than 0.001. On day 56, there was a slight downward trend in this correlation, but it was still significant (r = 0.452, ). At all time points, SGRs had the highest correlation values (r) (Table 3); thus, SGR was used as an independent variable in the regression model to estimate the optimal MOS requirement for the maximal growth rate of pompano (Table 3).

3.8. Relationship between MOS Concentrations and Haematological Index, Intestinal Microbes, and Nonspecific Immunity (Day 56)

Pearson correlation analyses on day 56 showed that the MOS concentrations in the diet were significantly positively correlated with RBC, WBC, and lymphocyte counts () and negatively correlated with monocyte, basophil, and Vibrio spp. counts (). At the end of the experiment (day 56), the immune parameters of fish fed graded levels of MOS were significantly and positively correlated with the MOS concentration in the diet () (Table 4). Among the haematological indices, intestinal microbes, and immune parameters, lysozyme showed the highest correlation coefficient (r) (Table 4). Thus, lysozyme activity was used to predict the optimal MOS requirement for the pompano to reach the maximal immune response.

3.9. Prediction of the Optimal Level of MOS Requirements for Maximal Growth of Pompano Fish, T. ovatus

On day 56, there was a positive correlation between MOS inclusion and growth, according to the quadratic polynomial model (R² ≥ 0.750). As fish weight increased, the estimated optimal concentrations of dietary MOS decreased. To obtain the maximal growth of pompano in the experiment, the optimum levels of MOS were estimated to be 0.440%, 0.385%, 0.371%, and 0.365% on days 14, 28, 42, and 56, respectively (Figure 9, Table 5).

3.10. Predicting MOS Level to Gain Maximal Immune Response in Pompano (Day 56)

At the end of the trial (day 56), in relation to haematological indices, intestinal Vibrio, and immune parameters, the lysozyme activity showed the highest significant correlations with MOS concentrations in the diet (Table 4). Therefore, lysozyme activity values were used as independent variable and MOS concentrations were used as dependent variable in the regression model to estimate the maximal immune response. The procedure for finding an appropriate prediction model was the same as that used for growth data. In this experiment, the quadratic polynomial model yielded the highest R² value. Hence, MOS-supplemented levels were predicted using a quadratic polynomial regression model, and the results showed that the MOS requirement was estimated to be 0.431% of diet for pompano to achieve the maximal lysozyme activity (R² = 0.817) (Figure 10).

3.11. Cumulative Mortalities, Relative Risk, and Hazard Ratio of Pompano Fish Challenged against Salinity (Day 56)

Kaplan–Meier curves and log-rank tests were used to compare the number of pompanos that died after being subjected to low salinity stress. After 4 hr of challenge in the 1 ppt salinity condition, there were significant differences in the survival rates among the treatments (). Pompano given diets containing 0.1%–0.4% MOS had significantly higher survival rates compared to the survival rate of pompano fed the control diet () (Figure 11).

In addition, the relative risk indices (RRI) were lower in pompano fed MOS diets when exposed to low salinity than in those fed the control diet. RRI values in pompano fed the MOS-supplemented diets were less than those fed the control diet, indicating that fish fed the MOS-supplemented diets had a higher capacity to tolerate salinity stress.

When compared to the RRI of pompano in control diets, the RRI values and confident intervals (CI) of fish fed MOS-enriched diets were computed as follows: MOS0.1: 0.256 (CI: 0.0791–0.830); MOS0.2: 0.182 (CI: 0.057–0.583); MOS0.4: 0.359 (CI: 0.108–1.195); MOS0.6: 0.547 (CI: 0.161–1.864); and MOS0.8: 0.598 (CI: 0.187–1.908). The results showed that when exposed to low salinity stress, the risks were significantly reduced in pompano fed diets containing 0.1%–0.4% MOS () (Figure 11).

3.12. Cumulative Mortality, Relative Risk, and Hazard Ratio of Pompanos Challenged with Steptococcus iniae

The pathogen challenge test was performed for 10 days, after 21 days of feeding with dietary MOSs. The cumulative survival rate was determined on the 10^th day and is shown in Figure 12. After challenge with S. iniae, the first mortality was recorded after 2 days in fish fed the control diet (MOS0.0), while in pompano fed MOS-supplemented diets, the first mortality was observed on day 4. After 10 days of challenge, the highest survival rate was observed in fish fed 0.2% MOS, followed by fish fed 0.10% MOS inclusion in the diet. The survival rates of all groups of pompano fed 0.1%–0.6% MOS supplementation in their diets were significantly higher than those fed the control diet ().

4. Discussion

This study demonstrated the effectiveness of dietary MOS in boosting growth, survival, haematological parameters, immune response, and resistance to low salinity stress and S. iniae challenge, and reducing abundance of intestinal Vibrio spp. in pompano.

The results of this study are in line with previous research indicating that MOS enriched diets enhance growth in common carp, Cyprinus carpio [31], Nile tilapia, Oreochromis niloticus [17], Atlantic salmon, Salmo salar [43], red sea bream, Pagrus major [21], and hybrid grouper, Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀ [30]. Conversely, dietary MOS suppressed the growth of Mexican sturgeon, Acipenser oxyrinchus desotoi [27]. According to Xue et al. [31], contradictory outcomes regarding the effect of MOS on fish growth may be dependent on fish species or developmental stage.

Haematological indices are useful indicators for estimating health, nutrition, and environmental factors affecting fish [44]. It has been recommended that leukocyte profiles be used to determine stress in vertebrates [45]. Moreover, lymphocytes, specifically B cells, play a crucial role in the immune system [46] by participating in antibody production in teleost fish [47]. Khosravi-Katuli et al. [48] reported that the addition of MOS to the diet of gilthead sea bream, Sparus aurata significantly boosted haematocrit, haemoglobin, lymphocytes, WBCs, and monocytes. In the current study, pompano fish fed 0.1%–0.6% MOS had significantly higher WBC, lymphocyte counts, and immune indices. Increased WBC, lymphocyte, and immunological parameters and a reduction in gut Vibrio in pompano fed a MOS diet may indicate that the fish’s innate immune system is being stimulated.

Gut microbes play a crucial role in fish metabolism, nutritional balance, immunity, and physiological processes [49–51] In line with our findings, other studies have indicated that MOS-supplemented diets decrease Vibrio and improve intestinal bacteria [52, 53]. Many studies have shown that probiotics, prebiotics, and their synbiotic can be used to control vibriosis in aquaculture [20]. Thus, the reduction in Vibrio in pompano fed MOS in the present study may indicate that they are healthier and reduce the chance of Vibrio infection. In aquaculture, many Vibrio species cause diseases in farmed animals, resulting in massive economic losses [54]. Also, the reduction of Vibrio counts in the gut of fish could indicate quality of food products and increase in food safety of cultured pompano. However, to fulfill this knowledge on effects of MOS on vibriosis, further research is needed to determine the diversity of the intestinal microbes.

Lysozymes and phagocytosis are nonspecific immune responses involved in the protection of the fish body against pathogenic invaders [55]. According to Luo et al. [56], lysozyme can deactivate the peptidoglycan layer in the cell walls of harmful microbes, resulting in a significant resistance to infection. In the present investigation, increased lysozyme activity, phagocytic activity, and WBC counts were observed in pompano fed diets containing 0.1%–0.6% MOS compared to fish fed the control diet. This implies an improvement in the bactericidal activity of phagocytic activity and immunity [57]. Similar to our findings, MOS has been shown to boost the immune response of the common carp [31], Nile tilapia [58], and rainbow trout [59]. Lu et al. [60] stated that the action of MOS begins with the activation of the local intestinal immunity, which is linked to the immune system of the entire body. Furthermore, the role of mannose receptor, a key molecule involved in antigen detection and phagocytosis, is another explanation for the immunomodulatory effects of MOSs [61]. Also, mannose-binding lectin activation via liver secretion is another way in which MOS may influence the immune system [62]. The current study did not detect any significant changes in neutrophil, eosinophil, or basophil counts in pompanos fed an MOS-supplemented diet. However, the increase in the number of WBCs, lymphocytes, and immunity, as well as an increase in the inherent immune system, in pompano fish fed an MOS diet may result in a strengthening of the defences, which may increase resistance to environmental stress or pathogens. This was confirmed by the finding that pompano fish exposed to Streptococcus and salinity stress had a higher survival rate.

Determining optimal nutrient levels is one of the most important aspects of aquaculture because supplying improper doses (excess or insufficient) of nutrients can cause adverse effects in cultured animals [33, 35, 63]. In fact, the majority of studies on dietary MOSs in aquaculture have utilized one or two “recommended” administration levels [64–68] rather than determining nutritional concentration requirements. The effects of MOS levels on growth performance and feed utilization have been reported previously [69–71]. For instance, Torrecillas et al. [72] reported that adding 0.4% dietary MOS increased growth performance in European Sea Bass, Dicentrarchus labrax, compared to fish fed 0.2% MOS and the control, which is an indication of dose impact on fish. However, limited research has determined the optimal MOS dose for optimal growth [69].

In the present study, we measured growth over time using dose–response models to determine the effect of MOS on growth. The determination method applied in this study was similar to that used in previous research that determined the nucleotide requirements for prawn growth [35], MOS for lobster [69], and β-glucan for pompano [3, 33]. Six regression models are used in this study. The model with the highest correlation coefficient (R²) was chosen to predict a suitable MOS concentration for the maximal growth of pompano. According to Ryan [73], the R² value is the most important indicator for determining the quality of the relationships between models.

Similar to previous studies [3, 33], the current findings demonstrated that either excessive or deficient amounts of MOS supplementation adversely affected pompano growth. The current study also revealed that the optimal level of MOS requirement in pompano diets decreases as fish size increases. This is possibly due to the higher growth rate of smaller fish than that of larger ones. On days 28 and 42, the highest correlation coefficients were observed between pompano growth and dietary MOS supplementation. Therefore, it is recommended that studies on the effects of MOS on pompano should be conducted over 2–4 weeks. However, because the size affects the MOS requirement, further examination of different sizes is required to support this statement.

Nutritional requirements are often determined based on growth data rather than immunological responses or disease resistance [74, 75]. In this study, among the investigated immune parameters, lysozyme activity showed the highest correlation with the levels of MOS in the diet; hence, lysozyme from fish fed different MOS levels was employed to predict the optimal MOS requirement for the highest level of immune response in juvenile pompano. To the authors’ knowledge, this is the first attempt to investigate the dietary MOS dosage required for the immune response in pompano. On day 56, the predicted MOS requirement for optimum growth in pompano was 0.365%; however, a slightly higher MOS concentration (0.431%) was required for pompano to achieve its maximum lysozyme activity value. Our results are consistent with earlier research which reported that MOS stimulates the immune system in aquatic species, but that the MOS dosage is crucial for achieving the desired outcomes [76]. Similar to this, a study on the rainbow trout, Oncorhynchus mykiss found that higher levels of MOS produced a more effective stimulant outcome compared to a lower level [77]. Additionally, when the amount of MOS in the diet increased, the phagocytic and lysozyme activities of milkfish, Chanos chanos, continually increased [29].

In the present study, MOS-supplemented diets enhanced the capacity of pompano to suffer from stress. Pompano fed 0.1%–0.4% MOS had higher survival rates when challenged with low-salinity conditions. In line with our results, other studies have revealed that dietary MOS supplementation improves the tolerance to low salinity stress in red sea bream [21], white sea bream (Diplodus sargus L.) larvae [78], and cobia larvae Rachycentron canadum [67]. In Vietnam, pompano cage farms are typically situated near the coast and are highly influenced by freshwater from the land during the rainy season. In this study, the survival rates of pompano fed 0.1%–0.4% MOS under low salinity stress conditions were significantly higher. This result is in line with earlier research that demonstrated red sea bream (Pagrus major) fed MOS had a higher tolerance to low salinity stress [21]. Also, MOS diet reduced stress in carp (Cyprinus carpio) under ammonia stress [31] or gilthead sea bream (Sparus aurata) under thermal stress [48]. Furthermore, in aquaculture, handling, transportation, air exposure, and environmental fluctuations such as salinity have a negative impact on immune response, mortality, and growth performance [79]. Salinity is an environmental element that adversely affects fish growth and reproduction [80]. High precipitation and salinity stress are increasing due to climate change worldwide [81]. According to Huang et al. [82], climate change has triggered high precipitation, resulting in salinity stress on aquatic creatures and has considerably increased the mortality of coral reefs and other coastal marine ecosystems. Thus, the findings of this study showed the effectiveness of the MOS diet in improving salinity tolerance in pompano, which has a meaningful role in aquaculture practice reducing the risk cause by weather. Research has revealed that fish secrete more stress hormones when exposed to stress, which affect immune function by suppressing lymphocyte and immunoglobulin synthesis [47]. In this study, we did not examine the hormones in pompano; however, the increase in WBC, lymphocyte, and nonspecific immune responses in pompano fed MOS diets may indicate a better response to growth, health, and stress tolerance.

The present study shows that fish fed with MOS could resist better against Streptococcus iniae. This is in agreement with other publications, which showed that dietary MOS increased survival rates of hybrid grouper (Epinephelus lanceolatus♂ × Epinephelus fuscoguttatus♀) when challenged with Vibrio harveyi [30], tilapia (Oreochromis niloticus) against Streptococcosis [83], and hybrid striped bass (Morone chrysops × Morone saxatilis) to Streptococcus iniae [84]. It has been reported that Streptococcus has caused $150 millions of dollars in economic loss in the aquaculture industry globally each year [7]. In addition, group A Streptococcus causes about 500,000 human deaths yearly [8]. Thus, the present result shows an improvement in tolerance of low salinity and Streptococcus in pompano fed MOS that could help aquaculture industry develop more sustainable particularly in the scenario of climate change. Reduction in disease infection would bring higher production and benefits for the farmers. The result in this study could partly contribute knowledge about the adaptation of pompano aquaculture to climate change.

It is known that the use of antibiotics in aquaculture may cause some risks such as an increase in the transfer of antibiotic resistance genes to terrestrial animals and human pathogens [85]. Our research revealed that the decrease in Vibrio count in the gut of pompano fed diets with MOS inclusion. Moreover, due to Vibrio causes illness in humans [86], the decrease in Vibrio in pompano fed MOS diets may indicate an improvement in food safety and an increase in the value of commercial products.

This study concluded that the addition of MOS to the diet of juvenile pompano (Trachinotus ovatus) improved growth performance, haematological indices, intestinal Vibrio reduction, immune parameters, and resistance to salinity and Streptococcus challenge. It was also determined that including MOS at a level of approximately 4.0 g kg⁻¹ was ideal for promoting the maximal growth of juvenile pompano and gaining a maximal immune response in pompano. However, other potential benefits of MOS supplementation, such as increased resistance to other environmental stressors or pathogens at various life stages and under physiological conditions, should be examined.

Data Availability

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

Disclosure

All coauthors have seen and agree with the contents of the manuscript. A preprint of this manuscript has previously been published in Research Square [87].

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This research was funded by the Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number 106.05-2019.04. The authors particularly would like to thank Dr. Michael Wang, Nguyen Gia Tuong, and Biorigin for generously providing Active-MOS® and also would like to express special thanks to Dr. Nguyen T.T.T., Nguyen T.K.B., Cao V.N, Hua T.A., and Tran L.K.H. for their great help.

References

FAO, The State of World Fisheries and Aquaculture 2022, Towards Blue Transformation, Rome, FAO, 2022.
View at: Publisher Site
W. Zhao, H.-H. Fang, B.-Y. Gao et al., “Dietary Tribonema sp. supplementation increased growth performance, antioxidant capacity, immunity and improved hepatic health in golden pompano (Trachinotus ovatus),” Aquaculture, vol. 529, Article ID 735667, 2020.
View at: Google Scholar
H. Do-Huu, N. T. Thanh Thuy, and H. T. An, “Supplementing the diet of pompano Trachinotus ovatus with MacroGard® to increase innate immunity, intestinal microbes, growth and ammonia tolerance,” Regional Studies in Marine Science, vol. 55, Article ID 102621, 2022.
View at: Google Scholar
C. Zhou, H. Lin, Z. Huang, J. Wang, Y. Wang, and W. Yu, “Functional Feed Additives to the Diet of Golden Pompano Trachinotus ovatus Juveniles,” in Ontogenetic development of pompano Trachinotus ovatus, Z. Ma, G. Yu, and J. G. Qin, Eds., pp. 181–193, Springer Nature Singapore, Singapore, 2022.
View at: Google Scholar
H. Van Doan, M. Soltani, A. Leitão et al., “Streptococcosis a re-emerging disease in aquaculture: significance and phytotherapy,” Animals, vol. 12, no. 18, Article ID 2443, 2022.
View at: Publisher Site | Google Scholar
S. Maekawa, Y.-T. Wang, T. Yoshida, P.-C. Wang, and S.-C. Chen, “Group C Streptococcus dysgalactiae infection in fish,” Journal of Fish Diseases, vol. 43, pp. 963–970, 2020.
View at: Google Scholar
C. Shoemaker and P. Klesius, “Streptococcal disease problems and control: a review,” in International Symposium on Talipia in Aquaculture, 1997.
View at: Google Scholar
J. R. Carapetis, A. C. Steer, E. K. Mulholland, and M. Weber, “The global burden of group a streptococcal diseases,” The Lancet Infectious Diseases, vol. 5, no. 11, pp. 685–694, 2005.
View at: Publisher Site | Google Scholar
S. P. Hernández, “Responsible use of antibiotics in aquaculture,” 2005, FAO Fisheries Technical Paper No 469 Rome, FAO 2005 97p.
View at: Google Scholar
T. Cherian, C. Ragavendran, S. Vijayan, S. Kurien, and W. J. G. M. Peijnenburg, “A review on the fate, human health and environmental impacts, as well as regulation of antibiotics used in aquaculture,” Environmental Advances, vol. 13, Article ID 100411, 2023.
View at: Publisher Site | Google Scholar
M. E. A. de Kraker, A. J. Stewardson, and S. Harbarth, “Will 10 million people die a year due to antimicrobial resistance by 2050?” PLOS Medicine, vol. 13, no. 11, Article ID e1002184, 2016.
View at: Publisher Site | Google Scholar
L. Burridge, J. S. Weis, F. Cabello, J. Pizarro, and K. Bostick, “Chemical use in salmon aquaculture: a review of current practices and possible environmental effects,” Aquaculture, vol. 306, no. 1–4, pp. 7–23, 2010.
View at: Publisher Site | Google Scholar
F. C. Cabello, “Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment,” Environmental Microbiology, vol. 8, no. 7, pp. 1137–1144, 2006.
View at: Publisher Site | Google Scholar
M. G. Bondad-Reantaso, B. MacKinnon, I. Karunasagar et al., “Review of alternatives to antibiotic use in aquaculture,” Reviews in Aquaculture, pp. 1–31, 2023.
View at: Google Scholar
M. A. O. Dawood, S. Koshio, and M. Á. Esteban, “Beneficial roles of feed additives as immunostimulants in aquaculture: a review,” Reviews in Aquaculture, vol. 10, pp. 950–974, 2018.
View at: Google Scholar
D. K. Meena, P. Das, S. Kumar et al., “Beta-glucan: an ideal immunostimulant in aquaculture (a review),” Fish Physiology and Biochemistry, vol. 39, no. 3, pp. 431–457, 2013.
View at: Publisher Site | Google Scholar
T. Wang, H.-X. Wu, W.-J. Li et al., “Effects of dietary mannan oligosaccharides (MOS) supplementation on metabolism, inflammatory response and gut microbiota of juvenile Nile tilapia (Oreochromis niloticus) fed with high carbohydrate diet,” Fish & Shellfish Immunology, vol. 130, pp. 550–559, 2022.
View at: Publisher Site | Google Scholar
S. Das, K. Mondal, and S. Haque, “A review on application of probiotic, prebiotic and synbiotic for sustainable development of aquaculture,” Journal of Entomology and Zoology Studies, vol. 5, pp. 422–429, 2017.
View at: Google Scholar
M. E. Sanders, D. J. Merenstein, G. Reid, G. R. Gibson, and R. A. Rastall, “Probiotics and prebiotics in intestinal health and disease: from biology to the clinic,” Nature Reviews Gastroenterology & Hepatology, vol. 16, pp. 605–616, 2019.
View at: Google Scholar
S. Yilmaz, E. Yilmaz, M. A. O. Dawood, E. Ringø, E. Ahmadifar, and H. M. R. Abdel-Latif, “Probiotics, prebiotics, and synbiotics used to control vibriosis in fish: a review,” Aquaculture, vol. 547, Article ID 737514, 2022.
View at: Google Scholar
M. A. O. Dawood, S. Koshio, S. E. Fadl et al., “The modulatory effect of mannanoligosaccharide on oxidative status, selected immune parameters and tolerance against low salinity stress in red sea bream (Pagrus major),” Aquaculture Reports, vol. 16, Article ID 100278, 2020.
View at: Google Scholar
L. W. Peterson and D. Artis, “Intestinal epithelial cells: regulators of barrier function and immune homeostasis,” Nature Reviews Immunology, vol. 14, no. 3, pp. 141–153, 2014.
View at: Publisher Site | Google Scholar
E. Ringø, R. E. Olsen, T. Ø. Gifstad et al., “Prebiotics in aquaculture: a review,” Aquaculture Nutrition, vol. 16, pp. 117–136, 2010.
View at: Publisher Site | Google Scholar
M. N. Akter, K. Zahan, M. A. Zafar, N. Khatun, M. S. Rana, and M. I. Mursalin, “Effects of dietary mannan oligosaccharide on growth performance, feed utilization, body composition and haematological parameters in Asian Catfish (Clarias batrachus) Juveniles,” Turkish Journal of Fisheries and Aquatic Sciences, vol. 21, pp. 559–567, 2021.
View at: Publisher Site | Google Scholar
Z.-Y. Lu, L. Feng, W.-D. Jiang et al., “Dietary mannan oligosaccharides strengthens intestinal immune barrier function via multipath cooperation during Aeromonas Hydrophila infection in grass carp (Ctenopharyngodon Idella),” Frontiers in Immunology, vol. 13, Article ID 1010221, 2022.
View at: Publisher Site | Google Scholar
M. A. Genc, E. Yilmaz, E. Genc, E. Genc, and M. Aktas, “Effects of dietary mannan oligosaccharides (MOS) on growth, body composition, and intestine and liver histology of the hybrid tilapia (Oreochromis niloticus x O. aureus),” The Israeli Journal of Aquaculture - Bamidgeh, vol. 59, pp. 10–16, 2007.
View at: Google Scholar
G. S. Pryor, J. B. Royes, F. A. Chapman, and R. D. Miles, “Mannanoligosaccharides in fish nutrition: effects of dietary supplementation on growth and gastrointestinal villi structure in gulf of Mexico sturgeon,” North American Journal of Aquaculture, vol. 65, no. 2, pp. 106–111, 2003.
View at: Publisher Site | Google Scholar
A. Dimitroglou, D. L. Merrifield, P. Spring, J. Sweetman, R. Moate, and S. J. Davies, “Effects of mannan oligosaccharide (MOS) supplementation on growth performance, feed utilisation, intestinal histology and gut microbiota of gilthead sea bream (Sparus aurata),” Aquaculture, vol. 300, pp. 182–188, 2010.
View at: Google Scholar
R. Harikrishnan, G. Devi, P. Balamurugan et al., “Immunostimulatory effect of mannan-oligosaccharides supplementation diet in milkfish (Chanos chanos),” Fish & Shellfish Immunology, vol. 133, Article ID 108568, 2023.
View at: Publisher Site | Google Scholar
Z. Ren, S. Wang, Y. Cai et al., “Effects of dietary mannan oligosaccharide supplementation on growth performance, antioxidant capacity, non-specific immunity and immune-related gene expression of juvenile hybrid grouper (Epinephelus lanceolatus♂ × Epinephelus fuscoguttatus♀),” Aquaculture, vol. 523, Article ID 735195, 2020.
View at: Google Scholar
S. Xue, B. Xia, B. Zhang et al., “Mannan oligosaccharide (MOS) on growth performance, immunity, inflammatory and antioxidant responses of the common carp (Cyprinus carpio) under ammonia stress,” Frontiers in Marine Science, vol. 9, 2022.
View at: Google Scholar
N. Akhter, B. Wu, A. M. Memon, and M. Mohsin, “Probiotics and prebiotics associated with aquaculture: a review,” Fish & Shellfish Immunology, vol. 45, pp. 733–741, 2015.
View at: Google Scholar
H. Do-Huu, H. M. Sang, and N. T. Thanh Thuy, “Dietary β-glucan improved growth performance, Vibrio counts, haematological parameters and stress resistance of pompano fish, Trachinotus ovatus Linnaeus, 1758,” Fish & Shellfish Immunology, vol. 54, pp. 402–410, 2016.
View at: Google Scholar
I. E. H. Belal, “A review of some fish nutrition methodologies,” Bioresource Technology, vol. 96, no. 4, pp. 395–402, 2005.
View at: Publisher Site | Google Scholar
H. Do-Huu, S. Tabrett, K. Hoffmann, P. Köppel, J. S. Lucas, and A. C. Barnes, “Dietary nucleotides are semi-essential nutrients for optimal growth of black tiger shrimp (Penaeus monodon),” Aquaculture, vol. 366-367, pp. 115–121, 2012.
View at: Google Scholar
P. C. Blaxhall and K. W. Daisley, “Routine haematological methods for use with fish blood,” Journal of Fish Biology, vol. 5, pp. 771–781, 1973.
View at: Google Scholar
C. J. Secombes, “Isolation of salmonid macrophages and analysis of their killing activity,” in Techniques in Fish Immunology, J. S. Stolen, T. C. Fletcher, D. P. Anderson, B. S. Roberson, and W. B. V. Muiswinkel, Eds., pp. 137–154, SOS Publications, Fair Haven, NJ, 1990.
View at: Google Scholar
A. K. Siwicki, D. P. Anderson, and G. L. Rumsey, “Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis,” Veterinary Immunology and Immunopathology, vol. 41, no. 1-2, pp. 125–139, 1994.
View at: Publisher Site | Google Scholar
P. K. Sahoo and S. C. Mukherjee, “Effect of dietary β-1,3 glucan on immune responses and disease resistance of healthy and aflatoxin B1-induced immunocompromised rohu (Labeo rohita Hamilton),” Fish & Shellfish Immunology, vol. 11, pp. 683–695, 2001.
View at: Google Scholar
A. Ellis, “Lysozyme assays,” in Techniques in Fish Immunology, J. S. Stolen, T. C. Fletcher, D. P. Anderson, B. S. Robertsen, and W. B. Va n Muiswinkel, Eds., p. 101e3, SOS Publications, Fair Haven, NJ, 1990.
View at: Google Scholar
H. Do-Huu, N. T. N. Hue, and T. V. Hich, Effects of Dietary β-glucan Supplementation on Growth, Innate Immune, and Capacity Against Pathogen Streptococcus iniae of Juvenile Pompano (Trachinotus ovatus), The Israeli Journal of Aquaculture, Bamidgeh, 2019.
D. F. Amend, “Potency testing of fish vaccines,” Fish Biologics: Serodiagnostics and Vaccines, vol. 49, pp. 447–454, 1981.
View at: Google Scholar
B. Grisdale-Helland, S. J. Helland, and D. M. Gatlin, “The effects of dietary supplementation with mannanoligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar),” Aquaculture, vol. 283, pp. 163–167, 2008.
View at: Google Scholar
A. Cnaani, S. Tinman, Y. Avidar, M. Ron, and G. Hulata, “Comparative study of biochemical parameters in response to stress in Oreochromis aureus, O. mossambicus and two strains of O. niloticus,” Aquaculture Research, vol. 35, pp. 1434–1440, 2004.
View at: Publisher Site | Google Scholar
A. K. Davis, D. L. Maney, and J. C. Maerz, “The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists,” Functional Ecology, vol. 22, pp. 760–772, 2008.
View at: Google Scholar
J. O. Sunyer, “Fishing for mammalian paradigms in the teleost immune system,” Nature Immunology, vol. 14, no. 4, pp. 320–326, 2013.
View at: Publisher Site | Google Scholar
D. Hoole, D. Bucke, P. Burgess, and I. Wellby, Diseases of Carp and Other Cyprinid Fishes, Wiley-Blackwell, 2008.
K. Khosravi-Katuli, Y. Mohammadi, M. Ranjbaran et al., “Effects of mannan oligosaccharide and synbiotic supplementation on growth performance and immune response of Gilthead Sea Bream (Sparus aurata) before and after thermal stress,” Aquaculture Research, vol. 52, no. 8, pp. 3745–3756, 2021.
View at: Publisher Site | Google Scholar
N. Cerf-Bensussan and V. Gaboriau-Routhiau, “The immune system and the gut microbiota: friends or foes?” Nature Reviews Immunology, vol. 10, no. 10, pp. 735–744, 2010.
View at: Publisher Site | Google Scholar
C. L. Maynard, C. O. Elson, R. D. Hatton, and C. T. Weaver, “Reciprocal interactions of the intestinal microbiota and immune system,” Nature, vol. 489, no. 7415, pp. 231–241, 2012.
View at: Publisher Site | Google Scholar
S. K. Nayak, “Role of gastrointestinal microbiota in fish,” Aquaculture Research, vol. 41, pp. 1553–1573, 2010.
View at: Publisher Site | Google Scholar
A. Dimitroglou, D. L. Merrifield, R. Moate et al., “Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaum),” Journal of Animal Science, vol. 87, no. 10, pp. 3226–3234, 2009.
View at: Publisher Site | Google Scholar
O. Gainza and J. Romero, “Effect of mannan oligosaccharides on the microbiota and productivity parameters of Litopenaeus vannamei shrimp under intensive cultivation in Ecuador,” Scientific Reports, vol. 10, no. 1, Article ID 2719, 2020.
View at: Publisher Site | Google Scholar
N. Mohamad, M. N. A. Amal, I. S. M. Yasin et al., “Vibriosis in cultured marine fishes: a review,” Aquaculture, vol. 512, Article ID 734289, 2019.
View at: Google Scholar
S. Saurabh and P. K. Sahoo, “Lysozyme: an important defence molecule of fish innate immune system,” Aquaculture Research, vol. 39, pp. 223–239, 2008.
View at: Publisher Site | Google Scholar
C. Luo, B. Gwekwe, P. Choto et al., “Bitter peptides from enzymatically hydrolyzed protein increase the number of leucocytes and lysozyme activity of large yellow croaker (Larimichthys crocea),” Fish & Shellfish Immunology, vol. 81, pp. 130–134, 2018.
View at: Google Scholar
M. Sakai, “Current research status of fish immunostimulants,” Aquaculture, vol. 172, pp. 63–92, 1999.
View at: Google Scholar
K. M. Selim and R. M. Reda, “Beta-glucans and mannan oligosaccharides enhance growth and immunity in Nile Tilapia,” North American Journal of Aquaculture, vol. 77, pp. 22–30, 2015.
View at: Google Scholar
U. Rodriguez-Estrada, S. Satoh, Y. Haga, H. Fushimi, and S. John, “Effects of single and combined supplementation of Enterococcus faecalis, mannan oligosaccharide and polyhydroxybutyrate acid on growth performance and immune response of rainbow trout Oncorhynchus mykiss,” Aquaculture Science, vol. 57, pp. 609–617, 2009.
View at: Google Scholar
J. Lu, C. Qi, S. M. Limbu et al., “Dietary mannan oligosaccharide (MOS) improves growth performance, antioxidant capacity, non-specific immunity and intestinal histology of juvenile Chinese mitten crabs (Eriocheir sinensis),” Aquaculture, vol. 510, pp. 337–346, 2019.
View at: Google Scholar
A. J. Engering, M. Cella, D. Fluitsma et al., “The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells,” European Journal of Immunology, vol. 27, no. 9, pp. 2417–2425, 1997.
View at: Publisher Site | Google Scholar
C. A. Janeway Jr, “How the immune system recognizes invaders,” Scientific American, vol. 269, no. 3, pp. 72–79, 1993.
View at: Publisher Site | Google Scholar
H. Nakagawa, M. Sato, and D. M. Gatlin, Dietary Supplements for the Health and Quality of Cultured Fish, CABI Publishing, Oxfordshire, 2007.
A. Dimitroglou, R. Moate, T. Janssens, P. Spring, J. W. Sweetman, and S. J. Davies, “Field observations on the effect of a mannan oligosaccharide on mortality and intestinal integrity of sole (Solea senegalensis, Kaup) infected by Photobacterium damselae subsp. piscicida,” Journal of Aquaculture Research & Development, Article ID 013, 2011.
View at: Publisher Site | Google Scholar
N. Gültepe, S. Salnur, B. HoŞSu, and O. Hisar, “Dietary supplementation with mannanoligosaccharides (MOS) from bio-mos enhances growth parameters and digestive capacity of gilthead sea bream (Sparus aurata),” Aquaculture Nutrition, vol. 17, pp. 482–487, 2011.
View at: Publisher Site | Google Scholar
B. C. Peterson, T. C. Bramble, and B. B. Manning, “Effects of Bio-Mos® on growth and survival of channel catfish challenged with Edwardsiella ictaluri,” Journal of the World Aquaculture Society, vol. 41, pp. 149–155, 2010.
View at: Google Scholar
G. Salze, E. McLean, M. H. Schwarz, and S. R. Craig, “Dietary mannan oligosaccharide enhances salinity tolerance and gut development of larval cobia,” Aquaculture, vol. 274, pp. 148–152, 2008.
View at: Google Scholar
S. Torrecillas, A. Makol, M. J. Caballero et al., “Effects on mortality and stress response in European sea bass, Dicentrarchus labrax (L.), fed mannan oligosaccharides (MOS) after Vibrio anguillarum exposure,” Journal of Fish Diseases, vol. 35, no. 8, pp. 591–602, 2012.
View at: Publisher Site | Google Scholar
H. Do-Huu and C. M. Jones, “Effects of dietary mannan oligosaccharide supplementation on juvenile spiny lobster Panulirus homarus (Palinuridae),” Aquaculture, vol. 432, pp. 258–264, 2014.
View at: Google Scholar
H. M. Sang and R. Fotedar, “Effects of mannan oligosaccharide dietary supplementation on performances of the tropical spiny lobsters juvenile (Panulirus ornatus, fabricius 1798),” Fish & Shellfish Immunology, vol. 28, no. 3, pp. 483–489, 2010.
View at: Publisher Site | Google Scholar
S. Torrecillas, A. Makol, T. Benitez-Santana et al., “Reduced gut bacterial translocation in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides (MOS),” Fish & Shellfish Immunology, vol. 30, no. 2, pp. 674–681, 2011.
View at: Publisher Site | Google Scholar
S. Torrecillas, A. Makol, M. J. Caballero et al., “Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides,” Fish & Shellfish Immunology, vol. 23, pp. 969–981, 2007.
View at: Google Scholar
T. P. Ryan, Modern Regression Methods, John Wiley, London, 2nd edition, 2008.
Y. Jin, L.-X. Tian, S.-L. Zeng et al., “Dietary lipid requirement on non-specific immune responses in juvenile grass carp (Ctenopharyngodon idella),” Fish & Shellfish Immunology, vol. 34, pp. 1202–1208, 2013.
View at: Google Scholar
V. Kiron, “Fish immune system and its nutritional modulation for preventive health care,” Animal Feed Science and Technology, vol. 173, pp. 111–133, 2012.
View at: Publisher Site | Google Scholar
H. M. Sang and R. Fotedar, “Prebiotic mannan oligosaccharide diet improves health status of the digestive system of marron, Cherax tenuimanus (Smith 1912),” Journal of Applied Aquaculture, vol. 22, pp. 240–250, 2010.
View at: Google Scholar
U. Rodriguez-Estrada, S. Satoh, Y. Haga, H. Fushimi, and J. Sweetman, “Effects of inactivated Enterococcus faecalis and mannan oligosaccharide and their combination on growth, immunity, and disease protection in rainbow trout,” North American Journal of Aquaculture, vol. 75, pp. 416–428, 2013.
View at: Publisher Site | Google Scholar
A. Dimitroglou, S. J. Davies, J. Sweetman, P. Divanach, and S. Chatzifotis, “Dietary supplementation of mannan oligosaccharide on white sea bream (Diplodus sargus L.) larvae: effects on development, gut morphology and salinity tolerance,” Aquaculture Research, vol. 41, pp. e245–e51, 2010.
View at: Publisher Site | Google Scholar
J. E. Bly, S. M. Quiniou, and L. W. Clem, “Environmental effects on fish immune mechanisms,” Developments in Biological Standardization, vol. 90, pp. 33–43, 1997.
View at: Google Scholar
D. Kültz, “Physiological mechanisms used by fish to cope with salinity stress,” Journal of Experimental Biology, vol. 218, pp. 1907–1914, 2015.
View at: Google Scholar
K. Y. Chong, C. K. Yeo, and A. T. K. Yee, “Changing climate threatens tropical rainforests too,” Nature, vol. 465, Article ID 420, 2010.
View at: Publisher Site | Google Scholar
H. Huang, Y. Yang, X. Li et al., “Benthic community changes following the 2010 Hainan flood: implications for reef resilience,” Marine Biology Research, vol. 10, pp. 601–611, 2014.
View at: Google Scholar
C. Samrongpan, N. Areechon, R. Yoonpundh, and P. Sirsapoome, “Effects of mannan-oligosaccharide on growth, survival and disease resistance of Nile tilapia (Oreochromis niloticus linnaeus) fry,” in 8th International Symposium on Tilapia in Aquaculture, pp. 345–353, Cairo Egypt, 2008.
View at: Google Scholar
P. Li, D. H. Lewis, and D. M. Gatlin, “Dietary oligonucleotides from yeast RNA influence immune responses and resistance of hybrid striped bass (Morone chrysops × Morone saxatilis) to Streptococcus iniae infection,” Fish & Shellfish Immunology, vol. 16, pp. 561–569, 2004.
View at: Google Scholar
R. A. Costa, R. L. Araújo, O. V. Souza, and R. H. S. d. F. Vieira, “Antibiotic-resistant vibrios in farmed shrimp,” BioMed Research International, vol. 2015, Article ID 505914, 5 pages, 2015.
View at: Publisher Site | Google Scholar
P. A. West, “The human pathogenic vibrios—a public health update with environmental perspectives,” Epidemiology and Infection, vol. 103, no. 1, pp. 1–34, 1989.
View at: Publisher Site | Google Scholar
H. Do-Huu, T. N. H. Nguyen, and H. T. Vo, “Effects of dietary administration of mannan oligosaccharides on growth performance, intestinal Vibrio, non-specific immunity and tolerance to low salinity in golden pompano, Trachinotus ovatus (Carangidae),” 2023, Research Square.
View at: Publisher Site | Google Scholar

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Copyright © 2023 Hoang Do-Huu 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.

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