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Article

Effects of Dietary Chlorogenic Acid on the Growth, Lipid Metabolism, Antioxidant Capacity, and Non-Specific Immunity of Asian Swamp Eel (Monopterus albus)

by
Hang Yang
1,2,†,
Chengcheng Wu
3,4,5,†,
Quan Yuan
1,2,
Weiwei Lv
1,2,
Junqiang Qiu
3,4,5,
Mingyou Li
3,4,5,
Qinghua Zhang
3,4,5,* and
Wenzong Zhou
1,2,*
1
Eco-Environmental Protection Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai 201403, China
2
Key Laboratory of Integrated Rice-Fish Farming Ecosystem, Ministry of Agriculture and Rural Affairs, Shanghai Academy of Agricultural Sciences, Shanghai 201403, China
3
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai 201306, China
4
China National Pathogen Collection Center for Aquatic Animals, Shanghai Ocean University, Shanghai 201306, China
5
Key Laboratory of Integrated Rice-Fish Farming, Ministry of Agriculture and Rural Affairs, Shanghai Ocean University, Shanghai 201306, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Fishes 2024, 9(12), 496; https://doi.org/10.3390/fishes9120496
Submission received: 21 October 2024 / Revised: 6 November 2024 / Accepted: 16 November 2024 / Published: 3 December 2024
(This article belongs to the Special Issue Growth, Metabolism, and Flesh Quality in Aquaculture Nutrition)
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Abstract

To investigate the dietary effects of chlorogenic acid (CGA) on the growth performance, lipid metabolism, antioxidant activity, and non-specific immunity of Asian swamp eel (Monopterus albus) during the domestication stage, a 28-day feeding experiment was conducted to supplement with CGA at levels of 0 (Cont.), 250 (CGA 0.50%), 500 (CGA 1.00%), and 750 (CGA 1.50%) mg/kg·bw by feeding with yellow mealworm (Tenebrio molitor). Compared with the control group, the addition of 250–750 mg/kg of CGA significantly increased the weight-gain rate (WG) of M. albus, and the CGA 1.0% group displayed the highest value. The content of hemoglobin and high-density lipoprotein in all CGA groups was markedly elevated (p < 0.05), while the triglyceride, glucose, low-density lipoprotein, and glycosylated serum protein levels were lowered (p < 0.05). Among the antioxidant enzymes, the glutathione peroxidase and catalase activity was significantly higher in all experimental groups than that of the control group, whereas the malondialdehyde activity was significantly reduced (p < 0.05). For a non-specific immune enzyme system, the lysozyme and alkaline phosphatase activity in all treatments and the superoxide dismutase and acid phosphatase activity in the CGA 0.5% group was markedly increased (p < 0.05). In conclusion, supplementation with CGA can enhance the growth performance and improve the lipid metabolism, antioxidant capacity, and non-specific immunity of M. albus during the domestication stage, and the optimal CGA supplementation for T. molitor as biocarrier bait is 500 mg/kg, corresponding to 405 mg/kg.
Keywords:
Monopterus albus; chlorogenic acid; growth; antioxidant capacity; non-specific immunity
Key Contribution: Dietary supplementation with CGA can enhance the growth performance and improve the lipid metabolism, antioxidant capacity, and non-specific immunity of M. albus during the domestication stage, and the optimal CGA supplementation for T. molitor as biocarrier bait is 500 mg/kg, corresponding to 405 mg/kg.

1. Introduction

The Asian swamp eel (Monopterus albus) belongs to Osteichthyes, Synbranchiformes, and Monopterus, and is an important freshwater cultured animal in the Southeast Asian region. Due to its rich nutritional components and its medicinal and economic value, M. albus has become one of the important special economic fish species in China, and its production exceeded 320,000 tons in 2023 [1]. With the rapid development of the M. albus industry, intensive aquaculture not only leads to a decline in the immunity of the fish, but also easily causes disease outbreaks. Currently, the prevention and treatment of diseases mainly rely on antibiotics and disinfectants, which can easily cause serious drug resistance problems, affecting the cultured environment and food-safety risks. Therefore, the development of antibiotic substitute products has become a trend in sustainable aquaculture. Owing to their naturalness, multifunctionality, and residue-free nature, herbal extractives have become immune additives for improving the functionality of aquaculture feed [2,3].
In recent years, the application of herbal medicine as a natural growth promoter in aquaculture has been increasing [4], and visible results have been achieved in some aspects such as growth, metabolism, reproduction, and diseases in fish [5]. Chlorogenic acid (CGA) is a phenylpropanoid compound produced by plants during aerobic respiration and is a condensed phenolic acid formed by the dehydration and condensation of caffeic acid and quinic acid. As a water-soluble phenolic compound, it has various biological activities and pharmacological effects such as antibacterial, anti-inflammatory, antioxidant, lipid-lowering, and blood-sugar-lowering [6].
Currently, the main sources for CGA extraction are Eucommiaceae, Caprifoliaceae, and Asteraceae, on account of their relatively high content [7]. A large number of studies have shown that dietary supplementation of CGA has the effects of promoting growth, regulating nutrient metabolism, improving reproductive performance, enhancing product quality, and reducing pollution in livestock and poultry animals [8,9,10,11]. Simultaneously, there are also related studies on CGA in aquatic animals. Studies have reported that the supplementation of CGA in diet can significantly improve the growth performance of grass carp Ctenopharyngodon idella [12], crucian carp Carassius auratus [13], and common carp Cyprinus carpio [14]; promote the antioxidant capacity of largemouth bass Micropterus salmoides [15], white shrimp Litopenaeus vannamei [16], and koi cyprinus carpio [17]; and enhance the immunity of rainbow trout Oncorhynchus mykiss [18], yellow catfish Pelteobagrus fulvidraco [19], and spotted sea bass Lateolabrax maculatus [20]. However, there are currently no studies on CGA in M. albus.
At present, M. albus juveniles are used to feeding on small fish, shrimp, and worms in nature, so they need to be domesticated during the feeding process, and yellow mealworms (Tenebrio molitor) are often used as an ideal domesticated bait for M. albus [21]. Therefore, the study aimed to determine the effects of different concentrations of CGA extracted from Eucommia ulmoides on growth, lipid metabolism, antioxidant capacity, and non-specific immunity of M. albus. These results will provide a theoretical basis for the application of CGA in the diet of M. albus during the domestication stage.

2. Materials and Methods

2.1. Experimental Materials

M. albus were provided by the Zhuanghang Comprehensive Experiment Station of the Shanghai Academy of Agricultural Sciences. CGA derived from Eucommia ulmoides was purchased from Xi’an RiboBio Biology Co., Ltd. (Xi’an, China), with a purity of 5%. The biological carrier bait was T. molitor, which was reared at the Zhuanghang Comprehensive Experiment Station of the Shanghai Academy of Agricultural Sciences. The main nutritional components of yellow mealworm were as follows: moisture 68.0%, crude protein 18.1%, crude fat 8.8%, crude fiber 5.5%, and crude ash 5.0%.

2.2. Experimental Design and Feeding Management

A total of 720 M. albus with an average initial body weight of 25.26 ± 0.16 g were randomly divided into four groups with three replicates in each group and 60 tails per replicate. The fish were fed with T. molitor as carrier bait with CGA intakes of 0 (control group), 0.50% (250 mg/kg·bw), 1.00% (500 mg/kg·bw), and 1.50% (750 mg/kg·bw), respectively. The method of addition was to evenly sprinkle CGA on the hungry T. molitor, which were fed to the fish within 30 min after eating. The actual content of CGA in the T. molitor after consuming CGA was determined by high-performance liquid chromatography (HPLC) to be 10.2 mg/kg, 143 mg/kg, 405 mg/kg, and 639 mg/kg, respectively.
The feeding experiment lasted for 4 weeks, and the feeding amount was 2–3% of the total weight of the M. albus at 4:00 pm every day. Each cement pond (1.0 × 2.0 × 1.0 m) was equipped with a water recirculation device and was switched on throughout the day during the experiment. Fish were cultured in the ambient photoperiod (14 L:10 D) with water temperatures of 26–28 °C and dissolved oxygen levels of 6.0–7.5 mg/L. During the experiment, the number and weight of dead M. albus needed to be recorded, and the total weight of M. albus in each group was measured after the experiment.

2.3. Sample Collection and Analysis

At the end of the feeding experiment, the M. albus were starved for 24 h, and then 5 fish were randomly selected from each group and anesthetized with MS-222 (100 mg/L) for blood collection. The blood collection was performed by decapitation, and the serum was obtained by leaving the whole blood at 4 °C overnight and centrifuging at 3000 r/min for 10 min. After blood collection, the livers were quickly dissected on ice, washed with physiological saline to remove the surface-floating blood, dried with filter paper, and weighed to determine antioxidant-enzyme and non-specific-immune-enzyme activity.

2.3.1. Growth Indicators

After the feeding experiment, the fish in each cement pond were weighed and counted, and the related growth performance indexes of M. albus were calculated. The specific formula is as follows:
Survival rate (SR, %) = (number of surviving fish/total number of fish) × 100;
Weight gain rate (WGR, %) = (mean overall weight of fish after growth − the mean body weight of fish before growth)/the mean body weight of fish before growth × 100;
Specific growth rate (SGR, %) = [Ln (final weight) − Ln (initial weight)]/days × 100.

2.3.2. Blood Physiological and Biochemical Indicators

Whole blood parameters were transferred to Wuhan Servicebio Technology Co., Ltd. (Wuhan, China) for determining the platelet crit (PCT), the platelet distribution width (PDW), the red blood cell distribution width coefficient of variation (RDW), the mean corpuscular volume (MCV), hemoglobin (HGB), hematocrit (HCT), red blood cells (RBC), and white blood cells (WBC) by using a Myriad Veterinary Automatic Hematology Analyzer (BC-2800vet).
Kits from the Nanjing Jiancheng Institute of Biotechnology (Nanjing, China) were used to measure glycosylated serum protein (GSP), glucose (GLU), low-density lipoprotein (LDL), high-density lipoprotein (HDL), cholesterol (CHO), and triglycerides (TG). The assay was performed by referring to the kit instructions. The levels of GSP and GLU were detected using a spectrophotometer with a wavelength of 550 nm and an optical diameter of 0.5 cm. The HDL and LDL contents were measured at 546 nm using a microplate method. The contents of CHO and TG in serum were detected at 510 nm using a single reagent colorimetry method.

2.3.3. Non-Specific Immunity and Antioxidant Enzyme Indexes

The liver tissues were weighed accurately, pre-cooled saline was added in the ratio of weight (g):volume (mL) = 1:10 and centrifuged at 2500 r/min for 10 min in a high-speed centrifuge, and the supernatant was collected for determination. The activity of total antioxidant capacity (T-AOC), catalase (CAT), malondialdehyde (MDA), glutathione peroxidase (GSH-PX), lysozyme (LZM), superoxide dismutase (SOD), alkaline phosphatase (AKP), and acid phosphatase (ACP) in the liver was determined using reagent kits (Jiancheng, Nanjing, China), and the assay was performed by referring to the kit instructions. Simply, the liver was homogenized to obtain the supernatant, and the total protein (TP) content was measured for error calibration. Lastly, the supernatant and reagents were combined and used for measuring the abovementioned parameters using a microplate reader or colorimetry methods.

2.4. Statistical Analysis

All experimental data were recorded in Excel spreadsheets and the SPSS 22.0 (IBM Corp., Armonk, NY, USA) software was used for one-way analysis of variance (ANOVA). When the difference was significant (p < 0.05), Duncan’s method was used for multiple comparisons. The results are expressed as the mean of the standard deviation (SD).

3. Results

3.1. Growth Performance

As shown in Table 1, CGA supplementation had significant effects on the growth performance of M. albus (p < 0.05). Compared with the control group, the addition of 250–750 mg/kg of CGA in diet significantly increased the WG and SGR, and the CGA 1.00% group displayed the highest values. The WG and SGR of the 1.00% CGA group were significantly higher than those of the 0.50% and 1.50% CGA groups (p < 0.05), and the SR of the 1.50% CGA group decreased significantly compared with the control group (p < 0.05).

3.2. Blood Parameters

Table 2 shows that the different levels of CGA had no significant effect on WBC, RBC, HCT, MCV, RDW, and PDW (p > 0.05). However, the addition of CGA in all diets caused a significant increase in HGB (p < 0.05), and the PCT in the CGA 1.00% and the CGA 0.50% groups significantly increased compared to the control group (p < 0.05).
As shown in Table 3, the content of TG, LDL GLU, and GSP in all CGA groups was significantly lower (p < 0.05), and HDL levels were higher than those of the control group (p < 0.05). In addition, the CGA 1.00% and CGA 1.50% groups were promoted in CHO content compared with the control and CGA 0.50% groups (p < 0.05).

3.3. Antioxidant Enzyme Activity

In Figure 1, the antioxidant enzyme activity was affected by the addition of GCA. The GSH-Px and CAT activity in all treatment groups was increased, and the MDA content was decreased compared with the control group (p < 0.05). Moreover, the T-AOC activity was markedly augmented by CGA addition with 250–500 mg/kg (p < 0.05).

3.4. Non-Specific Immune Enzyme Activity

As shown in Figure 2, the LZM and AKP activity was increased in all groups when compared with the control, while the CGA 0.5% and CGA 1.5% groups presented higher ACP activity than the control group (p < 0.05). Moreover, the SOD activity of the liver was significantly augmented in the 0.50% CGA group (p < 0.05).

4. Discussion

In the present study, CGA supplementation (0.50%, 1.00%, 1.50% expressed as 250 mg/kg, 500 mg/kg, 750 mg/kg) markedly altered the growth performance of M. albus (Table 1). Similarly, Zhao et al. [22] reported that the addition of 600 mg/kg CGA for 42 days significantly promoted the growth performance of rainbow trout. Moreover, 60 days of continuous supplementation with 200 mg/kg CGA also markedly affected the growth performance of crucian carp [13]. The mechanism might be that the CGA-induced improvement in lipase activity positively affected the height and density of intestinal villi, which would benefit the body’s full absorption of nutrients [23]. However, other studies reported that dietary supplementation with CGA did not affect the growth performance of grass carp [12], white shrimp [16], and koi [17]. This might reflect the differing requirements of animals at different developmental stages and the CGA dosage. The results of the present study showed that the growth performance of M. albus supplemented with 250 mg/kg and 750 mg/kg of CGA was not as good as that of M. albus supplemented with 500 mg/kg of CGA. Comparing the results for SR, WGR, and SGR, CGA at 500 mg/kg corresponding to 405 mg/kg would produce the optimal growth performance of M. albus.
In addition, the use of carrier-bait organisms for fish feeding was relatively rarely reported in this study. This is mainly because M. albus do not eat complementary pelleted feed before “open-mouth” at present, and can only be domesticated in stages by live baits such as yellow mealworms, earthworms, black gadflies, and fly maggots during the actual feeding process [21]. Moreover, the active components of the carrier bait will not be inactivated by the high temperature during the processing of pellet feed and the active ingredients will not dissolve in the water during the feeding process. At present, M. albus are mainly fed with bait during the domestication stage in practice, and the present experimental design simulates the feeding method in the actual production of M. albus, so the results of the experiment are more instructive for actual production.
Determining blood physiological and biochemical indexes has been proven to be an effective and repeatable method to monitor fish health. As a powerful tool in aquaculture research, it has become a reliable and accurate method to monitor fish growth [24]. Herein, the HGB content and PCT of M. albus increased significantly in experimental groups (Table 2). Similarly, in a toxicological study of mice, continuous supplementation of 60 mg/kg CGA for 21 days reversed the anemia caused by 4-tert-octylphenol [25]. In addition, the administration of CGA to injured mice accelerated wound healing [26]. The main function of HGB is to transport and store oxygen. However, it also has the functions of adjusting pH value, controlling the carbon monoxide level, and participating in the immune response [27]. Platelets are the main cellular mediators of hemostasis and have vital functions in immune and inflammatory reactions [28]. Our findings indicated that CGA supplementation in diet is beneficial for M. albus to take in oxygen, making it easier for it to survive in a low-dissolved-oxygen environment, and thus improving its antistress ability. By contrast, CGA supplementation is beneficial to meet the needs of various physiological and metabolic activities for blood oxygen. During the predatory behavior of M. albus, they can easily bite each other; therefore, adding an appropriate amount of CGA to the feed might effectively stop bleeding and improve the SR. We also showed that CGA supplementation altered the lipid metabolism of M. albus, manifesting as reduced serum TG and LDL levels, and increased HDL contents. Our results were consistent with those reported for grass carp [12] and mice [29]. However, the addition of CGA with 500 and 750 mg/kg led to an increased CHO content, which was different from the results of Yin et al. [15], who supplemented CGA at 300 and 600 mg/kg in largemouth bass fed with a high-fat diet. The different results might be due to species differences and the different dietary formulas. For fish life activities, the most direct energy source is glucose. Research evidence shows that CGA might affect glucose metabolism in hereditary metabolic diseases and decrease organ damage by decreasing the blood glucose concentration [30,31]. Our results also confirmed that dietary CGA supplementation reduced the contents of GLU and GSP. This is because CGA inhibits glucose release by blocking glucose-6-phosphatase activity in the liver and glucose absorption in the small intestine by blocking glucose-6-phosphate transferase 1 [6].
In addition, dietary CGA supplementation could improve the antioxidant activity of M. albus, with higher GSH-PX and CAT contents and decreased MDA activity, and the T-AOC level was improved significantly in response to CGA at 500 mg/kg. The activity of antioxidant enzymes is an important indicator of oxidative stress in fish [32], and a change of enzyme activity usually indicates oxidative stress, cell damage, and susceptibility to diseases [33]. Xu et al. [17] reported that dietary supplementation with CGA at 200–800 mg/kg could improve the antioxidant capacity of koi. Zhang et al. [34] also showed that supplementation with 200–600 mg/kg of CGA in the diet of catfish increased the T-AOC and GSH-PX activity, and reduced the MDA level. MDA is a by-product of lipid peroxidation caused by excessive free radicals (ROS) in cells, which have strong biological toxicity [35]. Previous studies have demonstrated activation of the NFE2 like BZIP transcription factor 2 (Nrf2) signaling pathway in response to CGA, which led to reduced ROS levels and performed an antioxidant role [36]. Moreover, there are five phenolic hydroxyl groups and one carboxyl group in the molecular structure of CGA. The phenolic hydroxyl groups readily react with free radicals to form antioxidant hydrogen free radicals [37], which further demonstrates the strong antioxidant ability of CGA. A comprehensive comparison of antioxidant indexes showed that 500 mg/kg CGA supplementation in the diet had the strongest antioxidant capacity.
Herein, dietary supplementation of CGA increased the activity of AKP and LZM and the levels of SOD and ACP in M. albus. Similarly, dietary CGA also increased the SOD, ACP, and AKP levels of crucian carp [13]. Organismal immunity is closely linked to SOD activity [38], and various phosphate groups are hydrolyzed by ACP and ALP, which are considered important indicators to evaluate the immune status of aquatic animals [39]. In addition, CGA dietary addition at 200–800 mg/kg improved the LZM activity of koi [17]. LZM is an alkaline enzyme that hydrolyzes and cleaves mucopolysaccharides in pathogenic bacteria, resulting in their release, thereby eliminating invasive foreign bodies [40]. As a non-specific immune factor, LZM participates in various immune responses [41]. The above results showed that CGA could enhance immunity, likely via its antioxidant capacity [42], which is also consistent with our results on the antioxidant activity of CGA. Besides, CGA interrupts the early signal cascade related to myeloid differentiation primary response 88 (MyD88) and directly inhibits the kinase activity of interleukin 1 receptor associated kinase 4 (IRAK4) or IRAK1, thus inhibiting the activation of nuclear factor kappa B (NF-κB) or activator protein 1 (AP-1) and improving non-specific immunity [43].

5. Conclusions

In conclusion, supplementation with CGA can enhance the growth performance and improve the lipid metabolism, antioxidant capacity, and non-specific immunity of M. albus during the domestication stage, and the optimal CGA supplementation for yellow mealworms as biocarrier bait is 500 mg/kg, corresponding to 405 mg/kg.

Author Contributions

Conceptualization, Q.Y.; methodology, W.L.; software, J.Q.; validation, W.L.; formal analysis, H.Y. and W.L.; investigation, H.Y.; resources, M.L.; data curation, Q.Y.; writing—original draft, H.Y. and C.W.; writing—review and editing, H.Y.; visualization, J.Q. and M.L.; supervision, W.Z. and Q.Z.; project administration, W.Z. and Q.Z.; funding acquisition, W.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Shanghai Municipal Agricultural Commission [2024-02-08-00-12-F00003]; the China Agriculture Research System of MOF and MARA (CARS-46); the Science and Technology Innovation Action Plan project of the Shanghai Municipal Commission of Science and Technology (No. 22YF1416600); and the Science and Technology Commission of Shanghai Municipality (22DZ2291200).

Institutional Review Board Statement

The ethical approval research scheme was approved by the Animal Care and Use Committee of the Shanghai Academy of Agricultural Sciences (Approval Code: SAASXM0524018; Approval Date: January 2024–December 2027).

Data Availability Statement

The datasets generated for this study are available on request to the corresponding authors.

Conflicts of Interest

The authors declare no conflicts of interest.

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Fishes 09 00496 g001
Figure 1. Antioxidant enzyme activity of M. albus liver in the different experimental groups. Different letters represent significant differences at p < 0.05; the same or no letter represents no significant difference (p > 0.05). Abbreviations: total antioxidant capacity (T-AOC), malondialdehyde (MDA), glutathione peroxidase (GSH-PX), catalase (CAT).
Figure 1. Antioxidant enzyme activity of M. albus liver in the different experimental groups. Different letters represent significant differences at p < 0.05; the same or no letter represents no significant difference (p > 0.05). Abbreviations: total antioxidant capacity (T-AOC), malondialdehyde (MDA), glutathione peroxidase (GSH-PX), catalase (CAT).
Fishes 09 00496 g001
Fishes 09 00496 g002
Figure 2. Non-specific immune enzyme activity of M. albus liver in the different experimental groups. Different letters represent significant differences at p < 0.05; the same or no letter represents no significant difference (p > 0.05). Abbreviations: superoxide dismutase (SOD), lysozyme (LZM), alkaline phosphatase (AKP), acid phosphatase (ACP).
Figure 2. Non-specific immune enzyme activity of M. albus liver in the different experimental groups. Different letters represent significant differences at p < 0.05; the same or no letter represents no significant difference (p > 0.05). Abbreviations: superoxide dismutase (SOD), lysozyme (LZM), alkaline phosphatase (AKP), acid phosphatase (ACP).
Fishes 09 00496 g002
Table 1. Effects of dietary CGA on the growth performance of M. albus.
Table 1. Effects of dietary CGA on the growth performance of M. albus.
ItemCont.0.50%1.00%1.50%
Initial weight (g)25.43 ± 0.3925.64 ± 0.3325.21 ± 0.2825.26 ± 0.24
Final weight (g)33.65 ± 0.79 c37.03 ± 0.84 b42.59 ± 0.95 a35.71 ± 0.87 b
WG (%)32.31 ± 1.58 c44.42 ± 4.40 b68.94 ± 2.36 a41.38 ± 3.38 b
SGR (%)0.86 ± 0.04 c1.23 ± 0.10 b1.88 ± 0.13 a0.88 ± 0.12 c
SR (%)96.13 ± 0.01 b97.77 ± 0.01 ab98.87 ± 0.01 a90.57 ± 0.02 c
The means in the same column with different superscript letters are significantly different (p < 0.05). Abbreviations: survival rate (SR), weight-gain rate (WG), specific growth rate (SGR).
Table 2. Effects of dietary CGA on whole blood indexes of M. albus.
Table 2. Effects of dietary CGA on whole blood indexes of M. albus.
ItemCont.0.50%1.00%1.50%
WBC (109/L)167.40 ± 17.18171.70 ± 14.24194.90 ± 19.63196.30 ± 23.21
RBC (1012/L)1.50 ± 0.321.28 ± 0.331.82 ± 0.251.71 ± 0.43
HGB (g/L)134.00 ± 28.48 b150.30 ± 19.34 a193.60 ± 22.03 a170.30 ± 33.86 a
HCT (%)25.03 ± 4.7122.93 ± 5.2832.50 ± 3.8429.43 ± 4.65
MCV (fL)168.10 ± 17.16180.30 ± 9.61179.30 ± 5.12175.10 ± 17.96
RDW (%)17.07 ± 4.2521.87 ± 13.4212.03 ± 0.6821.00 ± 13.86
PDW19.36 ± 0.4919.56 ± 0.1519.50 ± 0.4419.73 ± 0.32
PCT (‰)0.29 ± 0.01 a0.37 ± 0.08 b0.33 ± 0.03 b0.27 ± 0.06 a
The means in the same column with different superscript letters are significantly different (p < 0.05). Abbreviations: white blood cells (WBC), red blood cells (RBC), hemoglobin (HGB), hematocrit (HCT), mean corpuscular volume (MCV), red blood cell distribution width coefficient of variation (RDW), platelet distribution width (PDW), and platelet crit (PCT).
Table 3. Effects of dietary CGA on lipid metabolism of M. albus.
Table 3. Effects of dietary CGA on lipid metabolism of M. albus.
ItemCont.0.50%1.00%1.50%
TG (mmol/L)2.53 ± 0.35 a1.31 ± 0.08 b1.42 ± 0.19 b1.54 ± 0.33 b
CHO (mmol/L)3.23 ± 0.35 b3.71 ± 0.29 b4.93 ± 0.48 a5.40 ± 0.22 a
HDL (mmol/L)0.58 ± 0.09 d1.15 ± 0.07 c1.59 ± 0.03 b1.99 ± 0.01 a
LDL (mmol/L)1.56 ± 0.54 a0.67 ± 0.09 b0.72 ± 0.35 b0.68 ± 0.23 b
GLU (mmol/L)5.62 ± 0.31 a2.35 ± 0.33 d3.77 ± 0.14 c4.50 ± 0.42 b
GSP (mmol/L)2.08 ± 0.10 a0.96 ± 0.02 d1.10 ± 0.05 c1.43 ± 0.08 b
The means in the same column with different superscript letters are significantly different (p < 0.05). Abbreviations: triglycerides (TG), cholesterol (CHO), high-density lipoprotein (HDL), low-density lipoprotein (LDL), glucose (GLU), and glycosylated serum protein (GSP).
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Yang, H.; Wu, C.; Yuan, Q.; Lv, W.; Qiu, J.; Li, M.; Zhang, Q.; Zhou, W. Effects of Dietary Chlorogenic Acid on the Growth, Lipid Metabolism, Antioxidant Capacity, and Non-Specific Immunity of Asian Swamp Eel (Monopterus albus). Fishes 2024, 9, 496. https://doi.org/10.3390/fishes9120496

AMA Style

Yang H, Wu C, Yuan Q, Lv W, Qiu J, Li M, Zhang Q, Zhou W. Effects of Dietary Chlorogenic Acid on the Growth, Lipid Metabolism, Antioxidant Capacity, and Non-Specific Immunity of Asian Swamp Eel (Monopterus albus). Fishes. 2024; 9(12):496. https://doi.org/10.3390/fishes9120496

Chicago/Turabian Style

Yang, Hang, Chengcheng Wu, Quan Yuan, Weiwei Lv, Junqiang Qiu, Mingyou Li, Qinghua Zhang, and Wenzong Zhou. 2024. "Effects of Dietary Chlorogenic Acid on the Growth, Lipid Metabolism, Antioxidant Capacity, and Non-Specific Immunity of Asian Swamp Eel (Monopterus albus)" Fishes 9, no. 12: 496. https://doi.org/10.3390/fishes9120496

APA Style

Yang, H., Wu, C., Yuan, Q., Lv, W., Qiu, J., Li, M., Zhang, Q., & Zhou, W. (2024). Effects of Dietary Chlorogenic Acid on the Growth, Lipid Metabolism, Antioxidant Capacity, and Non-Specific Immunity of Asian Swamp Eel (Monopterus albus). Fishes, 9(12), 496. https://doi.org/10.3390/fishes9120496

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