Dietary microencapsulated oil improves immune function and intestinal health in Nile tilapia fed with high-fat diet
Introduction
Dietary fat is important because it provides energy and essential fatty acids for growth and development in fish (Watanabe, 1982). Because of the price of the protein sources that are superior to lipid sources, high-fat diet (HFD) has been commonly used in aquafeed industry to promote “protein sparing effects”. A number of studies had indicated that increasing dietary fat content within proper range could increase growth, feed efficiency, protein deposition and reduce production costs in several fish species, such as juvenile hybrid tilapia (Chou and Shiau, 1996) and hybrid snakehead (Zhang et al., 2017).
However, HFD also causes many negative effects. HFD is easy to be oxidized during storage, especially when the HFD contains the high amount of unsaturated fatty acids. It has been commonly known that oxidized oil is very toxic for fish (Gao et al., 2012; Moccia et al., 2010). Moreover, long-term feeding of HFD in fish would impair the energy homeostasis and cause severe fat deposition in the body, dyslipidemia and even destroy the normal structure and functions of cellular organelles (Du et al., 2006; Lu et al., 2013; Sagada et al., 2017). Additionally, the HFD diet would also impair fish immunity and anti-oxidative system. In turbot, HFD led to decreased catalase and superoxide dismutase activities, leucocytes amount of head kidney, respiratory burst activity in head kidney macrophage, phagocytic index, serum lysozyme activity and increased hepatic malondialdehyde level (Jia et al., 2017). Similar results were also found in blunt snout bream (Chen et al., 2016) and juvenile common carp (Sabzi et al., 2017). Recently, some studies also showed that HFD could also impair gut health by impairing intestinal structures and normal microbiota (Falcinelli et al., 2017; Yu et al., 2016). Therefore, it is very important to find efficient solutions to improve fish health during HFD feeding.
The microencapsulation technique, including oil microencapsulation, has been widely applied to the food industry. By using different wall materials (proteins and/or carbohydrate) and spray drying, small oil droplets are transformed into small dry fat granules that have powder-like flow characteristics (Wan et al., 2011). Currently, microencapsulated fish oil or linseed oil which contains high level polyunsaturated fatty acids (PUFAs) is commonly applied in food and medical products (Goyal et al., 2015; Higgins et al., 1999; Polavarapu et al., 2011). There are also other microencapsulated oils, such as palm oil, kenaf seed oil and walnut oil in food industries (Calvo et al., 2011; Ng et al., 2014; Rutz et al., 2017). Compared with liquid oils, the fat powder has many positive benefits, such as oxygen-isolation, extended shelf life, masking the unpleasant odor, improving taste, high nutritional density and nutritional availability, easy to transport and store (Wan et al., 2011). So far, the dietary microencapsulated blends of organic acids and essential oils have been successfully applied in land animals. It improved growth performance and increase fecal Lactobacillus, which is beneficial for gut health, in chicken (Gheisar et al., 2015), and improve growth and nutrient digestibility while decreasing fecal scores and pH in weanling pigs (Cho and Kim, 2015). However, in the aquaculture industry, only microencapsulated sodium butyrate (MSB) was reported to repair or prevent intestinal damage in juvenile common carp fed oxidized soybean oil (Liu et al., 2014) and improved growth and immune function in young grass carp (Tian et al., 2017). The comparison between the dietary supplemental effects of microencapsulated powder oil and common liquid oil in fish has not been carefully evaluated. Here, we hypothesized that dietary microencapsulated powder oil could have more benefits than common liquid oil in fish.
Tilapia is the second most farmed economic fish group over the world and the lipid content of tilapia feed keeps increasing trend in recent years (Ng and Romano, 2013). Our previous studies had shown that HFD (13% fat) could cause severe lipid accumulation and oxidative damage in Nile tilapia, as compared with low-fat diet (1% fat) and medium fat diet (7% fat) (He et al., 2015; Ning et al., 2017). Therefore, in order to evaluate the potential beneficial effects of microencapsulated oil in Nile tilapia, we used HFD in the present study. The HFD containing 15% of normal oil mixture or microencapsulated oil mixture was fed to juvenile Nile tilapia for 8 weeks. To further compare the effects between different microencapsulated oils with different fatty acid composition, two oil mixtures (PL: 60% palm oil +40% linseed oil; FL: 60% fish oil +40% linseed oil) were used. After feeding trial, the growth, body composition, resistance to pathogenic bacteria challenge, activities of immune enzymes and expressions of the genes related to inflammation were measured. The structure and junction protein of the intestine, and the intestinal microbiota status were also assayed.
Section snippets
Ethics
All experiments were conducted under the Guidance of the Care and Use of Laboratory Animals in China. This research was approved by the Committee on the Ethics of Animal Experiments of East China Normal University.
Experimental fish and diets
Experimental juvenile Nile tilapias were bought from the Aquaculture Genetics and Breeding Technology center at Shanghai Ocean University (Shanghai, China). All fish were fed a commercial diet (protein 50%, fat 8%, fiber 3%, ash 16%, moisture 12%, Ca 5%, P 1%, lysine 2%) for three
Fatty acid composition in common and microencapsulated oils and diets
The fatty acid composition of oils and diets are listed in Table 2 and Table 3, respectively. The results showed that the microencapsulation process didn't affect the fatty acid composition of PL oils (PLM vs PLC). However, in the FLM oil and FLM feeds, the percentages of C8:0, C12:0 and C20:3 were increased, and the percentages of C16:1 were decreased, as compared with FLC oil and FLC feed. Moreover, the n-3 PUFAs in FL oils were higher than those in PL oils.
Microencapsulated oil did not change growth and body composition but reduced visceral, mesenteric fat and spleen weight of the HFD-fed Nile tilapia
Dietary addition of
Microencapsulated oil has beneficial effects on metabolic regulation
Although microencapsulated sodium butyrate (MSB) had been reported to have beneficial effects in some aquatic animals (Liu et al., 2014; Tian et al., 2017), the application of microencapsulated oils, which are composed mainly by long-chain fatty acids (with no <16 carbons), has not been commonly used yet in aquaculture. Oil oxidation is a serious problem in the production and storage of aquatic feed, especially in the high-fat diet or the diet containing high levels of unsaturated fatty acids.
Conclusion
The usage of dietary microencapsulated oils in the Nile tilapia fed with HFD could reduce mesenteric fat, visceral mass, oxidative stress, inflammation and liver injury. It also promoted immune functions, mostly through improving intestinal health, including improving the intestinal structure and the positive changes of intestinal microflora. Between two oils, microencapsulated PL oil revealed better beneficial effects than the microencapsulated FL oil. Compared with common PL oil,
Acknowledgments
This study was funded by the National Basic Research Program of China (973 program 2014CB138603).
References (66)
- et al.
Probiotics and prebiotics associated with aquaculture: a review
Fish Shellfish Immunol.
(2015) - et al.
Bioequivalence of encapsulated and microencapsulated fish-oil supplementation
J. Funct. Foods
(2009) - et al.
Immune response of cows fed polyunsaturated fatty acids under high ambient temperatures
J. Dairy Sci.
(2009) - et al.
Effects of berberine on the growth and immune performance in response to ammonia stress and high-fat dietary in blunt snout bream Megalobrama amblycephala
Fish Shellfish Immunol.
(2016) - et al.
Dietary nucleotides influence immune responses and intestinal morphology of red drum Sciaenops ocellatus
Fish Shellfish Immunol.
(2011) - et al.
Optimal dietary lipid level for growth of juvenile hybrid tilapia, Oreochromis niloticus, X Oreochromis aureus
Aquaculture
(1996) - et al.
Effects of dietary oxidized fish oil with vitamin E supplementation on growth performance and reduction of lipid peroxidation in tissues and blood of red sea bream Pagrus major
Aquaculture
(2012) - et al.
Development and physico-chemical characterization of microencapsulated flaxseed oil powder: a functional ingredient for omega-3 fortification
Powder Technol.
(2015) - et al.
Paenibacillus polymyxa as a water additive improved immune response of Cyprinus carpio and disease resistance against Aeromonas hydrophila
Aquac. Rep.
(2016) - et al.
Dietary saturated fats and their food sources in relation to the risk of coronary heart disease in women
Am. J. Clin. Nutr.
(1999)
Ameliorative effect of vitamin E on hepatic oxidative stress and hypoimmunity induced by high-fat diet in turbot (Scophthalmus maximus)
Fish Shellfish Immunol.
Fatty acid profile and sensory characteristics of table eggs from laying hens fed diets containing microencapsulated fish oil
Anim. Feed Sci. Tech.
Dietary administration of Bacillus subtilis HAINUP40 enhances growth, digestive enzyme activities, innate immune responses and disease resistance of tilapia, Oreochromis niloticus
Fish Shellfish Immunol.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method
Methods
Hepatic triacylglycerol secretion, lipid transport and tissue lipid uptake in blunt snout bream (Megalobrama amblycephala) fed high-fat diet
Aquaculture
Probiotics and immunity: a fish perspective
Fish Shellfish Immunol.
Effect of total solids content in feed emulsion on the physical properties and oxidative stability of microencapsulated kenaf seed oil
LWT-Food Sci. Technol.
Inhibited fatty acid beta-oxidation impairs stress resistance ability in Nile tilapia (Oreochromis niloticus)
Fish Shellfish Immunol.
Physicochemical characterisation and oxidative stability of fish oil and fish oil–extra virgin olive oil microencapsulated by sugar beet pectin
Food Chem.
Occurrence and virulence of Pseudoalteromonas spp. in cultured gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). Molecular and phenotypic characterisation of P. undina strain U58
Aquaculture
Microencapsulation of palm oil by complex coacervation for application in food systems
Food Chem.
Effect of dietary l -carnitine and lipid levels on growth performance, blood biochemical parameters and antioxidant status in juvenile common carp (Cyprinus carpio)
Aquaculture
Optimizing protein and lipid levels in practical diet for juvenile northern snakehead fish (Channa argus)
Anim. Nutr.
Sodium butyrate improved intestinal immune function associated with NF-κB and p38MAPK signalling pathways in young grass carp (Ctenopharyngodon idella)
Fish Shellfish Immunol.
Physical and nutritional properties of baby food containing menhaden oil (Brevoortia tyrannus) and microencapsulated menhaden oil
LWT-Food Sci. Technol.
Lipid nutrition in fish
Comp. Biochem. Physiol. B: Comp. Biochem.
Dietary tryptophan modulates intestinal immune response, barrier function, antioxidant status and gene expression of TOR and Nrf2 in young grass carp (Ctenopharyngodon idella)
Fish Shellfish Immunol.
Effects of dietary protein and lipid levels on growth, body and plasma biochemical composition and selective gene expression in liver of hybrid snakehead (Channa maculata ♀×Channa argus ♂) fingerlings
Aquaculture
Effects of Bacillus subtilis on the growth performance, digestive enzymes, immune gene expression and disease resistance of white shrimp, Litopenaeus vannamei
Fish Shellfish Immunol.
Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obese mice
Food Chem.
N-3PUFA Differentially Modulate Palmitate-Induced Lipotoxicity through Alterations of its Metabolism in C2C12 Muscle Cells
Intestinal passage of microencapsulated fish oil in rats following oral administration
Food Funct.
Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta)
Br. J. Nutr.
Cited by (58)
Iron homeostasis of liver-gut axis alleviates inflammation caused by dietary cottonseed meal through dietary Fe<sup>2+</sup> supplementation in juvenile grass carp (Ctenopharyngodon idellus)
2022, AquacultureCitation Excerpt :Substantially improved fish growth performance and hepatic antioxidant capacity are powerful responses extremely pertinent to intestinal health and growth (Dawood, 2020; Jiang et al., 2015). Intestinal damage could impair nutrient absorption from ingested food and increase the risk of infections (Ma et al., 2018; Sitja-Bobadilla et al., 2016). Previous studies (e.g., Wei et al., 2020; Su et al., 2018) have demonstrated how certain indicators, such as IL, IW, ILI, and ISI, could reliably convey the intestinal growth in fish.