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Galactooligosaccharide and a Combination Of Galactooligosaccharide and a combination of yeast and β-glucan supplements enhance growth and improve intestinal condition in striped catfish Pangasianodon hypophthalmus fed soybean meal diets Amalia Sutriana, Roshada Hashim, Mst. Nahid Akter & Siti Azizah Mohd Nor Fisheries Science ISSN 0919-9268 Volume 84 Number 3 Fish Sci (2018) 84:523-533 DOI 10.1007/s12562-018-1195-4 1 23 Your article is protected by copyright and all rights are held exclusively by Japanese Society of Fisheries Science. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Fisheries Science (2018) 84:523–533 https://doi.org/10.1007/s12562-018-1195-4 ORIGINAL ARTICLE Aquaculture Galactooligosaccharide and a combination of yeast and β‑glucan supplements enhance growth and improve intestinal condition in striped catfsh Pangasianodon hypophthalmus fed soybean meal diets Amalia Sutriana1 · Roshada Hashim2 · Mst. Nahid Akter3 · Siti Azizah Mohd Nor4 Received: 3 August 2017 / Accepted: 14 February 2018 / Published online: 14 March 2018 © Japanese Society of Fisheries Science 2018 Abstract The efects of galactooligosaccharide (GOS) and a combination of yeast and β-glucan (YβG) supplementation of dietary soybean meal (SBM) on the growth and digestive performance of striped catfsh Pangasianodon hypophthalmus were evalu- ated. Four isonitrogenous (30% protein) and isocaloric (19 MJ/kg diet) diets were formulated to contain 100% fsh meal (FM) protein, 55% FM protein/45% SBM protein, FM-SBM supplemented with 1% GOS, and a combination of 1% yeast and 0.1% β-glucan, respectively. Each diet was fed for 12 weeks to three groups of 30 striped catfsh fngerlings (average weight 16.45 ± 0.07 g) maintained in circular fberglass tanks (600 l). Growth, feed utilization, and muscle protein composi- tion of fsh improved signifcantly after supplementation with either GOS or YβG compared to the unsupplemented SBM diet, but were similar to those of fsh fed the FM diet. Nutrient digestibility, digestive enzyme activities, villi and microvilli length were signifcantly increased in fsh fed the supplemented SBM diets. The gut microbiota ranking profle showed that supplementing the SBM diet with YβG and GOS gave a ranking of Verrucomicrobia, Spirochaetes, Bacteriodetes, and Act- inobacteria phyla similar to that of the FM diet. Thus, diet containing 45% protein from soybean supplemented with either GOS or YβG can be recommended to improve the growth and digestive performance of striped catfsh. Keywords Fish performance · Nutrient digestibility · Digestive enzyme · Villi · Gut microbiota Introduction competitive price compared to fsh meal (FM) (Biswas et al. 2007). However, the use of high levels of SBM in the diet For decades, soybean meal (SBM) has been used as an can cause a reduction in growth and feed utilization in rain- alternative plant protein source in the fsh farming indus- bow trout (Oliva-Teles et al. 1994), Atlantic salmon (Ref- try because of its high protein content, comparatively well- stie et al. 1998), and striped catfsh (Phumee et al. 2011), balanced amino acid profle, relative ease of availability, and as well as morphological and functional disruption, such as enteritis, increased susceptibility to bacterial infection, * Amalia Sutriana changes in absorptive cells, presence of infammatory cells, [email protected] and shortening of the villi and microvilli in the intestines of Atlantic salmon (van den Ingh et al. 1991; Baeverford and 1 Faculty of Veterinary Medicine, Syiah Kuala University, Krogdahl 1996; Bakke-McKellep et al. 2000), rainbow trout Banda Aceh, Aceh 23111, Indonesia (Rumsey et al. 1994) and common carp (Uran et al. 2008). 2 Faculty of Science and Technology, Universiti Sains Islam There is also evidence of a decrease in digestive enzyme Malaysia, 71800 Bandar Baru Nilai, Negeri Sembilan, Malaysia activities in the distal intestinal epithelial cell brush bor- ders as reported in Atlantic salmon fed a SBM-containing 3 Faculty of Fisheries, Hajee Mohammad Danesh Science and Technology University, Dinajpur 5200, Bangladesh diet, which was attributed to histopathological changes in the intestine (Bakke-McKellep et al. 2000; Krogdahl et al. 4 Institute of Marine Biotechnology, Universiti Malaysia Terengganu, 21300 Kuala Terengganu, Terengganu, Malaysia 2003). Additionally, SBM proteins are mainly compact and Vol.:(0123456789)1 3 Author's personal copy 524 Fisheries Science (2018) 84:523–533 globular (glycinin and β-conglycinin) making hydrolysis and Table 1 Ingredients and proximate composition (g/kg dry matter) of absorption slower than those of FM protein (Yamamoto et al. the experimental diets 1998); these characteristics of SBM proteins potentially Experimental diets reduce their digestibility in fsh. FM FM-SBM FM-SBM- FM-SBM-YβG In recent years, considerable attention has been paid to GOS the use of non-nutrient dietary components such as probi- Ingredients otics and prebiotics to mitigate the negative efects of the a SBM diet. Several studies have shown that prebiotic supple- FM 382.50 211.00 211.00 211.00 ments can signifcantly improve the nutritive value of SBM. Soybean – 267.00 267.00 267.00 meal For example, they protect the intestinal mucosa and reduce Corn starch 430.00 324.70 324.70 324.70 the risk of induced morphological changes in salmon gut Fish oil 28.70 43.70 43.70 43.70 (Dimitroglou et al. 2011); increase protein, organic matter, Soybean oil 58.80 53.60 53.60 53.60 and energy availability in red drum (Burr et al. 2008); and Cellulose 20.00 20.00 10.00 9.00 improve feed efciency in hybrid striped bass (Li and Gatlin GOS – – 10.00 – 2005) and red drum (Buentello et al. 2010) because of the Yeast – – – 10.00 upregulation of the activities of specifc digestive enzymes β-Glucan – – – 1.00 (Buentello et al. 2010). All these efects are a consequence CMC 30.00 30.00 30.00 30.00 of the benefcial modulation of the populations of good bac- b Vitamins 20.00 20.00 20.00 20.00 teria in the fsh intestine. c Minerals 20.00 20.00 20.00 20.00 Preliminary studies using probiotics and prebiotics, sin- Cr2O3 10.00 10.00 10.00 10.00 gly and in combination, in diets containing FM as the sole Proximate composition (g/kg) protein source, indicate that the prebiotic galactooligosac- Moisture 80.30 82.40 79.60 86.90 charide (GOS) and the combination of yeast and β-glucan Protein 306.20 309.60 313.00 305.80 (YβG) positively infuence growth performance and feed uti- Lipid 129.20 117.10 125.60 121.30 lization of striped catfsh (Sutriana 2017). Based on the fact Ash 80.20 89.40 79.60 81.70 that these supplements are able to improve nutrient digest- Fibre 24.10 42.20 49.60 49.00 ibility and gut microfora, the present study was designed to NFEd 460.30 441.70 432.20 442.20 investigate the infuence of GOS and yeast combined with GEe (MJ/kg) 19.02 18.91 19.68 19.43 β-glucan on growth, digestibility, intestinal morphology, and microbiota in striped catfsh, Pangasianodon hypophthalmus FM Fish meal, SBM soybean meal, GOS galactooligosaccharide, YβG fngerlings fed a diet containing SBM. As far as we know, yeast and β-glucan, CMC carboxymethyl cellulose, NFE nitrogen-free extract, GE gross energy this is the frst efort to evaluate the efect of GOS and YβG a Danish fsh meal supplementation to improve the nutritive value of SBM diet b Vitamin (Vit.) mix/kg (Rovitai, Chonburi, Thailand): Vit. A, 50 mil- in striped catfsh. lion international units (IU); Vit. D3, 10 million IU; Vit. E, 130 g; Vit. B1, 10 g; Vit. B2, 25 g; Vit. B6, 16 g; Vit. B12, 100 mg; biotin, 500 mg; pantothenic acid, 56 g; folic acid, 8 g; niacin, 200 g; anticak- Materials and methods ing agent, 20 g; antioxidant, 200 mg, Vit. K3, 10 g; Vit. C, 35 g c Mineral mix/kg: calcium phosphate (monobasic), 397.65 g; cal- Diet formulation and feeding cium lactate, 327 g; ferrous sulfate, 25 g; magnesium sulfate, 137 g; potassium chloride, 50 g; sodium chloride, 60 g; potassium iodide, 150 mg; copper sulfate, 780 mg; manganese oxide, 800 mg; cobalt Four diets were prepared containing 30% protein and 12% carbonate, 100 mg; zinc oxide, 1.5 g; sodium selenite, 20 mg lipid with a gross energy content of 19 MJ/kg (Table 1). d [100 − (protein + lipid + ash + fber)] The control diet contained 100% protein from FM and the e Measured using a Parr 6200 bomb calorimeter remaining three diets were formulated so that 45% of the protein was provided by SBM and 55% from FM (FM- SBM). Two of the latter diets were supplemented with 1% The ingredients were mixed thoroughly in a feed mixer GOS (FM-SBM-GOS) and a combination of 1% yeast and (model TR 202; Tyrone, UK); 1% chromium oxide was 0.1% β-glucan (FM-SBM-YβG), respectively. The replace- added as an inert marker for protein and dry matter digest- ment of 45% protein with SBM was based on the report by ibility determination. Distilled water was added, and the Phumee et al. (2011), who showed that inclusion of SBM moist dough was passed through a 3-mm die using a meat protein beyond 30% compromised fnal weight, specifc grinder (model MH 237; Miao Hsien, Taiwan).
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