Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromisniloticus

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Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus Mohamed S. Hassaan a,∗ , Magdy A. Soltan b , Ahmed M. Abdel-Moez c a b c

Fish Nutrition Research Laboratory, National Institute of Oceanography and Fisheries (NIOF), Egypt Animal Production Department, Faculty of Agriculture, Benha University, Egypt General Authority for Fish Resources Development, Ministry of Agriculture, Cairo, Egypt

a r t i c l e

i n f o

Article history: Received 12 February 2014 Received in revised form 7 January 2015 Accepted 9 January 2015 Available online xxx Keywords: Replacement Solid state fermentation Soybean meal Nile tilapia

a b s t r a c t Commercial soybean meal (CSBM) was fermented with Saccharomyces cerevisiae using the solid-state fermentation (SSF). Yeast fermentation increased the protein content of CSBM by 13.65%, increased the total of hydrolyzed amino acids by 16.27% and decreased phytic acid and tripsin inhibitor. A feeding trial was conducted to investigate the effect of yeast fermented soybean meal (YFSBM) on the growth, feed utilization, hematological and biochemical blood parameters of Nile tilapia Oreochromis niloticus. Five isonitrogenous (295 g/kg crude protein and isocaloric 19.5 MJ/kg gross energy) practical diets were formulated by replacing 0% (D-0), 25% (D-50), 75% (D-75) and 100% (D-100) of protein from fish meal with YFSBM. Each diet was fed to three replicate groups of fish with an initial weight 3.49 ± 0.09 g for 84 days. Using polynomial regression the best final body weight (FBW), weight gain (WG), specific growth rate (SGR), protein efficiency ratio (PER) and protein productive value (PPV) were recorded by fish fed D-25. Based on FCR, broken-line model estimated the optimum level of YFSBM to replace FM is at 37.4%. The best apparent digestibility coefficients (ADCs) were recorded by fish fed the D-25 followed by D-50 using a linear model. Best fit was obtained using a linear model for chemical composition. Body protein and ash contents tended to be higher and reached a plateau in fish fed D-25 and D-50. However, fit linear model showed that the lowest dry matter (DM), lipid and gross energy (GE) contents occurred at 0% replacement. Using linear regression analysis, non-significant effect of YFSBM inclusion level on Htc and Hb was found. The same pattern was observed in WBCs, RBCs, IGF-I, C3 and GH increased and ALT and AST decreased with D-25 and D-50, respectively and the best fit of the data were obtained using polynomial regressions. © 2015 Elsevier B.V. All rights reserved.

Abbreviations: ALT, alanine aminotransferase; ANFs, anti-nutritional factors; ADCs, apparent digestibility coefficients; AST, aspartate aminotransferase; CSBM, commercial soybean meal; DM, dry matter; DE, digestible energy; FBW, final body weight; FM, fish meal; GE, gross energy; GH, growth hormone; IGF-I, insulin-like growth factor-I; PER, protein efficiency ratio; PPV, protein productive value; RBCs, red blood cells; SGR, specific growth rate; SBM, soybean meals; SSF, solid-state fermentation; WBCs, white blood cells; YFSBM, yeast fermented soybean meal. ∗ Corresponding author. Tel.: +20 1229490090; fax: +20 227943226. E-mail address: Mohamed [email protected] (M.S. Hassaan). http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007 0377-8401/© 2015 Elsevier B.V. All rights reserved.

Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007

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1. Introduction Finding novel sustainable protein sources has become a major drive in the aquaculture sector in order to reduce dependency on fish meal (FM) as the main protein component in aqua feeds. The current fishmeal usage in aqua feeds is becoming unsustainable as aquaculture production continues to expand. Cost is also a major constraint to production with greater requirements for more strategic use of this commodity in feeds. This exacerbates pressures on wild fisheries which cannot be sustained to meet such demands. Traditionally, alternatives to protein meals have been sought from vegetable sources such as soybean meals and cottonseed meals due to their wide spread availability, relatively favorable amino acid profiles, reduced cost and sustainable nature (Hardy, 2010). However, the inclusion of plant based proteins in aquafeeds provides a number of problems which include the occurrence of anti-nutritional factors (ANFs), reduced digestibility, issues of palatability and limitations of certain essential amino acids (Oliva-Teles and Gonc¸alves, 2001). The ANFs in soybean meals (SBM) can cause pathomorphological changes in the distal intestine of fish (Yamamoto et al., 2010), that can reduce the absorptive capacity for nutrients (Nordrum et al., 2000). Heat-labile anti-nutritional factors like proteinase inhibitors and agglutinating lectins are largely deactivated by the toasting step when producing solvent extracted soybean meal (Maenz et al., 1999). However, several of the anti-nutritional factors are heat stable. Solid-state fermentation (SSF) is defined as any fermentation process performed on a non-soluble material that acts both as a physical support and a source of nutrients in the absence of free flowing liquid (Pandey, 2003). Solid-state fermentation has a long history of the production of traditional foods using different organisms. It was reported that in SSF, the production of metabolites, such as enzymes, antibiotics etc. were higher than that in the submerged fermentation (Hölker and Lenz, 2005). Techniques including heat treatment (Peres et al., 2003), and microbial fermentation (Liang et al., 2008) have been used to eliminate or reduce anti-nutritional factors. The fermentation of soybean was reported to be able to enhance nutrient digestibility and nutritional value, contributing important nutrients such as calcium and vitamin A (Kim et al., 1999). A little information is available on the effects of fermented soybean meal in fish feeds (Refstie et al., 2005). The nutritional value of a fermented soybean meal was regarded as a new protein resource, which has been improved after fermentation with mould and could lead to a reduction in trypsin inhibitor content and an increase in small-sized peptide concentration (Hong et al., 2004). However, little information is available on using this technique for fish feeds. Therefore, the aim of this study was to determine the effect of soybean meal fermented by Saccharomyces cerevisiae on anti-nutritional factors, nutritive values, growth performance, feed utilization, hematological and biochemical blood parameters of Nile tilapia, Oreochromis niloticus.

2. Materials and methods 2.1. Preparation of a yeast-fermented Soybean meal A commercially defatted soybean meal (CSBM) was purchased from a local company (Heliopolis-Cairo, Egypt) and ground to a particle size (<500 ␮m) by screen diameter. Three replicate fermentation were performed by a modification method of Yabaya et al. (2009). Each replicate, 2 kg CSBM, 60.5 mg of commercial dry yeast, S. cerevisiae, with a cell density of 3 × 106 cell/g (Fermipan®, GB ingredients, china) and 1.1 L of distilled water (50% moisture) was homogenized in a Hobart food mixer for 15 min. This provided a yeast density of 1 × 103 cell/g meal. Each replicate was conducted for 48 h in a 10 L glass jar covered with aluminum foil and incubated at 40 ◦ C which is the optimal growth temperature for S. cerevisiae. The yeast fermented soybean meal (YFSBM) was dried to constant weight at 70 ◦ C. In the beginning (0 h) and after 48 h of fermentation, 10 g of YFSBM were sampled to analyze the anti-nutritional factors and chemical composition. Crude protein lipids, ash and crude fiber were determined following the methods of the AOAC (1995) (Table 1).

Table 1 Chemical composition and anti-nutritional factors of commercial soybean meal and yeast fermented soybean meal. Items

CSBM*

YFSBM**

Crude protein (g/kg) Crude lipid (g/kg) Ash (g/kg) Crude fiber (g/kg) Nitrogen-free extracta (g/kg) Phytic acid (g/100 g) Trypsin inhibitor (IU/mg protein)

440 43 61 63 393 0.56 2080

500 48 71 32 349 0.04 1902

Data are presented as means (n = 3). * (CSBM) Commercial soybean meal. ** (YFSBM) Yeast fermented soybean meal. a Nitrogen-free extract = 100 − (crude protein + crude lipid + ash + fiber).

Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007

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Table 2 Hydrolyzed amino acid composition of commercial soybean meal and yeast fermented soybean meal. Items

Hydrolyzed amino acid composition g/kg in protein SBM

Essential amino acid Arginine Histidine Lysine Methionine Leucine Isoleucine Threonine Phenylalanine Valine None-essential amino acid Glutamate Aspartate Serine Glycine Alanine Tyrosine Cystine Proline Total amino acid

YFSBM

26.2 11.0 21.0 5.0 29.9 19.1 17.8 21.2 18.2

28.4 11.3 27.5 5.7 38.9 19.9 18.2 22.1 20.3

80.2 42.1 21.6 18.1 18.0 13.2 4.6 18.2 385.4

100.2 49.2 21.7 20.1 19.8 16.5 7.6 20.8 448.1

2.2. Determination of anti-nutritional factors and amino acid Phytic acid concentration was determined in CSBM and YFSBM using a spectrophotometric procedure according to the method of Vaintraub and Lapteva (1988). The color was measured at 830 nm against a blank. Results were calculated as mg phytic acid/100 g dry sample using standard phytic acid. Trypsin inhibitor activity (TIA) was determined according to the method of Smith et al. (1980). Results were expressed by mg trypsin inhibited per g of dry sample. The amino acid compositions of CSBM and YFSBM were determined using an automated amino acid analyzer after hydrolyzing the samples with 6 M HCl at 110 ◦ C for 24 h (Bassler and Buchholz, 1993). Sulphur-containing amino acids were oxidized using performic acid before the acid hydrolysis. The anti-nutrients/toxicants and amino acid of CSBM and YFSBM are shown in Tables 1 and 2. 2.3. Experimental diet Five isonitrogenous (295 g/kg crude protein) and isocaloric (19.5 MJ/kg gross energy) experimental diets were formulated and the proximate chemical composition of the experimental diets is presented in Table 3. The first is the control diet which contained 18 g FM/Kg diet (D-0). In the other four diets, FM protein was replaced with YFSBM at levels of 25% (D-25), 50% (D-50), 75% (D-75) and 100% (D-100), respectively. All dry ingredients of the fish meal, soybean meal, yellow corn and wheat bran were blended for 5 min and thoroughly mixed with soybean oil. Also each of the diets contained 5 g/kg chromic oxide (Cr2 O3 ) as a marker for nutrient digestibility measurements. The ingredients were mixed well and made into dry pellets using a laboratory pellet mill (California Pellet Mill, San Francisco, CA, USA). The pellets (2-mm die) were dried for 4 h at 60 ◦ C and stored at −20 ◦ C until use. 2.4. Experimental fish and facilities Nile tilapia (O. niloticus) fingerlings were obtained from the Arab fisheries hatchery, Abu-Hammad, Sharkia Governorate, Egypt. They were transferred to the fish nutrition lab, Faculty of Agriculture of Benha University. Prior to the beginning of the experiment, fish were acclimatized to the experimental conditions and fed commercial diet (300 g/kg crude protein) twice daily to apparent satiation by hand for 15 days. After acclimatization the fingerlings with an initial body weight of 3.5 ± 0.09 g were stocked into 15 one glass aquaria (100 × 40 × 50 cm, 200 L each). Three replicate aquaria were randomly assigned to each treatment to represent the five experimental treatments; each aquarium was stocked with 25 fish. All dietary treatments were tested in triplicate groups where each aquarium was considered as an experimental unit. The glass aquaria were supplied with de-chlorinated tap water and were continuously supplied with compressed air for oxygen requirement. About one-third of the water volume in each aquarium was daily replaced by new aerated fresh water after cleaning and removing of the accumulated excreta. A photoperiod of 12 h light, 12 h dark (08.00–20.00 h) was used. Fluorescent ceiling lights has supplied the illumination. Fish were fed their respective diets by hand one of five experimental diets for 84 days. The daily ration was divided into two equal amounts and offered two times a day (9:30 and 14.00 h). All fish in each aquarium were weighed biweekly and the amount of daily allowance feed was adjusted accordingly. There was no mortality during the entire experimental period. Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007

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Table 3 Formulation and proximate composition of the experiment diets (g/100 g diet). Experimental diets

Fish meal Soybean meal Fermented soybean meal Yellow corn Wheat bran soybean oil Vitamin and mineralsa Vitamin C Chromic oxide Proximate analysis Dry matter Crude protein Ether extract Ash Total carbohydrateb Gross energy (MJ/kg)c

D-0

D-25

D-50

D-75

D-100

18 35 0 31 8.5 4 2.7 0.3 0.5

13.5 35 5.2 31 7.8 4 2.7 0.3 0.5

9 35 10.44 31 7.06 4 2.7 0.3 0.5

4.5 35 15.66 31 6.34 4 2.7 0.3 0.5

0 35 20.88 31 5.62 4 2.7 0.3 0.5

90.01 29.85 7.50 6.02 56.63 19.73

89.81 29.7 7.24 5.91 57.15 19.68

89.61 29.60 7.00 5.86 57.54 19.62

89.29 29.50 6.79 5.82 57.89 19.58

89.21 29.39 6.75 5.71 58.15 19.59

a Vitamin and mineral mixture kg−1 of mixture contains: 4800 I.U. Vit A, 2400 IU cholecalciferol (vit. D), 40 g Vit E, 8 g Vit K, 4.0 g Vit B12 , 4.0 g Vit B2, 6 g Vit B6, 4.0 g, pantothenic acid, 8.0 g nicotinic acid, 400 mg folic acid, 20 mg biotin, 200 gm choline, 4 g copper, 0.4 g iodine, 12 g iron, 22 g manganese, 22 g zinc, 0.04 g selenium, folic acid, 1.2 mg; niacin, 12 mg; D-calcium pantothenate, 26 mg; pyridoxine. HCl 6 mg; riboflavin, 7.2 mg; thiamin. HCl, 1.2 mg; sodium chloride (NaCl, 39% Na, 61% Cl), 3077 mg; ferrous sulfate (FeSO4 ·7H2 O, 20% Fe), 65 mg; manganese sulfate (MnSO4 , 36% Mn), 89 mg; zinc sulfate (ZnSO4 ·7H2 O, 40% Zn), 150 mg; copper sulfate (CuSO4 ·5H2 O, 25% Cu), 28 mg; potassium iodide (KI, 24% K, 76% I). b Total carbohydrate = 100 − (CP + EE + Ash). c Gross energy calculated using gross calorific values of 0.2363, 0.3952 and 0.1715 MJ/g for protein, fat and carbohydrate, respectively according to Brett (1973).

Water temperature, dissolved oxygen, pH, and total ammonia were monitored during the study, to maintain water quality at optimal range for the Nile tilapia. Water temperature was recorded daily at 13.00 h using a mercuric thermometer suspended at 30 cm depth. Dissolved oxygen (DO) was measured daily at 07.00 h using YSI model 56 oxygen meter (YSI Company, Yellow Springs Instrument, Yellow Springs, OH, USA) and pH was recorded daily at 09.00 h using a pH meter (Orion pH meter, Abilene, TX, USA). Total ammonia was measured three times a week according to APHA (1992). During the period of the feeding trial, the water-quality parameters were averaged (±SD); water temperature was 26.17 ± 0.8 ◦ C; dissolved oxygen, 5.6 ± 0.8 mg/L; pH, 8.52 ± 0.3 and total ammonia, 0.18 ± 0.12 mg/L. All tested water quality criteria were suitable and within the acceptable limits for rearing the Nile tilapia O. niloticus fingerlings (Boyd, 1990). At the initiation and termination of the trail a random sample of five individual fish were sampled from each aquarium, then oven-dried 105 ◦ C for 24 h, ground, and stored at −20 ◦ C for subsequent analysis. Proximate analysis was conducted on CSMB, YFSBM, diets and fish samples. Moisture, total lipids, crude protein and ash contents were all determined by the standard (AOAC, 1995). Dry matter was determined after drying the samples in an oven (105 ◦ C) for 24 h. Ash by incineration at 550 ◦ C for 12 h (AOAC, 1995 method number 942.05). Crude protein was determined by micro-Kjeldhal method, N × 6.25 (using Kjeltech auto analyzer, Model 1030, Tecator, Höganäs, Sweden) (AOAC, 1995 method number 984.13) and crude fat by Soxhlet extraction with diethyl ether (40–60 ◦ C) (AOAC, 1995 method number 920.39). Crude fiber content of CSMB and YFSBM was determined using the method of Van Soest et al. (1991). Nitrogen-free extract was computed by taking the sum of values for crude protein, crude lipid, crude fiber, ash and moisture then subtracting this sum from 100. 2.5. Growth indices Records of initial body weight (IBW) and final body weight (FBW) of each individual fish were measured in all fish for each aquarium at the initiation and the termination of the feeding trail. Weight gain (WG), specific growth rate (SGR %), feed conversion ratio (FCR), protein efficiency ratio (PER) and protein productive value (PPV) were calculated using the following equations: WG (g/fish) = FBW − IBW; SGR% = [ln FBW − ln IBW]/t × 100, where FBW is final body weight (g); IBW is initial body weight (g); ln = natural logarithmic; t = time in days. FCR = FI/WG, where FI is feed intake (g); PER = WG/protein intake (g). PPV% = protein gain (g)/protein intake (g) × 100. 2.6. Digestibility study After 2-months from the experimental start, feces were collected from each aquarium once daily every morning for a 1-month period prior to feeding. The feces were collected on filter paper for drying as described by El-Saidy and Gaber (2002). The collected fecal samples were pooled and freeze-dried prior to analyses for a period for 10 days. The chemical analyses were conducted according to AOAC (1995). Chromic oxide was determined according to the procedure described Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007

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by Furukawa (1966). Apparent nutrient digestibility was calculated using the equations of Schneider et al. (2004) as follows:

ADCdietary nutruent = 1 − [(markerdiet )/(markerfeces )] × (nutrientfeces )/(nutrientdiet )

2.7. Hematological and biochemical blood indices At the end of the experiment blood samples were collected from the caudal vein of fish of all treatments (10 fish from each replicate) and were divided into two portions. The first portion was collected with anticoagulant 10% ethylenediaminetetraacetate (EDTA) to determine the hematocrit (Htc), hemoglobin (Hb), erythrocyte counts (RBCs) and total count of white blood cells (WBCs) according to the standard methods as described elsewhere by Rawling et al. (2009). A part of the first portion (0.5 ml) was centrifuged at 1000 rpm for 5 min to separate the plasma to measure the plasma growth hormone (GH) by a radioimmunoassay (RIA) kit from Tianjin Nine Tripods Medical and Bioengineering Co., Ltd. (Tianjin, China), following the manufacturer’s protocol. Insulin-like growth factor-I (IGF-I) was determined in undiluted samples by RIA after SepPak C18 chromatography (Waters Corp., Milford, MA, USA), as described earlier for mammals by Jevdjovic et al. (2005). The second portion of the blood sample was allowed to clot overnight at 4 ◦ C and then was centrifuged at 3000 rpm for 10 min. The non-hemolysed serum was collected and stored at −20 ◦ C until use. Levels of serum aspartate aminotransferase (AST), alanine aminotransferase (ALT) were estimated according to the method described by Reitman and Frankel (1957). The activity of the serum complements component (C3) was assayed using the C3 kit (Zhejiang Elikan Biological Technology Co., Ltd., Wenzhou, Zhejiang, China). Methods for C3 activity analysis included measurement of the increase in turbidity after immunity response of C3 and its increased antibody was done according to Thomas (1998).

2.8. Statistical analysis Chemical composition and ant-nutritional factor of commercial and fermented soybean meal data were analyzed using one way ANOVA with statistical software 218 SAS ANOVA procedures, statistical analysis system, 1993. Several curve fitting models including broken-line, linear, and polynomial regressions were performed for each response variable using mean ± SE. The model with the best coefficient of determination was chosen to estimate the growth, feed utilization, digestibility and hematology, and biochemical blood analysis of O. niloticus in response to YFSBM replacement. Regression analysis was performed with graphic software Sigma Plot version 8 (SPSS Inc. Chicago, IL, USA).

3. Results 3.1. Chemical composition, anti-nutritional factors and amino acid content Chemical composition and anti-nutritional factors of CSBM and YFSBM are presented in Table 1. Results indicated that YFSBM using SSF with S. cerevisiae significantly increased crude protein (P=0.002), lipid (P=0.004) and ash content (P=0.003). Moreover, SSF with S. cerevisiae significantly decreased fiber content (P=0.001) in YFSBM. While the phytic acid and trypsin inhibitor in YFSBM were significantly (P=0.001) decreased than CSBM. The total amino acid of YFSBM increased by 16.27% compared to CSBM (Table 2). Essential amino acids, including arginine, histidine, lysine, methionine, leucine, isoleucine, threonine, phenylalanine and valine in YFSBM increased by 8.39%, 2.72%, 30.95%, 14%, 30.10%, 4.19%, 2.25%, 4.25% and 11.53%, respectively compared to CSBM. Moreover, non-essential amino acid, glutamate, serine, glycine, alanine, tyrosine, cystine and proline in YFSBM increased by 24.93%, 16.86%, 0.46%, 11.05%, 10.00%, 25.00%, 65.22%, and 14.29%, respectively compared to CSBM.

3.2. Growth performance and feed utilization Fig. 1 shows the growth and feed utilization response of fish to the increasing YFSBM in diets of tilapia concerning some of the investigated traits. Using polynomial regression the best WG, SGR and FCR were recorded by fish fed D-25. Also, using regression analysis a significant effect of YFSBM inclusion level on FBW, FI, PER and PPV as: FBW: y = − 7.257x2 + 4.957x + 25.381, R2 = 0.958, residual standard deviation (RSD) = 0.653, (P=0.012); FI: y=−11.931x2 + 10.651x + 32.755, R2 = 0.719, RSD = 0.381, (P=0.032); PER: y = −0.549x2 + 0.357x + 2.299, R2 = 0.802, RSD = 0.566, (P=0.021) and PPV: y = −3.394x2 + 2.766x + 32.202, R2 = 0.647, RSD = 0.461, (P=0.041). Growth performance and feed efficiency above indicate that up to 50% FM could be replaced by FSBM without causing significant reduction in growth and feed utilization. The relationship of FCR to the replacement level of FM with YFSBM was expressed by broken-line model and a breakpoint at 37.4% was thought to be optimal for YFSBM to replace the percentage of FM (Fig. 2). Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007

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Wg (g)

SGR

FCR 2.6

Weight gain (WG) g/fish

24

2.4

23

2.2 22

2

21

1.8 1.6

20

1.4 19

1.2

18

1

0%

25%

50%

75%

100%

Spesific growth rate (SGR) and feed conversion rao (FCR)

6

Replacement level % Fig. 1. Effect of replacement of fish meal by yeast fermented soybean meal on FBW and WG. Data are means ± S.E. WG: Y = 7.726x2 + 5.261x + 21.876, R2 = 0.970, RSD = 0.681, (P=0.001); SGR: y = −0.354x2 + 0.246x + 2.360, R2 = 0.944, RSD = 0.324, (P=0.002); FCR: y = 0.32x2 − 0.192x + 1.472, R2 = 0.812, RSD = 0.132, (P=0.001).

Fig. 2. Effect of replacement levels of FM with YFSBM on FCR in O. niloticus fed experimental diets for 84 days. Y = 1.36 + 0.002 (x + 37.4); (37.4 − x) = 0 when X < 37.4; R2 = 0.9173. The breakpoint of the broken-line is 37.4%

DM

Protein

Lipid

DE

Apparent digestability

0.920 0.900 0.880 0.860 0.840 0.820 0.800 0.780 0.760 0.740 0.720 0.700 0%

25%

50%

75%

100%

Replacement level% Fig. 3. Effect of replacement of fish meal by yeast fermented soybean meal on DM, protein, lipid and DE. Data are means ± S.E. DM: y = −0.060x2 + 0.030x + 0.890, R2 = 0.870, RSD = 0.035, (P=0.036); protein: y = −0.094x2 + 0.063x + 0.874, R2 = 0.885, RSD = 0.065, (P=0.021); lipid: y = −0.058x2 + 0.030x + 0.890, R2 = 0.8698, RSD = 0.059, (P=0.031); DE Y = −0.017x + 0.7682,R2 = 0.590, RSD = 0.049, (P=0.042).

3.3. Apparent digestibility and proximate analysis of whole body fish The data extracted for ADCs of DM and digestible energy (DE) fitted a linear model but the data of protein and lipid fitted a nonlinear model (Fig. 3). According to these equations, the best ADCs were recorded by fish fed the D-25 followed by D-50. The best fit was obtained by using a linear model for chemical composition. Body protein and ash contents tended to be higher and reached a plateau in fish fed D-25 and D-50 and the regression model was as: protein content: y = 0.96x + 58.304, R2 = 0.401, RSD = 0.290, (P=0.046) and ash: y = 0.892x + 19.93, R2 = 0.825, RSD = 0.440 (P=0.021). However, fit linear model showed the lowest DM: y = 1.1x + 25.12, R2 = 0.790, RSD = 0.350, (P=0.041), lipid: y = 2.224x + 15.222, R2 = 0.591, RSD = 0.230, (P=0.032) and GE: Y = −2.62x + 24.338, R2 = 0.952, RSD = 0.610, (P=0.011) contents occurred at 0% replacement. Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007

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White blood cells (×104/ mm3) ALT (u/L) AST (u/L) Red blood cells(×106/ mm3)

107 103 99 95 91 87 83 79 75 71 67 63 59 55 51 47 43 39 35 31 27 23 19 15

1.93 1.92 1.91 1.9 1.89 1.88 1.87

0%

25%

50%

75%

1.86 100%

7

Red blood cells (×106/ mm3)

White blood cells (×104/ mm3) , ALT and ALT (U/L)

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Replacement level % Fig. 4. Effect of replacement of fish meal by yeast fermented soybean meal on Red blood cells, White blood cells, alanine aminotransferase (ALT) and aspartate aminotransferase (AST). Data are means ± S.E. Red blood cells: y = 0.427x3 + 0.651x2 + 0.205x + 1.901, R2 0.985, RSD = 0.469, (P=0.006); White blood cells: y = 28.693x3 + 49.954x2 + 19.821x + 36.398, R2 = 0.963, RSD = 0.517, (P=0.002); ALT: y = 10.514x2 + 8.354x + 97.826, R2 0.985, RSD = 0.485, (P=0.010); AST: y = 5.874x2 + 4.962x + 19.778, R2 = 0.679, RSD = 0.650, (P=0.022).

C3 g/l

GH ng/ml 1

10

0.9

8 0.8 6 0.7 4 0.6

2 0 0%

25%

50%

75%

0.5 100%

C3 g/ l and GH content ng/ ml

IGF-Icontent ng/ ml

IGF-I ng/ ml 12

Replacement level % Fig. 5. Effect of replacement of fish meal by yeast fermented soybean meal on IGF-I, C3 and GH. Data are means ± S.E. IGF-I: y = −1.531x + 0.963x + 9.523 R2 = 0.838, RSD = 0.280, (P=0.016); C3: y = −0.382x2 + 0.217x + 0.817, R2 = 0.888, RSD = 0.112, (P=0.032); GH: y = −0.256x2 + 0.176x + 0.673, R2 = 0.741, RSD = 0.114, (P=0.011).

3.4. Hematology and biochemical blood parameters Using linear regression analysis, non-significant effect of YFSBM inclusion level on Htc and Hb was found as: Htc: y = −0.12x + 25.32, R2 = 0.084, RSD = 0.062, (P=0.421) and Hb: y = 0.496x + 10.848, R2 = 0.395, RSD = 0.124, (P=0.623). The same pattern was observed in WBCs, RBCs, IGF-I, C3 and GH increased and ALT and AST decreased with D-25 and D-50, respectively and the and the best fit of the data was obtained using an polynomial regressions (Figs. 4 and 5). 4. Discussion Solid-state fermentation has been applied in the production of metabolites, such as enzymes, antibiotics and other value added products, such as organic compounds (Pandey, 2003). The current significant increase in the crude protein content of YFSBM may be due to the elevation in the level of amino acids during the process of fermentation, and this is in agreement with other previous studies (Jacqueline and Visser, 1996; Belewu and Sam, 2010). The increase in total essential amino acids (13.52%) was lower than that of non-essential amino acids (18.43%). This result may be due to the high production of the cell mass of yeast and consequently the production of protein within the yeast population. Furthermore, S. cerevisiae increased the methionine in YFSBM, by 14%, than that found in the current CSBM. These results were in parallel with the work of Kumar and Gomes (2005) on microorganisms in SBM fermentation. Hong et al. (2004) showed that amino acid content increased in SBM fermentation with Aspergillus oryzae GB-107. The reduction in crude fiber content of YFSBM, compared with CSBM in the present study may be due to the secretion of various enzymes, which degraded crude fiber and complex polysaccharides, as previously documented by Belewu et al., (2011). The fermentation of CSBM by S. cerevisiae was employed in the current study in order to reduce anti-nutritional factors such as phytic acid and trypsin inhibitor. Other studies have used other bacteria and fungi species to reduce anti-nutritional factors (Jacqueline and Visser, 1996; Belewu and Sam, 2010; Shiu et al., 2013). Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007

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The result of this study showed that up to 50% FM in the diets for Nile tilapia could be replaced by YFSBM in order to enhance the growth performance and the optimal performance at 37.4% inclusion. These results agree with recent study Yuan et al. (2013), showed that the replacement of fish meal protein up to 350 g/kg with YFSBM produced growth rate similar to that produced by fish meal-based diets for the juvenile Chinese sucker, Myxocyprinus asiaticus. On the other hand, substitution of brewer’s waste instead of fishmeal, up to 50%, did not have any significant difference on growth rate and feed utilization of Nile tilapia (Zerai et al., 2008). Gause and Trushenski (2011) showed that higher growth performance for sunshine bass was observed by replacing of FM with bio-ethanol yeast at substitution levels, 27–41%. The improvement of Nile tilapia growth, by replacing of FM with YFSBM in the present study, may be due to the increase of amino acids in submitted fermented yeast. S. cerevisiae has been considered as responsible for increasing the palatability of fish food items (Barnes et al., 2006). Yeasts are a good source of nucleotides, ␤-glucans, vitamins, arabinoxylan and mannan oligosaccharides (Oliva-Teles and Gonc¸alves, 2001). The reduction of growth and feed utilization observed in higher inclusions, 75% and 100%, of YFSBM, in the present study, may be due to anti-nutritional factors, lower digestibility of soybean protein and amino acid imbalance and other anti-nutritional factor introduced during the fermentation process (Zhou et al., 2011). In the present study, ADCs of the YFSBM was higher than 85%. The best ADCs were recorded by fish fed on D-25 followed by D-50. On the other hand, the decrease in ADCs as opposed to the increase level of YFSBM may be correlated with feed efficiency, as shown previously in the modified diets of juvenile Chinese sucker, M. asiaticus (Yuan et al., 2013). The ADCs of dry matter and energy were inversely related to the increase in dietary plant protein level, due to cellulose indigestibility (Eusebio et al., 2004). Dry matter, protein, lipid, and energy digestibility were significantly reduced at 20% FM when replaced by FSBM (Zhou et al., 2011). Body protein and ash contents reached to a plateau in fish were fed on D-25 and D-50. In contrast with body protein and ash contents, DM, lipid and GE contents decreased to the 0% feeding level. Yuan et al. (2013) revealed that no significant differences were observed in the body composition of juvenile Chinese sucker, M. asiaticus fed on diet containing fermented soybean meal. However, increasing of body protein content was recorded in fishes fed with diet having 15% fermented YSBM. The concentrations of essential amino acids were low in diets containing higher FSBM inclusion levels, and may be explained by induction in protein catabolism rather than anabolism (Zhou et al., 2011). Apparent digestibility coefficient for carbohydrates and gross energy were inversely correlated with dietary FSM level, while the ADC of crude protein and lipid were not affected by dietary fermented soybean meal level in black sea bream (Azarm and Lee, 2014). Blood indices have been used as indicators of the physiological condition of fish. As we mentioned above, replacing of YFSBM in diet with 25% or 50% of FM relatively improved the physiological parameters, such as Hb, Htc WBCs, RBCs, C3, ALT and AST. In Japanese flounder, Abdul Kader et al. (2012) have mentioned that the replacing of FM with dietary mixture of fermented soybean meal and squid meal, up to 48%, had no significant effect in Htc value, while total serum protein tended to increase (P<0.05) with the increasing FM replacement levels in diets. Fermented soybean meal has increased the nonspecific immune responses of parrot fish, Oplegnathus fasciatus and Japanese flounder (Kim et al., 2009, 2010). On the other hand, rainbow trout, Oncorhynchus mykiss fed with diet containing a yeast exhibited 5 g/kg diet had a non-significant increase in Hct and RBCs, compared with the control group (Heidarieh et al., 2013). The decline in hepatic enzymes ALT and AST for D-25 and D-50, in the present study, may be correlated with the dietary FSBM, including (nucleotides), which may be beneficial to the health of fish since they improve liver functions (Tahmasebi-Kohyani et al., 2012). However, creatinine and uric acid in rainbow trout fed with graded levels of plant protein were significantly higher (P<0.05) than the control diet (Kumar et al., 2011). Current increasing in C3 in D-25 and D-50 groups came in parallel with serum complement component concentrations (C3 and C4), which increased significantly (P<0.001) in hybrid tilapia fed with S. cerevisiae fermentation product (He et al., 2011). Also, dietary mannan-oligosaccharides, as the ingredient of S. cerevisiae fermentation product may alter the immune response due to the presence of mannose receptors on many cells of the immune system (Djeraba and Quere, 2000). In the present study, IGF-I and GH level increased in Nile tilapia fed on D-25 and D-50. To our knowledge, there is a lack of information on IGF-I and GH levels in relation to growth rate as influenced by diet composition for Nile tilapia. The replacement of FM by plant protein sources leads to a decrease in IGF-I levels, and significantly affects the activity of the GH-liver axis was by dietary protein sources of gilthead sea bream, Sparus aurata (Gómez-Requeni et al., 2004). Overall, enhanced health parameters of fish in the present study might partly be associated with the fermentation process in which the protein content is hydrolyzed into peptides and amino acids; some of which have immunomodulatory effects (Sachindra and Bhaskar, 2008). 5. Conclusion In conclusion, fermentation of soybean meal with S. cerevisiae for 48 h could improve the nutritive value of soybean meal. This study showed that up to 37.4% FM in diets could be replaced by YFSBM without any adverse effect on growth performance, nutrient digestibility and physiological condition. From these findings, feed manufacturers will encourage to utilize plant proteins more efficiently to produce low-cost product. Conflict of interest The authors declare that there are no conflict of interests. Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007

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Acknowledgement This study was supported by a grant from the National Institute of Oceanography and Fisheries, Egypt and Animal Production of Faculty of Agriculture, Benha University, Egypt.

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Please cite this article in press as: Hassaan, M.S., et al., Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Anim. Feed Sci. Tech. (2015), http://dx.doi.org/10.1016/j.anifeedsci.2015.01.007