Influence of fermentation concentrate of Hericium caput-medusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers

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Influence of fermentation concentrate of Hericium caput-medusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers H.M. Shang a,b,c , H. Song a,d,∗ , Y.Y. Jiang a , G.D. Ding a , Y.L. Xing a , S.L. Niu a , B. Wu a , L.N. Wang a a b c d

School of Life Sciences, Jilin Agricultural University, Changchun 130118, China College of Animal Science and Technology, Jilin Agricultural University, Changchun 130118, China Key Laboratory of Animal Nutrition and Feed Science of Jilin Province, Jilin Agricultural University, Changchun, 130118, China Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Changchun 130118, China

a r t i c l e

i n f o

Article history: Received 31 March 2014 Received in revised form 3 September 2014 Accepted 12 September 2014 Available online xxx Keywords: Hericium caput-medusae (Bull.:Fr.) Pers. Broilers Growth performance Antioxidant status Meat quality

a b s t r a c t This study was conducted to evaluate the effects of supplementation with the fermentation concentrate of Hericium caput-medusae (Bull.:Fr.) Pers. (HFC) on growth performance, antioxidant status, and meat quality of broilers. A total of 600 female Arbor Acres broilers were randomly divided into five dietary treatments (20 broilers per pen with 6 pens per treatment): CON (basal diet), ANT (basal diet supplemented with 5 mg flavomycin/kg diet) and HFC (basal diet supplemented with 6, 12 and18 g HFC/kg diets). The experiment lasted for 6 weeks. Performance parameters were recorded on days 21 and 42, and the other response criteria on day 42. The average daily feed intake was not affected by HFC inclusion during the entire experimental period. Incorporation of dried HFC in chicken diet improved the daily gain compared with the control and ANT treatments, and the average daily gain increased (P<0.001) quadratically when the HFC levels increased. The superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GSH-Px) values increased (P<0.05) quadratically, while the malondialdehyde (MDA) level in the serum, liver, and breast muscle of broilers decreased (P<0.001) quadratically with the increasing of dietary HFC level. The pH24 h value of the breast muscle increased (P<0.001) quadratically, while the drip loss and cooking loss decreased (P<0.01) quadratically when the HFC levels increased. Dietary supplementation with HFC had no significant effects on shear force of broilers. The L* value decreased (P<0.01) quadratically, while the a* and b* values of the breast muscle increased (P<0.01) quadratically when the HFC levels increased. These results demonstrate that HFC has promising antioxidant potential to enhance oxidative status and meat quality of broiler chickens. © 2014 Elsevier B.V. All rights reserved.

Abbreviations: ADG, average daily gain; ADFI, average daily feed intake; CAT, catalase; FCR, feed conversion ratio; GAE, gallic acid equivalents; GSH-Px, glutathione peroxidase; HFC, fermentation concentrate of Hericium caput-medusae (Bull.:Fr.) Pers.; MDA, malondialdehyde; SOD, superoxide dismutase; SEM, pooled standard error of the mean. ∗ Corresponding author at: School of Life Sciences, Jilin Agricultural University, Changchun 130118, China. Tel.: +86 431 84532885; fax: +86 431 84532885. E-mail address: [email protected] (H. Song). http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011 0377-8401/© 2014 Elsevier B.V. All rights reserved.

Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011

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1. Introduction Currently, consumers are increasingly aware of the health benefits and nutritional quality of the food they consume (Lee et al., 2012). Oxidative rancidity is one of the major causes of deterioration of food for consumption, and it typically causes losses in the texture, consistency, flavor, appearance, and nutritional value of meat products (Colindres and Brewer, 2011). Improved oxidative status in the living animal and increased oxidative stability of the raw product are considered to be beneficial for the processing industry and the consumer (Jiang et al., 2007). Natural antioxidants are currently receiving considerable attention in human and animal nutrition fields due to their association with food-quality characteristics (Choi et al., 2010). Mushrooms have great potential for producing useful bioactive metabolites, such as phenolic compounds, polyketides, terpenes, steroids and polysaccharides (Breene, 1990; Reis et al., 2012). Currently, mushrooms are considered to have antioxidant properties in broilers (Giannenas et al., 2010a,b). It has been reported that Agaricus bisporus presented tissue antioxidant-protective activity when supplemented in broiler chicken diets (Giannenas et al., 2010a). Pleurotus eryngii stalk residue decreased lipid peroxidation and improved meat quality in broilers (Lee et al., 2012). Hericium caput-medusae (Bull.:Fr.) Pers. belongs to the Basidiomycota, Basidiomycetes, Aphyllophorales, Hericiaceae, and Hericium families and is a well-known edible and medicinal mushroom in East Asia. Modern medical and pharmacological researches showed that Hericium have remarkable efficacy on restraining tumor, resisting inflammation, anti-aging, and arresting oxidization (Shang et al., 2014). In China, several preparations from the fermentation concentrate of Hericium caput-medusae (Bull.:Fr.) Pers. (HFC) are on the market for treating chronic stomach diseases (Mizuno, 1999; Ulrike et al., 2005). However, little information is available regarding the influence of dietary supplementation with HFC powder in the broiler diet. Therefore, the objective of the present study was to investigate the effects of HFC on growth performance, antioxidant status, and meat quality of broilers. 2. Materials and methods 2.1. HFC preparation and analysis The strain of H. caput-medusae (Bull.:Fr.) Pers. was obtained from the Bethune Pharmaceutical Factory of Jilin University in China. The H. caput-medusae (Bull.:Fr.) Pers. was maintained on agarslantculture-medium of potato/dextrose agar (PDA) at 4 ◦ C and shifted onto the new agarslantculture-medium after 3 months. The seed culture of H. caput-medusae (Bull.:Fr.) Pers. was grown in a 250-ml Erlenmeyer flask containing 100 ml of potato/dextrose broth on a rotary shaker (model HZQ-C, Harbin Donglian Electronic Technology Development CO., LTD., Harbin, Heilongjiang, China) at 27 ◦ C at 180 rpm. After 7 days, the seed culture broth was aseptically homogenized and inoculated at 1% (v/v) into a culture medium with the following composition (g/L): glucose, 30; KH2 PO4 , 0.3; peptone, 3; NaCl, 0.5; vitamin B1 , 0.1. The cultivation was carried out in 500-ml Erlenmeyer flask containing 200 ml of culture medium on a rotary shaker at 27 ◦ C for 7 days at 180 rpm. Culture broth was harvested by centrifugation (10,000 × g/20 min) and the supernatant was dried using a spray dryer (model DC1500, Shanghai Attainpak Co., Ltd., Shanghai, China), yielding the HFC powder. For chemical analysis, HFC was milled through a 1 mm sieve. Six representative samples were obtained and analyzed in triplicate for proximate components, starch, Ca and P according to the procedures of AOAC International (2000). The selenium content in HFC was determined using inductively coupled plasma mass spectrometry (Agilent 7500s, Agilent Technologies, Waldbronn, Germany) according to Nisianakis et al. (2009). Total phenolics content was measured using Folin–Ciocalteau reagent (Sigma, Santa Clara, CA) according to the method of Giannenas et al. (2010b) and expressed as mg of gallic acid equivalents (GAE) per gram of dry weight (mg GAE/g dry weight). The ergosterol and adenosine contents in HFC were determined by HPLC according to the method of Lee et al. (2011). Vanillin–acetic acid, and perchloric acid were used for the qualitative detection of crude triterpenoids with colorimetry as previously described (Chen et al., 2007). Water soluble polysaccharides in HFC were determined according to Guo et al. (2004a). The HFC was extracted with hot water, and protein was partially removed with an equal volume of 100 g/L tri-chloroacetic acid. Finally, three volumes of abosolute ethanol were used to extract the polysaccharide precipitate. The precipitate was dried using vacuum freeze-drying equipment (FD-1B, Beijing Boyikang Experimental Instrument Co., Ltd., Beijing, China). The yield of the polysaccharide fraction was collected and total sugars were determined according to the method of Dubois et al. (1956); the dry matter content of the polysaccharide extract was determined according to the procedure described by the AOAC International (2000); the ˇ-glucan content was determined by a method that was previously described (McClear and Glennie-Holmes, 1985). The composition of HFC is shown in Table 1. 2.2. Birds, diets and management A total of 600 one-day-old female Arbor Acres broilers were purchased from a commercial hatchery. The chickens were randomly allotted to 5 dietary treatments, each consisting of 6 replicate pens (20 birds/pen). The dietary treatments were as follows: CON (basal diet), ANT (basal diet supplemented with 5 mg flavomycin/kg diet) and HFC (basal diet supplemented with 6, 12 and18 g HFC/kg diets). The experiment lasted for 42 days. All feed were formulated to meet the nutrient requirements for broilers suggested by the Arbor Acres recommendations (Aviagen, Huntsville, AL). The proximate composition Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011

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Table 1 Analysis of proximate ingredients and active ingredients in HFC.a Ingredient

Composition of HFCc

Moisture (g/kg) Crude protein (N × 6.25) (g/kg) Crude fat (g/kg) Crude ash (g/kg) Crude fiber (g/kg) Nitrogen free extract (g/kg) Calcium (g/kg) Phosphorus (g/kg) Selenium (g/kg) Starch (g/kg) Adenosine (g/kg) Ergosterol (g/kg) Total phenolics (mg GAE/g)b Crude triterpenoid (g/kg) Yield of water soluble polysaccharide extract (g/kg) Dry matter of the polysaccharide extract (g/kg) Total sugar content of the polysaccharide extract (g/kg) ˇ-Glucan content of the polysaccharide extract (g/kg)

104 217 19.6 103 3.63 553 5.40 3.59 0.081 60.7 0.495 1.09 5.43 1.39 255 945 775 1.75

a b c

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

2.3 1.9 1.0 2.3 0.19 3.8 0.12 0.08 0.003 2.4 0.022 0.04 0.22 0.03 2.9 5.1 2.8 0.07

HFC, fermentation concentrate of Hericium caput-medusae (Bull.:Fr.) Pers. Total phenolics content is expressed as dry weight basis in milligrams of gallic acid equivalents (GAE) per gram (mg of GAE/g). The value is expressed as the mean ± standard deviation (n = 6).

of feed was analyzed according to the methods of AOAC (2000). Diets, in mash form, and water were provided ad libitum throughout the study. The composition of the starter (days 1–21) and finisher (days 22–42) diets are shown in Table 2. The experiment design and procedures were approved by the Animal Care and Use Committee of Jilin Agricultural University following the requirements of the Regulations for the Administration of Affairs Concerning Experimental Animals of China. The birds were housed in stainless steel pens. The temperature of the room was maintained at 33 ± 1 ◦ C during the Table 2 Ingredients and chemical composition of experimental diets (g/kg, as fed basis). Item

Starter (days 1–21)

Finisher (days 22–42)

ANTc

ANT

HFC (g/kg) 0 (CON)

Ingredient (g/kg) Corn Soybean meal (450 g/kg CP) HFC Corn oil dl-Methionine CaHPO4 ·2H2 O Limestone Salt Premixa Flavomycin Total (g) Calculated analysisb (g/kg) Crude protein Crude fiber Ether extract Crude ash Calcium Phosphorus Metabolizable energy (MJ/kg) Methionine Lysine Threonine Methionine + Cystine

548.0 372.9 0.0 35.0 2.0 19.0 11.0 2.1 10.0 0.005 1000 220.5 21.6 85.4 60.8 10.5 4.7 12.8 5.2 12.0 8.5 9.2

548.0 372.9 0.0 35.0 2.0 19.0 11.0 2.1 10.0 – 1000 220.4 21.7 85.3 60.9 10.4 4.7 12.8 5.2 12.0 8.5 9.2

6

12

541.6 373.3 6.0 35.0 2.0 19.0 11.0 2.1 10.0 – 1000 220.5 21.8 85.4 60.8 10.5 4.7 12.8 5.2 12.0 8.5 9.2

534.7 374.2 12.0 35.0 2.0 19.0 11.0 2.1 10.0 – 1000 220.5 21.8 85.3 60.9 10.5 4.7 12.8 5.2 12.0 8.5 9.2

18 524.8 378.1 18.0 35.0 2.0 19.0 11.0 2.1 10.0 – 1000 220.5 21.8 85.3 60.9 10.4 4.7 12.8 5.2 12.0 8.5 9.2

HFC (g/kg) 0 (CON)

596.0 331.0 0.0 34.0 1.0 13.0 13.0 2.0 10.0 0.005 1000 205.2 23.4 90.3 62.4 9.5 4.2 13.1 4.0 11.0 7.8 7.7

596.0 331.0 0.0 34.0 1.0 13.0 13.0 2.0 10.0 – 1000 205.2 23.3 90.3 62.5 9.5 4.2 13.1 4.0 11.0 7.8 7.7

6

12

589.0 331.0 6.0 35.0 1.0 13.0 13.0 2.0 10.0 – 1000 205.2 23.4 90.2 62.5 9.4 4.2 13.1 4.0 11.0 7.8 7.7

582.0 332.0 12.0 35.0 1.0 13.0 13.0 2.0 10.0 – 1000 205.1 23.4 90.3 62.5 9.4 4.2 13.1 4.0 11.0 7.8 7.7

18 575.0 333.0 18.0 35.0 1.0 13.0 13.0 2.0 10.0 – 1000 205.2 23.3 90.2 62.4 9.5 4.2 13.1 4.0 11.0 7.8 7.7

a Premix provided the following per kilogram of diet: Vitamin A (retinyl palmitate), 10000 IU; vitamin D3 , 4000 IU; vitamin E (dl-␣-tocopheryl acetate), 30.0 mg; vitamin K, 1.0 mg; vitamin B1 , 2.0 mg; vitamin B6 , 3.5 mg; vitamin B12 , 0.01 mg; riboflavin, 7.5 mg; niacin, 35.0 mg; pantothenic acid, 10.0 mg; folic acid, 1.0 mg; biotin, 0.18 mg; choline chloride, 400 mg; Mn, 60.0 mg; Zn, 40.0 mg; Fe, 80.0 mg; Cu, 8.0 mg; I, 0.70 mg; Se, 0.3 mg. b The values were calculated from NRC (1994). c ANT, basal diet + 5 mg flavomycin/kg diet; CON, basal diet; HFC (basal diet supplemented with 6, 12, and 18 g/kg diet HFC); the CON was considered as 0 g/kg diet HFC.

Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011

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first 3 days, after which the temperature was gradually lowered by 3 ◦ C a week until reaching 24 ◦ C. The temperature of the room was then maintained at 24 ◦ C for the remainder of the study. Light was provided according to the following schedule 24 h light: 0 h dark from days 1 to 3, and 23 h light:1 h dark from day 4 to the end of experiment.

2.3. Sample collection Body weight and feed intake were monitored on a pen basis on days 1, 21, and 42. This information was then used to calculate average daily gain (ADG), average daily feed intake (ADFI), and feed conversion ratio (FCR; ADFI: ADG). During the trial, all mortalities were removed from the pens and recorded. At 42 days of age, 24 birds were randomly selected from each group (4 birds per pen) and blood samples were withdrawn from the wing vein with a sterile syringe. The blood was centrifuged at 3000 × g for 15 min to obtain the serum and was stored at −20 ◦ C until it was analyzed. After blood collection, the same birds were euthanized by cervical dislocation. The liver and breast muscle (pectoralis major) were excised, perfused with 0.9% ice-cold saline, and then chopped into small pieces on ice. A 10% (w/v) homogenate was prepared in 10 mM phosphate buffer (pH 7.4) and centrifuged at 12,000 × g for 10 min at 4 ◦ C. The supernatant was collected and stored at −80 ◦ C to assay for antioxidant enzyme activity and malondialdehyde (MDA) content. The muscle from the breast was packed individually in sealable plastic bag and stored at 4 ◦ C pending meat quality analysis.

2.4. Antioxidant status determination The activities of superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GSH-Px) were assayed by colorimetric methods. Units of SOD activity were defined by the amount of enzyme required to inhibit the rate of formazan dye formation by 50% under defined conditions (Cao et al., 2012). The CAT activity was estimated by the decomposition of H2 O2 to yield H2 O and O2 , and changes in absorbance at 240 nm for 2 min were monitored (Cohen et al., 1970). One unit of CAT activity was expressed as the amount of enzyme catalyzing the decomposition of 1 ␮mol of H2 O2 per minute at 25 ◦ C and pH 7.0. GSH-Px activity was determined according to the method of Lawrence and Burk (1976). One unit of GSH-Px is expressed as the amount of GSH-Px needed to oxidize 1 ␮mol of NADPH per min. The MDA level was detected with thiobarbituric acid, and the change in absorbance at 532 nm was monitored with a spectrophotometer (Giannenas et al., 2011). All of the samples were measured in triplicate. Antioxidative enzyme activities were expressed as units (U) per milligram of protein for liver and muscles and U per milliliter of serum. Tissue proteins were determined by the method of Bradford (1976), using bull serum albumin as a standard.

2.5. Meat quality measurements Moisture, crude protein, and crude fat contents of muscles were analyzed according to the methods of AOAC (2000). The breast pH value were measured at 15 min (pH15 min ) and 24 h (pH24 h ) after slaughter with a portable meter (FC 230B, Hanna Instruments, Italy) equipped with an insertion electrode that was calibrated in buffers at pH 4 and 7 at ambient temperature. The determination method was described by Cao et al. (2012). The pH probe was inserted at an angle of 45◦ into the muscles and rinsed with deionised water between samples. Each sample was measured three times, and their average value was taken as the final result. Drip loss was assayed as described by Cao et al. (2012) and Lee et al. (2013). In brief, about 15 g (wet weight) of regularshaped muscle [4 cm (length) × 3 cm (width) × 1.5 cm (thickness)], cut from the same location in the breast muscle was weighted, and placed in plastic bags and freely suspended using a steel wire hook at 4 ◦ C. Care was taken to minimize the contact between the muscle and the inside surface of the bag. Twenty-four hours later, the samples (breast muscle) were wiped and re-weighted to evaluate the drip loss, which was expressed as a percentage: [(initial weight − final weight)/initial weight] × 100. To determine the cooking loss and shear force, at 24 h postmortem, the samples (breast muscle) were weighted, placed into individual plastic bags, and vacuum sealed. Subsequently, the vacuum-sealed samples were cooked in a water bath kettle set at 85 ◦ C until an internal temperature of 77 ◦ C. After cooking, residual moisture was absorbed from each sample with filter papers and the samples were re-weighted. Cooking loss was calculated as a percentage: [(raw weight − cooked weight)/raw weight] × 100, as described by Schilling et al. (2008). Then, cooked samples were cooled to room temperature, from which at the same location rectangular-shaped samples [2 cm (length) × 1 cm (width) × 1 cm (thickness)] were removed to measure tenderness using a TA-XT2 texture analyzer (Stable Micro Systems, Godalming, UK) (Molette et al., 2003; Yang et al., 2010). Shear force was measured perpendicular to the axis of muscle fibers in six replicates for each sample. Color measurements were taken in duplicate at 24 h postmortem. Lightness (L*), redness (a*), and yellowness (b*) values were determined using a Minolta chromameter (CR410, Konica Minolta Sensing Inc., Osaka, Japan). The measurements were taken at three locations on the medial portion of meat at room temperature (25 ± 2 ◦ C), and average values were reported (Cao et al., 2012). Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011

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Table 3 Effects of dietary HFC on the performance of broilers.a , b , c . Item

ANT

HFC (g/kg) 0(CON)

Starter period (days 1–21) 36.7y ADG (g/d/bird) 51.3 ADFI (g/d/bird) 1.40 FCR 0.93 Mortality (%) Finisher period (days 22–42) ADG (g/d/bird) 70.1yz ADFI (g/d/bird) 139.7 1.99x FCR 0.98 Mortality (%) Overall experiment (days 1–42) 53.4y ADG (g/d/bird) 95.5 ADFI (g/d/bird) 1.79xy FCR 1.91 Mortality (%)

SEM 6

12

18

P-valued T

L

Q

35.7z 50.8 1.42 1.59

37.6x 51.8 1.38 1.24

38.2x 51.9 1.36 1.56

38.0x 51.8 1.36 1.24

0.190 0.240 0.008 0.134

<0.001 0.568 0.0380 0.583

<0.001 0.207 0.012 0.858

<0.001 0.255 0.013 0.958

69.7z 139.0 2.00x 1.69

70.2yz 139.2 1.98xy 1.31

72.1x 139.5 1.93y 1.63

71.1y 139.3 1.96xy 1.31

0.192 0.375 0.007 0.142

<0.001 0.984 0.024 0.575

0.001 0.772 0.048 0.878

<0.001 0.949 0.069 0.967

55.2w 95.7 1.73z 3.19

54.5x 95.6 1.75yz 2.55

0.166 0.196 0.006 0.276

<0.001 0.778 <0.001 0.579

<0.001 0.308 0.002 0.868

<0.001 0.446 <0.001 0.963

52.7z 94.9 1.80x 3.28

53.9y 95.5 1.77xyz 2.55

Means within a row without common superscripts differ significantly (P<0.05). a The dietary treatment were: CON (basal diet); ANT (basal diet + 5 mg flavomycin/kg diet); HFC (basal diet supplemented with 6, 12, and 18 g/kg diet HFC). The CON was considered as 0 g/kg diet HFC. b Data are means of 6 pens. c ADG, average daily gain; ADFI, average daily feed intake; FCR, feed conversion ratio; SEM, pooled standard error of the mean. d T, overall effect of treatment; L, linear effect of increasing HFC; Q, quadratic effect of increasing HFC (0, 6, 12 and 18 g/kg diet).

2.6. Statistical analyses Pen was used as the experimental unit and one-way analysis of variance was performed using GLM procedure with SAS software (SAS Institute Inc., Cary, NC, USA) in a completely randomized design. Probability values less than 0.05 were considered significant. When significant differences were determined among treatments means, they were separated by using Tukey’s HSD test. In addition, orthogonal polynomial contrasts were used to determine linear and quadratic response to increasing dietary HFC levels (0, 6, 12 and 18 g HFC/kg diet).

3. Results 3.1. Components of HFC The components of HFC have been shown in Table 1. The HFC contained moisture 104 g/kg, crude protein 217 g/kg, crude fat 19.6 g/kg, crude ash 103 g/kg, crude fiber 3.63 g/kg, nitrogen free extract 553 g/kg, and starch 60.7 g/kg of the dry matter. Total phenolics content was found to be 5.43 mg of GAE per g expressed as dry weight. Yield of polysaccharide extract expressed on the basis of the dry matter of HFC was found to be 255 g/kg. The dry matter content of the polysaccharide extract was 945 g/kg. Total sugar content of the extract was found to be 775 g/kg of the dry weight. HFC also contain ␤glucans (1.75 g/kg dry weight), adenosine (0.495 g/kg dry weight), ergosterol (1.09 g/kg dry weight), and crude triterpenoid (1.39 g/kg dry weight).

3.2. Animal performance The effects of HFC on growth performance in broilers are summarized in Table 3. There was no difference in ADFI and mortality observed among different treatment groups in each period. During the starter period (days 1–21) and the finisher period (days 22–42), the ADG of broilers increased (P<0.001) quadratically when the HFC levels increased. Over the entire experiment period (days 1–42), the ADG of birds increased (P<0.001) quadratically, and the FCR of birds decreased (P<0.001) quadratically when the HFC levels increased.

3.3. Antioxidant status Table 4 presents the effects of dietary HFC supplementation on the levels of antioxidant enzymes and MDA in the serum, liver, and meats of broilers after 42 days. The SOD, CAT, and GSH-Px values in the serum of broilers increased (P<0.05) quadratically, while the MDA level in the serum of broilers decreased (P<0.001) quadratically with the increasing of dietary HFC level. Similar trends were observed of these indexes in the liver, and breast muscle of broilers. Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011

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Table 4 Effects of dietary HFC on the antioxidant status of broilers.a , b , c . Item

ANT

Serum SOD (U/mL) CAT (U/mL) GSH-Px (U/mL) MDA (nmol/mL) Liver SOD (U/mg of protein) CAT (U/mg of protein) GSH-Px (U/mg of protein) MDA (nmol/mg of protein) Breast muscle SOD (U/mg of protein) CAT (U/mg of protein) GSH-Px (U/mg of protein) MDA (nmol/mg of protein)

HFC (g/kg)

P-valued

SEM

0(CON)

6

12

18

138.7z 5.39y 117.0xy 4.98y

135.3z 4.63z 113.4y 5.49x

146.3yz 5.17yz 119.1xy 4.86y

165.4x 6.08x 123.3x 4.14z

153.1xy 5.81xy 120.4xy 4.61yz

119.9y 13.2xy 18.6xy 0.72xy

113.3z 11.8y 17.7y 0.83w

126.1x 12.6y 19.3xy 0.74x

138.2w 14.8x 21.3x 0.64z

39.7z 0.70xy 7.81y 0.46y

36.5z 0.55y 7.36y 0.51x

50.7x 0.75x 8.66x 0.42z

43.7y 0.66xy 7.86y 0.46y

T

L

Q

2.40 0.11 0.95 0.10

<0.001 <0.001 0.007 <0.001

<0.001 <0.001 0.007 <0.001

<0.001 <0.001 0.002 <0.001

130.9x 13.8xy 19.9xy 0.69yz

1.70 0.27 0.37 0.01

<0.001 0.002 0.020 <0.001

<0.001 0.001 0.025 <0.001

<0.001 0.001 0.014 <0.001

45.0y 0.74x 7.97y 0.44yz

0.97 0.02 0.10 0.01

<0.001 0.014 <0.001 <0.001

<0.001 0.002 0.012 <0.001

<0.001 0.003 <0.001 <0.001

Means within a row without common superscripts differ significantly (P<0.05). a The dietary treatment were: CON (basal diet); ANT (basal diet + 5 mg flavomycin/kg diet); HFC (basal diet supplemented with 6, 12, and 18 g/kg diet HFC). The CON was considered as 0 g/kg diet HFC. b Data are means of 6 pens. c SOD, superoxide dismutase; CAT, catalase; GSH-Px, glutathione peroxidase; MDA, malondialdehyde. d T, overall effect of treatment; L, linear effect of increasing HFC; Q, quadratic effect of increasing HFC (0, 6, 12 and 18 g/kg diet). Table 5 Effects of dietary HFC on the meat quality of broilers.a , b , c . HFC (g/kg)

SEM

P-valued

Item

ANT

0(CON)

6

12

18

T

L

Q

pH15 min pH24 h Drip loss (%) Cooking loss (%) Shear force (kg) Color L* a* b*

6.42 5.90y 2.95xy 13.0xy 19.3

6.39 5.73z 3.38x 13.3x 19.6

6.41 5.92y 2.69y 12.4xy 19.5

6.43 6.09x 2.58y 11.7y 19.3

6.43 6.05x 2.67y 12.1xy 19.5

0.01 0.03 0.08 0.17 0.15

0.899 <0.001 0.007 0.009 0.973

0.302 <0.001 0.007 0.012 0.809

0.579 <0.001 0.002 0.008 0.848

48.9xy 4.61x 16.6x

50.0x 4.25y 14.8y

48.4xy 4.79x 15.9xy

47.8y 4.94x 17.4x

48.0y 4.81x 16.7x

0.23 0.06 0.23

0.007 <0.001 0.002

0.004 <0.001 0.002

0.002 <0.001 0.001

Means within a row without common superscripts differ significantly (P<0.05). a The dietary treatment were: CON (basal diet); ANT (basal diet + 5 mg flavomycin/kg diet); HFC (basal diet supplemented with 6, 12, and 18 g/kg diet HFC). The CON was considered as 0 g/kg diet HFC. b Data are means of 6 pens. c L*, lightness; a*, redness; b*, yellowness. d T, overall effect of treatment; L, linear effect of increasing HFC; Q, quadratic effect of increasing HFC (0, 6, 12 and 18 g/kg diet).

3.4. Meat quality Table 5 presents the effects of HFC supplementation on the meat quality in breast muscle of broilers after 42 days. The pH24 h value increased (P<0.001) quadratically, while the drip loss and cooking loss decreased (P<0.01) quadratically when the HFC levels increased. Dietary supplementation with HFC had no significant effects on shear force of broilers. The meat color in the broiler meat, as expressed by L*, a*, and b*, was significantly influenced (P<0.05) by dietary supplementation with HFC powder. The L* value decreased (P<0.01) quadratically, while the a* and b* values of the breast muscle increased (P<0.01) quadratically when the HFC levels increased. 3.5. Proximate composition of meat The proximate composition of the breast muscle of the birds that received HFC supplementation for 42 days is shown in Table 6. No significant differences in the moisture and crude protein contents were observed among the treatments. The crude fat content of the breast muscle decreased (P<0.001) quadratically with the increasing levels of HFC in the diet. 4. Discussion The active ingredients of mushrooms could be obtained from fruit bodies, mycelium, and culture filtrate (Mizuno, 2002; Liu et al., 2002). HFC used in the present study is obtained from culture filtrate by liquid fermentation. There are several Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011

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Table 6 Effects of dietary HFC on the proximate composition of broilers meat.a , b Item

ANT

Moisture (%) Crude protein (%) Crude fat (%)

71.5 23.0 4.11x

HFC (g/kg)

SEM

0(CON)

6

12

18

72.5 22.9 4.18x

72.2 23.0 3.74y

71.6 22.9 3.61y

71.5 22.9 3.67y

0.17 0.09 0.05

P-valuec T

L

Q

0.192 0.999 <0.001

0.051 0.921 <0.001

0.070 0.993 <0.001

Means within a row without common superscripts differ significantly (P<0.05). a The dietary treatment were: CON (basal diet); ANT (basal diet + 5 mg flavomycin/kg diet); HFC (basal diet supplemented with 6, 12, and 18 g/kg diet HFC). The CON was considered as 0 g/kg diet HFC. b Data are means of 6 pens. c T, overall effect of treatment; L, linear effect of increasing HFC; Q, quadratic effect of increasing HFC (0, 6, 12 and 18 g/kg diet).

advantages of the liquid fermentation over solid culture on active ingredients production: shorter fermentation period, lower cost, better quality control, higher product concentration, and easier downstream processing (Lee et al., 2004; Papagianni, 2004; Wu et al., 2006). The present study was designed to evaluate the effects of sustained consumption of a natural product such as HFC by broiler chickens. The first objective was to investigate the effects on growth performance of broilers. The second objective was to investigate whether the intake of HFC could beneficially affect the antioxidant status and meat quality of broilers. Giannenas et al. (2010a) reported that dietary supplementation of Agaricus bisporus improved growth performance of broiler chicken at 42 days of age. Willis et al. (2007) found that shiitake mushroom extract supplementation improved performance, promoted bifidobacteria growth in chicken. Guo (2003) have suggested that water-soluble polysaccharides of the Lentinus edodes and Tremella fuciformis mushrooms can enhance growth performance in broiler chicken. Our data are consistent with the work of these authors. Guo et al. (2004b) suggested that polysaccharide extracts increased the activity of intestinal microflora and fermentation end products, such as volatile fatty acids, and increased proliferation of the gastrointestinal tract. Dried HFC has abundant crude soluble polysaccharide (255 g/kg dry weight). The differences in sugar composition, molecular weights, chemical structure and other properties of the polysaccharides may have some impact on their bioactivities, medicinal properties, and other effects. However, it should be noted that the relationship between the polysaccharide structure and its bioactive functions is not well understood (Guo et al., 2004a; Giannenas et al., 2011). Further research is needed in order the poly or oligo-saccharide content of various mushrooms and specifically of HFC to be qualified and quantified. When this is completed, oxidative status and growth performance studies will focus on the use of specific saccharides fractions. Less information is available regarding the influence of dietary supplementation with HFC in broiler chickens. The crude soluble polysaccharide content of HFC was 255 g/kg dry weight, and the ␤-glucans content of HFC was 1.75 g/kg dry weight. The primary polysaccharides in plants and fungi are derived from the cell wall and its metabolites. Mushroom polysaccharides primarily exist as linear and branched glucans with different types of glycosidic linkages, such as ␤-(1 − 3), (1 − 6)-glucans and ␣-(1 − 3)-glucans; however, some are true heteroglycans containing glucuronic acid, xylose, galactose, mannose, arabinose, or ribose (Lee et al., 2012). In addition to providing the requirements for biological metabolism and energy, these polysaccharides also exhibit antiviral, antibacterial, and antiparasitic functions (Wasser and Weis, 1999; Liu et al., 2010). ␤1-3-d-Glucan and its derivatives possess immune-stimulating activity and various levels of free-radical-scavenging activity (Tsiapali et al., 2001). The activity of the mesmeric ␤-glucan unit was 10-fold higher than its monomeric counterpart at the same concentration level. Phenolic compounds are widely found as secondary metabolites in plants and mushrooms, and the contents can be used as a critical index for determining the antioxidant capacity (Wu and Hansen, 2008; Liu et al., 2010). Some mushrooms have been found to possess significant in vitro antioxidant activity, which was well correlated with their total phenolic content (Mau et al., 2002; Yang et al., 2002; Cheung et al., 2003; Lo and Cheung, 2005; Ferreira et al., 2007; Reis et al., 2012). However, in vivo studies about the effects of mushrooms on antioxidant status in animal models are very limited. In a previous study conducted by Giannenas et al. (2010a), it was found that dietary supplementation of Agaricus bisporus reduced lipid peroxidation during refrigerated storage on broiler chicken at 42 days of age. The total phenolic content of HFC was 5.43 mg of GAE per g expressed as dry weight. The active compounds react directly with free radicals, such as hydroxyl radicals, superoxide anion radicals, and hydrogen peroxide (H2 O2 , as oxygen in the non-free-radical state), to minimize cellular damage and inhibit or delay lipid oxidation (Jiang et al., 2007). Certain soluble, low molecular weight polyphenolic compounds can be absorbed by the intestine, reaching the plasma and target organs (Giannenas et al., 2011). Although their levels in the circulation are low, with a reduced net absorption and relatively fast excretion half lives, the consumption of phenolic compounds has also been associated with an enhanced oxidative status in animals and humans (Battula et al., 2008; Monino et al., 2008; Giannenas et al., 2010a). HFC included active ingredients that, when added to the broiler’s diet, may reduce oxidant levels and improve the quality of meats. Antioxidant enzymes are synthesized and regulated endogenously, which are important indexes of the oxidative status of animal tissues (Giannenas et al., 2010a; Lee et al., 2012). SOD catalyzes the dismutation of a superoxide anion into H2 O2 and prevents the generation of free radicals, CAT converts H2 O2 into H2 O (Lee et al., 2012). In the present study, activity of the various enzymes (SOD, CAT, and GSH-Px) in the serum and different tissues were increased by HFC supplementation Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011

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in broilers’ diet. GSH-Px is one kind of selenoenzyme in the HFC-supplemented group compared with control birds. The high selenium content in mushroom might contribute to this desired property (Vetter and Lelley, 2004). Elevated GSH-Px activitiy could be due to active induction of glutathione synthetic enzymes due to higher selenium uptake or passive sparing of glutathione by decreasing the oxidative load on the cells. Although the latter seems more plausible because MDA formation was found to be reduced in HFC-supplemented groups, additional studies are required to determine which mechanism is responsible. The dietary mushroom-supplemented (Agaricus bisporus) group displayed elevated GSH-Px and reduced MDA formation in the liver, thigh, and breast tissues when compared with the non-supplemented group (Giannenas et al., 2010a). The authors suggested that the cells may utilize the mushrooms’ antioxidant properties, thus sparing the intracellular antioxidant systems, such as GSH-Px (Giannenas et al., 2010a). Compared with other meats, chicken meat is relatively abundant in polyunsaturated fatty acid, including the key n3 polyunsaturated fatty acids, and is easily attacked by free radicals (Asghar et al., 1990). Lipid oxidation results in the production of free radicals, which may lead to the oxidation of meat pigments and generation of rancid odors and flavors (Faustman and Cassens, 1990). The extent of lipid peroxidation in muscle by reactive oxygen can be monitored by evaluating the MDA levels (Placer et al., 1966; Descalzo and Sancho, 2008). In the present study, dietary supplementation with HFC resulted in lower MDA values in the serum, liver, and breast muscle when compared to the CON group. Plant-derived antioxidants, such as ascorbic acid and ␣-tocopherol, have been shown to reduce MDA production in chickens’ pectoralis muscles and reduce drip loss because the improved oxidative status protects against a stress-induced increase in lipid oxidation (Young et al., 2003). In the current study, the MDA concentration was reduced, and the enzymatic activities of SOD, CAT, and GSH-Px were improved in the serum, liver, and breast muscle of the HFC-supplemented birds when compared to the control birds. This result suggests that dietary HFC supplementation in birds may decrease lipid peroxidation and enhance oxidative status in broilers. The pH value directly reflects the muscle acidity and affects numerous meat quality attributes, such as meat color, tenderness, and water holding capacity (drip loss and cooking loss) of muscle (Cao et al., 2012; Lee et al., 2012). In addition, a rapid postmortem pH decline can lead to protein denaturation that may result in pale color and low water holding capacity (Briskey and Wismer-Pedersen, 1961; Cao et al., 2012). In the present experiment, breast muscle pH values 24 h postmortem increased in response to the dietary HFC supplementation. The results indicated that dietary HFC was effective in maintaining a relatively higher pH value of meat. Lower water holding capacity could induce liquid outflow and the loss of soluble nutrients and flavor; these processes could lead to the formation of dry, hard, tasteless muscles and decreased meat quality (Lee et al., 2012). In the present trial, the drip loss decreased in response to the dietary HFC supplementation. The improvement of pH and water holding capacity must be related to the enhanced antioxidative status, and the sparing effect of dietary total polysaccharides and phenolic may play a beneficial role. In broiler meat, L* is used to estimate the incidence of paleness; a pale, soft, and exudative condition; or both (Van Laack et al., 2000). In the present study, treatments with HFC powder showed lower L* values and higher a* and b* values. A previous study demonstrated that increased L* and decreased a* values may be associated with increased metmyoglobin formation of the muscles (Fernández-Lo´ıpez et al., 2005). The presence of natural antioxidant compounds may retard metmyoglobin formation in meat and result in a decreased L* value (Fernández-Lo´ıpez et al., 2005). Added oregano (30 g/kg) conferred a higher b* value than in a non-supplemented group in chicken muscles (Young et al., 2003). Aksu and Kaya (2005) also found the un-added antioxidant kavurma (a cooked meat product) had lower b* values than those produced with antioxidant. HFC contains abundant secondary metabolites (antioxidants), such as phenolic compounds, and may be insusceptible to prooxidant substances that can react with oxymyoglobin; therefore, HFC may decrease autoxidation in metmyoglobin formation, causing increased color stability in meats. 5. Conclusions In conclusion, the results reported herein imply that HFC, a fermentation product of mushroom, contains a variety of secondary metabolites that can improve the performance, antioxidative capacity, and meat quality of broiler chickens. Therefore, HFC is a potential antioxidant that could be used in broilers feed. However, future experiments are required to elucidate the mechanisms for potential enhanced antioxidant activity, and determine the components responsible for these activities. Conflicts of interest The authors declare that there are no conflicts of interest. Acknowledgments This work was financially supported by the World Bank-financed Project for Quality and Safety of Agricultural Products in Jilin Province of China (No. 2011-Y18) and the Talent Cultivation Plan of Scientific Research Green Shoots in universities of the Education Department of Jilin Province of China (No. 201447). Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011

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Please cite this article in press as: Shang, H.M., et al., Influence of fermentation concentrate of Hericium caputmedusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Anim. Feed Sci. Tech. (2014), http://dx.doi.org/10.1016/j.anifeedsci.2014.09.011