Influence of fasting on muscle composition and antioxidant defenses of market-size Sparus macrocephalus

Influence of fasting on muscle composition and antioxidant defenses of market-size Sparus macrocephalus 1 3 first-author †E-mail:xiaodong_zh@163.comwutx@tianbang.com †E-mail:xiaodong_zh@163.comwutx@tianbang.com xiaodong_zh@163.com 2 corresp ‡Corresponding Author ‡Corresponding Author †E-mail:xiaodong_zh@163.comwutx@tianbang.com †E-mail:xiaodong_zh@163.comwutx@tianbang.com xiaodong_zh@163.com 3 1 3 School of Animal Sciences, Zhejiang University, Hangzhou 310027, China School of Animal Sciences, Zhejiang University, Hangzhou 310027, China Department of Chemistry, Zhejiang University, Hangzhou 310027, China Department of Chemistry, Zhejiang University, Hangzhou 310027, China Key Laboratory for Molecular Design and Nutrition Engineering, Ningbo Institute of Technology, Zhejiang University, Ningbo 315100, China Key Laboratory for Molecular Design and Nutrition Engineering, Ningbo Institute of Technology, Zhejiang University, Ningbo 315100, China The study was conducted to investigate fasting effects on flesh composition and antioxidant defenses of market-size Sparus macrocephalus . Two hundred fish (main initial weight 580 g) were divided into two groups (control and fasted) and reared in 6 cages. After two weeks of adaptation, group I fasted for 28 d; group II was fed normally as a control. In 3, 7, 14, 21 and 28 d, 6 fish per group were sampled for proximate flesh composition, liver antioxidant enzyme activities and malondialdehyde flesh content analyses. In fasted fish, the reduction of lipid content in muscle occurred after day 3, and, compared to controls, the content of protein decreased from day 14, the activities of liver antioxidative enzymes superoxide dismutase (SOD) and glutathione peroxidase (GPX) increased from day 3, and flesh malondialdehyde levels increased from day 21. Flesh fat reduction shows that fasting may be used as a technique to reduce flesh lipid content in Sparus macrocephalus . However, considering flesh protein loss and the subsequent oxidative stress, the fasting technique should be used with precautions. Antioxidant defenses Fasting Muscle composition Sparus macrocephalus INTRODUCTION 1 Under normal feeding situations, fish grow and store energy reserves, while metabolic demands to maintain life processes in fasted fish are met by mobilizing body nutrient stores leading to alterations in muscle proximate composition (Collins and Anderson, 1997 1997 ; Guderley et al., 2003 2003 ; Paul et al., 1995 1995 ; Power et al., 2000 2000 ). Unlike mammals, fish may survive long periods of starvation, so it is possible to use fasting as a technique to improve product quality by reducing flesh lipid content (Einen and Thomassen, 1998 1998 ; Rasmussen et al., 2000 2000 ). Studies in mammals showed that reactive oxygen species generated by fasting could not be adequately removed when the antioxidant defenses were overcome by pro-oxidant forces. The increased generation of ROS caused pro-oxidant effects, resulting in aging, lipid peroxidation and other body damages (Di Simplicio et al., 1997 1997 ; Robinson et al., 1997 1997 ; Bhat et al., 2007 2007 ; Vogt and Richie, 1993 1993 ). Lipid peroxidation is directly linked to rancidity in fish, which has a large influence on flesh quality (Gatta et al., 2000 2000 ; Ruff et al., 2003 2003 ). However, studies regarding the influence of fasting on antioxidant defenses and flesh lipid oxidation in fish are scarce (Bastrop et al., 1992 1992 ; Blom et al., 2000 2000 ; Guderley et al., 2003 2003 ; Pascual et al., 2003 2003 ; Viganò et al., 1993 1993 ), and it is important to study the effect of fasting on flesh quality from this respect. The aim of the present study was to investigate the effects of food deprivation on flesh composition and antioxidant defenses in market-size Sparus macrocephalus . This was performed to evaluate the possibility of using the fasting technique to manipulate the end product quality of Sparus macrocephalus and to establish the suitable duration of fasting. MATERIALS AND METHODS 1 Fish and rearing conditions 2 Sparus macrocephalus weighting (580±32) g were purchased from a private fish farm (Xiangshan Port, Zhejiang Province, China). Two hundred fish collected from a single net-cage were placed in 6 cages of 3 m 3 (1.5 m×1 m×2 m) in size and divided into 2 groups (three replicates each group). During adaptation to experimental conditions for 2 weeks, all fish were fed daily with a natural diet (trash fish) to apparent satiation. Following the adaptation period, one group was continuously fed (the control group) and another group fasted for 28 d. During the experimental period, water temperature and salinity were 22~29 °C and 38 g/L, respectively. Sampling 2 On days 3, 7, 14, 21 and 28, 6 Sparus macrocephalus per group (2 fish randomly captured from each replicate) were sampled and dissected in a box containing sea water and ice. After removal, liver samples were carefully cleaned of adhering then stored in liquid nitrogen prior to analysis for hepatic antioxidant defense enzyme activities. Each fish was filleted from the left side after discarding the skin. Four pieces of fillet from different part of the fish [upper and lower (belly flap side)] were obtained. Flesh samples were stored in liquid nitrogen until analyses for proximate composition and malondialdehyde (MDA) content. Proximate composition analysis 2 The proximate composition analysis of flesh was carried out according to the AOAC International ( 1999 1999 ) and reported on a wet weight basis. Tissue preparation for analytic procedure 2 Livers and fillets were rapidly thawed and manually homogenized, using a potter homogenizer with a glass pestle, in 9 volumes of ice-cold normal saline (0.86%). All procedures were performed on ice. Homogenates were frozen at −20 °C for 5 min and centrifuged for 15 min at 4000×g (Hitachi CPWX centrifuge, Hitachi Koki Co., Ltd., Japan), and the resultant supernatants were collected for biochemical assays. Detection of superoxide dismutase (SOD) 2 The activity of SOD was assayed by the method of Oyanagui ( 1984 1984 ). Superoxide anion radical, produced in the reaction of xanthine with O 2 catalyzed by xanthine oxydase, reacts with hydroxylamine producing nitric ion. After nitric ion reacting with naphthalene diamine, sulfanilic acid produces a colored product. The concentration of this mixture is proportional to the amount of produced superoxide anion radical. Increase of absorbance is assayed at 550 nm. Liver SOD activity is expressed in unit per milligram of protein (U/mg protein). One unit (U) means 50% of inhibition by SOD of nitric ion production in this condition. Detection of glutathione peroxidase 2 The activity of GPX was determined by quantifying the rate of H 2 O 2 -induced oxidation of reduced glutathione (GSH) to oxidized glutathione (GSSH). A yellow product which had absorbance at 412 nm could be formed as GSH reacted with dithiobisnitrobenzoic acid (Xia and Zhu, 1987 1987 ). One unit (U) of GPX was defined as the amount that reduced the level of GSH by 1 μmol/L in 1 min per milligram of liver protein. Liver GPX activity was expressed in milli-unit per milligram of protein (mU/mg protein). Detection of lipid oxidation 2 The level of lipid peroxidation was indicated by the content of MDA in muscle tissue. Thiobarbituric acid reaction (TBAR) method was used to determine the MDA which can be measured at the wavelength of 532 nm by reacting with thiobarbituric acid (TBA) to form a stable chromophoric production (Ohkawa et al., 1979 1979 ). MDA content was expressed as nanomoles per milligram of protein (nmol/mg protein). Statistical analysis 2 The SPSS 10.0 (SPSS Inc., Chicago, IL, USA) package was used for the statistical analysis. A multiple comparison (Student-Neuwman-Keuls) was used to determine the difference within groups. The differences between groups were evaluated with a Paired-Samples t -test. RESULTS 1 Fasting had a notable influence on flesh proximate composition (Table 1 1 ). In fasted fish, the flesh moisture increased significantly ( P < 0.05) after day 14 and remained high to the end. The content of protein in muscle decreased significantly ( P < 0.05) from day 14 to day 28. A significant ( P < 0.05) reduction of lipid content occurred from day 3 in fasted fish and kept low levels to the end. Group I was fasted group; Group II was fed group. Means in the same column with different lowercase superscript were significantly different ( P < 0.05) in the same group at different sampling dates. Means in the same row with different uppercase superscript were significantly different ( P < 0.05) at the same sampling date between two groups ( n =6) 2 Days of fasting 2 Moisture 2 Lipid 2 Protein Group I Group II Group I Group II Group I Group II 3 754.0±6.9 aA 748.0±8.1 aA 42.5±1.9 aA 48.4±2.6 aB 179.1±7.0 aA 180.2±5.8 aA 7 758.5±9.8 aA 751.3±7.7 aA 32.7±4.5 bA 50.1±4.3 aB 176.1±4.9 aA 175.7±6.9 aA 14 769.2±10.9 bA 755.7±4.6 aB 18.9±5.2 cA 48.2±2.7 aB 168.9±5.0 aA 177.9±4.3 aB 21 772.3±5.6 cA 747.2±8.3 aB 12.4±2.1 cA 47.5±3.1 aB 159.4±6.6 bA 182.8±7.6 aB 28 778.8±8.6 cA 743.5±7.4 aB 10.3±2.4 dA 51.4±3.6 aB 156.9±5.8 bA 187.0±7.7 aB Hepatic activities of SOD in fasted group significantly ( P < 0.05) increased from day 3 and kept high to the end of the experiment compared to the fed group (Fig. 1 1 ). Hepatic activities of GPX in fasted fish also increased from day 3 and kept high to day 28 compared to the controls. At day 21 the GPX activity in fasted group was higher than that in the fed group, but the difference was not significant ( P =0.134) (Fig. 2 2 ). Within the fasted group, hepatic activities of SOD and GPX did not vary significantly at different days of sampling. Fasting had a notable influence on lipid peroxidation in the flesh of Sparus macrocephalus (Fig. 3 3 ). Fasting did not affect the level of MDA on day 3, 7, or 14. The levels of MDA were significantly ( P < 0.05) higher in fasted group than those in the fed group on days 21 and 28. The highest MDA levels were found in fasted fish at day 28, reaching level of (19.9±2.5) nmol/mg protein. DISCUSSION AND CONCLUSION 1 There are remarkable differences in flesh quality, especially the flesh lipid content, between reared and wild fish (Bergstrom, 1989 1989 ; Rueda et al., 1997 1997 ; Stroud and Dalgarno, 1982 1982 ). In comparison with intensively reared fish, wild fish are usually considered as non-fatty fish. Higher lipid level in cultured fish is a general phenomenon observed for a variety of species studied (Ackman and Takeuchi, 1986 1986 ; Aubourg et al., 2007 2007 ; George and Bhopal, 1995 1995 ; Grigorakis et al., 2002 2002 ). The high content of lipid in reared fish is highly susceptible to oxidation, one of the major problems of flesh quality postslaughter (Baker, 2001 2001 ; Ruff et al., 2003 2003 ; Waagbø et al., 1993 1993 ). Fasting can lead to alterations in muscle proximate composition and fat depots, and this technique has been already proved effective in end product improvement of the salmonids (Einen and Thomassen, 1998 1998 ; Rasmussen et al., 2000 2000 ) and gilthead sea bream (Grigorakis and Alexis, 2005 2005 ). However, the energy utilization differs among aquatic species and fasting technique is not always effective. For example, perivisceral adipose tissue was utilized first in rainbow trout during the starvation (Jezierska et al., 1982 1982 ). In this study, the significant reduction of flesh lipid content in fasted fish occurred from day 3 and kept low levels to day 28 compared to controls. The flesh protein content in fasted fish decreased significantly after day 14 in comparison with the controls, while no difference was found before day 7. This suggests that, in fasted Sparus macrocephalus , protein starts to mobilize after the fat depots. It seems that the energy utilization in Sparus macrocephalus is similar to the gilthead sea bream ( Sparus aurata L.), but the gilthead sea bream saved protein for 3 weeks (Grigorakis and Alexis, 2005 2005 ). However, the present results differ from findings in red porgy ( Pagrus pagrus L.) that showed an initial protein mobilization during the first 14 d of fasting (Rueda et al., 1998 1998 ). Thus, this fasting technique may not be fit for other farmed aquatic species. The results in the present study indicate that fasting technique is effective to decrease flesh lipid content in Sparus macrocephalus , thus improving end product quality. To avoid protein loss, the fasting duration ought to be controlled within 7 d. To evaluate the effects of fasting on the antioxidant defenses in Sparus macrocephalus , we examined the hepatic activity of some antioxidative enzymes and the levels of flesh MDA. With respect to antioxidative enzymes, our results showed a significant increase of SOD activity (Fig. 1 1 ) in the liver of fasted fish from day 3, which suggests that a rise in the O 2 − generation rate might have taken place. The increased SOD activity in fasted fish would result in a higher generation of H 2 O 2 . Actually, results of the H 2 O 2 -scavenging enzyme seem to confirm this fact. Hepatic activity of GPX (Fig. 2 2 ) in fasted fish increased after day 3 and kept high to day 28. An increase of hepatic SOD activity had also been reported in sea bream ( S . aurata ) deprived of food for 46 d (Pascual et al., 2003 2003 ). In Dentex dentex deprived of food for 5 weeks, the increases of hepatic SOD and GPX activities had also been reported (Morales et al., 2004 2004 ). These results indicate that the fasting technique gradually generates oxidative stress. MDA is a metabolite derived from lipid peroxidation and has been widely used as an indicator of oxidative damage and flesh quality (Frigg et al., 1990 1990 ; Halliwell and Gutteridge, 1996 1996 ; Winston and Di Giulio, 1991 1991 ). The flesh MDA levels in Sparus macrocephalus (fasted and fed) are shown in Fig. 3 3 . Fasting did not affect the levels of MDA at the initial days, but started to increase after 21 d. Compared to the controls, the highest MDA levels were found in fish at day 28, where an eight-fold increase in MDA levels was observed compared to the control. These results show that the antioxidant defenses are overcome by pro-oxidant forces, and reactive oxygen species are not adequately removed from day 21. Partial food deprivation has been also reported to increase MDA levels in the livers of rainbow trout, O . mykiss (Hidalgo et al., 2002 2002 ) and S . aurata (Pascual et al., 2003 2003 ). Our results suggest that fasting enhanced reactive oxygen species generation in Sparus macrocephalus and that from day 21 the body defenses were not able to effectively scavenge these reactive oxygen species, thus leading to flesh lipid peroxidation. This lipid peroxidation phenomenon might have a large influence on flesh quality postslaughter, along with autolytic and bacterial spoilage (Watanabe et al., 1996 1996 ); therefore, the fasting duration should be carefully controlled. The present study demonstrated effects of fasting on fish flesh proximate composition, hepatic activity of some antioxidative enzymes and the levels of flesh MDA in Sparus macrocephalus . The overall balanced data show that fasting can effectively decrease flesh lipid content during autumn (water temperature were 22~29 °C). Considering flesh protein losses and the flesh lipid peroxidation, we suggest the duration of fasting for Sparus macrocephalus should not be longer than 7 d. References RG Ackman , T Takeuchi . Comparison of fatty acids and lipids of smolting hatchery fed and wild Atlantic salmon Salmo salar . Lipids , 1986 . 21 ( 2 ): 117 - 120 . 3959772 DOI: 10.1007/BF02534431 http://doi.org/10.1007/BF02534431 . Comparison of fatty acids and lipids of smolting hatchery fed and wild Atlantic salmon Salmo salar AOAC (Association of Analytical Chemist) International Official Methods of Analysis of the Association of Analytical Chemists International , 1999 . 16 Ed : Gaithersburg, Maryland, USA AOAC International , . Official Methods of Analysis of the Association of Analytical Chemists International SP Aubourg , V Losada , R Prego . Distribution of lipids and trace minerals in different muscle sites of farmed and wild turbot ( Psetta maxima ) . Int J Food Sci Technol , 2007 . OnlineEarly Articles DOI: 10.1111/j.1365-2621.2006.01364.x http://doi.org/10.1111/j.1365-2621.2006.01364.x . Distribution of lipids and trace minerals in different muscle sites of farmed and wild turbot (Psetta maxima) RTM Baker . SC Kestin , PD Warriss . The Effect of Certain Micronutrients on Fish Flesh Quality . Farmed Fish Quality , 2001 . : Oxford, UK Blackwell Science Ltd , 180 - 191 . . The Effect of Certain Micronutrients on Fish Flesh Quality R Bastrop , K Jürss , R Wacke . Biochemical parameters as a measure of food availability and growth in immature rainbow trout ( Oncorhynchus mykiss ) . Comp Biochem Physiol Part A: Physiol , 1992 . 102 ( 1 ): 151 - 161 . DOI: 10.1016/0300-9629(92)90028-O http://doi.org/10.1016/0300-9629(92)90028-O . Biochemical parameters as a measure of food availability and growth in immature rainbow trout (Oncorhynchus mykiss) E Bergstrom . Effect of natural and artificial diets on seasonal changes in fatty acid composition and total body lipid content of wild and hatchery reared Atlantic salmon ( Salmo salar L.) parr-smolt . Aquaculture , 1989 . 82 ( 1-4 ): 205 - 217 . DOI: 10.1016/0044-8486(89)90409-2 http://doi.org/10.1016/0044-8486(89)90409-2 . Effect of natural and artificial diets on seasonal changes in fatty acid composition and total body lipid content of wild and hatchery reared Atlantic salmon (Salmo salar L.) parr-smolt MS Bhat , G Rao , KD Murthy , PG Bhat . Housing in pyramid counteracts neuroendocrine and oxidative stress caused by chronic restraint in rats . Oxford Journals , 2007 . 4 ( 1 ): 35 - 42 . DOI: 10.1093/ecam/nel049 http://doi.org/10.1093/ecam/nel049 . Housing in pyramid counteracts neuroendocrine and oxidative stress caused by chronic restraint in rats S Blom , TB Andersson , L Förlin . Effects of food deprivation and handling stress on head kidney 17α-hydroxyprogesterone 21-hydroxylase activity, plasma cortisol and the activities of liver detoxification enzymes in rainbow trout . Aquat Toxicol , 2000 . 48 ( 2-3 ): 265 - 274 . 10686331 DOI: 10.1016/S0166-445X(99)00031-4 http://doi.org/10.1016/S0166-445X(99)00031-4 . Effects of food deprivation and handling stress on head kidney 17α-hydroxyprogesterone 21-hydroxylase activity, plasma cortisol and the activities of liver detoxification enzymes in rainbow trout AL Collins , TA Anderson . The influence of changes in food availability on the activities of key degradative and metabolic enzymes in the liver and epaxial muscle of the golden perch . J Fish Biol , 1997 . 50 ( 6 ): 1158 - 1165 . DOI: 10.1111/j.1095-8649.1997.tb01644.x http://doi.org/10.1111/j.1095-8649.1997.tb01644.x . The influence of changes in food availability on the activities of key degradative and metabolic enzymes in the liver and epaxial muscle of the golden perch P Di Simplicio , R Rossi , S Falcinelli , R Ceserani , ML Formento . Antioxidant status of various tissues of themouse after fasting and swimming stress . Eur J Appl Physiol , 1997 . 76 ( 4 ): 302 - 307 . DOI: 10.1007/s004210050252 http://doi.org/10.1007/s004210050252 . Antioxidant status of various tissues of themouse after fasting and swimming stress O Einen , MS Thomassen . Starvation prior to slaughter in Atlantic salmon ( Salmo salar ) II. White muscle composition and evaluation of freshness, texture and colour characteristics in raw and cooked fillets . Aquaculture , 1998 . 169 ( 1-2 ): 37 - 53 . DOI: 10.1016/S0044-8486(98)00332-9 http://doi.org/10.1016/S0044-8486(98)00332-9 . Starvation prior to slaughter in Atlantic salmon (Salmo salar) II. White muscle composition and evaluation of freshness, texture and colour characteristics in raw and cooked fillets M Frigg , AL Prabucki , EU Ruhdel . Effect of dietary vitamin E levels on oxidative stability of trout fillets . Aquaculture , 1990 . 84 ( 2 ): 145 - 158 . DOI: 10.1016/0044-8486(90)90344-M http://doi.org/10.1016/0044-8486(90)90344-M . Effect of dietary vitamin E levels on oxidative stability of trout fillets PP Gatta , M Pirini , S Testi , G Vignola , PG Monetti . The influence of different levels of dietary vitamin E on sea bass Dicentrarchus labrax flesh quality . Aquacult Nutr , 2000 . 6 ( 1 ): 47 - 52 . DOI: 10.1046/j.1365-2095.2000.00127.x http://doi.org/10.1046/j.1365-2095.2000.00127.x . The influence of different levels of dietary vitamin E on sea bass Dicentrarchus labrax flesh quality R George , R Bhopal . Fat composition of free living and farmed sea species: implications for human diet and sea-farming techniques . Br Food J , 1995 . 97 ( 8 ): 19 - 22 . DOI: 10.1108/00070709510100073 http://doi.org/10.1108/00070709510100073 . Fat composition of free living and farmed sea species: implications for human diet and sea-farming techniques K Grigorakis , MN Alexis . Effects of fasting on the meat quality and fat deposition of commercial-size farmed gilthead sea bream ( Sparus aurata L.) fed different dietary regimes . Aquac Nutr , 2005 . 11 ( 5 ): 341 - 344 . DOI: 10.1111/j.1365-2095.2005.00351.x http://doi.org/10.1111/j.1365-2095.2005.00351.x . Effects of fasting on the meat quality and fat deposition of commercial-size farmed gilthead sea bream (Sparus aurata L.) fed different dietary regimes K Grigorakis , MN Alexis , KDA Taylor , M Hole . Comparison of wild and cultured gilthead sea bream ( Sparus aurata ): composition, appearance and seasonal variations . Int J Food Sci Technol , 2002 . 37 ( 5 ): 477 - 484 . DOI: 10.1046/j.1365-2621.2002.00604.x http://doi.org/10.1046/j.1365-2621.2002.00604.x . Comparison of wild and cultured gilthead sea bream (Sparus aurata): composition, appearance and seasonal variations H Guderley , D Lapointe , M Bédard , JD Dutil . Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L . Comp Biochem Physiol Part A: Mol Integr Physiol , 2003 . 135 ( 2 ): 347 - 356 . DOI: 10.1016/S1095-6433(03)00089-8 http://doi.org/10.1016/S1095-6433(03)00089-8 . Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L B Halliwell , JMC Gutteridge . B Halliwell , JMC Gutteridge . Lipid Peroxidation: A Radical Chain Reaction . Free Radicals in Biology and Medicine , 1996 . : Oxford Clarendon Press , 188 - 266 . . Lipid Peroxidation: A Radical Chain Reaction MC Hidalgo , A Expósito , JM Palma , M de la Higuera . Oxidative stress generated by dietary Zn-deficiency: studies in rainbow trout ( Oncorhynchus mykiss ) . Int J Biochem Cell Biol , 2002 . 34 ( 2 ): 183 - 193 . 11809421 DOI: 10.1016/S1357-2725(01)00105-4 http://doi.org/10.1016/S1357-2725(01)00105-4 . Oxidative stress generated by dietary Zn-deficiency: studies in rainbow trout (Oncorhynchus mykiss) B Jezierska , JR Hazel , SD Gerking . Lipid mobilization during starvation in the rainbow trout, Salmo gairdneri Richardson, with attention to fatty acids . J Fish Biol , 1982 . 21 ( 6 ): 681 - 692 . DOI: 10.1111/j.1095-8649.1982.tb02872.x http://doi.org/10.1111/j.1095-8649.1982.tb02872.x . Lipid mobilization during starvation in the rainbow trout, Salmo gairdneri Richardson, with attention to fatty acids AE Morales , A Pérez-Jiménez , M Carmen Hidalgo , E Abellán , G Cardenete . Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver . Comp Biochem Physiol Part C: Toxicol Pharmacol , 2004 . 139 ( 1-3 ): 153 - 161 . DOI: 10.1016/j.cca.2004.10.008 http://doi.org/10.1016/j.cca.2004.10.008 . Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver H Ohkawa , N Ohishi , K Yagi . Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction . Anal Biochem , 1979 . 95 ( 2 ): 351 - 358 . 36810 DOI: 10.1016/0003-2697(79)90738-3 http://doi.org/10.1016/0003-2697(79)90738-3 . Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Y Oyanagui . Reevaluation of assay methods and establishment of kit for superoxide dismutase activity . Anal Bichem , 1984 . 142 ( 2 ): 290 - 294 . DOI: 10.1016/0003-2697(84)90467-6 http://doi.org/10.1016/0003-2697(84)90467-6 . Reevaluation of assay methods and establishment of kit for superoxide dismutase activity P Pascual , JR Pedrajas , F Toribio , J López-Barea , J Peinado . Effect of food deprivation on oxidative stress biomarkers in fish ( Sparus aurata ) . Chem Biol Interact , 2003 . 145 ( 2 ): 191 - 199 . 12686495 DOI: 10.1016/S0009-2797(03)00002-4 http://doi.org/10.1016/S0009-2797(03)00002-4 . Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata) AJ Paul , JM Paul , RL Smith . Compensatory growth in Alaska yellowfin sole, Pleuronectes asper , following food deprivation . J Fish Biol , 1995 . 46 ( 3 ): 442 - 448 . DOI: 10.1111/j.1095-8649.1995.tb05984.x http://doi.org/10.1111/j.1095-8649.1995.tb05984.x . Compensatory growth in Alaska yellowfin sole, Pleuronectes asper, following food deprivation DM Power , J Melo , CRA Santos . The effect of food deprivation and refeeding on the liver, thyroid hormones and transthyretin in sea bream . J Fish Biol , 2000 . 56 ( 2 ): 374 - 387 . DOI: 10.1111/j.1095-8649.2000.tb02112.x http://doi.org/10.1111/j.1095-8649.2000.tb02112.x . The effect of food deprivation and refeeding on the liver, thyroid hormones and transthyretin in sea bream RS Rasmussen , TH Ostenfeld , E McLean . Growth and feed utilisation of rainbow trout subjected to changes in feed lipid concentrations . Aquac Int , 2000 . 8 ( 6 ): 531 - 542 . DOI: 10.1023/A:1009291227550 http://doi.org/10.1023/A:1009291227550 . Growth and feed utilisation of rainbow trout subjected to changes in feed lipid concentrations MK Robinson , RR Rustum , EA Chambers , JD Rounds , DW Wilmore , DO Jacobs . Starvation enhances hepatic free radical release following endotoxemia . J Surg Res , 1997 . 69 ( 2 ): 325 - 330 . 9224401 DOI: 10.1006/jsre.1997.5062 http://doi.org/10.1006/jsre.1997.5062 . Starvation enhances hepatic free radical release following endotoxemia FM Rueda , JA Lopez , FJ Martinez , S Zamora , P Divanach , M Kentouri . Fatty acids in muscle of wild and farmed red porgy, Pagrus pagrus . Aquac Nutr , 1997 . 3 ( 3 ): 161 - 165 . DOI: 10.1046/j.1365-2095.1997.00088.x http://doi.org/10.1046/j.1365-2095.1997.00088.x . Fatty acids in muscle of wild and farmed red porgy, Pagrus pagrus FM Rueda , FJ Martinez , M Kentouri , P Divanach . Effect of fasting and refeeding on growth and body composition of red porgy, Pagrus pagrus L . Aquac Res , 1998 . 29 ( 6 ): 447 - 452 . DOI: 10.1046/j.1365-2109.1998.00228.x http://doi.org/10.1046/j.1365-2109.1998.00228.x . Effect of fasting and refeeding on growth and body composition of red porgy, Pagrus pagrus L N Ruff , RD FitzGerald , TF Cross , K Hamre , JP Kerry . The effect of dietary vitamin E and C level on market-size turbot ( Scophthalmus maximus ) fillet quality . Aquac Nutr , 2003 . 9 ( 2 ): 91 - 103 . DOI: 10.1046/j.1365-2095.2003.00230.x http://doi.org/10.1046/j.1365-2095.2003.00230.x . The effect of dietary vitamin E and C level on market-size turbot (Scophthalmus maximus) fillet quality GD Stroud , EJ Dalgarno . Wild and farmed lobsters ( Homarus gammarus ). A comparison of yield, proximate chemical composition and sensory properties . Aquaculture , 1982 . 29 ( 1-2 ): 147 - 153 . DOI: 10.1016/0044-8486(82)90041-2 http://doi.org/10.1016/0044-8486(82)90041-2 . Wild and farmed lobsters (Homarus gammarus). A comparison of yield, proximate chemical composition and sensory properties L Viganò , A Arillo , M Bagnasco , C Bennicelli , F Melodia . Xenobiotic metabolizing enzymes in uninduced and induced rainbow trout ( Oncorhynchus mykiss ): effects of diets and food deprivation . Comp Biochem Physiol Part C: Comp Pharmacol , 1993 . 104 ( 1 ): 51 - 55 . DOI: 10.1016/0742-8413(93)90110-7 http://doi.org/10.1016/0742-8413(93)90110-7 . Xenobiotic metabolizing enzymes in uninduced and induced rainbow trout (Oncorhynchus mykiss): effects of diets and food deprivation BL Vogt , JP Richie . Fasting-induced depletion of glutathione in the aging mouse . Biochem Pharmacol , 1993 . 46 ( 2 ): 257 - 263 . 8347148 DOI: 10.1016/0006-2952(93)90412-P http://doi.org/10.1016/0006-2952(93)90412-P . Fasting-induced depletion of glutathione in the aging mouse R Waagbø , K Sandnes , OJ Torrisen , A Sandvin , Ø Lie . Chemical and sensory evaluation of fillets from Atlantic salmon ( Salmo salar ) fed three levels on n-3 polyunsaturated fatty acids at two levels of vitamin E . Food Chem , 1993 . 46 ( 4 ): 361 - 366 . DOI: 10.1016/0308-8146(93)90005-Z http://doi.org/10.1016/0308-8146(93)90005-Z . Chemical and sensory evaluation of fillets from Atlantic salmon (Salmo salar) fed three levels on n-3 polyunsaturated fatty acids at two levels of vitamin E F Watanabe , M Goto , K Abe , Y Nakano . Glutathione peroxidase activity during storage of fish muscle . J Food Sci , 1996 . 61 ( 4 ): 734 - 735 . DOI: 10.1111/j.1365-2621.1996.tb12192.x http://doi.org/10.1111/j.1365-2621.1996.tb12192.x . Glutathione peroxidase activity during storage of fish muscle GW Winston , RT Di Giulio . Prooxidant and antioxidant mechanisms in aquatic organisms . Aquat Toxicol , 1991 . 19 ( 2 ): 137 - 161 . DOI: 10.1016/0166-445X(91)90033-6 http://doi.org/10.1016/0166-445X(91)90033-6 . Prooxidant and antioxidant mechanisms in aquatic organisms YM Xia , LZ Zhu . Detection of glutathione peroxidase: DTNB method . J Hyg Res , 1987 . 16 ( 4 ): 29 - 32 . (in Chinese) . Detection of glutathione peroxidase: DTNB method 10.1631/jzus.2007.B0906 Project (No. 2006C12098) supported by the Science and Technology Department of Zhejiang Province, China 2007-08-06 2007-10-19 2022-01-05 Copyright © 2007, Journal of Zhejiang University Science 2007 Journal of Zhejiang University-SCIENCE B (Biomedicine and Biotechnology) 12 08