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Sesame oil in diets for lambari: Effects on growth parameters, corporal chemical composition and physiological alterations

Óleo de gergelim em dietas para lambari: Efeitos sobre o desempenho zootécnico, composição química corporal e alterações fisiológicas

ABSTRACT:

The inclusion of sesame oil associated with soybean, linseed and freshwater fish residue oil in the diets fed to LambarisAstyanax altiparanaewas evaluated by the growth performance parameters, body composition and possible physiological changes (GARUTTI & BRISTSKI, 2000). The experiment was a completely randomized design in two factorial parameters tested: three oil types (soy oil (SO), linseed oil (LO) and freshwater fish residue oil (FRO)), combined or not with sesame oil (SEO), totalizing six treatments and four replications 24 cages, capacity of 0.70m3 (density of 251 fish m-3). The fish (mean weight 2.35g±0.62g and mean length 5.25cm±0.68cm) were fed with the experimental diets twice a day. After 75 days, the following parameters were determined: body chemical composition and fatty acid profile, glycemia, liver (LG) and muscle glycogen (MG) levels, and lipid peroxidation (TBARS). Fish fed with diets containing SEO had higher desaturation index values of LNA while those fed with SEO combined with LO displayed reduced hepatic lipid oxidation. Inclusion of SEO improved the fatty acid profile and stability, without causing problems related to fish performance and health.

Key words:
Astyanax altiparanae ; fatty acids; nutrition; sesamin.

RESUMO:

Este trabalho fez a inclusão de óleo de gergelim associado ao óleo de soja, de linhaça e de resíduo de peixes de água doce nas dietas para avaliar o desempenho zootécnico, a composição química corporal e as possíveis alterações fisiológicas de lambariAstyanax altiparanae. O delineamento experimental foi inteiramente casualizado, avaliando-se dois parâmetros: três tipos de óleo (óleo de soja (SO), óleo de linhaça (LO) e óleo de resíduo de peixe de água doce (FRO)), associado ou não ao óleo de gergelim (SEO), totalizando seis tratamentos e quatro repetições (24 tanques-rede de capacidade útil de 0,70m3 (densidade de 251 peixes m-3). Os peixes (peso médio 2,35g±0,62g) e comprimento médio de 5,25cm±0,68cm) foram alimentados duas vezes ao dia com as dietas experimentais. Após 75 dias, foram feitas as análises de composição química e perfil de ácidos graxos corporal, glicemia, glicogênio hepático (LG) e muscular (MG), e peroxidação lipídica (TBARS) do tecido hepático. Os indivíduos que receberam dietas contendo SEO apresentaram valores mais altos de taxa de dessaturação de ácido linolênico; aqueles que receberam SEO e LO combinados demonstraram níveis reduzidos de oxidação lipídica do tecido hepático. A inclusão de SEO melhora o perfil de ácidos graxos e a estabilidade, sem provocar problemas relacionados ao desempenho e saúde dos peixes.

Palavras-chave:
ácidos graxos; Astyanax altiparanae ; nutrição; sesamina.

INTRODUCTION:

The interest for vegetal oils as an alternative lipid source has increased (NAYLOR et al., 2000NAYLOR, R.L. et al. Effect of aquaculture on world fish supplies. Nature, v.405, p.1017-1024, 2000. Available from: <Available from: http://10.1038/35016500 >. Accessed: Nov. 21, 2009. doi: 10.1038/35016500.
http://10.1038/35016500...
) because the inclusion of fishmeal and fish oil in the diet fed to fish led to increasing ration prices. However, it has been reported that in some marine fish species, the substitution of these ingredients can interfere with growth parameters, cause problems related to fish metabolism and consequently, the oxidative homeostasis, promoting the appearance of reactive oxygen species (ROS) (OLSVIK et al., 2011OLSVIK, P.A. et al. Hepatic oxidative stress in Atlantic salmon (Salmo salar L.) transferred from a diet based on marine feed ingredients to a diet based on plant ingredients., Aquaculture Nutrition v.17, p.424-436, 2011. Available from: <Available from: http://10.1111/j.1365-2095.2010.00778.x >. Accessed: Feb. 12, 2012. doi: 10.1111/j.1365-2095.2010.00778.x.
http://10.1111/j.1365-2095.2010.00778.x...
).

In tropical fish species such as Nile tilapia Oreochromis niloticus, the linolenic acid (LNA) included in the diets is converted to high unsaturated fatty acid (HUFA) such as the docosahexanoic acid (DHA). The LNA addition decreased the linoleic acid (LA) desaturation to HUFA n-6 due to the high affinity of the enzymes involved in desaturation and elongation processes with the n-3 fatty acids (CHEN et al., 2013CHEN, C. et al. N-3 essential fatty acids in Nile tilapia, Oreochromis niloticus: Quantification of optimum requirement of dietary linolenic acid in juvenile fish. Aquaculture, v.416-417, p.99-104, 2013. Available from: <Available from: http://10.1016/j.aquaculture.2013.09.003 >. Accessed: Sept. 23, 2014. doi: 10.1016/j.aquaculture.2013.09.003.
http://10.1016/j.aquaculture.2013.09.003...
). Likewise, the lambari Astyanax altiparanae(Garutti & Bristski, 2000) is also able to convert LNA into eicosapentaenoic acid (EPA) and DHA, and LA into arachidonic acid (AA) (GONÇALVES et al., 2012GONÇALVES, L.U. et al. Effect of the inclusion of fish residue oils in diets on the fatty acid profile of muscles of males and females lambari (Astyanax altiparanae)., Revista Brasileira de Zootecnia v.41, p.1967-1974, 2012. Available from: <Available from: http://10.1590/S1516-35982012000900001 >. Accessed: Feb. 23, 2014. doi: 10.1590/S1516-35982012000900001.
http://10.1590/S1516-35982012000900001...
; CAMPELO et al., 2014CAMPELO, D.A.V. et al. Conjugated linoleic acid in diets for lambari (Astyanax altiparanae) (Garutti & Britski, 2000). Aquaculture Nutrition, p. n/a-n/a, 2014. Available from: <Available from: http://doi.wiley.com/10.1111/anu.12203 >. Accessed: May 25, 2015. doi: 10.1111/anu.12203.
http://doi.wiley.com/10.1111/anu.12203...
).

The therapeutic properties of sesame oil (SEO) have been verified in experiments with rats. The SEO-containing diets reduced glycemia, blood cholesterol and triglyceride levels and prevented pathological problems like formation of hepatic steatosis, and renal sepsis caused by lipopolysaccharide (LPS) (HSU et al., 2005HSU, D.-Z. et al. Effect of sesame oil on oxidative-stress-associated renal injury in endotoxemic rats: involvement of nitric oxide and proinflammatory cytokines. Shock (Augusta, Ga.), v.24, n.3, p.276-280, 2005. Available from: <Available from: http://10.1097/01.shk.0000172366.73881.c7 >. Accessed: Aug. 22, 2013. doi: 10.1097/01.shk.0000172366.73881.c7.
http://10.1097/01.shk.0000172366.73881.c...
; GUIMARÃES & MACEDO, 2013GUIMARÃES, R.; MACEDO, M. Sesame and flaxseed oil: nutritional quality and effects on serum lipids and glucose in rats. Food Science and techonology, v.33, n.1, p.209-217, 2013. Available from: <Available from: http://dx.doi.org/10.1590/S0101-20612013005000029 >. Accessed: Jul. 21, 2014. doi: 10.1590/S0101-20612013005000029.
http://dx.doi.org/10.1590/S0101-20612013...
; PERIASAMY et al., 2014PERIASAMY, S. et al. Sesame oil mitigates nutritional steatohepatitis via attenuation of oxidative stress and inflammation: a tale of two-hit hypothesis. Journal of Nutritional Biochemistry, v.25, n.2, p.232-240, 2014. Available from: <Available from: http://10.1016/j.jnutbio.2013.10.013 >. Accessed: Mar. 22, 2015. doi: 10.1016/j.jnutbio.2013.10.013.
http://10.1016/j.jnutbio.2013.10.013...
). Moreover, the lignans contained in SEO such as sesamin, episamin and sesamolin, may promote the formation of fatty acids as the DHA, from the desaturation and elongation of LNA (TRATTNER et al., 2008aTRATTNER, S. et al. Sesamin increases alpha-linolenic acid conversion to docosahexaenoic acid in atlantic salmon (Salmo salar L.) hepatocytes: role of altered gene expression. Lipids, v.43, p.999-1008, 2008a. Available from: <Available from: http://10.1007/s11745-008-3229-7 >. Accessed: May 21, 2012. doi: 10.1007/s11745-008-3229-7.
http://10.1007/s11745-008-3229-7...
; KÖSE & YILDIZ, 2013KÖSE, I.; YILDIZ, M. Effect of diets containing sesame oil on growth and fatty acid composition of rainbow trout (Oncorhynchus mykiss). Journal of Applied Ichthyology, v.29, p.1318-1324, 2013. Available from: <Available from: http://10.1111/jai.12184 >. Accessed: Mar. 23, 2015. doi: 10.1111/jai.12184.
http://10.1111/jai.12184...
).

Therefore, this study evaluated how the inclusion of sesame oil associated with soy oil (SO), linseed oil (LO) or FRO (freshwater fish residue oil) in diets fed to lambari Astyanax altiparanae(Garutti & Bristski, 2000) affected the growth performance parameters, body chemical composition and determined possible physiological alterations.

MATERIALS AND METHODS:

Table 1 shows the formulation (COTAN et al., 2006COTAN, J.L.V. et al. Níveis de energia digestível e proteína bruta em rações para alevinos de lambari tambiú. Revista Brasileira de Zootecnia, v.35, n.3, p.634-640, 2006. Available from: <Available from: http://www.scielo.br/pdf/rbz/v35n3/30051.pdf >. Accessed: Jun. 21, 2015.
http://www.scielo.br/pdf/rbz/v35n3/30051...
) and composition of the extruded experimental diets (A.O.A.C, 1990A.O.A.C. (ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS). Official methods of the analysis. 15.ed. Arlington, Virginia: Association of Official Analytical chemists, 1990, v.1, 1117p.), and lipid profiles (A.O.A.C, 2005A.O.A.C. (ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS). Official methods of analysis of the Associaton of Official Analytical Chemists. 18.ed., Gaitherburg, Mayland: AOAC, 2005; method 996.06, p20-25.) are shown in table 2. During the experimental period of 75 days, 4,224 fish (mean weight 0.95g±0.46g and mean length 4.21cm±2.77cm) were distributed in 24 cages (capacity 0.70m3, density 251 fishes m-3). Fish were fed ad libitum twice a day (at 9:00 and 16:00). Water quality parameters such as temperature, dissolved oxygen rate, and pH were measured using the Multi-Parameter Water Quality Monitoring Meter (Horiba U-10), on alternate days. Ammonia and nitrite levels were monitored using kits and meters from Hanna Instruments, United States. Fish were weighed on days 0, 35 and 75, anesthetized with clove oil (50mg L-1 of water) (PEREIRA-DA-SILVA et al., 2009PEREIRA-SILVA, E.M. et al. Efeito anestésico do óleo de cravo em alevinos de lambari. Ciência Rural, v.39, p.1851-1856, 2009. Available from: <Available from: http://10.1590/S0103-84782009005000127 >. Accessed: Mar. 23, 2012. doi: 10.1590/S0103-84782009005000127.
http://10.1590/S0103-84782009005000127...
)cinco grupos de 30 alevinos (0,6/ufffd0,1g and euthanized via cranial drilling.

Table 1
Formulation and composition of experimental diets.
Table 2
Lipid profile of experimental diets, expressed in g/100g of total fatty acids.

The sampled fish were collected from those that fasted for 24 hours prior to sampling. The following variables were determined: diet consumption (DC), apparent feed conversion (AFC), weight gain (WG), specific growth rate (SGR) and protein efficiency rate (PER). The body chemical composition of whole fish was performed following the A.O.A.C. (1990A.O.A.C. (ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS). Official methods of the analysis. 15.ed. Arlington, Virginia: Association of Official Analytical chemists, 1990, v.1, 1117p.) methodology to determine dry matter (DM), crude protein (CP), mineral matter (MM), ethereal extract (EE), and crude energy (CE). A total of 25 fish were sampled per experimental unit, eviscerated and used to determine the fatty acid profile following the A.O.A.C. (2005A.O.A.C. (ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS). Official methods of analysis of the Associaton of Official Analytical Chemists. 18.ed., Gaitherburg, Mayland: AOAC, 2005; method 996.06, p20-25.) methodology. Lipid was extracted according to the BLIGH & DYER (1959BLIGH, E.G.; DYER, W.J. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, v.37, p.911-917, 1959. Available from: <Available from: http://10.1139/o59-099 >. Accessed: Apr. 21, 2014. doi: 10.1139/o59-099.
http://10.1139/o59-099...
) methodology.

Fish glycemia levels (n=10 per treatment) were measured by a portable glucose meter (Roche, Brazil) in a 5-µL blood aliquot that was collected in the caudal vein region using heparinized insulin type syringes. The glycogen was quantified in 10mg of liver samples (LG) (n=14 per treatment) and 100mg of muscles (MG) (n=4 per treatment) following DUBOIS et al. (1956) modified by BIDINOTTO et al. (1997BIDINOTTO, M. et al. Hepatic glycogen and glucose in eight tropical fresh-water teleost cist for field determination of micro-samples. Boletim Tecnológico do Centro de Pesquisa e Treinamento em Aquicultura (CEPTA), v.10, p.53-70, 1997. Available from: <Available from: http://www.icmbio.gov.br/cepta/images/stories/producao_cientifica/hepatic_1997_01.pdf >. Accessed: Nov. 24, 2012.
http://www.icmbio.gov.br/cepta/images/st...
).

The thiobarbituric acid reactive substances (TBARS) were determined in hepatic tissues (n=6 per treatment) following the VYNCKE (1970VYNCKE, W. Direct determination of the thiobarbituric acid value in trichloracetic acid extracts of fish as a measure of oxidative rancidity. Fatte Seifen Anstrichmittel, v.72, p.1084-1087, 1970. Available from: <Available from: http://10.1002/lipi.19700721218 >. Accessed: Nov. 21, 2012. doi: 10.1002/lipi.19700721218.
http://10.1002/lipi.19700721218...
) methodology adapted to microplate reader by modifying the proportions described by this author. The data were submitted to ANOVA (GLM procedure), using the SAS (2002SAS INSTITUTE. SAS/STAT user's guide. Cary, NC, 2002. Version 9.2.) software. The F-test results showed significant differences among treatments. The LG and TBARS data were previously treated by the SAS/LAB command.

RESULTS AND DISCUSSION:

Water quality parameters such as temperature, dissolved oxygen and pH were kept between 23.42 and 27.07ºC; 3.62 and 6.45mg L-1; and, 6.63 and 7.23, respectively. Ammonia and nitrite levels did not exceed 0.34 and 0.41mg L-1, respectively. The growth parameters and body chemical composition (P<0.05) were not significantly different for fish fed with diets containing SO, LO and FRO, combined or not with SEO. However, the addition of SEO to the diets affected significantly glycemia and lipid peroxidation of hepatic tissue (TBARS) (Table 3). In addition, independent of the treatment, the glycemic levels above 49mg DL-1 (PEREIRA-DA-SILVA et al., 2014PEREIRA-DA-SILVA, E.M. et al. Menthol as anaesthetic for lambari Astyanax altiparanae (Garutti & Britski 2000): attenuation of stress responses. Aquaculture Research, p. n/a-n/a, 2014. Available from: <Available from: http://10.1111/are.12599 >. Accessed: Jun. 23, 2014. doi: 10.1111/are.12599.
http://10.1111/are.12599...
) indicated that the fish underwent handling and capture stress during sampling (BARTON, 2002BARTON, B.A. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology, v.42, p.517-525, 2002. Available from: <Available from: http://10.1093/icb/42.3.517 >. Accessed: Dec. 21, 2013. doi: 10.1093/icb/42.3.517>.
http://10.1093/icb/42.3.517...
). Addition of SEO to the LO diet increased the blood glucose levels in fish. For the lambari, the lipid sources did not change the hepatic and muscular glycogen levels significantly. However, some fatty acids may have interfered with glycogen formation, such as the oleic acid, which modifies the activity of the enzymes involved in the glucose metabolism and hepatic reserves of rainbow trout (LIBRÁN-PÉREZ et al., 2013LIBRÁN-PÉREZ, M. et al. Response of hepatic lipid and glucose metabolism to a mixture or single fatty acids: possible presence of fatty acid-sensing mechanisms. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology, v.164, n.1, p.241248, 2013. Available from: <Available from: http://10.1371/journal.pone.0059507 >. Accessed: Dec. 21, 2014. doi: 10.1371/journal.pone.0059507.
http://10.1371/journal.pone.0059507...
).

Table 3
Mean values of growth performance variables, body chemical composition and physiologic state.

The high lipid peroxidation observed in the fish fed with LO diet can be explained by the probable high quantity of PUFA n-3 in the hepatic tissues. Lower quantity of PUFA n-3 in the diets reduces fish susceptibility to these oxidative reactions. This fact has been demonstrated in a seabass Lateolabrax japonicus study, in which the fish were fed with diets that contained palm oil associated with fish oil and presented lower malondialdehyde levels (MDA) (GAO et al., 2012GAO, J. et al. Effects of dietary palm oil supplements with oxidized and non-oxidized fish oil on growth performances and fatty acid compositions of juvenile Japanese sea bass, Lateolabrax japonicus., Aquaculture v.324-325, p.97-103, 2012. Available from: <Available from: http://www.sciencedirect.com/science/article/pii/S0044848611008477 >. Accessed: Sept. 24, 2014. doi: 10.1016/j.aquaculture.2011.10.031.
http://www.sciencedirect.com/science/art...
). The ingested PUFAs are stocked in the liver and are susceptible to peroxidation due to the activation of the peroxisome proliferator-activated receptor (PPARα) that produces hydrogen peroxide and causes tissue damages. Thus, liver is the first organ susceptible to stress oxidative reactions and, consequently, lipid peroxidation (TAKAHASHI et al., 2002TAKAHASHI, M. et al. Fish oil feeding alters liver gene expressions to defend against PPARalpha activation and ROS production. American Journal of Physiology. Gastrointestinal and liver physiology, v.282, p.G338-G348, 2002. Available from: <Available from: http://10.1152/ajpgi.00376.2001 >. Accessed: Nov. 23, 2014. doi: 10.1152/ajpgi.00376.2001.
http://10.1152/ajpgi.00376.2001...
). In this research, SEO had a positive effect only on/when combined with LO.

Lipid profile of oils as shown in the lipid profile of the diets, changed significantly the saturated (SFA), monounsaturated (MUFA) and polyunsaturated (PUFA) fatty acids profiles of lambari, especially, the C14:0, C16:0, C16:1, oleic acid (C18:1n-9), linoleic acid (LA), linolenic acid (LNA), arachidonic acid (AA), eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) (Table 4). The addition of SEO increased the MUFA levels in fish fed the SO and LO diets. This oil is considered a source of MUFA since it contains about 46% in the lipid profile (KOCHHAR, 2002KOCHHAR, S.P. Sesame, rice-bran and flaxseed oils. In: GUNSTONE, F.D. (Ed.). Vegetable oils in food technology: composition, propreties and uses. Florida: Blackwell, 2002. p.297-326. ). However, the same tendency was not observed for the diets FRO combined or not with SEO due to the similar MUFA quantities in these diets composition (Table 1). The higher desaturation rates of LNA to HUFA n-3 were observed in fish that were fed with SEO in the diets. Also, it was verified that the SEO efficiently promotes DHA formation in fish fed with diets with reduced LNA levels (Table 4).

Table 4
Profiles of eviscerated fishes, describing main fatty acids, expressed in g/100g of total fatty acids.

The probable higher desaturation of LNA to HUFA-3 and the formation of DHA could be related to the presence of the bioactive compounds in SEO, such as sesamin. The addition of sesamin in diets containing linseed and sunflower oil modified significantly lipid metabolism and increased the DHA quantities in the white muscle of rainbow trouts Oncorhynchus mykiss and hepatocytes of Atlantic salmon Salmo salarL. (TRATTNER et al., 2008aTRATTNER, S. et al. Sesamin increases alpha-linolenic acid conversion to docosahexaenoic acid in atlantic salmon (Salmo salar L.) hepatocytes: role of altered gene expression. Lipids, v.43, p.999-1008, 2008a. Available from: <Available from: http://10.1007/s11745-008-3229-7 >. Accessed: May 21, 2012. doi: 10.1007/s11745-008-3229-7.
http://10.1007/s11745-008-3229-7...
, 2008bTRATTNER, S. et al. Sesamin supplementation increases white muscle docosahexaenoic acid (DHA) levels in rainbow trout (Oncorhynchus mykiss) fed high alpha-linolenic acid (ALA) containing vegetable oil: metabolic actions., Lipids v.43, p.989-997, 2008b. Available from: <Available from: http://10.1007/s11745-008-3228-8 >. Accessed: Apr. 22, 2012. doi: 10.1007/s11745-008-3228-8.
http://10.1007/s11745-008-3228-8...
) hepatocytes were incubated without or with a mixture of sesamin and episesamin in order to test for possible effects on lipid metabolism. Sesamin/episesamin exposure (0.05 mM, final concentration. This compound also increased the activity of enzymes related to β mitochondrial and peroxisomal oxidation, by activating PPARα in rats, and fish as the rainbow trout Oncorhynchus mykiss and Lates calcarifer (ASHAKUMARY et al., 1999ASHAKUMARY, L. et al. Sesamin, a sesame lignan, is a potent inducer of hepatic fatty acid oxidation in the rat. Metabolism: Clinical and Experimental, v.48, n.10, p.1303-1313, 1999. Available from: <Available from: http://www.metabolismjournal.com/article/S0026-0495(99)90272-X/abstract >. Accessed: Aug. 24, 2014. doi: 10.1016/S0026-0495(99)90272-X.
http://www.metabolismjournal.com/article...
; TRATTNER et al., 2008aTRATTNER, S. et al. Sesamin increases alpha-linolenic acid conversion to docosahexaenoic acid in atlantic salmon (Salmo salar L.) hepatocytes: role of altered gene expression. Lipids, v.43, p.999-1008, 2008a. Available from: <Available from: http://10.1007/s11745-008-3229-7 >. Accessed: May 21, 2012. doi: 10.1007/s11745-008-3229-7.
http://10.1007/s11745-008-3229-7...
; ALHAZZAA et al., 2012 ALHAZZAA, R. et al. Sesamin modulation of lipid class and fatty acid profile in early juvenile teleost, Lates calcarifer, fed different dietary oils. Food Chemistry, v.134, p.2057-2065, 2012. Available from: <Available from: http://dx.doi.org/10.1016/j.foodchem.2012.04.004 >. Accessed: Sept. 22, 2014. doi: 10.1016/j.foodchem.2012.04.004.
http://dx.doi.org/10.1016/j.foodchem.201...
).

CONCLUSION

The inclusion of sesame oil increased the DHA levels in fish tissues verified by the higher rates of desaturation of LNA to HUFAn-3, improving the lipid quality and promoting the oxidative stability of hepatic tissue, without altering the growth performance and fish health.

ACKNOWLEDGMENTS

The authors thanks the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the financial support (Process nº 2012/11101-0) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), by the grant for the first author.

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  • 1
    CR-2015-1011.R2

Publication Dates

  • Publication in this collection
    30 Apr 2016
  • Date of issue
    2016

History

  • Received
    13 July 2015
  • Accepted
    30 Jan 2016
  • Reviewed
    16 Apr 2016
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