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Serum metabolomic fingerprints of lambs fed chitosan and its association with performance and meat quality traits

Published online by Cambridge University Press:  15 April 2020

T. L. Pereira
Affiliation:
Department of Animal Science, Universidade Federal da Grande Dourados, Dourados, MS79804-970, Brazil
A. R. M. Fernandes
Affiliation:
Department of Animal Science, Universidade Federal da Grande Dourados, Dourados, MS79804-970, Brazil
E. R. Oliveira
Affiliation:
Department of Animal Science, Universidade Federal da Grande Dourados, Dourados, MS79804-970, Brazil
N. R. B. Cônsolo
Affiliation:
Department of Animal Science, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Duque de Caxias Norte 225, Pirassununga, SP13635-900, Brazil
O. F. C. Marques
Affiliation:
Department of Animal Science, Universidade Federal da Grande Dourados, Dourados, MS79804-970, Brazil
T. P. Maciel
Affiliation:
Department of Animal Science, Universidade Federal de Goias, Goiania, GO74690-900, Brazil
N. M. Pordeus
Affiliation:
Department of Animal Science, Universidade Federal da Grande Dourados, Dourados, MS79804-970, Brazil
L. C. G. S. Barbosa
Affiliation:
Department of Animal Science, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Duque de Caxias Norte 225, Pirassununga, SP13635-900, Brazil
V. L. M. Buarque
Affiliation:
Department of Animal Science, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Duque de Caxias Norte 225, Pirassununga, SP13635-900, Brazil
A. R. H. Padilla
Affiliation:
EMBRAPA Instrumentação, XV de Novembro 1452, São Carlos, SP13560-970, Brazil
L. A. Colnago
Affiliation:
EMBRAPA Instrumentação, XV de Novembro 1452, São Carlos, SP13560-970, Brazil
J. R. Gandra*
Affiliation:
Department of Animal Science, Universidade Federal da Grande Dourados, Dourados, MS79804-970, Brazil
*
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Abstract

Chitosan (CHI) is a natural biopolymer with antimicrobial, anti-inflammatory, antioxidant and digestive modulatory effects, which can be used in the ruminant diet to replace antibiotics. The aim of this study was to evaluate the effects of CHI on lamb growth traits, nutrients digestibility, muscle and fatty deposition, meat fatty acid (FA) profile, meat quality traits and serum metabolome. Thirty 30-month-old male lambs, half Suffolk and half Dorper, with an average BW of 21.65 ± 0.86 kg, were fed in a feedlot system for a total of 70 days. The lambs were separated into two groups according to the diet: the control (CON) group which received the basal diet and the CHI group which received the basal diet with the addition of CHI as 2 g/kg of DM in the diet. Lambs supplemented with CHI had a greater (P < 0.05) final BW, DM intake, final body metabolic weight (P < 0.05) and lower residual feed intake than the CON group. Animals fed CHI had a greater (P < 0.05) starch digestibility at 14 and 28 days, average daily gain at 14, 42 and 56 days, greater feed efficiency at 28 days and feed conversation at 14 and 42 days in feedlot. Most of the carcass traits were not affected (P > 0.05) by the treatment; however, the CHI supplementation improved (P < 0.05) dressing and longissimus muscle area. The treatments had no effect (P > 0.05) on the meat colour and other quality measurements. Meat from the CHI-fed lambs had a greater concentration (P < 0.05) of oleic-cis-9 acid, linoleic acid, linolenic-trans-6 acid, arachidonic acid and eicosapentaenoic acid. According to the variable importance in projection score, the most important metabolites to differentiate between the CON and the CHI group were hippurate, acetate, hypoxanthine, arginine, malonate, creatine, choline, myo-inositol, 2-oxoglutarate, alanine, glycerol, carnosine, histidine, glutamate and 3-hydroxyisobutyrate. Similarly, fold change (FC) analysis highlighted succinate (FC = 1.53), arginine (FC = 1.51), hippurate (FC = 0.68), myo-inositol (FC = 1.48), hypoxanthine (FC = 1.45), acetate (FC = 0.73) and malonate (FC = 1.35) as metabolites significantly different between groups. In conclusion, the present data showed that CHI changes the muscle metabolism improving muscle mass deposition, the lamb’s performance and carcass dressing. In addition, CHI led to an alteration in the FA metabolism, changes in the meat FA profile and improvements in meat quality.

Type
Research Article
Copyright
© The Animal Consortium 2020

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References

Association of Official Analytical Chemists 2000. Official methods of analysis, 17th edition. AOAC International, Gaithersburg, Maryland, USA.Google Scholar
American Meat Science Association 1995. Research guidelines for cookery, sensory evaluation and instrumental tenderness measurements of fresh meat. AMSA, Chicago, IL, USA.Google Scholar
Araújo, APC, Venturelli, BC, Santos, MCB, Gardinal, R, Cônsolo, NRB, Calomeni, GD, Freitas, JE, Barletta, RV, Gandra, JR, Paiva, PG and Rennó, FP 2015. Chitosan affects total nutrient digestion and ruminal fermentation in Nellore steers. Animal Feed Science and Technology 206, 114118.CrossRefGoogle Scholar
Boerboom, G, Van Kempen, T, Navarro-villa, A and Adriano, P 2018. Unraveling the cause of white striping in broilers using metabolomics. Poutry Science 97, 39773986.CrossRefGoogle ScholarPubMed
Bokura, H and Kobayashi, S 2003. Chitosan decreases total cholesterol in women: A randomized, double-blind, placebo-controlled trial. European Journal of Clinical Nutrition 57, 721725.CrossRefGoogle ScholarPubMed
Bowman, CE, Rodriguez, S, Selen Alpergin, ES, Acoba, MG, Zhao, L, Hartung, T, Claypool, SM, Watkins, PA and Wolfgang, MJ 2017. The mammalian malonyl-CoA synthetase ACSF3 is required for mitochondrial protein malonylation and metabolic efficiency. Cell Chemical Biology 24, 673684.e4.CrossRefGoogle Scholar
Bryant, TC, Wagner, JJ, Tatum, JD, Galyean, ML, Anthony, RV and Engle, TE 2010. Effect of dietary supplemental vitamin A concentration on performance, carcass merit, serum metabolites, and lipogenic enzyme activity in yearling beef steers. Journal of Animal Science 88, 14631478.CrossRefGoogle ScholarPubMed
Christie, WW 1982. A simple procedure for rapid transmethylation of glycerolipids and cholesteryl esters. Journal of Lipid Research 23, 10721075.Google ScholarPubMed
Cônsolo, NRB, Silva, J, Buarque, VLM, Higuera-padilla, A, Barbosa, LCGS, Zawadzki, A, Colnago, LA, Saran Netto, A, Gerrard, DE and Silva, SL 2020. Selection for growth and precocity alters muscle metabolism in Nellore cattle. Metabolites 58, 112.Google Scholar
Costa, MB da, Cônsolo, NRB, Silva, J, Buarque, VLM, Padilla, ARH, Coutinho, ID, Barbosa, LCGS, Colnago, LA, Silva, SL and Saran Netto, A 2019. Performance, carcass traits and serum metabolomic profile of Nellore males with different genetic potential for post-weaning growth. Animal 14, 873880.CrossRefGoogle ScholarPubMed
Delgado, R, Abad-Guamán, R, Nicodemus, N, Diaz-Perales, A, García, J, Carabaño, R and Menoyo, D 2019. Effect of pre- and post-weaning dietary supplementation with arginine and glutamine on rabbit performance and intestinal health. BMC Veterinary Research 15, 112.CrossRefGoogle ScholarPubMed
Dzúrik, R, Spustová, V, Krivošíková, Z and Gazdíková, K 2003. Hippurate participates in the correction of metabolic acidosis. Kidney International 59, S278S281.CrossRefGoogle Scholar
Falcão-e-Cunha, L, Castro-Solla, L, Maertens, L, Marounek, M, Pinheiro, V, Freire, J and Mourão, JL 2007. Alternatives to antibiotic growth promoters in rabbit feeding: a review. World Rabbit Science 15, 127140.Google Scholar
Gandra, JR, Takiya, CS, de Oliveira, ER, de Paiva, PG, de Goes, RHTB, Gandra, ÉRS and Araki, HMC 2016. Nutrient digestion, microbial protein synthesis, and blood metabolites of Jersey heifers fed chitosan and whole raw soybeans. Revista Brasileira de Zootecnia 45, 130137.10.1590/S1806-92902016000300007CrossRefGoogle Scholar
Goiri, I, Oregui, LM and Garcia-Rodriguez, A 2010. Use of chitosans to modulate ruminal fermentation of a 50:50 forage-to-concentrate diet in sheep. Journal of Animal Science 88, 749755.CrossRefGoogle Scholar
Guillou, H, Zadravec, D, Martin, PGP and Jacobsson, A 2010. Progress in Lipid Research The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice. Progress in Lipid Research 49, 186199.CrossRefGoogle ScholarPubMed
Hara, A and Radin, NS 1978. Lipid extraction of tissues with a low toxicity solvent. Analytical Biochemistry 90, 420426.10.1016/0003-2697(78)90046-5CrossRefGoogle ScholarPubMed
Jang, C, Oh, SF, Wada, S, Rowe, GC, Liu, L, Chan, MC, Rhee, J, Hoshino, A, Kim, B and Ibrahim, A 2016. A branched-chain amino acid metabolite drives vascular fatty acid transport and causes insulin resistance. Nature Medicine 22, 421426.10.1038/nm.4057CrossRefGoogle ScholarPubMed
Khambualai, O, Yamauchi, K and Tangtaweewipat, S 2009. Growth performance and intestinal histology in broiler chickens fed with dietary chitosan. British Poutry Science 50, 592597.CrossRefGoogle ScholarPubMed
Kobayashi, S, Terashima, Y and Itoh, H 2002. Effects of dietary chitosan on fat deposition and lipase activity in digesta in broiler chickens. British Poultry Science 43, 270273.10.1080/00071660120121490CrossRefGoogle ScholarPubMed
Koch, RM, Chambers, D and Gregory, KE 1963. Efficiency of feed use in beef cattle. Journal of Animal Science 22, 486494.CrossRefGoogle Scholar
Kramer, JKG, Fellner, V and Dugan, MER 1997. Evaluating acid and base catalysts in the methylation of milk and rumen fatty acids with special emphasis on conjugated dienes and total trans fatty acids. Lipids 32, 12191228.CrossRefGoogle ScholarPubMed
Lourenço, M, Ramos-Morales, E and Wallace, RJ 2010. The role of microbes in rumen lipolysis and biohydrogenation and their manipulation. Animal 4, 10081023.10.1017/S175173111000042XCrossRefGoogle ScholarPubMed
Mingoti, RD, Freitas, JE, Gandra, JR, Gardinal, R, Calomeni, GD, Barletta, RV, Vendramini, THA, Paiva, PG and Rennó, FP 2016. Dose response of chitosan on nutrient digestibility, blood metabolites and lactation performance in holstein dairy cows. Livestock Science 187, 3539.CrossRefGoogle Scholar
Moon, J, Kim, H, Koo, HC, Joo, Y-S, Nam, H, Park, YH and Kang, M-I 2007. The antibacterial and immunostimulative effect of chitosan-oligosaccharides against infection by Staphylococcus aureus isolated from bovine mastitis. Applied Microbiology and Biotechnology 75, 989998.CrossRefGoogle ScholarPubMed
National Research Council 2007. Nutrient requirements of small ruminants: sheep, goats, cervids, and new world camelids, 6th edition (updated). NRC, Washington, DC, USA.Google Scholar
Nelson, DL, Lehninger, AL and Cox, MM 2008. Lehninger principles of biochemistry, 5th edition. W.H. Freeman, New York, NY, USA.Google Scholar
Orlowski, S, Flees, J, Greene, ES, Ashley, D, Lee, SO, Yang, FL, Owens, CM, Kidd, M, Anthony, N and Dridi, S 2018. Effects of phytogenic additives on meat quality traits in broiler chickens. Journal of Animal Science 96, 37573767.10.1093/jas/sky238CrossRefGoogle Scholar
Paiva, PG, de Jesus, EF, Del Valle, TA, de Almeida, GF, Costa, AGBVB, dos Santos, FCR, Galvao, VC and Renno, FP 2016. Effect of chitosan in dairy cows diets on ruminal fermentation, milk yield and composition. Journal of Animal Science 93, 485.Google Scholar
Pereira, FM, Carvalho, GGP, Magalhães, TS, Freitas Júnior, JE, Pinto, LFB, Mourão, GB, Pires, AJV, Eiras, CE, Novais-Eiras, D, Azevêdo, JAG and Eustáquio Filho, A 2018. Effect of chitosan on production performance of feedlot lambs. Journal of Agricultural Science 156, 11381144.CrossRefGoogle Scholar
Razdan, BYA and Pettersson, D 1994. Effect of chitin and chitosan on nutrient digestibility and plasma lipid concentrations in broiler chickens. British Journal of Nutrition 72, 277288.CrossRefGoogle ScholarPubMed
Rivaroli, D, Guerrero, A, Velandia, M, Zawadzki, F, Emanuel, C, Campo, M, Sañudo, C, Mendes, A and Nunes, I 2016. Effect of essential oils on meat and fat qualities of crossbred young bulls finished in feedlots. Meat Science 121, 278284.CrossRefGoogle ScholarPubMed
Russell, JB 1987. A proposed mechanism of monensin action in inhibiting ruminal bacterial growth: effects on ion flux and protonmotive force. Journal of Animal Science 64, 15191525.10.2527/jas1987.6451519xCrossRefGoogle ScholarPubMed
Swiatkiewicz, S, Swiatkiewicz, M, Arczewska-Wlosek, A and Jozefiak, D 2015. Chitosan and its oligosaccharide derivatives (chito-oligosaccharides) as feed supplements in poultry and swine nutrition. Journal of Animal Physiology and Animal Nutrition 99, 112.CrossRefGoogle ScholarPubMed
Tang, Z, Yin, Y, Nyachoti, CM, Huang, R-L, Li, T-J, Yang, C, Yang, X, Gong, J, Peng, J, Qi, D, Xing, J, Sun, Z-H and Fan, MZ 2005. Effect of dietary supplementation of chitosan and galacto-mannan-oligosaccharide on serum parameters and the insulin-like growth factor-I mRNA expression in early-weaned piglets. Domestic Animal Endocrinology 28, 430441.10.1016/j.domaniend.2005.02.003CrossRefGoogle ScholarPubMed
Usami, Y, Okamoto, Y, Minami, S, Matsuhashi, A, Kumazawa, NH, Tanioka, S and Shigemasa, Y 1994. Migration of canine neutrophils to chitin and chitosan. Journal of Veterinary Medice Sceince 56, 761762.CrossRefGoogle ScholarPubMed
Valle, TA Del, Paiva, PG De, de Jesus, EF, de Almeida, GF, Zanferari, F, Costa, AGBVB, Bueno, ICS and Rennó, FP 2017. Dietary chitosan improves nitrogen use and feed conversion in diets for mid-lactation dairy cows. Livestock Science 201, 2229.CrossRefGoogle Scholar
Vendramini, THA, Takiya, CS, Silva, TH, Zanferari, F, Rentas, MF, Bertoni, JC, Consentini, CEC, Gardinal, R, Acedo, TS and Rennó, FP 2016. Effects of a blend of essential oils, chitosan or monensin on nutrient intake and digestibility of lactating dairy cows. Animal Feed Science and Technology 214, 1221.CrossRefGoogle Scholar
Virgili, F, Maiani, G, Zahoor, Z, Ciarapica, D, Raguzzini, A and Ferro-Luzzi, A 1994. Relationship between fat-free mass and urinary excretion of creatinine and 3MH in adult humans. Journal of Applied Physiology 76, 19461950.CrossRefGoogle Scholar
Wahrmund-Wyle, JL, Harris, KB and Savell, JY 2000. Beef Retail Cut Composition: 2. Proximate analysis. Journal of Food Composition and Analysis 13, 243251.CrossRefGoogle Scholar
Wang, Y and Li, J 2011. Effects of chitosan nanoparticles on survival, growth and meat quality of tilapia, Oreochromis nilotica. Nanotoxicology 5, 425431.10.3109/17435390.2010.530354CrossRefGoogle ScholarPubMed
Wheeler, TL, Shackelford, SD and Koohmaraie, M 2005. Shear force procedures for meat tenderness measurement. Retrieved April 16, 2018, from http://www.ars.usda.gov/SP2UserFiles/Place/30400510/protocols/ShearForceProcedures.pdfGoogle Scholar
Wydro, P, Krajewska, B and Hac-Wydro, K 2007. Chitosan as a lipid binder: a langmuir monolayer study of chitosan – lipid interactions. Biomacromolecules 8, 26112617.CrossRefGoogle ScholarPubMed
Zanferari, F, Vendramini, THA, Rentas, MF, Gardinal, R, Calomeni, GD, Mesquita, LG, Takiya, CS and Rennó, FP 2018. Effects of chitosan and whole raw soybeans on ruminal fermentation and bacterial populations, and milk fatty acid profile in dairy cows. Journal of Dairy Science 101, 1093910952.10.3168/jds.2018-14675CrossRefGoogle ScholarPubMed
Zinn, RA, Barreras, A, Corona, L, Owens, FN and Ware, RA 2007. Starch digestion by feedlot cattle: predictions from analysis of feed and fecal starch and nitrogen. Journal Animal Science 85, 17271730.CrossRefGoogle Scholar