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Addition of fermented and unfermented grape skin in broilers’ diets: effect on digestion, growth performance, intestinal microbiota and oxidative stability of meat

Published online by Cambridge University Press:  19 December 2019

M. Nardoia ,
C. Romero Open the ORCID record for C. Romero [Opens in a new window] ,
A. Brenes ,
I. Arija ,
A. Viveros ,
C. Ruiz-Capillas  and
S. Chamorro Open the ORCID record for S. Chamorro [Opens in a new window]
M. Nardoia
Affiliation:
Instituto de Ciencia y Tecnología de Alimentos y Nutrición (ICTAN-CSIC), José Antonio Novais, 10, 28040Madrid, Spain Department of Agricultural, Environmental and Food Sciences, University of Molise, 86100Campobasso, Italy
C. Romero
Affiliation:
Facultad de Ciencias y Artes, Universidad Católica de Ávila, Canteros s/n, 05005Ávila, Spain
A. Brenes
Affiliation:
Instituto de Ciencia y Tecnología de Alimentos y Nutrición (ICTAN-CSIC), José Antonio Novais, 10, 28040Madrid, Spain
I. Arija
Affiliation:
Departamento de Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040Madrid, Spain
A. Viveros
Affiliation:
Departamento de Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040Madrid, Spain
C. Ruiz-Capillas
Affiliation:
Instituto de Ciencia y Tecnología de Alimentos y Nutrición (ICTAN-CSIC), José Antonio Novais, 10, 28040Madrid, Spain
S. Chamorro*
Affiliation:
Instituto de Ciencia y Tecnología de Alimentos y Nutrición (ICTAN-CSIC), José Antonio Novais, 10, 28040Madrid, Spain
*
†E-mail: [email protected]
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Abstract

Grape skin is a source of polyphenols with antioxidant and antimicrobial properties. Little information is available regarding its application in animal feeding. The present study investigated the effect of inclusion of fermented (FS) and unfermented (UFS) grape skin at two different doses (30 g/kg, FS30 and UFS30, and 60 g/kg, FS60 and UFS60) and 200 mg/kg vitamin E (α-tocopheryl acetate) in a corn–soybean diet on growth performance, ileal protein digestibility, ileal and excreta total extractable polyphenols content and digestibility, intestinal microbiota and thigh meat oxidation in broiler chickens. Growth performance was depressed in chickens fed UFS and FS diets. A reduction in ileal protein digestibility was also observed in birds fed UFS, being this effect more pronounced in those fed 60 g/kg. The dietary inclusion of grape skin increased both ileal and excreta polyphenols contents, being higher in birds fed UFS than in those fed FS. Excreta moisture content increased in birds fed UFS and FS diets. No effect of dietary inclusion of grape skin was observed on ileal counts of lactic-acid bacteria and Clostridium, but UFS inclusion in the diet reduced ileal count of Escherichia coli as compared with FS dietary inclusion. After 7 days of refrigerated storage, values of thiobarbituric acid reactive substances (TBARS) were lower in chicken meat when grape skin was added in the diet at 60 g/kg instead of 30 g/kg, and meat from birds fed 60 g/kg of grape skin reached TBARS values similar to those of birds supplemented with vitamin E. In conclusion, high doses of grape skin polyphenols depressed growth performance and protein digestibility, and increased excreta moisture content. Unfermented grape skin contained more polyphenols than FS, and its inclusion in the diet led to higher ileal and excreta polyphenols contents and to a lower ileal count of E. coli. Furthermore, the antioxidant potential of the polyphenols present in grape skin was observed after 7 days of meat storage, with the dose of 60 g/kg of grape skin being as effective as vitamin E supplementation in maintaining oxidative stability of meat.

Keywords

polyphenolsgrape byproductsantioxidantintestinal bacteriachickens
Type
Research Article
Information
animal , Volume 14 , Issue 7 , July 2020 , pp. 1371 - 1381
Copyright
© The Animal Consortium 2019

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References

Abu Hafsa, SH and Ibrahim, SA 2018. Effect of dietary polyphenol-rich grape seed on growth performance, antioxidant capacity and ileal microflora in broiler chicks. Journal of Animal Physiology and Animal Nutrition 102, 268–275.CrossRefGoogle ScholarPubMed
Association of Official Analytical Chemists (AOAC) 1995. Official methods of analysis, 16th edition. Association of Official Analytical Chemists International, Arlington, VA, USA.Google Scholar
Botsoglou, NA, Fletouris, DJ, Papageorgiu, GE, Vassilopoulos, VN, Mantis, AJ and Trakatellis, AG 1994. Rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissue, food, and feedstuff samples. Journal of Agricultural and Food Chemistry 42, 1931–1937.CrossRefGoogle Scholar
Braune, A and Blaut, M 2016. Bacterial species involved in the conversion of dietary flavonoids in the human gut. Gut Microbes 7, 216–234.CrossRefGoogle ScholarPubMed
Brenes, A, Viveros, A, Chamorro, S and Arija, I 2016. Use of polyphenol-rich grape by-products in monogastric nutrition. A review. Animal Feed Science and Technology 211, 1–17.CrossRefGoogle Scholar
Brenes, A, Viveros, A, Goñi, I, Centeno, C, Ayerdy, SG, Arija, I and Calixto, FS 2008. Effect of grape pomace concentrate and vitamin E on digestibility of polyphenols and antioxidant activity in chicken. Poultry Science 87, 307–316.CrossRefGoogle Scholar
Brenes, A, Viveros, A, Goñi, I, Centeno, C, Saura, CF and Arija, I 2010. Effect of grape seed extract on growth performance, protein and polyphenol digestibilities and antioxidant activity in chicken. Spanish Journal of Agricultural Research 8, 326–333.CrossRefGoogle Scholar
Chamorro, S, Romero, C, Brenes, A, Sánchez-Patán, F, Bartolomé, B, Viveros, A and Arija, I. 2019. Impact of a sustained consumption of grape extract on digestion, gut microbial metabolism and intestinal barrier in broiler chickens. Food & Function 10, 1444–1454.CrossRefGoogle ScholarPubMed
Chamorro, S, Viveros, A, Centeno, C, Romero, C, Arija, I and Brenes, A 2013. Effects of dietary grape seed extract on growth performance, amino acid digestibility and plasma lipids and mineral content in broiler chicks. Animal 7, 555–561.CrossRefGoogle ScholarPubMed
Chamorro, S, Viveros, A, Rebolé, A, Arija, I, Romero, C, Álvarez, I, Rey, A and Brenes, A. 2017. Addition of exogenous enzymes to diets containing grape pomace: Effects on intestinal utilization of catechins and antioxidant status of chickens. Food Research International 96, 226–234.CrossRefGoogle ScholarPubMed
Chamorro, S, Viveros, A, Rebolé, A, Rica, BD, Arija, I and Brenes, A 2015. Influence of dietary enzyme addition on polyphenol utilization and meat lipid oxidation of chicks fed grape pomace. Food Research International 73, 197–203.CrossRefGoogle Scholar
Deng, Q, Penner, M and Zhao, Y 2011. Chemical composition of dietary fiber and polyphenols of five different varieties of wine grape pomace skins. Food Research International 44, 2712–2720.CrossRefGoogle Scholar
Frazier, RA, Deaville, ER, Green, RJ, Stringano, E, Willoughby, I, Plant, J and Mueller-Harvey, I 2010. Interactions of tea tannins and condensed tannins with proteins. Journal of Pharmaceutical and Biomedical Analysis 51, 490–495.CrossRefGoogle ScholarPubMed
Goñi, I, Brenes, A, Centeno, C, Viveros, A, Saura-Calixto, F, Rebolé, A, Arija, I and Estevez, R 2007. Effect of dietary grape pomace and vitamin E on growth performance, nutrient digestibility and susceptibility to meat lipid oxidation in chickens. Poultry Science 86, 508–516.CrossRefGoogle ScholarPubMed
Hajati, H, Hassanabadi, A, Golian, AG, Nassiri-Moghaddam, H and Nassiri, MR 2015. The effect of grape seed extract and vitamin C feed supplements on carcass characteristics, gut morphology and ileal microflora in broiler chickens exposed to chronic heat stress. Iranian Journal of Applied Animal Science 5, 155–165.Google Scholar
Ky, I, Lorrain, B, Kolbas, N, Crozier, A and Teissedre, PL 2014. Wine by-products: phenolic characterization and antioxidant activity evaluation of grapes and grape pomaces from six different French grape varieties. Molecules 19, 482–506.CrossRefGoogle ScholarPubMed
Mateos-Martín, ML, Pérez-Jiménez, J, Fuguet, E and Torres, JL 2012. Non-extractable proanthocyanidins from grapes are a source of bioavailable (epi)catechin and derived metabolites in rats. British Journal of Nutrition 108, 290–297.CrossRefGoogle ScholarPubMed
Monagas, M, Urpi-Sarda, M, Sánchez-Patán, F, Lorach, R, Garrido, I, Gómez-Cordovés, C, Andrés-Lacueva, C and Bartolomé, B 2010. Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites. Food & Function 1, 233–253.CrossRefGoogle Scholar
Montreau, FR 1972. Sur le dosage des composés phénoliques totaux dans les vins par la méthode Folin-Ciocalteau. Journal International des Sciences de la Vigne et du Vin 6, 397–404.Google Scholar
Muñoz-González, I, Chamorro, S, Pérez-Jiménez, J, López-Andrés, P, Álvarez-Acero, I, Herrero, AM, Nardoia, M, Brenes, A, Viveros, A, Arija, I, Rey, A and Ruiz-Capillas, C 2019. Phenolic metabolites in plasma and thigh meat of chickens supplemented with grape byproducts. Journal of Agricultural and Food Chemistry 67, 4463–4471.CrossRefGoogle ScholarPubMed
Nardoia, M 2016. Effect of dietary polyphenol-rich grape by-products on growth performance, some physiological parameters and meat products quality in chickens. PhD thesis, University of Molise, Campobasso, Italy.Google Scholar
Nardoia, M, Chamorro, S, Viveros, A, Arija, I, Ruiz-Capillas, C and Brenes, A 2017a. Effect of dietary fermented and unfermented grape skin on broiler chickens. In Proceedings of the EAAP 68th Annual Meeting, 30th August 2017, Tallinn, Estonia, Session 36.Google Scholar
Nardoia, M, Ruiz-Capillas, C, Herrero, AM, Jiménez-Colmenero, F, Chamorro, S and Brenes, A 2017b. Effect of added grape seed and skin on chicken thigh patties during chilled storage. International Journal of Food and Nutritional Science 4, 67–73.Google Scholar
Nyachoti, CM, Atkinson, JL and Leeson, S 1997. Sorghum tannins: a review. World’s Poultry Science Journal 53, 5–21.CrossRefGoogle Scholar
Ortiz, LT, Centeno, C and Treviño, J 1993. Tannins in faba bean seeds: effects on the digestion of protein and amino acids in growing chicks. Animal Feed Science and Technology 41, 271–278.CrossRefGoogle Scholar
Özkan, G, Sagdic, O, Baydar, NG and Kurumahmutoglu, Z 2004. Antibacterial activities and total phenolic contents of grape pomace extracts. Journal of the Science of Food and Agriculture 84, 1807–1811.CrossRefGoogle Scholar
Pascariu, SM, Pop, IM, Simeanu, D, Pavel, G and Solcan, C 2017. Effects of wine by-products on growth performance, complete blood count and total antioxidant status in broilers. Brazilian Journal of Poultry Science 19, 191–202.CrossRefGoogle Scholar
Pérez-Jiménez, J, Diaz-Rubio, E and Saura-Calixto, F 2013. An overview of dietary NEPP: their nature, occurrence in the diet, metabolic fate and possible health effects. Nutrition Research Reviews 26, 118–129.CrossRefGoogle Scholar
Pérez-Jiménez, J and Saura-Calixto, F 2008. Grape products and cardiovascular disease risk factors. Nutrition Research Reviews 21, 158–173.CrossRefGoogle ScholarPubMed
Pompeu, MA, Cavalcanti, LFL and Toral, FLB 2018. Effect of vitamin E supplementation on growth performance, meat quality, and immune response of male broiler chickens: a meta-analysis. Livestock Science 208, 5–13.CrossRefGoogle Scholar
Rababah, TM, Ereifej, KI, Al-Mahasneh, MA and Al-Rababah, MA 2006. Effect of plant extract on physicochemical properties of chicken breast meat cooked using conventional electric oven or microwave. Poultry Science 85, 148–154.CrossRefGoogle ScholarPubMed
Requena, T, Monagas, M, Pozo-Bayón, MA, Martín-Álvarez, PJ, Bartolomé, B, Campo, R, Ávila, M, Martínez-Cuesta, MC, Peláez, C and Moreno-Arribas, MV 2010. Perspectives of the potential implications of wine polyphenols on human oral and gut microbiota. Trends in Food Science & Technology 21, 332–344.CrossRefGoogle Scholar
Rodríguez-Montealegre, R, Romero, R, Chacón, JL, Martínez, J and García, E 2006. Phenolic compounds in skins and seeds of ten grape Vitis vinifera varieties grown in a warm climate. Journal of Food Composition and Analysis 19, 687–693.CrossRefGoogle Scholar
Siriwan, P, Bryden, WL, Mollah, Y and Annison, EF 1993. Measurements of endogenous amino acid losses in poultry. British Poultry Science 34, 939–949.CrossRefGoogle Scholar
Souquet, JM, Cheynier, V, Brossaud, F and Moutounet, M 1996. Polymeric proanthocyanidins from grape skins. Phytochemistry 43, 509–512.CrossRefGoogle Scholar
Tsang, C, Auger, C, Mullen, W, Bornet, A, Rouanet, JM, Crozier, A and Teissedre, PL 2005. The absorption, metabolism and excretion of flavan-3-ols and procyanidins following the ingestion of a grape seed extract by rats. British Journal of Nutrition 94, 170–181.CrossRefGoogle ScholarPubMed
Van der Hoeven-Hangoor, E, Paton, ND, Van de Linde, IB, Verstegen, MWA and Hendriks, WH 2013. Moisture content in broiler excreta is influenced by excreta nutrient contents. Journal of Animal Science 91, 5705–5713.CrossRefGoogle ScholarPubMed
Vergara-Salinas, JR, Bulnes, P, Zuñiga, MC, Perez-Jimenez, J, Torres, JL, Mateos-Martin, ML, Agosin, E and Perez-Correa, JR 2013. Effect of pressurized hot water extraction on antioxidants from grape pomace before and after enological fermentation. Journal of Agricultural and Food Chemistry 61, 6929–6936.CrossRefGoogle ScholarPubMed
Vivas, N, Nonier, MF, Vivas de Gaulejac, N, Absalon, C, Bertrand, A and Mirabel, M 2004. Differentiation of proanthocyanidin tannins from seeds, skins and stems of grapes (Vitis vinifera) and heartwood of Quebracho (Schinopsis balansae) by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and thioacidolysis/liquid chromatography/electrospray ionization mass spectrometry. Analytica Chimica Acta 513, 247–256.CrossRefGoogle Scholar
Viveros, A, Chamorro, S, Pizarro, M, Arija, I, Centeno, C and Brenes, A 2011. Effects of dietary polyphenol rich grape products on intestinal microflora and gut morphology in broiler chicks. Poultry Science 90, 566–578.CrossRefGoogle ScholarPubMed
Wiseman, J, Edmundo, BK and Shepperson, N 1992. The apparent metabolizable energy of sunflower oil and sunflower acid oil for broiler chickens. Animal Feed Science and Technology 36, 41–51.CrossRefGoogle Scholar
Yilmaz, Y, Goksel, Z, Erdogan, SS, Ozturk, A, Atak, A and Ozer, C 2015. Antioxidant activity and phenolic content of seed, skin and pulp parts of 22 grape (Vitis vinifera L.) cultivars (4 common and 18 registered or candidate for registration). Journal of Food Processing and Preservation 39, 1682–1691.CrossRefGoogle Scholar