Red propolis extract reduces the lipid oxidation of lamb meat
João Wilian Dias Silva A , Vitor Visintin Silva de Almeida B , Aline Cardoso Oliveira B , Leandro Soares Santos A , Tarcísio Ribeiro Paixão A , Ana Paula Gomes da Silva A , Laize Vieira Santos A , Dorgival Morais de Lima Júnior
C * and Robério Rodrigues Silva A
A
B
C
Abstract
Brazilian red propolis stands out for its diverse composition, which includes phenolic compounds whose effects may be similar to those of synthetic feed additives.
The objective of this study was to evaluate the effects of red propolis extract on the carcass and meat characteristics of lambs finished under confinement conditions.
The meat quality characteristics of the longissimus lumborum muscle were evaluated in 35 Santa Inês lambs, with an average age of 5 months and an initial average body weight of 17.08 ± 2.36 kg (mean ± s.d.), submitted to five distinct treatments (0, 7, 14, 21, 28 mL of red propolis extract/animal.day) over 68 days.
The use of propolis did not affect (P > 0.05) the characteristics of the carcass, as well as the chemical composition and cholesterol content. Among the physico-chemical parameters of meat, only the shear force had a quadratic effect (P < 0.05). There was also an exponential effect for lipid oxidation (P < 0.05), where the treatment with propolis had greater antioxidant effect. Meat with a lower content (P < 0.05) of saturated fatty acids was observed in sheep that received extract. There was also an increase (P < 0.05) in the content of monounsaturated acids and consequently an improvement in nutritional quality, atherogenicity and thrombogenicity indexes of desirable fatty acids.
The red propolis extract improved the lipid profile of the lamb meat. We recommend the inclusion of 7 mL red propolis extract/animal.day (or 59.50 mg total flavoloids/animal.day) in the diet of lambs finished under confinement conditions.
The red propolis extract proved to be a viable alternative as a natural feed additive.
Keywords: additive, bioactive components, Dalbergia ecastophyllum, fatty acids, flavonoids, meat oxidation, phenolic compounds, sheep.
References
Abdallah A, Zhang P, Elemba E, Zhong Q, Sun Z (2019) Carcass characteristics, meat quality, and functional compound deposition in sheep fed diets supplemented with Astragalus membranaceus by-product. Animal Feed Science and Technology 259, 114346.
| Crossref | Google Scholar |
Ackman RG (1972) The analysis of fatty acids and related materials by gas-liquid chromatography. Progress in the Chemistry of Fats and other Lipids 12, 165-284.
| Crossref | Google Scholar |
Aguiar SC, Cottica SM, Boeing JS, Samensari RB, Santos GT, Visentainer JV, Zeoula LM (2014) Effect of feeding phenolic compounds from propolis extracts to dairy cows on milk production, milk fatty acid composition, and the antioxidant capacity of milk. Animal Feed Science and Technology 193, 148-154.
| Crossref | Google Scholar |
Aldana-Mejía JA, Ccana-Ccapatinta GV, Ribeiro VP, Arruda C, Veneziani RCS, Ambrósio SR, Bastos JK (2021) A validated HPLC-UV method for the analysis of phenolic compounds in Brazilian red propolis and Dalbergia ecastaphyllum. Journal of Pharmaceutical and Biomedical Analysis 198, 114029.
| Crossref | Google Scholar | PubMed |
Andrés S, Tejido ML, Bodas R, Morán L, Prieto N, Blanco C, Giráldez FJ (2013) Quercetin dietary supplementation of fattening lambs at 0.2% rate reduces discolouration and microbial growth in meat during refrigerated storage. Meat Science 93, 207-212.
| Crossref | Google Scholar | PubMed |
Andrés S, Morán L, Aldai N, Tejido ML, Prieto N, Bodas R, Giráldez FJ (2014) Effects of linseed and quercetin added to the diet of fattening lambs on the fatty acid profile and lipid antioxidant status of meat samples. Meat Science 97, 156-163.
| Crossref | Google Scholar | PubMed |
Arruda PCL, Pereira ES, Pimentel PG, Bomfim MAD, Mizubuti IY, Ribeiro ELA, Fontenele RM, Regadas Filho JGL (2012) Fatty acids profile in Longissimus dorsi of Santa Inês lambs fed with different energy levels. Semina: Ciências Agrárias 33, 1229-1240.
| Google Scholar |
Bannon CD, Craske JD, Hai NT, Harper NL, O’Rourke KL (1982) Analysis of fatty acid methyl esters with high accuracy and reliability. Journal of Chromatography 247, 63-69.
| Crossref | Google Scholar |
Bezerra LS, Barbosa AM, Carvalho GGP, Simionato JI, Freitas JE, Jr, Araujo MLGML, Pereira L, Silva RR, Lacerda ECQ, Carvalho BMA (2016) Meat quality of lambs fed diets with peanut cake. Meat Science 121, 88-95.
| Crossref | Google Scholar | PubMed |
Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT – Food Science and Technology 28, 25-30.
| Crossref | Google Scholar |
Chikwanha OC, Muchenje V, Nolte JE, Dugan MER, Mapiye C (2019) Grape pomace (Vitis vinifera L. cv. Pinotage) supplementation in lamb diets: effects on growth performance, carcass and meat quality. Meat Science 147, 6-12.
| Crossref | Google Scholar | PubMed |
Cimmino R, Barone CMA, Claps S, Varricchio E, Rufrano D, Caroprese M, Albenzio M, De Palo P, Campanile G, Neglia G (2018) Effects of dietary supplementation with polyphenols on meat quality in Saanen goat kids. BMC Veterinary Research 14, 181.
| Crossref | Google Scholar | PubMed |
Dantas Silva RP, Machado BAS, Barreto GdA, Costa SS, Andrade LN, Amaral RG, Carvalho AA, Padilha FF, Barbosa JDV, Umsza-Guez MA (2017) Antioxidant, antimicrobial, antiparasitic, and cytotoxic properties of various Brazilian propolis extracts. PLoS ONE 12, e0172585.
| Crossref | Google Scholar | PubMed |
de Aguiar SC, Zeoula LM, Franco SL, Peres LP, Arcuri PB, Forano E (2013) Antimicrobial activity of Brazilian propolis extracts against rumen bacteria in vitro. World Journal of Microbiology and Biotechnology 29, 1951-1959.
| Crossref | Google Scholar | PubMed |
de Lima Júnior DM, de Carvalho FFR, da Silva FJS, Rangel AHdN, Novaes LP, Difante GdS (2016) Intrinsic factors affecting sheep meat quality: a review. Revista Colombiana de Ciencias Pecuarias 29, 03-15.
| Crossref | Google Scholar |
De Smet S, Vossen E (2016) Meat: the balance between nutrition and health. A review. Meat Science 120, 145-156.
| Crossref | Google Scholar | PubMed |
Diaz-Sanchez S, D’Souza D, Biswas D, Hanning I (2015) Botanical alternatives to antibiotics for use in organic poultry production. Poultry Science 94, 1419-1430.
| Crossref | Google Scholar | PubMed |
Dibner JJ, Richards JD (2005) Antibiotic growth promoters in agriculture: history and mode of action. Poultry Science 84, 634-643.
| Crossref | Google Scholar | PubMed |
dos Reis BQ, Rojas Moreno DA, Nacimento RA, Luiz VT, Alves LKS, Giannetti BF, Gameiro AH (2021) Economic and environmental assessment using emergy of sheep production in Brazil. Sustainability 13, 11595.
| Crossref | Google Scholar |
Duckett SK, Klein TA, Leckie RK, Thorngate JH, Busboom JR, Snowder GD (1998) Effect of freezing on calpastatin activity and tenderness of callipyge lamb. Journal of Animal Science 76, 1869-1874.
| Crossref | Google Scholar | PubMed |
D’Aurea EMO, Ezequiel JMB, Santos VC, D’Aurea AP, Carvalho VB, Almeida MTC, Perez HL (2018) Glycerin in nutrition of sheep finished in confinement: quantitative characteristics of the carcass and qualitative characteristics of the meat. Brazilian Archive of Veterinary Medicine and Animal Science 70, 1950-1958.
| Google Scholar |
Ferlay A, Martin B, Lerch S, Gobert M, Pradel P, Chilliard Y (2010) Effects of supplementation of maize silage diets with extruded linseed, vitamin E and plant extracts rich in polyphenols, and morning v. evening milking on milk fatty acid profiles in Holstein and Montbeliárde cows. Animal 4, 627-640.
| Crossref | Google Scholar | PubMed |
Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497-509.
| Crossref | Google Scholar | PubMed |
Hopkins DL, Hegarty RS, Walker PJ, Pethick DW (2006) Relationship between animal age, intramuscular fat, cooking loss, pH, shear force and eating quality of aged meat from sheep. Australian Journal of Experimental Agriculture 46, 879-884.
| Crossref | Google Scholar |
Hughes JM, Oiseth SK, Purslow PP, Warner RD (2014) A structural approach to understanding the interactions between colour, water-holding capacity and tenderness. Meat Science 98, 520-532.
| Crossref | Google Scholar | PubMed |
Inserra L, Priolo A, Biondi L, Lanza M, Bognanno M, Gravador R, Luciano G (2014) Dietary citrus pulp reduces lipid oxidation in lamb meat. Meat Science 96, 1489-1493.
| Crossref | Google Scholar | PubMed |
Ítavo CCBF, Morais MG, Costa C, Ítavo LCV, Macedo FAF, Tomich TR (2009) Carcass characteristics, body components and cut yields of confined lambs receiving a diet with propolis or monesin sodium. Brazilian Journal of Animal Science 38, 898-905.
| Google Scholar |
Jiang J, Xiong YL (2016) Natural antioxidants as food and feed additives to promote health benefits and quality of meat products: a review. Meat Science 120, 107-117.
| Crossref | Google Scholar | PubMed |
Jouany J-P, Morgavi DP (2007) Use of ‘natural’ products as alternatives to antibiotic feed additives in ruminant production. Animal 1, 1443-1466.
| Crossref | Google Scholar | PubMed |
Jung S, Choe JH, Kim B, Yun H, Kruk ZA, Jo C (2010) Effect of dietary mixture of gallic acid and linoleic acid on antioxidative potential and quality of breast meat from broilers. Meat Science 86, 520-526.
| Crossref | Google Scholar | PubMed |
Khliji S, van de Ven R, Lamb TA, Lanza M, Hopkins DL (2010) Relationship between consumer ranking of lamb colour and objective measures of colour. Meat Science 85, 224-229.
| Crossref | Google Scholar | PubMed |
Kunrath CA, Savoldi DC, Mileski JPF, Novello CR, Alfaro AT, Marchi JF, Tonial IB (2017) Application and evaluation of propolis, the natural antioxidant in Italian-type salami. Brazilian Journal of Food Technology 20, e2016035.
| Crossref | Google Scholar |
Lanza M, Scerra M, Bognanno M, Buccioni A, Cilione C, Biondi L, Priolo A, Luciano G (2015) Fatty acid metabolism in lambs fed citrus pulp. Journal of Animal Science 93, 3179-3188.
| Crossref | Google Scholar | PubMed |
Mansbridge RJ, Blake JS (1997) Nutritional factors affecting the fatty acid composition of bovine milk. British Journal of Nutrition 78, S37-S47.
| Crossref | Google Scholar | PubMed |
Martemucci G, D’Alessandro AG (2013) Progress in nutritional and health profile of milk and dairy products: a novel drug target. Endocrine, Metabolic & Immune Disorders – Drug Targets 13, 209-233.
| Crossref | Google Scholar | PubMed |
Molyneux P (2004) The use of the stable free radical diphenylpicryl-hydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin Journal of Science and Technology 26, 211-219.
| Google Scholar |
Morsy AS, Soltan YA, El-Zaiat HM, Alencar SM, Abdalla AL (2021) Bee propolis extract as a phytogenic feed additive to enhance diet digestibility, rumen microbial biosynthesis, mitigating methane formation and health status of late pregnant ewes. Animal Feed Science and Technology 273, 114834.
| Crossref | Google Scholar |
Nakamura M, Katoh K (1985) Influence of thawing method on several properties of rabbit meat. Bulletin of Ishikawa Prefecture College of Agriculture 11, 45-49.
| Google Scholar |
North MK, Dalle Zotte A, Hoffman LC (2019) The use of dietary flavonoids in meat production: a review. Animal Feed Science and Technology 257, 114291.
| Crossref | Google Scholar |
Oskoueian E, Abdullah N, Oskoueian A (2013) Effects of flavonoids on rumen fermentation activity, methane production, and microbial population. BioMed Research International 2013, 1-8.
| Crossref | Google Scholar |
Pontes MLCd, Vasconcelos IRA, Diniz MdFFDM, Pessôa HdLF (2018) Chemical characterization and pharmacological action of Brazilian red propolis. Acta Brasiliensis 2, 34-39.
| Crossref | Google Scholar |
Prache S, Schreurs N, Guillier L (2022) Factors affecting sheep carcass and meat quality. Animal 16, 100330.
| Crossref | Google Scholar | PubMed |
Raharjo S, Sofos JN, Schmidt GR (1992) Improved speed, specificity, and limit of determination of an aqueous acid extraction thiobarbituric acid-C18 method for measuring lipid peroxidation in beef. Journal of Agricultural and Food Chemistry 40, 2182-2185.
| Crossref | Google Scholar |
Rufatto LC, Luchtenberg P, Garcia C, Thomassigny C, Bouttier S, Henriques JAP, Roesch-Ely M, Dumas F, Moura S (2018) Brazilian red propolis: chemical composition and antibacterial activity determined using bioguided fractionation. Microbiological Research 214, 74-82.
| Crossref | Google Scholar | PubMed |
Saldanha T, Mazalli MR, Bragagnolo N (2004) Comparative evaluation of two methods for the determination of cholesterol in meat and milk. Food Science and Technology 24, 109-113.
| Crossref | Google Scholar |
Schwingshackl L, Hoffmann G (2012) Monounsaturated fatty acids and risk of cardiovascular disease: synopsis of the evidence available from systematic reviews and meta-analyses. Nutrients 4, 1989-2007.
| Crossref | Google Scholar | PubMed |
Schäberle TF, Hack IM (2014) Overcoming the current deadlock in antibiotic research. Trends in Microbiology 22, 165-167.
| Crossref | Google Scholar |
Simitzis PE, Charismiadou MA, Goliomytis M, Charalambous A, Ntetska I, Giamouri E, Deligeorgis SG (2018) Antioxidant status, meat oxidative stability and quality characteristics of lambs fed with hesperidin, naringin or α-tocopherol acetate supplemented diets. Journal of the Science of Food and Agriculture 276, 114925.
| Google Scholar |
Singleton VL, Rossi JA, Jr (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture 16, 144-158.
| Crossref | Google Scholar |
Singleton VL, Orthofer R, Lamuela-Raventós RM (1998) Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods in Enzymology 299, 152-178.
| Crossref | Google Scholar |
Soltan YA, Patra AK (2020) Bee propolis as a natural feed additive: bioactive compounds and effects on ruminal fermentation pattern as well as productivity of ruminants. Indian Journal of Animal Health 59, 50-61.
| Crossref | Google Scholar |
Stradiotti D, Jr, Queiroz AC, Lana RP, Pacheco CG, Eifert EC, Nunes PMM (2004) Propolis effects on amino acid deamination and ruminal fermentation. Brazilian Journal of Animal Science 33, 1086-1092.
| Google Scholar |
Torres RNS, Paschoaloto JR, Ezequiel JMB, da Silva DAV, Almeida MTC (2021) Meta-analysis of the effects of essential oil as an alternative to monensin in diets for beef cattle. The Veterinary Journal 272, 105659.
| Crossref | Google Scholar | PubMed |
Ulbricht TLV, Southgate DAT (1991) Coronary heart disease: seven dietary factors. The Lancet 338, 985-992.
| Crossref | Google Scholar |
Vedovatto M, Da Silva Pereira C, Marin Beltrame JA, Cortada Neto IM, De Lucca Bento AL, Dalla Martha GdO, Morais MdG, Franco GL (2020) Inclusion of concentrate and growth promoters additives in sheep diets on intake, digestibility, degradability, ruminal variables and nitrogen balance. Revista Mexicana de Ciencias Pecuarias 11, 132-152.
| Crossref | Google Scholar |
Wheeler TT, Cundiff LV, Koch RM (1995) Effects of marbling degree on palatability and caloric content of beef. Beef Research – Progress Report 71, 133-134.
| Google Scholar |
Wood JD, Enser M, Fisher AV, Nute GR, Sheard PR, Richardson RI, Hughes SI, Whittington FM (2008) Fat deposition, fatty acid composition and meat quality: a review. Meat Science 78, 343-358.
| Crossref | Google Scholar | PubMed |
Zhao J, Li K, Su R, Liu W, Ren Y, Zhang C, Du M, Zhang J (2017) Effect of dietary Tartary buckwheat extract supplementation on growth performance, meat quality and antioxidant activity in ewe lambs. Meat Science 134, 79-85.
| Crossref | Google Scholar | PubMed |
