Dietary supplementation with papaya (Carica papaya L.) leaf affects abundance of rumen methanogens, fermentation characteristics and blood plasma fatty acid composition in goats
The objective of this study was to test the effect of feeding papaya leaf (PL) on rumen microbial population, fermentation characteristics, blood fatty acid composition and antioxidant activity in goats. Three rumen fistulated male goats were assigned in a 3×3 latin square design using three levels of PL: no addition of PL in basal diet (control, CON, 50% concentrate + 50% alfalfa hay), 25% of alfalfa hay in basal diet replaced by PL (medium PL, MPL) and 50% of alfalfa hay in basal diet replaced by PL (high PL, HPL). Rumen fluid and blood plasma were sampled from the animals at the end of feeding trial (third week). Papaya leaf treatments (MPL and HPL) showed significant differences (p<0.05) in terms of rumen fermentation parameters as compared to the CON group at different times of measurement. The concentration of methanogenic archaea (log10cell/L) decreased (p<0.05) in both PL treatment groups as compared with CON group at all sampling times. The concentration of α-linolenic acid and total conjugated linoleic acid (CLA) were also higher (p<0.05) in the blood of goats fed PL especially HPL, compared to the CON. Blood plasma malondialdehyde concentration (mM/mL) of PL treatment groups showed a significant reduction as compared with CON. Supplementation of PL allowed the modulation of rumen characteristics which might represent a feeding strategy to reduce methane emission by directly inhibiting methanogens while improving the health benefits of ruminant products.
Adler SA, Jensen SK, Thuen E, Gustavsson AM, Harstad OM, Steinshamn H, 2013. Effect of silage botanical composition on ruminal biohydrogenation and transfer of fatty acids to milk in dairy cows. J Dairy Sci 96 (2): 1135-1147. https://doi.org/10.3168/jds.2012-5757
Allen MS, 1997. Relationship between fermentation acid production in the rumen and the requirement for physically effective fiber. J Dairy Sci 80: 447-462. https://doi.org/10.3168/jds.S0022-0302(97)76074-0
Anantasook N, Wanapat M, Cherdthong A, 2013. Manipulation of ruminal fermentation and methane production by supplementation of rain tree pod meal containing tannins and saponins in growing dairy steers. J Anim Physiol Anim Nutr 98: 50-55. https://doi.org/10.1111/jpn.12029
AOAC. 1990. Official Method of Analysis, 15th ed. Association of Analytical Chemists, Arlington, VA, USA.
Ayoola PB, Adeyeye A, 2010. Phytochemical and nutrient evaluation of Carica papaya (pawpaw) leaves. Intl J Res Rev Appl Sci 5: 3.
Bauman DE, Baumgard LH, Corl BA, Griinari DJ, 2000. Biosynthesis of conjugated linoleic acid in ruminants. J Anim Sci 77: 1-15. https://doi.org/10.2527/jas2000.77E-Suppl1f
Belanche A, Pinloche E, Preskett D, Newbold CJ, 2016. Effects and mode of action of chitosan and ivy fruit saponins on the microbiome, fermentation and methanogenesis in the rumen simulation technique. FEMS Microbiol Ecology 92: 1.
Bhatta R, Saravanan M, Baruah L, Sampath KT, Prasad CS, 2013. Effect of plant secondary compounds on in vitro methane, ammonia production and ruminal protozoa population. J Appl Microbiol 115: 455-465. https://doi.org/10.1111/jam.12238
Bouchard K, Wittenberg KM, Legesse G, Krause DO, Khafipour E, Buckley KE, Ominski KH, 2015. Comparison of feed intake, body weight gain, enteric methane emission and relative abundance of rumen microbes in steers fed sainfoin and lucerne silages under western Canadian conditions. Grass Forage Sci 70: 116-29. https://doi.org/10.1111/gfs.12105
Buccioni A, Pauselli M, Minieri S, Roscini V, Mannelli F, Rapaccini S, Lupi P, Conted G, Serra A, Cappucci A, et al., 2017. Chestnut or quebracho tannins in the diet of grazing ewes supplemented with soybean oil: Effects on animal performances, blood parameters and fatty acid composition of plasma and milk lipids. Small Ruminant Res 153: 23-30. https://doi.org/10.1016/j.smallrumres.2017.05.006
Bueno ICS, Brandi RA, Franzolin R, Benete G, Fagundes GM, Abdalla AL, Louvandini H, Muir JP, 2015. In vitro methane production and tolerance to condensed tannins in ﬁve ruminant species. Anim Feed Sci Technol 205: 1-9. https://doi.org/10.1016/j.anifeedsci.2015.03.008
Busquet M, Calsamiglia S, Ferret A, Kamel C, 2006. Plant extracts affect in vitro rumen microbial fermentation. J Dairy Sci 89: 761-771. https://doi.org/10.3168/jds.S0022-0302(06)72137-3
Caldeira A, Belo C, Santos M, Vazques A, Portugal AV, 2007. The effect of body condition score on blood metabolites and hormonal profiles in ewes. Small Rumin Res 68: 233-241. https://doi.org/10.1016/j.smallrumres.2005.08.027
Cherdthong A, Wanapat M, Kongmun P, Pilajun R, Khekornsart P, 2010. Rumen fermentation, microbial protein synthesis and cellulolytic bacterial population of swamp buffaloes as affected by roughage to concentrate ratio. J Anim Vet 9: 1667-1675. https://doi.org/10.3923/javaa.2010.1667.1675
Ebrahimi M, Rajion MA, Goh YM, Farjam AS, Oskoueian E, Jafari S, 2015. Diet high in α-linolenic acid up-regulate PPAR-α gene expression in the liver of goats. Elect J Biotechnol 18: 210-214. https://doi.org/10.1016/j.ejbt.2015.03.009
EL-Sabagh, MR, Eldaim MA, Mahboub DH, Abdel-Daim M, 2014. Effects of spirulina platensis algae on growth performance, antioxidative status and blood metabolites in fattening lambs. J Agri Sci 6: 92.
Ikram EHK, Stanley R, Netzel M, Fanning K, 2015. Phytochemicals of papaya and its traditional health and culinary uses-A review. J Food Compos Anal 41: 201-211. https://doi.org/10.1016/j.jfca.2015.02.010
Jafari S, Alizadeh A, Imani A, Goh YM, Rajion MA, Ebrahimi M, 2015. In situ degradation of almond (Prunus dulcis L.) hulls, a potential feed material for ruminants. Turk J Vet Anim Sci 39: 676-681. https://doi.org/10.3906/vet-1505-28
Jafari S, Goh YM, Rajion MA, Jahromi MF, Ebrahimi M, 2016a. Manipulation of rumen microbial fermentation by polyphenol rich solvent fractions from papaya leaf to reduce green-house gas methane and biohydrogenation of C18 PUFA. J Agri Food Chem 64 (22): 4522-30. https://doi.org/10.1021/acs.jafc.6b00846
Jafari S, Goh YM, Rajion MA, Jahromi MF, Ebrahimi M, 2016b. Ruminal methanogenesis and biohydrogenation reduction potential of papaya (Carica papaya) leaf: an in vitro study. It J Anim Sci 15: 157-165. https://doi.org/10.1080/1828051X.2016.1141031
Jafari S, Goh YM, Rajion MA, Jahromi MF, Ebrahimi M, 2017. Papaya (Carica papaya) leaf methanolic extract modulates in vitro rumen methanogenesis and rumen biohydrogenation. J Anim Sci 88 (2): 267-276. https://doi.org/10.1111/asj.12634
Jafari S, Ebrahimi M, Goh YM, Rajion MA, Jahromi MF, 2018. Dietary supplementation of papaya (Carica papaya l.) leaf affects abundance of Butyrivibrio fibrisolvens and modulates biohydrogenation of C18 polyunsaturated fatty acids in the rumen of goats. It J Anim Sci 17 (2): 326-335. https://doi.org/10.1080/1828051X.2017.1361796
Jayanegara A, Marquardt S, Wina E, Kreuzer M, Leiber F, 2013. In vitro indications for favourable non-additive effects on ruminal methane mitigation between high-phenolic and high-quality forages. Br J Nutri 109: 615-622. https://doi.org/10.1017/S0007114512001742
Khalel MS, Shwerab AM, Hassan AA, Yacout MH, El-Badawi AY, Zaki MS, 2014. Nutritional evaluation of Moringa oleifera fodder in comparison with Trifolium alexandrinum (berseem) and impact offeeding on lactation performance of cows. Life Sci J 11: 1040-1054.
Maisarah AM, Asmah R, Fauziah O, 2014. Proximate analysis, antioxidant and antiproliferative activities of different parts of Carica papaya. J Nutr Food Sci 4: 267.
NRC, 2007. Nutrient requirements of small ruminants, 6th ed, Nat Acad Press, Washington DC, USA. 384 pp.
Patra AK, Saxena J, 2011. Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. J Sci Food Agri 91: 24-37. https://doi.org/10.1002/jsfa.4152
Rana MS, Tyagi A, Asraf AS, Tyagi AK, 2012. Effect of tanniniferous Terminalia chebula extract on rumen biohydrogenation, Δ9-desaturase activity, CLA content and fatty acid composition in longissimus dorsi muscle of kids. Meat Sci 90 (3): 558-563. https://doi.org/10.1016/j.meatsci.2011.09.016
Riss J, Ecord EKD, Sutra T, 2007. Phycobiliprotein C-phycocyanin from Spirulina platensis is powerfully responsible for reducing oxidative stress and NADPH oxidase expression induced by an atherogenic diet in hamsters. J Agr Food Chem 55: 7962-7967. https://doi.org/10.1021/jf070529g
SAS. 2003. SAS User's Guide Statistics, vers. 9.1 Edition. SAS Inst., Cary, NC, USA.
Sylvester JT, Karnati SKR, Yu Z, Morrison M, Firkins JL, 2004. Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR. J Nutri 134: 3378-3384. https://doi.org/10.1093/jn/134.12.3378
Thao NT, Wanapat M, Kang S, Cherdthong A, 2015. Effects of supplementation of eucalyptus (E. camaldulensis) leaf meal on feed intake and rumen fermentation efficiency in swamp buffaloes. Asian-Aust J Anim 28: 951-957. https://doi.org/10.5713/ajas.14.0878
Tug T, Karatas F, Terzi SM, Ozdemir N, 2005. Comparison of serum malondialdehyde levels determined by two different methods in patients with copd: HPLC or TBARS methods. Lab Med 36: 41-44. https://doi.org/10.1309/WTEET9TJ2LUMB3C3
Van Soest PJ, Robertson JB, Lewis BA, 1991. Methods for dietary ﬁber, neutral detergent ﬁber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74: 3583-3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
Vasta V, Mele M, Serra A, Scerra M, Luciano G, Lanza M, Priolo A, 2009. Metabolic fate of fatty acids involved in ruminal biohydrogenation in sheep fed concentrate or herbage with or without tannins. J Anim Sci 87: 2674-2684. https://doi.org/10.2527/jas.2008-1761
Vuong QV, Hiruna S, Roach PD, Bowyer MC, Phillips PA, Scarlett CJ, 2013. Effect of extraction conditions on total phenolic compounds and antioxidant activities of Carica papaya leaf aqueous extracts. J Herb Med 3: 104-110. https://doi.org/10.1016/j.hermed.2013.04.004
Wanapat M, Kang S, Polyorach S, 2013. Development of feeding systems and strategies of supplementation to enhance rumen fermentation and ruminant production in the tropics. J Anim Sci Biotechnol 4: 32. https://doi.org/10.1186/2049-1891-4-32
Wencelová M, Váradyová Z, Pristaš P, Čobanová K, Plachá I, Kišidayová S, 2015. Effects of diet supplementation with herbal blend and sunflower seeds on fermentation parameters, microbial population, and fatty acid profile in rumen of sheep. Czech J Anim Sci 12: 551-559.
Yañez-Ruiz DR, Garcia M, Moumen AI, Molina A, Alcaide E, 2004. Ruminal fermentation and degradation patterns, protozoa population and urinary purine derivatives excretion in goats and wethers fed diets based on olive leaves. J Anim Sci 82: 3006-3014. https://doi.org/10.2527/2004.82103006x
Zamiri MJ, Azizabadi E, Momeni Z, Rezvani MR, Atashi H, Akhlaghi A, 2015. Effect of thymol and carvacrol on nutrient digestibility in rams fed high or low concentrate diets. Iran J Vet Res 16 (4): 335-340.
Zhang CM, Guo YQ, Yuan ZP, Wu YM, Wang JK, Liu JX, Zhu WY, 2008. Effect of octadeca carbon fatty acids on microbial fermentation, methanogenesis and microbial flora in vitro. Anim Feed Sci Technol 146: 259-269. https://doi.org/10.1016/j.anifeedsci.2008.01.005
Zhou CS, Xiao WJ, Tan ZL, Salem AZM, Geng MM, Tang SX, Wang M, Han XF, Kang JH, 2012. Effects of dietary supplementation of tea saponins (Ilex kudingcha C.J.Tseng) on ruminal fermentation, digestibility and plasma antioxidant parameters in goats. Anim Sci Technol 176: 163-169. https://doi.org/10.1016/j.anifeedsci.2012.07.019
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