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A composite polyphenol-rich extract improved growth performance, ruminal fermentation and immunity, while decreasing methanogenesis and excretion of nitrogen and phosphorus in growing buffaloes

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Abstract

The effects of a composite polyphenolic-rich extract (CPRE) on ruminal fermentation, nutrient utilisation, growth performance, excretion of nitrogen and phosphorus and methane emission were studied in growing buffaloes. Four herbal dry extracts prepared from Acacia arabica (babul; bark), Acacia catechu (cutch; bark), Punica granatum (pomegranate; peel) and Eugenia jambolana (Indian blackberry; seeds) were mixed in an equal proportion (1:1:1:1) to prepare the CPRE that contained mainly phenolic compounds (146 g/kg), flavonoids (41.7 g/kg) and saponins (40.5 g/kg). First, in vitro tests were performed for ruminal fermentation and feed degradability using ruminal fluid as inocula and CPRE at 0 to 40 g/kg substrate to decide an optimal dose of CPRE for an in vivo study on buffaloes. In the animal study, 20 buffaloes were randomly assigned to two groups (n = 10)—a control diet and a CPRE diet (control diet added with extra 20 g/kg of CPRE). The in vitro tests suggested that addition of CPRE at 20 g/kg substrate increased degradability of substrate, short-chain fatty acid concentration and propionate proportion, and reduced methane production, acetate proportion, acetate:propionate ratio and ammonia concentration in fermentation media, which were also noted in the rumen of buffaloes. Feeding CRPE to buffaloes did not affect feed intake, but increased daily body weight gain, dry matter and crude protein digestibility and nitrogen and phosphorus retention in the body. Total bacteria, methanogens and protozoal numbers were similar between two groups, but Fibrobacter succinogenes increased in the rumen of buffaloes fed CPRE. Concentrations of total, essential, non-essential and glucogenic amino acids were greater in the plasma of CPRE-fed buffaloes. Cell-mediated immune response improved in the CPRE-fed buffaloes compared with the control group. Estimated methane production and excretion of nitrogen and phosphorus per unit of body weight gain decreased in the CPRE group. The comprehensive results of this study clearly suggested that the composite polyphenol-rich feed additive at 20 g/kg diet improved growth performance, ruminal fermentation, immunity and plasma amino acids profile, whereas it reduced indicators of environmental impacts of buffalo production.

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References

  • Abbas AK, Lichtman AH, Pillai S (2014) Cellular and molecular immunology. 8th Edn, Elsevier Health Sciences, Philadelphia, USA

  • Abbasi IHR, Abbasi F, Abd El-Hack ME, Abdel-Latif MA, Soomro RN, Hayat K, Mohamed MEA, Bodinga BM, Yao J, Cao Y (2018) Critical analysis of excessive utilization of crude protein in ruminants ration: impact on environmental ecosystem and opportunities of supplementation of limiting amino acids—a review. Environ Sci Pollut Res 25:181–190. https://doi.org/10.1007/s11356-017-0555-4

    Article  CAS  Google Scholar 

  • AOAC International (2007) Official methods of analysis of AOAC International, 18th Edn, 2nd Revision, Gaithersburg, MD, USA

  • Apajalahti J, Vienola K, Raatikainen K, Holder V, Moran CA (2019) Conversion of branched-chain amino acids to corresponding isoacids—an in vitro tool for estimating ruminal protein degradability. Front Vet Sci 6:311. https://doi.org/10.3389/fvets.2019.00311

    Article  Google Scholar 

  • Armenta JM, Cortes DF, Pisciotta JM, Shuman JL, Blakeslee K, Rasoloson D, Ogunbiyi O, Sullivan DJ Jr, Shulaev V (2010) Sensitive and rapid method for amino acid quantitation in malaria biological samples using AccQ.Tagultra performance liquid chromatography-electrospray ionization-MS/MS with multiple reaction monitoring. Anal Chem 82:548–558. https://doi.org/10.1021/ac901790q

    Article  CAS  Google Scholar 

  • Baliga MS, Bhat HP, Baliga BRV, Wilson R, Palatty PL (2011) Phytochemistry, traditional uses and pharmacology of Eugenia jambolana Lam. (black plum): a review. Food Res Int 44:1776–1789. https://doi.org/10.1016/j.foodres.2011.02.007

    Article  CAS  Google Scholar 

  • Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on earth. Proc Natl Acad Sci USA 115:6506–6511

    Article  CAS  Google Scholar 

  • Blummel M, Makkar HPS, Becker K (1997) The relationship between in vitro gas production, in vitro microbial mass yield and 15N incorporation and its implications for the prediction of voluntary feed intake of roughages. Br J Nutr 77:911–921

    Article  CAS  Google Scholar 

  • Borneman WS, Akin DE, Van Eseltine WP (1986) Effect of phenolic monomers on ruminal bacteria. Appl Environ Microbiol 52:1331–1339. https://doi.org/10.1128/aem.52.6.1331-1339.1986

    Article  CAS  Google Scholar 

  • Brouwer E (1965) Report of subcommittee on constants and factors. In: Blaxter KL (Ed) Energy Metabolism of Farm Animals. EAAP Publ. No. 11. London, UK, pp 441–443

  • Cattani M, Tagliapietra F, Bailoni L, Schiavon S (2012) Synthetic and natural polyphenols with antioxidant properties stimulate rumen microbial growth in vitro. Anim Prod Sci 52:44–50. https://doi.org/10.1071/AN11096

    Article  CAS  Google Scholar 

  • Chowdhury S, Mandal GP, Patra AK (2018) Different essential oils in diets of chickens: 1. Growth performance, nutrient utilisation, nitrogen excretion, carcass traits and chemical composition of meat. Anim Feed Sci Technol 236:86–97. https://doi.org/10.1016/j.anifeedsci.2017.12.002

    Article  CAS  Google Scholar 

  • Cline JH, Hershberger TV, Bentley OG (1958) Utilization and/or synthesis of valeric acid during the digestion of glucose, starch and cellulose by rumen microorganisms. J Anim Sci 17:284–292

    Article  CAS  Google Scholar 

  • Cottyn BG, Boucque CV (1968) Rapid methods for the gas chromatographic determination of volatile acids in rumen fluid. J Agric Food Chem 16:105–107

    Article  CAS  Google Scholar 

  • Denman SE, McSweeney CS (2006) Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiol Ecol 58:572–582

    Article  CAS  Google Scholar 

  • Denman SE, Tomkins NW, McSweeney CS (2007) Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. FEMS Microbiol Ecol 62:313–322

    Article  CAS  Google Scholar 

  • Dijkstra J, Reynolds CK, Kebreab E, Bannink A, Ellis JL, France J, van Vuuren AM (2013) Challenges in ruminant nutrition: towards minimal nitrogen losses in cattle. In: Oltjen JW, Kebreab E, Lapierre H (eds) Energy and protein metabolism and nutrition in sustainable animal production, vol 134. Wageningen Academic Publishers, Wageningen. https://doi.org/10.3920/978-90-8686-781-3_3

  • Gerber PJ, Steinfeld H, Henderson B, Mottet A, Opio C, Dijkman J, Falcucci A, Tempio G (2013) Tackling climate change through livestock—a global assessment of emissions and mitigation opportunities. Food and Agriculture Organization of the United Nations, Rome, Italy

  • Gracious R, Selvasubramanian R, Jayasundar S (2001) Immunomodulatory activity of Punica granatum in rabbits—a preliminary study. J Ethnopharmacol 78:85–87

    Article  Google Scholar 

  • Grosse Brinkhaus A, Bee G, Silacci P, Kreuzer M, Dohme-Meier F (2016) Effect of exchanging Onobrychis viciifolia and Lotus corniculatus for Medicago sativa on ruminal fermentation and nitrogen turnover in dairy cows. J Dairy Sci 99:4384–4397. https://doi.org/10.3168/jds.2015-9911

    Article  CAS  Google Scholar 

  • Guo Y, Tong B, Wu Z, Ma W, Ma L (2019) Dietary manipulation to reduce nitrogen and phosphorus excretion by dairy cows. Livest Sci 228:61–66. https://doi.org/10.1016/j.livsci.2019.08.001

    Article  Google Scholar 

  • Herrero M, Grace D, Njuki J, Johnson N, Enahoro D, Silvestri S, Rufino MC (2013) The roles of livestock in developing countries. Animal 7(S1):3–18

    Article  Google Scholar 

  • Huang H, Szumacher-Strabel M, Patra AK, Ślusarczyk S, Lechniak D, Vazirigohar M, Varadyova Z, Kozłowska M, Cieslak M (2021) Chemical and phytochemical composition, in vitro ruminal fermentation, methane production, and nutrient degradability of fresh and ensiled Paulownia hybrid leaves. Anim Feed Sci Technol 279:115038. https://doi.org/10.1016/j.anifeedsci.2021.115038

    Article  CAS  Google Scholar 

  • Hundal JS, Singh I, Wadhwa M, Singh C, Uppal C, Kaur G (2019) Effect of Punica granatum and Tecomella undulata supplementation on nutrient utilization, enteric methane emission and growth performance of Murrah male buffaloes. J Anim Feed Sci 28(2019):110–119

    Article  Google Scholar 

  • ICAR (2013) Nutrient requirements of cattle and buffalo. Nutrient requirements of animals, Indian Council of Agricultural Research, New Delhi

  • Ineichen S, Kuenzler AD, Kreuzer M, Marquardt S, Reidy B (2019) Digestibility, nitrogen utilization and milk fatty acid profile of dairy cows fed hay from species rich mountainous grasslands with elevated herbal and phenolic contents. Anim Feed Sci Technol 247:210–221

    Article  CAS  Google Scholar 

  • Koenig R, Johnson C (1942) Calorimetric determination of phosphorous in biological materials. Ind Eng Chem Anal Ed 14:155–156. https://doi.org/10.1021/i560102a026

    Article  CAS  Google Scholar 

  • Krausmann F, Erb KH, Gingrich S, Lauk C, Haberl H (2008) Global patterns of socioeconomic biomass flows in the year 2000: a comprehensive assessment of supply, consumption and constraints. Ecol Econ 65:471–487

    Article  Google Scholar 

  • Kumar R, Mahey S, Arora R, Mahajan J, Kumar V, Arora S (2019) Insights into biological properties of less explored bark of industrially important Acacia catechu Wild. Ind Crops Prod 138:111486. https://doi.org/10.1016/j.indcrop.2019.111486

    Article  CAS  Google Scholar 

  • Lagrange S, Villalba JJ (2019) Tannin-containing legumes and forage diversity influence foraging behavior, diet digestibility, and nitrogen excretion by lambs. J Anim Sci 97:3994–4009

    Article  Google Scholar 

  • Liu HW, Zhou DW, Li K (2013) Effects of chestnut tannins on performance and antioxidative status of transition dairy cows. J Dairy Sci 96:5901–5907

    Article  CAS  Google Scholar 

  • Liu R, Li J, Cheng Y, Huo T, Xue J, Liu Y, Liu J, Chen X (2015) Effects of ellagic acid-rich extract of pomegranates peel on regulation of cholesterol metabolism and its molecular mechanism in hamsters. Food Funct 6:780–787. https://doi.org/10.1039/c4fo00759j

    Article  CAS  Google Scholar 

  • Makkar HP, Francis G, Becker K (2007) Bioactivity of phytochemicals in some lesser-known plants and their effects and potential applications in livestock and aquaculture production systems. Animal 1:1371–1391. https://doi.org/10.1017/s1751731107000298

    Article  CAS  Google Scholar 

  • Mayuresh AH, Wadhwa M, Hundal JS, Bakshi MPS, Sharma A, Kaur S, Bansal BK (2019) Effect of supplementing Syzygium cumini (jamun) fruit shreds to total mixed ration on the performance of lactating crossbred cows. Indian J Anim Nutr 36:342–346

    Article  CAS  Google Scholar 

  • Menke KH, Steingass H (1988) Estimation of energetic feed value obtained by chemical analysis and in vitro gas production using rumen fluid. Anim Res Develop 28:7–55

    Google Scholar 

  • Mohammad R, Shariq S, Roohi Z, Malik I (2014) Bark of Acacia arabica—a nature’s gift: an overview. Int Res J Med Sci 2:20–24

    Google Scholar 

  • Moss AR, Jouany JP, Newbold J (2000) Methane production by ruminants: its contribution to global warming. Ann Zoot 49:231–253

    Article  CAS  Google Scholar 

  • Mueller ND, Lassaletta L (2020) Nitrogen challenges in global livestock systems. Nat Food 1:400–401. https://doi.org/10.1038/s43016-020-0117-7

    Article  CAS  Google Scholar 

  • NRC (2001) Nutrient requirements of dairy cattle: seventh revised edition 2001, The National Academies Press, Washington, DC

  • Oh J, Wall EH, Bravo DM, Hristov AN (2017) Host-mediated effects of phytonutrients in ruminants: a review. J Dairy Sci 100:5974–5983. https://doi.org/10.3168/jds.2016-12341

    Article  CAS  Google Scholar 

  • Olagaray KE, Bradford BJ (2019) Plant flavonoids to improve productivity of ruminants—a review. Anim Feed Sci Technol 251:21–36

    Article  CAS  Google Scholar 

  • Oliveira RA, Narciso CD, Bisinotto RS, Perdomo MC, Ballou MA, Dreher M (2010) Effects of feeding polyphenols from pomegranate extract on health, growth, nutrient digestion, and immunocompetence of calves. J Dairy Sci 93:4280–4291

    Article  CAS  Google Scholar 

  • Orskov ER (1975) Manipulation of rumen fermentation for maximum food utilization. World Rev Nutr Diet 22:153–182

    Google Scholar 

  • Pal K, Patra AK, Sahoo A, Kumawat PK (2015) Evaluation of several tropical tree leaves for methane production potential, degradability and rumen fermentation in vitro. Livest Sci 180:98–105

    Article  Google Scholar 

  • Patra AK (2017) Accounting methane and nitrous oxide emissions, and carbon footprints of livestock food products in different states of India. J Clean Prod 162:678–686

    Article  CAS  Google Scholar 

  • Patra AK (2018) Interactions of plant bioactives with nutrient transport systems in gut of livestock. Indian J Anim Health 57:125–136

    Article  Google Scholar 

  • Patra AK, Saxena J (2009) Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie Van Leeuwenhoek 96:363–375. https://doi.org/10.1007/s10482-009-9364-1

    Article  CAS  Google Scholar 

  • Patra AK, Saxena J (2010) A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry 71:1198–1222

    Article  CAS  Google Scholar 

  • Patra AK, Saxena J (2011) Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. J Sci Food Agric 91:24–37

    Article  CAS  Google Scholar 

  • Patra AK, Yu Z (2015) Effects of adaptation of in vitro rumen culture to garlic oil, nitrate, and saponin and their combinations on methanogenesis, fermentation, and abundances and diversity of microbial populations. Front Microbiol 6:1434. https://doi.org/10.3389/fmicb.2015.01434

    Article  Google Scholar 

  • Patra AK, Park T, Kim M, Yu Z (2017) Rumen methanogens and mitigation of methane emission by anti-methanogenic compounds and substances. J Anim Sci Biotechnol 8:13. https://doi.org/10.1186/s40104-017-0145-9

    Article  CAS  Google Scholar 

  • Patra AK, Amasheh S, Aschenbach JR (2019) Modulation of gastrointestinal barrier and nutrient transport function in farm animals by natural plant bioactive compounds—a comprehensive review. Crit Rev Food Sci Nutr 59:3237–3266

    Article  CAS  Google Scholar 

  • Patra AK, Pal K, Lalhriatpuii M (2020) Prediction of nitrogen excretion in buffalo production systems using dietary and animal variables. Agric Syst 182:102845. https://doi.org/10.1016/j.agsy.2020.102845182

    Article  Google Scholar 

  • Patra AK, Min BR, Saxena J (2012) Dietary tannins on microbial ecology of the gastrointestinal tract in ruminants. In: Patra AK (ed), Dietary Phytochemicals and Microbes, Springer, Dordrenct, The Netherlands, pp 237–262

  • Patra AK (2012) An overview of antimicrobial properties of different classes of phytochemicals. In: Patra A (ed) Dietary phytochemicals and microbes. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-3926-0_1

  • Patra AK (2015) Urea/ammonia metabolism in the rumen and toxicity in ruminants. In: Puniya A, Singh R, Kamra D (eds) Rumen microbiology: from evolution to revolution. Springer, New Delhi, pp 329–341. https://doi.org/10.1007/978-81-322-2401-3_22

  • Patra AK (2020) Characteristics of ruminal microbial community: evolutionary and ecological perspectives. Indian J Anim Health 59(S):114–127. https://doi.org/10.36062/ijah.59.2SPL.2020.114-127

  • Pelletier N, Tyedmers P (2010) Forecasting potential global environmental costs of livestock production 2000–2050. Proc Natl Acad Sci USA 107:18371–18374. https://doi.org/10.1073/pnas.1004659107

    Article  Google Scholar 

  • Rajvaidhya S, Nagori BP, Singh GK, Dubey BP, Desai P, Jain S (2012) A review on Acacia Arabica—an Indian medicinal plant. Int J Pharmaceut Sci Res 3:1995–2005

    Google Scholar 

  • Rice-Evans C (1995) Plant polyphenols: free radical scavengers or chain-breaking antioxidants? Biochem Soc Symp 61:103–116. https://doi.org/10.1042/bss0610103

    Article  CAS  Google Scholar 

  • Roque BM, Salwen JK, Kinley R, Kebreab E (2019) Inclusion of Asparagopsis armata in lactating dairy cows’ diet reduces enteric methane emission by over 50 percent. J Clean Prod 234:132–138. https://doi.org/10.1016/j.jclepro.2019.06.193

    Article  CAS  Google Scholar 

  • Rothwell SA, Doody DG, Johnston C, Forber KJ, Cencic O, Rechberger H, Withers P (2020) Phosphorus stocks and flows in an intensive livestock dominated food system. Resour Conserv Recycl 163:105065. https://doi.org/10.1016/j.resconrec.2020.105065

    Article  CAS  Google Scholar 

  • Salmon GR, MacLeod M, Claxton JR, Pica Ciamarra U, Robinson T, Duncan A, Peters AR (2020) Exploring the landscape of livestock “Facts.” Glob Food Sec 25:100329. https://doi.org/10.1016/j.gfs.2019.100329

    Article  CAS  Google Scholar 

  • SAS (2001) SAS/STAT User’s Guide, Version 8, SAS Institute Inc, Cary, NC, USA

  • Scott RI, Yarlett N, Hillman K, Lloyd D (1983) Presence of oxygen in rumen liquor and its effects upon methanogenesis. J Appl Bacteriol 55:143–149

    Article  Google Scholar 

  • Seymour EM, Bennink MR, Bolling SF (2013) Diet-relevant phytochemical intake affects the cardiac AhR and nrf2 transcriptome and reduces heart failure in hypertensive rats. J Nutr Biochem 24:1580–1586

    Article  CAS  Google Scholar 

  • Singh B, Singh JP, Kaur A, Singh N (2018) Phenolic compounds as beneficial phytochemicals in pomegranate (Punica granatum L.) peel: a review. Food Chem 261:75–86. https://doi.org/10.1016/j.foodchem.2018.04.039

    Article  CAS  Google Scholar 

  • Singh P, Hundal JS, Patra AK, Wadhwa M, Sharma A (2021) Sustainable utilization of Aloe vera waste in the diet of lactating cows for improvement of milk production performance and reduction of carbon footprint. J Clean Prod 288:125118. https://doi.org/10.1016/j.jclepro.2020.125118

    Article  CAS  Google Scholar 

  • Singla A, Hundal JS, Patra AK, Wadhwa M, Nagarajappa V, Malhotra P (2021) Effect of dietary supplementation of Emblica officinalis fruit pomace on methane emission, ruminal fermentation, nutrient utilization, and milk production performance in buffaloes. Environ Sci Pollut Res 28:18120–18133. https://doi.org/10.1007/s11356-020-12008-z

    Article  CAS  Google Scholar 

  • Sinz S, Marquardt S, Soliva CR, Braun U, Liesegang A, Kreuzer M (2019) Phenolic plant extracts are additive in their effects against in vitro ruminal methane and ammonia formation. Asian-Australas J Anim Sci 32:966–976

    Article  CAS  Google Scholar 

  • SPSS (2009) PASW Statistics for Windows, Version 18.0. Chicago: SPSS Inc

  • Sylvester JT, Karnati SKR, Yu Z, Newbold CJ, Firkins JL (2005) Evaluation of a real-time PCR assay quantifying the ruminal pool size and duodenal flow of protozoal nitrogen. J Dairy Sci 88:2083–2095

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wadhwa M, Sidhu PK, Bakshi MPS (2020) Herbal feed additives containing tannins: impact on in vitro fermentation and methane mitigation from total mixed ration. Turk J Vet Anim Sci 44:47–58

    Article  CAS  Google Scholar 

  • Wang Z, Li S, Ge S, Lin S (2020) Review of distribution, extraction methods, and health benefits of bound phenolics in food plants. J Agric Food Chem 68:3330–3343. https://doi.org/10.1021/acs.jafc.9b06574

    Article  CAS  Google Scholar 

  • Williams R, Hannah MC, Jacobs JL, Wales WJ, Moate PJ (2019) Volatile fatty acids in ruminal fluid can be used to predict methane yield of dairy cows. Animals 9:1006. https://doi.org/10.3390/ani9121006

    Article  Google Scholar 

  • Yeoman CJ, Fields CJ, Lepercq P, Ruiz P, White BA, Mosoni P (2021) In vivo competitions between Fibrobacter succinogenes, Ruminococcus flavefaciens, and Ruminoccus albus in a gnotobiotic sheep model revealed by multi-omic analyses. Mbio 12:e03533-e3620. https://doi.org/10.1128/mbio.03533-20

    Article  CAS  Google Scholar 

  • Zhang XM, Gruninger RJ, Alemu AW, Wang M, Tan ZL, Kindermann M, Beauchemin KA (2020) 3-Nitrooxypropanol supplementation had little effect on fiber degradation and microbial colonization of forage particles when evaluated using the in situ ruminal incubation technique. J Dairy Sci 103:8986–997. https://doi.org/10.3168/jds.2019-18077

  • Zhou L, Xie M, Yang F, Liu J (2020) Antioxidant activity of high purity blueberry anthocyanins and the effects on human intestinal microbiota. Lebensmittel-Wissenschaft Technologie 117:108621. https://doi.org/10.1016/j.lwt.2019.108621

    Article  CAS  Google Scholar 

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Funding

This study was supported by the Department of Animal Nutrition, Guru Angad Dev Veterinary and Animal Sciences, Ludhiana, Punjab, India.

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JSH and SS conceived and designed research. SS and JSH conducted experiments. SS, RSS and AS performed laboratory analyses. JSH and AKP analysed the data. AKP and JSH wrote the manuscript.

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Correspondence to Amlan Kumar Patra.

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11356_2021_17674_MOESM1_ESM.doc

Table S1. Effect of inclusion of a composite polyphenolic-rich extract (CPRE; at 20 g/kg diet) to the total mixed ration on the blood plasma amino acid concentration (g Amino acids/100g of blood protein) of growing male buffaloes

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Singh, S., Hundal, J.S., Patra, A.K. et al. A composite polyphenol-rich extract improved growth performance, ruminal fermentation and immunity, while decreasing methanogenesis and excretion of nitrogen and phosphorus in growing buffaloes. Environ Sci Pollut Res 29, 24757–24773 (2022). https://doi.org/10.1007/s11356-021-17674-1

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