DOI QR코드

DOI QR Code

Dietary phytosterols improves the metabolic status of perinatal cows as evidenced by plasma metabolomics and faecal microbial metabolism

  • Jian Gao (Laboratory of Gastrointestinal Microbiology, National Centre for International Research on Animal Gut Nutrition, Nanjing Agricultural University) ;
  • Donghai Lv (Laboratory of Gastrointestinal Microbiology, National Centre for International Research on Animal Gut Nutrition, Nanjing Agricultural University) ;
  • Zichen Wu (Laboratory of Gastrointestinal Microbiology, National Centre for International Research on Animal Gut Nutrition, Nanjing Agricultural University) ;
  • Zhanying Sun (Laboratory of Gastrointestinal Microbiology, National Centre for International Research on Animal Gut Nutrition, Nanjing Agricultural University) ;
  • Xiaoni Sun (Laboratory of Gastrointestinal Microbiology, National Centre for International Research on Animal Gut Nutrition, Nanjing Agricultural University) ;
  • Suozhu Liu (College of Animal Science, Tibet Agricultural and Husbandry University) ;
  • Zhankun Tan (College of Animal Science, Tibet Agricultural and Husbandry University) ;
  • Weiyun Zhu (Laboratory of Gastrointestinal Microbiology, National Centre for International Research on Animal Gut Nutrition, Nanjing Agricultural University) ;
  • Yanfen Cheng (Laboratory of Gastrointestinal Microbiology, National Centre for International Research on Animal Gut Nutrition, Nanjing Agricultural University)
  • Received : 2023.10.16
  • Accepted : 2024.03.28
  • Published : 2024.10.01

Abstract

Objective: Previous research reported that dietary addition with phytosterols improved the energy utilisation of the rumen microbiome, suggesting its potential to alleviate the negative energy balance of perinatal cows. This experiment aimed to explore the effects of feeding phytosterols on the metabolic status of perinatal cows through plasma metabolomics and faecal bacteria metabolism. Methods: Ten perinatal Holstein cows (multiparous, 2 parities) with a similar calving date were selected four weeks before calving. After 7 days for adaptation, cows were allocated to two groups (n = 5), which respectively received the basal rations supplementing commercial phytosterols at 0 and 200 mg/d during a 42-day experiment. The milk yield of each cow was recorded daily after calving. On days 1 and 42, blood and faeces samples were all collected from perinatal cows before morning feeding for analysing plasma biochemicals and metabolome, and faecal bacteria metabolism. Results: Dietary addition with phytosterols at 200 mg/d had no effects on plasma cholesterol and numerically increased milk yield by 1.82 kg/d (p>0.10) but attenuated their negative energy balance in perinatal cows as observed from the significantly decreased plasma level of β-hydroxybutyric acid (p = 0.002). Dietary addition with phytosterols significantly altered 12 and 15 metabolites (p<0.05) within the plasma and faeces of perinatal cows, respectively. Of these metabolites, 5 upregulated plasma fatty acids indicated an improved energy status (i.e., C18:1T, C14:0, C17:0, C18:0, and C16:0). Milk yield negatively correlated with plasma concentrations of ketone bodies (p = 0.035) and 5-methoxytryptamine (p = 0.039). Furthermore, dietary addition with phytosterols at 200 mg/d had no effects on fermentation characteristics and bacterial diversity of cow faeces (p>0.10) but improved potentially beneficial bacteria such as Christensenellaceae family (p<0.05) that positively correlated with feed efficiency. Conclusion: Dietary addition with phytosterols at 200 mg/d could effectively improve the energy status in perinatal cows by attenuating their negative energy balance.

Keywords

Acknowledgement

The authors gave special thanks to Shanghai Biotree Biotech Co., Ltd. for the technical support for the metabolomics analyses.

References

  1. De Smet E, Mensink RP, Plat J. Effects of plant sterols and stanols on intestinal cholesterol metabolism: suggested mechanisms from past to present. Mol Nutr Food Res 2012;56:1058-72. https://doi.org/10.1002/mnfr.201100722
  2. Cedo L, Santos D, Ludwig IA, et al. Phytosterol-mediated inhibition of intestinal cholesterol absorption in mice is independent of liver X receptor. Mol Nutr Food Res 2017;61:1700055. https://doi.org/10.1002/mnfr.201700055
  3. Valerio M, Awad AB. β-Sitosterol down-regulates some pro-inflammatory signal transduction pathways by increasing the activity of tyrosine phosphatase SHP-1 in J774A.1 murine macrophages. Int Immunopharmacol 2011;11:1012-7. https://doi.org/10.1016/j.intimp.2011.02.018
  4. Awaisheh SS, Khalifeh MS, Al-Ruwaili MA, Khalil OM, Al-Ameri OH, Al-Groom R. Effect of supplementation of probiotics and phytosterols alone or in combination on serum and hepatic lipid profiles and thyroid hormones of hypercholesterolemic rats. J Dairy Sci 2013;96:9-15. https://doi.org/10.3168/jds.2012-5442
  5. Xi YM, Jin ZH, Lin LJ, Han ZY. Effect of phytosterols on rumen fermentation in vitro. Genet Mol Res 2014;13:3869-75. https://doi.org/10.4238/2014.May.16.12
  6. Xie Y, Jin ZH, Zhu J, Han ZY. Effects of phytosterols on production performance, blood cholesterol and antioxidant capacity of dairy cows. China Dairy Cattle 2020;2:12-8. (in Chinese with English Abstract)
  7. Lv D, Gao J, Wu Z, et al. Multiomic analyses reveal the effects of supplementing phytosterols on the metabolic function of the rumen microbiota in perinatal cows. Appl Environ Microbiol 2022;88:e00992-22. https://doi.org/doi:10.1128/aem.00992-22
  8. Overton TR, McArt JAA, Nydam DV. A 100-year review: metabolic health indicators and management of dairy cattle. J Dairy Sci 2017;100:10398-417. https://doi.org/10.3168/jds.2017-13054
  9. Vernon RG. Lipid metabolism during lactation: a review of adipose tissue-liver interactions and the development of fatty liver. J Dairy Res 2005;72:460-9. https://doi.org/10.1017/S0022029905001299
  10. Nydam DV, Ospina PA, McArt JA, Oetzel G, Overton TR. Monitoring negative energy balance in transition dairy cows for herd results. In: Proceedings of the 22nd Tri-State Dairy Nutrition Conference 2013; 2013 April 23-24: Fort Wayne, Indiana, USA: Michigan State University; 2013. pp. 9-22.
  11. Gao J, Yang DY, Sun ZY, et al. Changes in blood metabolic profiles reveal the dietary deficiencies of specific nutrients and physiological status of grazing yaks during the cold season in Qinghai province of China. Metabolites 2022;12:738. https://doi.org/10.3390/metabo12080738
  12. Sun HZ, Wang DM, Wang B, et al. Metabolomics of four biofluids from dairy cows: potential biomarkers for milk production and quality. J Proteome Res 2015;14:1287-98. https://doi.org/10.1021/pr501305g
  13. Ostlund Jr RE, McGill JB, Zeng CM, et al. Gastrointestinal absorption and plasma kinetics of soy Δ5-phytosterols and phytostanols in humans. Am J Physiol Endocrinol Metab 2002;282:E911-6. https://doi.org/10.1152/ajpendo.00328.2001
  14. Dixon RM, Nolan JV. Studies of the large intestine of sheep: 1. fermentation and absorption in sections of the large intestine. Br J Nutr 1982;47:289-300. https://doi.org/10.1079/bjn19820038
  15. Gu F, Zhu S, Hou J, et al. The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process. Microbiome 2023;11:87. https://doi.org/10.1186/s40168-023-01535-9
  16. Broderick GA, Kang JH. Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. J Dairy Sci 1980;63:64-75. https://doi.org/10.3168/jds.S0022-0302(80)82888-8
  17. Makkar HPS, Sharma OP, Dawra RK, Negi SS. Simple determination of microbial protein in rumen liquor. J Dairy Sci 1982;65:2170-3. https://doi.org/10.3168/jds.S0022-0302(82)82477-6
  18. Jin W, Li Y, Cheng YF, Mao SY, Zhu WY. The bacterial and archaeal community structures and methanogenic potential of the cecal microbiota of goats fed with hay and high-grain diets. Antonie Van Leeuwenhoek 2018;111:2037-49. https://doi.org/10.1007/s10482-018-1096-7
  19. Burgmann H, Pesaro M, Widmer F, Zeyer J. A strategy for optimizing quality and quantity of DNA extracted from soil. J Microbiol Methods 2001;45:7-20. https://doi.org/10.1016/s0167-7012(01)00213-5
  20. Fadrosh DW, Ma B, Gajer P, et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2014;2:6. https://doi.org/10.1186/2049-2618-2-6
  21. Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
  22. Sieber R. Cholesterol removal from animal food-can it be justified?. LWT-Food Sci Technol 1993;26:375-87. https://doi.org/10.1006/fstl.1993.1076
  23. Cuevas-Tena M, del Pulgar EMG, Benitez-Paez A, Sanz Y, Alegria A, Lagarda MJ. Plant sterols and human gut microbiota relationship: an in vitro colonic fermentation study. J Funct Foods 2018;44:322-9. https://doi.org/10.1016/j.jff.2018.03.023
  24. Coppock CE, Wilks DL. Supplemental fat in high-energy rations for lactating cows: effects on intake, digestion, milk yield, and composition. J Anim Sci 1991;69:3826-37. https://doi.org/10.2527/1991.6993826x
  25. Xia GL, Sun J, Fan YT, et al. β-sitosterol attenuates high grain diet-induced inflammatory stress and modifies rumen fermentation and microbiota in sheep. Animals 2020;10:171. https://doi.org/10.3390/ani10010171
  26. Neves AL, Yu J, Suzuki Y, et al. Accelerated discovery of novel glycoside hydrolases using targeted functional profiling and selective pressure on the rumen microbiome. Microbiome 2021;9:229. https://doi.org/10.1186/s40168-021-01147-1
  27. Salehi-Sahlabadi A, Varkaneh HK, Shahdadian F, et al. Effects of phytosterols supplementation on blood glucose, glycosylated hemoglobin (HbA1c) and insulin levels in humans: a systematic review and meta-analysis of randomized controlled trials. J Diabetes Metab Disord 2020;19:625-32. https://doi.org/10.1007/s40200-020-00526-z
  28. Cozzi G, Ravarotto L, Gottardo F, et al. Short communication: reference values for blood parameters in Holstein dairy cows: effects of parity, stage of lactation, and season of production. J Dairy Sci 2011;94:3895-901. https://doi.org/10.3168/jds.2010-3687
  29. McArt JAA, Nydam DV, Oetzel GR. Epidemiology of subclinical ketosis in early lactation dairy cattle. J Dairy Sci 2012;95:5056-66. https://doi.org/10.3168/jds.2012-5443
  30. Ospina PA, Nydam DV, Stokol T, Overton TR. Association between the proportion of sampled transition cows with increased nonesterified fatty acids and β-hydroxybutyrate and disease incidence, pregnancy rate, and milk production at the herd level. J Dairy Sci 2010;93:3595-601. https://doi.org/10.3168/jds.2010-3074
  31. van Knegsel ATM, van den Brand H, Dijkstra J, Tamminga S, Kemp B. Effect of dietary energy source on energy balance, production, metabolic disorders and reproduction in lactating dairy cattle. Reprod Nutr Dev 2005;45:665-88. https://doi.org/10.1051/rnd:2005059
  32. Zammit VA. Ketogenesis in the liver of ruminants-adaptations to a challenge. J Agric Sci 1990;115:155-62. https://doi.org/10.1017/S0021859600075080
  33. Bergseth S, Christiansen EN, Bremer J. The effect of feeding fish oils, vegetable oils and clofibrate on the ketogenesis from long chain fatty acids in hepatocytes. Lipids 1986;21:508-14. https://doi.org/10.1007/BF02535638
  34. Tessari R, Berlanda M, Morgante M, et al. Changes of plasma fatty acids in four lipid classes to understand energy metabolism at different levels of non-esterified fatty acid (NEFA) in dairy cows. Animals 2020;10:1410. https://doi.org/10.3390/ani10081410
  35. Douglas GN, Rehage J, Beaulieu AD, Bahaa AO, Drackley JK. Prepartum nutrition alters fatty acid composition in plasma, adipose tissue, and liver lipids of periparturient dairy cows. J Dairy Sci 2007;90:2941-59. https://doi.org/10.3168/jds.2006-225
  36. Rukkwamsuk T, Geelen MJH, Kruip TAM, Wensing T. Interrelation of fatty acid composition in adipose tissue, serum, and liver of dairy cows during the development of fatty liver postpartum. J Dairy Sci 2000;83:52-9. https://doi.org/10.3168/jds.S0022-0302(00)74854-5
  37. Loften JR, Linn JG, Drackley JK, Jenkins TC, Soderholm CG, Kertz AF. Invited review: palmitic and stearic acid metabolism in lactating dairy cows. J Dairy Sci 2014;97:4661-74. https://doi.org/10.3168/jds.2014-7919
  38. Stipanuk MH, Coloso RM, Garcia RA, Banks MF. Cysteine concentration regulates cysteine metabolism to glutathione, sulfate and taurine in rat hepatocytes. J Nutr 1992;122:420-7. https://doi.org/10.1093/jn/122.3.420
  39. Lang U, Aubert ML, Rivest RW, Vinas-Bradtke JC, Sizonenko PC. Inhibitory action of exogenous melatonin, 5-methoxytryptamine, and 6-hydroxymelatonin on sexual maturation of male rats: activity of 5-methoxytryptamine might be due to its conversion to melatonin. Biol Reprod 1985;33:618-28. https://doi.org/10.1095/biolreprod33.3.618
  40. Auldist MJ, Turner SA, McMahon CD, Prosser CG. Effects of melatonin on the yield and composition of milk from grazing dairy cows in New Zealand. J Dairy Res 2007;74:52-7. https://doi.org/10.1017/S0022029906002160
  41. Li Y, Gao J, Xue Y, et al. Nutrient availability of roughages in siocaloric and isonitrogenous diets alters the bacterial networks in the whole gastrointestinal tract of Hu sheep. BMC Microbiol 2023;23:70. https://doi.org/10.1186/s12866-023-02814-z
  42. Shang QH, Liu HS, Liu SJ, He TF, Piao XS. Effects of dietary fiber sources during late gestation and lactation on sow performance, milk quality, and intestinal health in piglets. J Anim Sci 2019;97:4922-33. https://doi.org/10.1093/jas/skz278
  43. Welch CB, Lourenco JM, Krause TR, et al. Evaluation of the fecal bacterial communities of angus steers with divergent feed efficiencies across the lifespan from weaning to slaughter. Front Vet Sci 2021;8:597405. https://doi.org/10.3389/fvets.2021.597405