Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-18T05:57:37.882Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of triterpenoid saponins from Saponaria officinalis on some blood hormones, metabolic parameters and fatty acid composition in dairy cows

Published online by Cambridge University Press:  09 November 2015

K. SZKUDELSKA ,
M. SZUMACHER-STRABEL ,
J. SZCZECHOWIAK ,
M. BRYSZAK ,
E. PERS-KAMCZYC ,
A. STOCHMAL  and
A. CIESLAK
K. SZKUDELSKA
Affiliation:
Department of Animal Physiology and Biochemistry, Faculty of Veterinary Medicine and Animal Sciences, Poznan University of Life Sciences, Wołynska 35, 60-637 Poznan, Poland
M. SZUMACHER-STRABEL
Affiliation:
Department of Animal Nutrition and Feed Management, Faculty of Veterinary Medicine and Animal Sciences, Poznan University of Life Sciences, Wołynska 33, 60-637 Poznan, Poland
J. SZCZECHOWIAK
Affiliation:
Department of Animal Nutrition and Feed Management, Faculty of Veterinary Medicine and Animal Sciences, Poznan University of Life Sciences, Wołynska 33, 60-637 Poznan, Poland
M. BRYSZAK
Affiliation:
Department of Animal Nutrition and Feed Management, Faculty of Veterinary Medicine and Animal Sciences, Poznan University of Life Sciences, Wołynska 33, 60-637 Poznan, Poland
E. PERS-KAMCZYC
Affiliation:
Institute of Dendrology, Polish Academy of Sciences, Kornik, Poland
A. STOCHMAL
Affiliation:
Department of Biochemistry and Crop Quality, Institute of Soil Science and Plant Cultivation, Pulawy, Poland
A. CIESLAK*
Affiliation:
Department of Animal Nutrition and Feed Management, Faculty of Veterinary Medicine and Animal Sciences, Poznan University of Life Sciences, Wołynska 33, 60-637 Poznan, Poland
*
*To whom all correspondence should be addressed. Email: adamck@up.poznan.pl
Get access Rights & Permissions [Opens in a new window]

Summary

An experiment was performed to determine the effect of triterpenoid saponins from powdered root of Saponaria officinalis L. (SO) on some blood metabolic parameters and hormone concentrations in dairy cows. Three dairy Polish Holstein-Friesian cows were used in the experiment in a 3 × 3 Latin Square arrangement. Animals were fed twice a day with a control diet and two experimental diets – a diet supplemented with either 440 or 660 g/d of the powdered S. officinalis root (SO1 and SO2, respectively). Each of the three experimental cycles lasted for 26 days, including a 23-day adaptation period and a 3-day sample collection period. Blood samples were collected from the jugular vein from 24th to 26th day of the experiment. Total high-density lipoproteins cholesterol (HDL) and low-density lipoproteins cholesterol (LDL), as well as triglycerides, free fatty acids (FFA) and glucose, were assayed in serum. Fatty acid composition in the blood was also analysed. Moreover, concentrations of insulin, glucagon, leptin, triiodothyronine (T3) and thyroxine (T4) were measured. It was demonstrated that total and HDL-cholesterol concentrations were significantly elevated in the blood of cows treated with experimental diets; however, LDL-cholesterol remained unchanged. No concentrations of triglycerides, FFA or glucose were influenced by saponins. Two fatty acids (C16 : 0 and C16 : 1c9) were markedly reduced when SO was used, while C18 : 1t11 decreased with increasing levels of SO. The significant increase of C20 : 4n-6 in animals treated with SO was observed. Both saponin diets resulted in a slight increase in insulin concentration and the SO2 diet evoked an emphatic rise of glucagon concentration. The concentration of T3 also increased after consumption of the experimental diet. The current study shows for the first time that triterpenoid saponins from S. officinalis can alter blood parameters in ruminants. These effects seem to result from saponin-induced changes in the rumen.

Type
Animal Research Papers
Information
The Journal of Agricultural Science , Volume 154 , Issue 3 , April 2016 , pp. 532 - 541
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anantasook, N., Wanapat, M., Cherdthong, A. & Gunun, P. (2015). Effect of tannins and saponins in Samanea saman on rumen environment, milk yield and milk composition in lactating dairy cows. Journal of Animal Physiology and Animal Nutrition 99, 335–344.CrossRefGoogle ScholarPubMed
AOAC (2007). Official Methods of Analysis. 18th edn, Gaithersburg, MD: AOAC.Google Scholar
Aronis, K. N., Khan, S. M. & Mantzoros, C. S. (2012). Effects of trans fatty acids on glucose homeostasis: a meta-analysis of randomized, placebo-controlled clinical trials. American Journal of Clinical Nutrition 96, 1093–1099.Google Scholar
Ascherio, A. (2006). Trans fatty acids and blood lipids. Atherosclerosis Supplements 7 (Suppl. 2), 25–27.CrossRefGoogle ScholarPubMed
Bomford, R. (1980). Saponin and other haemolysins (vitamin A, aliphatic amines, polyene antibiotics) as adjuvants for SRBC in the mouse. Evidence for a role for cholesterol-binding in saponin adjuvanticity. International Archives of Allergy and Applied Immunology 63, 170–177.Google Scholar
Brogna, D. M., Nasri, S., Salem, H. B., Mele, M., Serra, A., Bella, M., Priolo, A., Makkar, H. P. & Vasta, V. (2011). Effect of dietary saponins from Quillaja saponaria L. on fatty acid composition and cholesterol content in muscle Longissimus dorsi of lambs. Animal 5, 1124–1130.Google Scholar
Brouwer, I. A., Wanders, A. J. & Katan, M. B. (2010). Effect of animal and industrial trans fatty acids on HDL and LDL cholesterol levels in humans-a quantitative review. PLoS ONE 5, e9434. doi: 10.1371/journal.pone.0009434.Google Scholar
Budan, A., Tessier, N., Saunier, M., Gillmann, L., Hamelin, J., Chicoteau, P., Richomme, P. & Guilet, D. (2013). Effect of several saponin containing plant extracts on rumen fermentation in vitro, Tetrahymena pyriformis and sheep erythrocytes. Journal of Food, Agriculture & Environment 11, 576–582.Google Scholar
Budan, A., Bellenot, D., Freuze, I., Gillmann, L., Chicoteau, P., Richomme, P. & Guilet, D. (2014). Potential of extracts from Saponaria officinalis and Calendula officinalis to modulate in vitro rumen fermentation with respect to their content in saponins. Bioscience, Biotechnology and Biochemistry 78, 288–295.Google Scholar
Calvert, G. D., Blight, L., Illman, R. J., Topping, D. L. & Potter, J. D. (1981). A trial of the effects of soya-bean flour and soya-bean saponins on plasma lipids, faecal bile acids and neutral sterols in hypercholesterolaemic men. British Journal of Nutrition 45, 277–281.CrossRefGoogle ScholarPubMed
Chilliard, Y., Ferlay, A., Rouel, J. & Lamberet, G. (2003). A review of nutritional and physiological factors affecting goat milk lipid synthesis and lipolysis. Journal of Dairy Science 86, 1751–1770.Google Scholar
Cieslak, A., Machmüller, A., Szumacher-Strabel, M. & Scheeder, M. R. L. (2009). A comparison of two extraction methods used to quantify the C18 fatty acids in feed and digesta of ruminants. Journal of Animal and Feed Sciences 18, 362–367.Google Scholar
Cieslak, A., Szumacher-Strabel, M., Stochmal, A. & Oleszek, W. (2013). Plant components with specific activities against rumen methanogens. Animal 7, (Suppl. 2), 253–265.CrossRefGoogle ScholarPubMed
Cieslak, A., Zmora, P., Stochmal, A., Pecio, L., Oleszek, W., Pers-Kamczyc, E., Szczechowiak, J., Nowak, A. & Szumacher-Strabel, M. (2014). Rumen antimethanogenic effect of Saponaria officinalis L. phytochemicals in vitro . Journal of Agricultural Science, Cambridge 152, 981–993.Google Scholar
Danfaer, A., Tetens, V. & Agergaard, N. (1995). Review and an experimental study on the physiological and quantitative aspects of gluconeogenesis in lactating ruminants. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 111, 201–210.Google Scholar
Demeyer, D. & Doreau, M. (1999). Targets and procedures for altering ruminant meat and milk lipids. Proceedings of the Nutrition Society 58, 593–607.Google Scholar
Duncombe, W. G. (1964). The colorimetric micro-determination of nonesterified fatty acids in plasma. Clinica Chimica Acta 9, 122–125.Google Scholar
Duntas, L. H. & Wartofsky, L. (2007). Cardiovascular risk and subclinical hypothyroidism: focus on lipids and new emerging risk factors. What is the evidence? Thyroid 17, 1075–1084.CrossRefGoogle ScholarPubMed
FASS (2010). The Care and Use of Agricultural Animals in Research and Teaching. 3rd edn, Champaign, IL: FASS.Google Scholar
Fernandez, M. L. & West, K. L. (2005). Mechanisms by which dietary fatty acids modulate plasma lipids. Journal of Nutrition 135, 2075–2078.Google Scholar
Flåøyen, A., Wilkins, A. L. & Sandvik, M. (2002). Ruminal metabolism in sheep of saponins from Yucca schidigera . Veterinary Research Communications 26, 159–169.CrossRefGoogle ScholarPubMed
Francis, G., Kerem, Z., Makkar, H. P. S. & Becker, K. (2002). The biological action of saponins in animal systems: a review. British Journal of Nutrition 88, 587–605.Google Scholar
Gerrits, W. J., Decuypere, E., Verstegen, M. W. & Karabinas, V. (1998). Effect of protein and protein-free energy intake on plasma concentrations of insulin-like growth factor I and thyroid hormones in preruminant calves. Journal of Animal Science 76, 1356–1363.Google Scholar
Grummer, R. R. & Carroll, D. J. (1988). A review of lipoprotein cholesterol metabolism: importance to ovarian function. Journal of Animal Science 66, 3160–3173.Google Scholar
Gutierrez, J. & Davis, R. E. (1962). Culture and metabolism of the rumen ciliate Epidinium ecaudatum Crawley. Applied Microbiology 10, 305–308.Google Scholar
Hammond, A. C., Huntington, G. B. & Bitman, J. (1984). Effect of nitrogen intake on and rhythmicity of circulating thyroid hormones in steers. Domestic Animal Endocrinology 1, 29–42.CrossRefGoogle Scholar
Harwood, H. J. Jr, Chandler, C. E., Pellarin, L. D., Bangerter, F. W., Wilkins, R. W., Long, C. A., Cosgrove, P. G., Malinow, M. R., Marzetta, C. A., Pettini, J. L., Savoy, Y. E. & Mayne, J. T. (1993). Pharmacologic consequences of cholesterol absorption inhibition: alteration in cholesterol metabolism and reduction in plasma cholesterol concentration induced by the synthetic saponin beta-tigogenin cellobioside (CP-88818; tiqueside). Journal of Lipid Research 34, 377–395.Google Scholar
Hess, H. D., Beuret, R. A., Lötscher, M., Hindrichsen, I. K., Machmüller, A., Carulla, J. E., Lascano, C. E. & Kreuzer, M. (2004). Ruminal fermentation, methanogenesis and nitrogen utilization of sheep receiving tropical grass hay-concentrate diets offered with Sapindus saponaria fruits and Cratylia argentea foliage. Animal Science 79, 177–189.Google Scholar
Hocquette, J. F. & Bauchart, D. (1999). Intestinal absorption, blood transport and hepatic and muscle metabolism of fatty acids in preruminant and ruminant animals. Reproduction Nutrition Development 39, 27–48.Google Scholar
Hoffmann, E. M., Selje-Assmann, N. & Becker, K. (2008). Dose studies on anti-proteolytic effects of a methanol extract from Knautia arvensis on in vitro ruminal fermentation. Animal Feed Science and Technology 145, 285–301.CrossRefGoogle Scholar
Holtshausen, L., Chaves, A. V., Beauchemin, K. A., McGinn, S. M., McAllister, T. A., Odongo, N. E., Cheeke, P. R. & Benchaar, C. (2009). Feeding saponin-containing Yucca schidigera and Quillaja saponaria to decrease enteric methane production in dairy cows. Journal of Dairy Science 92, 2809–2821.Google Scholar
Hu, W., Liu, J., Wu, Y., Guo, Y. & Ye, J. (2006). Effects of tea saponins on in vitro ruminal fermentation and growth performance in growing Boer goat. Archives of Animal Nutrition 60, 89–97.Google Scholar
INRA Iz, Instytut Zootechniki (1993). Normy Żywienia Bydła, Owiec i Kóz [Feed requirements for Cattle, Sheep and Goats]. Warsaw, Poland: Omnitech Press.Google Scholar
Ishii, Y. & Tanizawa, H. (2006). Effects of soyasaponins on lipid peroxidation through the secretion of thyroid hormones. Biological and Pharmaceutical Bulletin 29, 1759–1763.CrossRefGoogle ScholarPubMed
Jenkins, K. J. & Atwal, A. S. (1994). Effects of dietary saponins on fecal bile acids and neutral sterols, and availability of vitamins A and E in the chick. Journal of Nutritional Biochemistry 5, 134–138.Google Scholar
Kwon, D. Y., Kim, Y. S., Hong, S. M. & Park, S. (2009). Long-term consumption of saponins derived from Platycodi radix (22 years old) enhances hepatic insulin sensitivity and glucose-stimulated insulin secretion in 90% pancreatectomized diabetic rats fed a high-fat diet. British Journal of Nutrition 101, 358–366.Google Scholar
Lee, J. S., Choi, M. S., Seo, K. I., Lee, J., Lee, H. I., Lee, J. H., Kim, M. J. & Lee, M. K. (2014). Platycodi radix saponin inhibits α-glucosidase in vitro and modulates hepatic glucose-regulating enzyme activities in C57BL/KsJ-db/db mice. Archives of Pharmacal Research 37, 773–782.Google Scholar
Lee, W. K., Kao, S. T., Liu, I. M. & Cheng, J. T. (2006). Increase of insulin secretion by ginsenoside Rh2 to lower plasma glucose in Wistar rats. Clinical and Experimental Pharmacology and Physiology 33, 27–32.Google Scholar
Lorent, J., Le Duff, C. S., Quetin-Leclercq, J. & Mingeot-Leclercq, M. P. (2013). Induction of highly curved structures in relation to membrane permeabilization and budding by the triterpenoid saponins, α- and δ-Hederin. Journal of Biological Chemistry 288, 14000–14017.Google Scholar
Mader, T. L. & Brumm, M. C. (1987). Effect of feeding Sarsaponin in cattle and swine diets. Journal of Animal Science 65, 9–15.Google Scholar
Makkar, H. P. S. & Becker, K. (1996). Effect of Quillaja saponins on in vitro rumen fermentation. In Saponins used in Food and Agriculture (Eds Waller, G. R. & Yamasaki, K.), pp. 387–394. Advances in Experimental Medicine and Biology vol. 405. New York: Springer-Verlag.Google Scholar
Makkar, H. P. S., Sen, S., Blümmel, M. & Becker, K. (1998). Effects of fractions containing saponins from Yucca schidigera, Quillaja saponaria, and Acacia auriculoformis on rumen fermentation. Journal of Agricultural and Food Chemistry 46, 4324–4328.Google Scholar
Meagher, L. P., Smith, B. L. & Wilkins, A. L. (2001). Metabolism of diosgenin-derived saponins: implications for hepatogenous photosensitization diseases in ruminants. Animal Feed Science and Technology 91, 157–170.Google Scholar
Megraw, R. E., Dunn, D. E. & Biggs, H. G. (1979). Manual and continuous-flow colorimetry of triacylglycerols by a fully enzymic method. Clinical Chemistry 25, 273–284.Google Scholar
Navas-Camacho, A., Laredo, M. A., Cuesta, A., Anzola, H. & Leon, J. C. (1993). Effect of supplementation with a tree legume forage on rumen function. Livestock Research for Rural Development 5, 58–71.Google Scholar
Ness, G. C. (1991). Thyroid hormone. Basis for its hypocholesterolemic effect. Journal of the Florida Medical Association 78, 383–385.Google Scholar
Oakenfull, D. & Sidhu, G. S. (1990). Could saponins be a useful treatment for hypercholesterolemia? European Journal of Clinical Nutrition 44, 79–88.Google Scholar
Ooi, E. M., Ng, T. W., Watts, G. F. & Barrett, P. H. (2013). Dietary fatty acids and lipoprotein metabolism: new insights and updates. Current Opinion in Lipidology 24, 192–197.Google Scholar
Park, M. W., Ha, J. & Chung, S. H. (2008). 20(S)-ginsenoside Rg3 enhances glucose-stimulated insulin secretion and activates AMPK. Biological and Pharmaceutical Bulletin 31, 748–751.Google Scholar
Patra, A. K. & Saxena, J. (2009). The effect and mode of action of saponins on the microbial populations and fermentation in the rumen and ruminant production. Nutrition Research Reviews 22, 204–219.Google Scholar
Patra, A. K. & Yu, Z. (2014). Effects of vanillin, Quillaja saponin, and essential oils on in vitro fermentation and protein-degrading microorganisms of the rumen. Applied Microbiology and Biotechnology 98, 897–905.Google Scholar
Petersen, M. B. & Jensen, S. K. (2014). Biohydrogenation of fatty acids is dependent on plant species and feeding regimen of dairy cows. Journal of Agricultural and Food Chemistry 62, 3570–3576.CrossRefGoogle ScholarPubMed
Roberts, C. G. P. & Ladenson, P. W. (2004). Hypothyroidism. Lancet 363, 793–803.Google Scholar
Shim, K. S. (2010). Effects of emulsified sausage supplemented with ginseng saponin on lipid metabolism in rat. Korean Journal for Food Science of Animal Resources 30, 582–589.Google Scholar
Sindambiwe, J. B., Calomme, M., Geerts, S., Pieters, L., Vlietinck, A. J. & Vanden Berghe, D. A. (1998). Evaluation of biological activities of triterpenoid saponins from Maesa lanceolata . Journal of Natural Products 61, 585–590.Google Scholar
Singh, S., Farswan, M., Ali, S., Afzal, M., Al-Abbasi, F. A., Kazmi, I. & Anwar, F. (2014). Antidiabetic potential of triterpenoid saponin isolated from Primula denticulate . Pharmaceutical Biology 52, 750–755.Google Scholar
Sliwinski, B. J., Kreuzer, M., Sutter, F., Machmuller, A. & Wettstein, H. R. (2004). Performance, body nitrogen conversion and nitrogen emission from manure of dairy cows fed diets supplemented with different plant extracts. Journal of Animal Feed and Science 13, 73–91.Google Scholar
Szczechowiak, J., Szumacher-Strabel, M., Stochmal, A., Nadolna, M., Pers-Kamczyc, E., Nowak, A., Kowalczyk, M. & Cieslak, A. (2013). Effect of Saponaria officinalis L. or Panax ginseng C. A Meyer triterpenoid saponins on ruminal fermentation in vitro . Annals of Animal Science 13, 815–827.Google Scholar
Trinder, P. (1969). Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Annals of Clinical Biochemistry 6, 24–27.Google Scholar
Ulbricht, T. L. V. & Southgate, D. A. T. (1991). Coronary heart disease: seven dietary factors. Lancet 338, 985–992.Google Scholar
Van Soest, P. J., Robertson, J. B. & Lewis, B. A. (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.Google Scholar
Voutquenne, L., Guinot, P., Froissard, C., Thoison, O., Litaudon, M. & Lavaud, C. (2005). Haemolytic acylated triterpenoid saponins from Harpullia austro-caledonica . Phytochemistry 66, 825–835.Google Scholar
Wallace, R. J., Arthaud, L. & Newbold, C. J. (1994). Influence of Yucca shidigera extract on ruminal ammonia concentrations and ruminal microorganisms. Applied and Environmental Microbiology 60, 1762–1767.Google Scholar
Wang, J. K., Ye, J. A. & Liu, J. X. (2012). Effects of tea saponins on rumen microbiota, rumen fermentation, methane production and growth performance-a review. Tropical Animal Health and Production 44, 697–706.Google Scholar
Wang, Y. X., McAllister, T. A., Newbold, C. J., Cheeke, P. R. & Cheng, K. J. (1997). Effects of Yucca extract on fermentation and degradation of saponins in the rusitec. Proceedings, Western Section, American Society of Animal Science 48, 149–152.Google Scholar
Weng, Y., Yu, L., Cui, J., Zhu, Y. R., Guo, C., Wei, G., Duan, J. L., Yin, Y., Guan, Y., Wang, Y. H., Yang, Z. F., Xi, M. M. & Wen, A. D. (2014). Antihyperglycemic, hypolipidemic and antioxidant activities of total saponins extracted from Aralia taibaiensis in experimental type 2 diabetic rats. Journal of Ethnopharmacology 152, 553–560.Google Scholar
Wina, E., Muetzel, S. & Becker, K. (2005). The impact of saponins or saponin-containing plant materials on ruminant production – a review. Journal of Agricultural and Food Chemistry 53, 8093–8105.CrossRefGoogle ScholarPubMed
Wu, J. H., Leung, G. P. H., Kwan, Y. W., Sham, T. T., Tang, J. Y., Wang, Y. H., Wan, J. B., Lee, S. M. Y. & Chan, S. W. (2013). Suppression of diet-induced hypercholesterolaemia by saponins from Panax notoginseng in rats. Journal of Functional Foods 5, 1159–1169.CrossRefGoogle Scholar