References

Adams NR. Detection of the effects of phytoestrogens on sheep and cattle. J Anim Sci. 1995; 73:(5)1509-1515 https://doi.org/10.2527/1995.7351509x

Adams NR, Croker K. Clover infertility of sheep: continuing problem. J Depart Agri Western Austr. Series 4. 1987; 28:(4)119-122

Andersen C, Nielsen TS, Purup S Phyto-oestrogens in herbage and milk from cows grazing white clover, red clover, lucerne or chicory-rich pastures. Anim. 2009; 3:(8)1189-1195 https://doi.org/10.1017/S1751731109004613

Austin AR, Aston K, Drane HM, Saba N. The fertility of heifers consuming red clover silage. Grass Forage Sci. 1982; 37:(2)101-106 https://doi.org/10.1111/J.1365-2494.1982.TB01584.X

Bennetts HW, Underwood EJ, Shier FL. A specific breeding problem of sheep on subterranean clover pastures in Western Australia. Aust Vet J. 1946; 22:(1)2-12 https://doi.org/10.1111/j.1751-0813.1946.tb15473.x

Braden AWH, Thain RI, Shutt DA. Comparison of plasma phyto-oestrogen levels in sheep and cattle after feeding on fresh clover. Aust J Agric Res. 1971; 22:(4)663-670 https://doi.org/10.1071/AR9710663

Cantero A, Sancha JL, Flores JM, Rodriguez A, Gonzalez T. Histopathological changes in the reproductive organs of Manchego ewes grazing on lucerne. Zentralbl Veterinarmed A. 1996; 43:(6)325-330 https://doi.org/10.1111/j.1439-0442.1996.tb00459.x

Cederroth CR, Zimmermann C, Beny JL Potential detrimental effects of a phytoestrogen-rich diet on male fertility in mice. Mol Cell Endocrinol. 2010; 321:(2)152-60 https://doi.org/10.1016/j.mce.2010.02.011

Coop IE, Clark VR. The reproductive performance of ewes mated on lucerne. New Zealand J Agri Res. 1960; 3:(6)922-933 https://doi.org/10.1080/00288233.1960.10419307

Cunningham IJ, Hogan KG. Oestrogens in New Zealand pasture plants. New Zealand Vet J. 1954; 2:(4)128-134 https://doi.org/10.1080/00480169.1954.33166

Daems F, Decruyenaere V, Agneessens R, Lognay G, Romnee JM, Froidmont É. Changes in the isoflavone concentration in red clover (Trifolium pratense L.) during ensiling and storage in laboratory-scale silos. Anim Feed Sci Technol. 2016; 217:36-44 https://doi.org/10.1016/j.anifeedsci.2016.04.008

Duncan AM, Phipps WR, Kurzer MS. Phyto-oestrogens. Best Pract Res Clin Endocrinol Metab. 2003; 17:(2)253-271 https://doi.org/10.1016/s1521-690x(02)00103-3

Galbraith H, Singh SB, Scaife JR. Response of castrated male sheep to oestrogenic and androgenic compounds implanted alone or in combination. Anim Sci. 1997; 64:(2)261-269 https://doi.org/10.1017/S1357729800015824

Jones RAC, Ferris DG. Virus infection stimulates phyto-oestrogen production in pasture legume plants growing in grazed swards. Ann Appl Biol. 2001; 138:(2)171-179 https://doi.org/10.1111/j.1744-7348.2001.tb00099.x

Kallela K, Heinonen K, Saloniemi H. Plant oestrogens; the cause of decreased fertility in cows. A case report. Nord Vet Med. 1984; 36:(3-4)124-129

Kelly RW, Shackell GH, Allison AJ. Reproductive performance of ewes grazing red clover (Grasslands Pawera) or white clover—grass pasture at mating. New Zealand J Experiment Agri. 1980; 8:(2)87-91 https://doi.org/10.1080/03015521.1980.10426240

Marshall T, Fels HE, Neil HG, Rossiter RC. Pasture legume varieties and ewe fertility. J Depart Agric Western Aust. 1971; 12:(4)110-112

Miesner MD, Anderson DE. Management of uterine and vaginal prolapse in the bovine. Vet Clin North Am Food Anim Pract. 2008; 24:(2)409-419 https://doi.org/10.1016/j.cvfa.2008.02.008

Moravcová J, Kleinová T, Loučka R Coumestrol content of alfalfa following ensilage. Anim Feed Sci Technol. 2004; 115:(1–2)159-167 https://doi.org/10.1016/J.ANIFEEDSCI.2004.01.005

Mustonen E, Taponen S, Andersson M, Sukura A, Katila T, Taponen J. Fertility and growth of nulliparous ewes after feeding red clover silage with high phyto-oestrogen concentrations. Animal. 2014; 8:(10)1699-705 https://doi.org/10.1017/S175173111400161X

Mustonen EA, Tuori M, Kurki P, Isolahti M, Taponen J, Vanhatalo A. Variety, time of harvest and conditions during growing season have impact on red clover isoflavone content. Agricultural and Food Science. 2018; 27:(2)102-109 https://doi.org/10.23986/afsci.6978

Nwannenna AI, Lundh TJ, Madej A, Fredriksson G, Björnhag G. Clinical changes in ovariectomized ewes exposed to phytoestrogens and 17β-estradiol implants. Proc Soc Exp Biol Med. 1995; 208:(1)92-97 https://doi.org/10.3181/00379727-208-43838

Oldfield JE, Fox CW, Bahn AV, Bickoff EM, Kohler GO. Coumestrol in alfalfa as a factor in growth and carcass quality in lambs. Journal of Animal Science. 1966; 25:(1)167-174 https://doi.org/10.2527/jas1966.251167x

Pace V, Carbone K, Spirito F The effects of subterranean clover phytoestrogens on sheep growth, reproduction and carcass characteristics. Meat Science. 2006; 74:(4)616-622 https://doi.org/10.1016/j.meatsci.2006.05.00

Pace V, Contò G, Carfì F, Chiariotti A, Catillo G. Short-and long-term effects of low estrogenic subterranean clover on ewe reproductive performance. Small Rumin Res. 2011; 97:(1–3)94-100 https://doi.org/10.1016/j.smallrumres.2011.02.011

Oestrogenic effects of lucerne in female sheep. 2015. https://tinyurl.com/yre9x6rp (accessed 14 October 2022)

Pugh DG. Theriogenology of sheep goats, 1st edn. In: Schrefer JA (ed). Saunders, Philadelphia (PA): Saunders; 2002

Ramòn JP, Valderràbano J, Folch J. Reproductive performance of Rasa Aragonesa ewes mated on lucerne (Medicago sativa cv. aragon) pastures. Small Rumin Res. 1993; 11:(4)323-329 https://doi.org/10.1016/0921-4488(93)90003-Z

Reed KFM. Fertility of herbivores consuming phytoestrogen-containing Medicago and Trifolium species. Agriculture. 2016; 6:(3) https://doi.org/10.3390/agriculture6030035

Saloniemi H, Wähälä K, Nykänen-Kurki P, Kallela K, Saastamoinen I. Phytoestrogen content and estrogenic effect of legume fodder. Proc Soc Exp Biol Med. 1995; 208:(1)13-17 https://doi.org/10.3181/00379727-208-43825

Sarelli L, Tuori M, Saastamoinen I, Syrjälä-Qvist L, Saloniemi H. Phytoestrogen content of birdsfoot trefoil and red clover: Effects of growth stage and ensiling method. Acta Agric Scandinav. Section A. Animal Sci. 2003; 53:(1)58-63 https://doi.org/10.1080/09064700310002053

Schinckel PG. Infertility in ewes grazing subterranean clover pastures. Observations on breeding behaviour following transfer to” sound” country. Austr Vet J. 1948; 24:(11)289-294 https://doi.org/10.1111/j.1751-0813.1948.tb04593.x

Shackell GH, Kelly RW. Residual effects of short term grazing of red clover pastures on the reproductive performance of ewes. New Zealand Journal of Experimental Agriculture. 1984; 12:(2)113-117 https://doi.org/10.1080/03015521.1984.10421420

Sivesind E, Seguin P. Effects of the environment, cultivar, maturity, and preservation method on red clover isoflavone concentration. J Agric Food Chem. 2005; 53:(16)6397-6402 https://doi.org/10.1021/jf0507487

Testa I, Salvatori C, Di Cara G Soy-based infant formula: are phyto-oestrogens still in doubt?. Front Nutr. 2018; 5 https://doi.org/10.3389/fnut.2018.00110

Wocławek-Potocka I, Mannelli C, Boruszewska D, Kowalczyk-Zieba I, Waśniewski T, Skarżyński DJ. Diverse effects of phytoestrogens on the reproductive performance: cow as a model. Int J Endocrinol. 2013; 2013 https://doi.org/10.1155/2013/650984

Sheep
Farm practice

Impact of phyto-oestrogens on reproductive health of sheep

02 November 2022
Clinical
11 mins read
02 November 2022
Volume 27 · Issue 6
Figure 1. Red clover (Trifolium pratense), a perennial legume, that will last 3–5 years. It is higher in protein content and has greater nitrogen fixing capacity than white clover seen below in Figure 2.
Figure 1. Red clover (Trifolium pratense), a perennial legume, that will last 3–5 years. It is higher in protein content and has greater nitrogen fixing capacity than white clover seen below in Figure 2.

Abstract

Phyto-oestrogens are plant compounds that mimic the effects of oestrogen. They are mainly found in legumes, especially red and subterranean clover and lucerne. Levels vary with cultivar, season, growing stage and stress to the plant. Consumption of oestrogenic pasture or conserved forage has been shown to have negative effects on reproductive performance of sheep — in particular, a decrease in fecundity and an increase in barren rate. Prolonged exposure may lead to irreversible changes to cervical structure and reproductive performance. Evidence for the impact of phyto-oestrogens on cattle is much weaker than for sheep. The many advantages of clover and lucerne should be exploited, but an understanding of phyto-oestrogenism is needed to avoid unwanted negative impacts on livestock reproductive performance.

Phyto-oestrogens are non-steroidal compounds produced by plants that mimic the effect of the hormone oestrogen. There are reports of phyto-oestrogens having profound impacts on female reproductive performance — particularly in sheep — however, they do not appear to affect male fertility. Similarly, the sensitivity of different species to phyto-oestrogens is varied, with ruminants much more susceptible to their reproductive effects than humans. Owing to their high feed value (protein levels in particular), drought tolerance and ability to fix nitrogen, interest in the inclusion of legumes (especially red clover) in seed mixes for grazing leys and silage production has increased. As a result, there is an increased focus on the potential risk that phyto-oestrogens pose to livestock.

Phyto-oestrogens are all non-steroidal compounds that can bind to oestrogen receptors. The compounds found in plants of agricultural and veterinary importance include isoflavones and coumestans. The effect of phyto-oestrogens on different species varies with the endogenous oestrogen activity of those species. In cattle and sheep, endogenous oestrogen levels are low, so phyto-oestrogens display an oestrogenic effect. In humans, with higher endogenous oestrogen levels, phyto-oestrogens act as oestrogen antagonists.

Register now to continue reading

Thank you for visiting UK-VET Companion Animal and reading some of our peer-reviewed content for veterinary professionals. To continue reading this article, please register today.

Register
Or continue by

Signing in with your registered email address

sheep
cattle
phyto-oestrogens
clover
fertility