Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

The relationship between milk oestradiol concentrations and oestrus activity in lactating Holstein–Friesian cows

Hawar M. Zebari A , S. Mark Rutter B and Emma C. L. Bleach https://orcid.org/0000-0002-2277-255X C *
+ Author Affiliations
- Author Affiliations

A Department of Animal Production, College of Agriculture, University of Duhok, Duhok, 42003 Kurdistan Region, Iraq.

B Department of Animal Health, Welfare and Behaviour, Harper Adams University, Newport, Shropshire TF10 8NB, UK.

C Department of Agriculture and Environment, Harper Adams University, Newport, Shropshire TF10 8NB, UK.

* Correspondence to: ebleach@harper-adams.ac.uk

Handling Editor: Penny Back

Animal Production Science 63(5) 441-449 https://doi.org/10.1071/AN22068
Submitted: 18 January 2022  Accepted: 2 November 2022   Published: 25 November 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Detecting oestrus to facilitate the optimal timing of artificial insemination is key to optimal reproductive performance in dairy cows.

Aims: The aims of the present study were to investigate the relationship between activity and milk oestradiol concentrations during oestrus.

Methods: Accelerometers (IceQubes, IceRobotics Ltd, UK) were used to monitor the activity (the number of steps per day) of 37 lactating Holstein–Friesian cows during the peri-oestrus period. Daily milk samples were analysed for oestradiol and progesterone concentrations.

Key results: An increase in activity sufficient to generate an oestrus alert (behavioural oestrus) from an activity sensor (GEA Rescounter II) was detected in 29 of 37 (78%) cows. Milk oestradiol increased from 2.0 ± 0.5 pg/mL 4 days before oestrus to 8.3 ± 1.1 pg/mL on the day of behavioural oestrus, then fell to 2.6 ± 0.6 pg/mL by 3 days afterwards. Similarly, activity also increased and peaked on the day of oestrus. However, in 8 of 37 (22%) cows, although milk oestradiol concentrations increased following the fall in progesterone, there was no significant increase in activity (silent oestrus). Milk oestradiol concentrations were positively correlated (r = 0.37; P = 0.03) with activity on the day of oestrus. Cows that subsequently became pregnant took a similar number of steps (2806 ± 282.3 vs 2850 ± 372.5 steps for PD+ vs PD− cows respectively) but had higher oestradiol concentrations (11.2 ± 2.06 vs 5.1 ± 0.51 pg/mL for PD+ vs PD− cows respectively) on the day of oestrus than did cows that did not become pregnant.

Conclusions: Increases in oestradiol concentrations above a threshold of approximately 10 pg/mL are associated with an increased activity, and higher oestral oestradiol concentrations are associated with a higher rate of pregnancy following insemination.

Implications: This study has demonstrated the significance of oestradiol concentration to the fertility of dairy cows. Thus, strategies to enhance oestradiol secretion may enhance fertility. Further, milk oestradiol measures may be developed as an aid to oestrus detection in lactating dairy cows, although further studies are required to determine whether on-farm assessment of milk oestradiol concentration can be developed to add to the repertoire of biomarkers of oestrus in lactating cattle.

Keywords: activity, dairy cow, milk, oestradiol, oestrus, pregnancy, silent oestrus, steps.


References

Abeyawardene SA, Hathorn DJ, Glencross RG (1984) Concentrations of oestradiol-17β and progesterone in bovine plasma and defatted milk during the post-partum anovulatory period, during oestrous cycles and following ovariectomy. British Veterinary Journal 140, 458–467.
Concentrations of oestradiol-17β and progesterone in bovine plasma and defatted milk during the post-partum anovulatory period, during oestrous cycles and following ovariectomy.Crossref | GoogleScholarGoogle Scholar |

AHDB (n.d.) Body condition scoring. AHDB, Warwickshire, UK. Available at https://ahdb.org.uk/knowledge-library/body-condition-scoring [accessed 13 April 2021]

Allrich RD (1994) Endocrine and neural control of estrus in dairy cows. Journal of Dairy Science 77, 2738–2744.
Endocrine and neural control of estrus in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Aungier SPM, Roche JF, Duffy P, Scully S, Crowe MA (2015) The relationship between activity clusters detected by an automatic activity monitor and endocrine changes during the periestrous period in lactating dairy cows. Journal of Dairy Science 98, 1666–1684.
The relationship between activity clusters detected by an automatic activity monitor and endocrine changes during the periestrous period in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |

Båge R, Gustafsson H, Larsson B, Forsberg M, Rodríguez-Martínez H (2002) Repeat breeding in dairy heifers: follicular dynamics and estrous cycle characteristics in relation to sexual hormone patterns. Theriogenology 57, 2257–2269.
Repeat breeding in dairy heifers: follicular dynamics and estrous cycle characteristics in relation to sexual hormone patterns.Crossref | GoogleScholarGoogle Scholar |

Balendran A, Gordon M, Pretheeban T, Singh R, Perera R, Rajamahedran R (2008) Decreased fertility with increasing parity in lactating dairy cows. Canadian Journal of Animal Science 88, 425–428.
Decreased fertility with increasing parity in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |

Bloch A, Folman Y, Kaim M, Roth Z, Braw-Tal R, Wolfenson D (2006) Endocrine alterations associated with extended time interval between estrus and ovulation in high-yield dairy cows. Journal of Dairy Science 89, 4694–4702.
Endocrine alterations associated with extended time interval between estrus and ovulation in high-yield dairy cows.Crossref | GoogleScholarGoogle Scholar |

Boer HMT, Veerkamp RF, Beerda B, Woelders H (2010) Estrous behavior in dairy cows: identification of underlying mechanisms and gene functions. Animal 4, 446–453.
Estrous behavior in dairy cows: identification of underlying mechanisms and gene functions.Crossref | GoogleScholarGoogle Scholar |

Butler WR, Smith RD (1989) Interrelationships between energy balance and postpartum reproductive function in dairy cattle. Journal of Dairy Science 72, 767–783.
Interrelationships between energy balance and postpartum reproductive function in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Chapinal N, de Passillé AM, Weary DM, von Keyserlingk MAG, Rushen J (2009) Using gait score, walking speed, and lying behavior to detect hoof lesions in dairy cows. Journal of Dairy Science 92, 4365–4374.
Using gait score, walking speed, and lying behavior to detect hoof lesions in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Chebel RC, Santos JEP, Reynolds JP, Cerri RLA, Juchem SO, Overton M (2004) Factors affecting conception rate after artificial insemination and pregnancy loss in lactating dairy cows. Animal Reproduction Science 84, 239–255.
Factors affecting conception rate after artificial insemination and pregnancy loss in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |

Coe BL, Allrich RD (1989) Relationship between endogenous estradiol-17β and estrous behavior in heifers. Journal of Animal Science 67, 1546–1551.
Relationship between endogenous estradiol-17β and estrous behavior in heifers.Crossref | GoogleScholarGoogle Scholar |

Cook DL, Winters TA, Horstman LA, Allrich RD (1986) Induction of estrus in ovariectomized cows and heifers: effects of estradiol benzoate and gonadotropin releasing hormone. Journal of Animal Science 63, 546–550.
Induction of estrus in ovariectomized cows and heifers: effects of estradiol benzoate and gonadotropin releasing hormone.Crossref | GoogleScholarGoogle Scholar |

Cruppe LH (2001) The effect of preovulatory concentration of estradiol and length of proestrus on fertility in beef cattle. PhD thesis, The Ohio State University, USA.

Dobson H (1978) Plasma gonadotrophins and oestradiol during oestrus in the cow. Journal of Reproduction and Fertility 52, 51–53.
Plasma gonadotrophins and oestradiol during oestrus in the cow.Crossref | GoogleScholarGoogle Scholar |

Dolecheck KA, Silvia WJ, Heersche G, Chang YM, Ray DL, Stone AE, Wadsworth BA, Bewley JM (2015) Behavioral and physiological changes around estrus events identified using multiple automated monitoring technologies. Journal of Dairy Science 98, 8723–8731.
Behavioral and physiological changes around estrus events identified using multiple automated monitoring technologies.Crossref | GoogleScholarGoogle Scholar |

Domènech A, Pich S, Arís A, Plasencia C, Bach A, Serrano A (2011) Heat identification by 17β-estradiol and progesterone quantification in individual raw milk samples by enzyme immunoassay. Electronic Journal of Biotechnology 14, 10
Heat identification by 17β-estradiol and progesterone quantification in individual raw milk samples by enzyme immunoassay.Crossref | GoogleScholarGoogle Scholar |

Foote RH (1979) Time of artificial insemination and fertility in dairy cattle. Journal of Dairy Science 62, 355–358.
Time of artificial insemination and fertility in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Fricke PM, Carvalho PD, Giordano JO, Valenza A, Lopes G, Amundson MC (2014) Expression and detection of estrus in dairy cows: the role of new technologies. Animal 8, 134–143.
Expression and detection of estrus in dairy cows: the role of new technologies.Crossref | GoogleScholarGoogle Scholar |

Garcia E, Hultgren J, Fällman P, Geust J, Algers B, Stilwell G, Gunnarsson S, Rodriguez-Martinez H (2011) Oestrous intensity is positively associated with reproductive outcome in high-producing dairy cows. Livestock Science 139, 191–195.
Oestrous intensity is positively associated with reproductive outcome in high-producing dairy cows.Crossref | GoogleScholarGoogle Scholar |

Glencross RG (1987) Effect of pulsatile infusion of gonadotrophin-releasing hormone on plasma oestradiol-17β concentrations and follicular development during naturally and artificially maintained high levels of plasma progesterone in heifers. Journal of Endocrinology 112, 77–85.
Effect of pulsatile infusion of gonadotrophin-releasing hormone on plasma oestradiol-17β concentrations and follicular development during naturally and artificially maintained high levels of plasma progesterone in heifers.Crossref | GoogleScholarGoogle Scholar |

Glencross RG, Abeywardene SA (1983) Concentrations of oestradiol-17β and progesterone in plasma and defatted milk of cattle during the oestrous cycle. British Veterinary Journal 139, 49–51.
Concentrations of oestradiol-17β and progesterone in plasma and defatted milk of cattle during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar |

Glencross RG, Pope GS (1981) Concentrations of oestradiol-17β and progesterone in the plasma of dairy heifers before and after cloprostenol-induced and natural luteolysis and during early pregnancy. Animal Reproduction Science 4, 93–106.
Concentrations of oestradiol-17β and progesterone in the plasma of dairy heifers before and after cloprostenol-induced and natural luteolysis and during early pregnancy.Crossref | GoogleScholarGoogle Scholar |

Glencross RG, Esslemont RJ, Bryant MJ, Pope GS (1981) Relationships between the incidence of pre-ovulatory behaviour and the concentrations of oestradiol-17β and progesterone in bovine plasma. Applied Animal Ethology 7, 141–148.
Relationships between the incidence of pre-ovulatory behaviour and the concentrations of oestradiol-17β and progesterone in bovine plasma.Crossref | GoogleScholarGoogle Scholar |

Gwazdauskas FC, Lineweaver JA, McGilliard ML (1983) Environmental and management factors affecting estrous activity in dairy cattle. Journal of Dairy Science 66, 1510–1514.
Environmental and management factors affecting estrous activity in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Gyawu P, Pope GS (1983) Oestrogens in milk. Journal of Steroid Biochemistry 19, 877–882.
Oestrogens in milk.Crossref | GoogleScholarGoogle Scholar |

Gyawu P, Pope GS (1990) Post-partum, ovarian function in dairy cows as revealed by concentrations of oestradiol-17β and progesterone in defatted milk. British Veterinary Journal 146, 194–204.
Post-partum, ovarian function in dairy cows as revealed by concentrations of oestradiol-17β and progesterone in defatted milk.Crossref | GoogleScholarGoogle Scholar |

Inchaisri C, Jorritsma R, Vos PL, van der Weijden GC, Hogeveen H (2010) Economic consequences of reproductive performance in dairy cattle. Theriogenology 74, 835–846.
Economic consequences of reproductive performance in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Isobe N, Yoshimura T, Yoshida C, Nakao T (2004) Incidence of silent ovulation in dairy cows during post partum period. Deutsche Tierarztliche Wochenschrift 111, 35–38.

Kaneko H, Terada T, Taya K, Watanabe G, Sasamoto S, Hasegawa Y, Igarashi M (1991) Ovarian follicular dynamics and concentrations of oestradiol-17 beta, progesterone, luteinizing hormone and follicle stimulating hormone during the periovulatory phase of the oestrous cycle in the cow. Reproduction, Fertility and Development 3, 529–535.
Ovarian follicular dynamics and concentrations of oestradiol-17 beta, progesterone, luteinizing hormone and follicle stimulating hormone during the periovulatory phase of the oestrous cycle in the cow.Crossref | GoogleScholarGoogle Scholar |

Lopez H, Bunch TD, Shipka MP (2002) Estrogen concentrations in milk at estrus and ovulation in dairy cows. Animal Reproduction Science 72, 37–46.
Estrogen concentrations in milk at estrus and ovulation in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Lopez H, Satter LD, Wiltbank MC (2004) Relationship between level of milk production and estrous behavior of lactating dairy cows. Animal Reproduction Science 81, 209–223.
Relationship between level of milk production and estrous behavior of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |

López-Gatius F, Santolaria P, Mundet I, Yániz JL (2005) Walking activity at estrus and subsequent fertility in dairy cows. Theriogenology 63, 1419–1429.
Walking activity at estrus and subsequent fertility in dairy cows.Crossref | GoogleScholarGoogle Scholar |

López-Gatius F, Mirzaei A, Santolaria P, Bech-Sàbat G, Nogareda C, García-Ispierto I, Hanzen C, Yániz JL (2008) Factors affecting the response to the specific treatment of several forms of clinical anestrus in high producing dairy cows. Theriogenology 69, 1095–1103.
Factors affecting the response to the specific treatment of several forms of clinical anestrus in high producing dairy cows.Crossref | GoogleScholarGoogle Scholar |

Lyimo ZC, Nielen M, Ouweltjes W, Kruip TAM, van Eerdenburg FJCM (2000) Relationship among estradiol, cortisol and intensity of estrous behavior in dairy cattle. Theriogenology 53, 1783–1795.
Relationship among estradiol, cortisol and intensity of estrous behavior in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Madureira AML, Silper BF, Burnett TA, Polsky L, Cruppe LH, Veira DM, Vasconcelos JLM, Cerri RLA (2015) Factors affecting expression of estrus measured by activity monitors and conception risk of lactating dairy cows. Journal of Dairy Science 98, 7003–7014.
Factors affecting expression of estrus measured by activity monitors and conception risk of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |

Mann GE, Lamming GE (2001) Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction 121, 175–180.
Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows.Crossref | GoogleScholarGoogle Scholar |

Mann GE, Fray MD, Lamming GE (2006) Effects of time of progesterone supplementation on embryo development and interferon-τ production in the cow. The Veterinary Journal 171, 500–503.
Effects of time of progesterone supplementation on embryo development and interferon-τ production in the cow.Crossref | GoogleScholarGoogle Scholar |

Meisterling EM, Dailey RA (1987) Use of concentrations of progesterone and estradiol-17β in milk in monitoring postpartum ovarian function in dairy cows. Journal of Dairy Science 70, 2154–2161.
Use of concentrations of progesterone and estradiol-17β in milk in monitoring postpartum ovarian function in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Mondal M, Rajkhowa C, Prakash BS (2006) Relationship of plasma estradiol-17β, total estrogen, and progesterone to estrus behavior in mithun (Bos frontalis) cows. Hormones and Behavior 49, 626–633.
Relationship of plasma estradiol-17β, total estrogen, and progesterone to estrus behavior in mithun (Bos frontalis) cows.Crossref | GoogleScholarGoogle Scholar |

Monk EL, Erb RE, Mollett TA (1975) Relationships between immunoreactive estrone and estradiol in milk, blood, and urine of dairy cows. Journal of Dairy Science 58, 34–40.
Relationships between immunoreactive estrone and estradiol in milk, blood, and urine of dairy cows.Crossref | GoogleScholarGoogle Scholar |

Opsomer G, Gröhn YT, Hertl J, Coryn M, Deluyker H, de Kruif A (2000) Risk factors for post partum ovarian dysfunction in high producing dairy cows in Belgium: a field study. Theriogenology 53, 841–857.
Risk factors for post partum ovarian dysfunction in high producing dairy cows in Belgium: a field study.Crossref | GoogleScholarGoogle Scholar |

Palmer MA, Olmos G, Boyle LA, Mee JF (2010) Estrus detection and estrus characteristics in housed and pastured Holstein–Friesian cows. Theriogenology 74, 255–264.
Estrus detection and estrus characteristics in housed and pastured Holstein–Friesian cows.Crossref | GoogleScholarGoogle Scholar |

Pape-Zambito DA, Magliaro AL, Kensinger RS (2007) Concentrations of 17β-estradiol in Holstein whole milk. Journal of Dairy Science 90, 3308–3313.
Concentrations of 17β-estradiol in Holstein whole milk.Crossref | GoogleScholarGoogle Scholar |

Pape-Zambito DA, Magliaro AL, Kensinger RS (2008) 17β-estradiol and estrone concentrations in plasma and milk during bovine pregnancy. Journal of Dairy Science 91, 127–135.
17β-estradiol and estrone concentrations in plasma and milk during bovine pregnancy.Crossref | GoogleScholarGoogle Scholar |

Pursley JR, Silcox RW, Wiltbank MC (1998) Effect of time of artificial insemination on pregnancy rates, calving rates, pregnancy loss, and gender ratio after synchronization of ovulation in lactating dairy cows. Journal of Dairy Science 81, 2139–2144.
Effect of time of artificial insemination on pregnancy rates, calving rates, pregnancy loss, and gender ratio after synchronization of ovulation in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |

Reith S, Hoy S (2012) Relationship between daily rumination time and estrus of dairy cows. Journal of Dairy Science 95, 6416–6420.
Relationship between daily rumination time and estrus of dairy cows.Crossref | GoogleScholarGoogle Scholar |

Ribeiro ES, Monteiro APA, Lima FS, Ayres H, Bisinotto RS, Favoreto M, Greco LF, Marsola RS, Thatcher WW, Santos JEP (2012) Effects of presynchronization and length of proestrus on fertility of grazing dairy cows subjected to a 5-day timed artificial insemination protocol. Journal of Dairy Science 95, 2513–2522.
Effects of presynchronization and length of proestrus on fertility of grazing dairy cows subjected to a 5-day timed artificial insemination protocol.Crossref | GoogleScholarGoogle Scholar |

Roelofs JB, Bouwman EG, Dieleman SJ, Van Eerdenburg FJCM, Kaal-Lansbergen LMTE, Soede NM, Kemp B (2004) Influence of repeated rectal ultrasound examinations on hormone profiles and behaviour around oestrus and ovulation in dairy cattle. Theriogenology 62, 1337–1352.
Influence of repeated rectal ultrasound examinations on hormone profiles and behaviour around oestrus and ovulation in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Roelofs JB, van Eerdenburg FJCM, Soede NM, Kemp B (2005a) Pedometer readings for estrous detection and as predictor for time of ovulation in dairy cattle. Theriogenology 64, 1690–1703.
Pedometer readings for estrous detection and as predictor for time of ovulation in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Roelofs JB, van Eerdenburg FJCM, Soede NM, Kemp B (2005b) Various behavioral signs of estrous and their relationship with time of ovulation in dairy cattle. Theriogenology 63, 1366–1377.
Various behavioral signs of estrous and their relationship with time of ovulation in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Silper BF, Madureira AML, Kaur M, Burnett TA, Cerri RLA (2015) Short communication: comparison of estrus characteristics in Holstein heifers by 2 activity monitoring systems. Journal of Dairy Science 98, 3158–3165.
Short communication: comparison of estrus characteristics in Holstein heifers by 2 activity monitoring systems.Crossref | GoogleScholarGoogle Scholar |

Tong JJ, Thompson IM, Zhao X, Lacasse P (2018) Effect of 17β-estradiol on milk production, hormone secretion, and mammary gland gene expression in dairy cows. Journal of Dairy Science 101, 2588–2601.
Effect of 17β-estradiol on milk production, hormone secretion, and mammary gland gene expression in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Valenza A, Giordano JO, Lopes G, Vincenti L, Amundson MC, Fricke PM (2012) Assessment of an accelerometer system for detection of estrus and treatment with gonadotropin-releasing hormone at the time of insemination in lactating dairy cows. Journal of Dairy Science 95, 7115–7127.
Assessment of an accelerometer system for detection of estrus and treatment with gonadotropin-releasing hormone at the time of insemination in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar |

Van Vliet JH, Van Eerdenburg FJCM (1996) Sexual activities and oestrus detection in lactating Holstein cows. Applied Animal Behaviour Science 50, 57–69.
Sexual activities and oestrus detection in lactating Holstein cows.Crossref | GoogleScholarGoogle Scholar |

Walker SL, Smith RF, Jones DN, Routly JE, Dobson H (2008) Chronic stress, hormone profiles and estrus intensity in dairy cattle. Hormones and Behavior 53, 493–501.
Chronic stress, hormone profiles and estrus intensity in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Walker SL, Smith RF, Jones DN, Routly JE, Morris MJ, Dobson H (2010) The effect of a chronic stressor, lameness, on detailed sexual behaviour and hormonal profiles in milk and plasma of dairy cattle. Reproduction in Domestic Animals 45, 109–117.
The effect of a chronic stressor, lameness, on detailed sexual behaviour and hormonal profiles in milk and plasma of dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Walsh SW, Williams EJ, Evans ACO (2011) A review of the causes of poor fertility in high milk producing dairy cows. Animal Reproduction Science 123, 127–138.
A review of the causes of poor fertility in high milk producing dairy cows.Crossref | GoogleScholarGoogle Scholar |

Walton JS, Veenhuizen LP, King GJ (1987) Relationships between time of day, estrous behavior, and the preovulatory luteinizing hormone surge in Holstein cows after treatment with cloprostenol. Journal of Dairy Science 70, 1652–1663.
Relationships between time of day, estrous behavior, and the preovulatory luteinizing hormone surge in Holstein cows after treatment with cloprostenol.Crossref | GoogleScholarGoogle Scholar |

Zebari HM (2019) Investigations of factors that influence oestrus expression in dairy cattle. PhD thesis, Harper Adams University, UK.

Zebari HM, Rutter SM, Bleach ECL (2018) Characterizing changes in activity and feeding behaviour of lactating dairy cows during behavioural and silent oestrus. Applied Animal Behaviour Science 206, 12–17.
Characterizing changes in activity and feeding behaviour of lactating dairy cows during behavioural and silent oestrus.Crossref | GoogleScholarGoogle Scholar |