Semen quality, testosterone values, and testicular and accessory gland parameters in rams receiving sustained stimulation with low doses of buserelin
Caroline Gomes do Espírito Santo A , Mario Felipe Alvarez Balaro A , Juliana Dantas Rodrigues Santos A , Lucas Francisco Leodido Correia A , Clara Vieira de Souza A , Augusto Ryonosuke Taira A , Marta Maria Campos Pereira da Costa A , Ana Beatriz da Silva Carvalho A , Rodolfo Ungerfeld B and Felipe Zandonadi Brandão A *A Faculdade de Veterinária, Universidade Federal Fluminense, Avenida Vital Brasil Filho, 64, CEP 24230-340, Niterói, RJ, Brazil.
B Facultad de Veterinaria de la Universidad de la Republica, Alberto Lasplaces 1550, 11600 Montevideo, Uruguay.
Animal Production Science 62(2) 152-162 https://doi.org/10.1071/AN20679
Submitted: 29 December 2020 Accepted: 6 September 2021 Published: 12 October 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: The use of buserelin, a gonadotropin-releasing hormone (GnRH) agonist, can improve semen quality. Nevertheless, the appropriate dosage, and frequency and time of application, remain to be established owing to the subsequent negative feedback on endogenous production of testosterone described so far.
Aims: This study aimed to propose a new buserelin application protocol for sperm improvement in Santa Inês rams.
Methods: Fifteen Santa Inês rams were divided into two experimental groups: the first group (n = 8) received 2.5 μg buserelin acetate; and the second group (n = 7) received saline solution. Treatments were applied for 21 days at intervals of 6 h, totalling four hormonal or saline applications per day. In all animals, macroscopic and microscopic seminal characteristics and freezability, plasma testosterone, pixels of testicular parenchyma, and biometric analysis of testicular and accessory sex glands by ultrasound were evaluated throughout the period of hormonal application and for a further 7 days.
Key results: Rams receiving buserelin showed a peak of testosterone after the first week (Day 7) of application, with a drop in values at Day 14, followed by negative feedback at Day 21 and return to basal concentrations at Day 28. They also showed improvement of kinetics parameters such as straight line velocity (μm/s: +buserelin 51.5 ± 1.5 > control 46.6 ± 1.6) and linearity coefficient (%: +buserelin 53.5 ± 1.8 > control 47.5 ± 1.9). Ultrasound parameters, pixels of testicular parenchyma, and freezability were not affected by treatment.
Conclusions: The administration of buserelin was able to improve some sperm kinetics parameters of Santa Inês rams.
Implications: Low doses of this GnRH analogue can be used; however, further adjustments to the hormonal protocol are needed to obtain an effective improvement in sperm quality.
Keywords: andrology, gonadotropin releasing hormone, hormone levels, number of pixels, reproduction, sperm freezability, sperm kinetics, ultrasound.
References
Aksoy M, Kaya A, Vatansev H, Tekeli T (2002) Testosterone secretion and semen plasma enzyme activity in rams with genital pathology stimulated with GnRH. Theriogenology 57, 1907–1916.| Testosterone secretion and semen plasma enzyme activity in rams with genital pathology stimulated with GnRH.Crossref | GoogleScholarGoogle Scholar | 12041694PubMed |
Baril G, Remy B, Leboeuf B, Beckers JF, Saumande J (1996) Synchronization of estrus in goats: the relationship between eCG binding in plasma, time of occurrence of estrus and fertility following artificial insemination. Theriogenology 45, 1553–1559.
| Synchronization of estrus in goats: the relationship between eCG binding in plasma, time of occurrence of estrus and fertility following artificial insemination.Crossref | GoogleScholarGoogle Scholar |
Baruselli PS, Ferreira RM, Sá Filho MF, Bó GA (2018) Review: Using artificial insemination v. natural service in beef herds. Animal 12, s45–s52.
| Review: Using artificial insemination v. natural service in beef herds.Crossref | GoogleScholarGoogle Scholar | 29554986PubMed |
Beracochea F, Viera MN, Acevedo L, Santiago‐Moreno J, Ungerfeld R (2018) Equine Chorionic Gonadotropin (eCG) improves bucks’ semen quality during the nonbreeding season. Reproduction in Domestic Animals 53, 1096–1102.
| Equine Chorionic Gonadotropin (eCG) improves bucks’ semen quality during the nonbreeding season.Crossref | GoogleScholarGoogle Scholar | 29885006PubMed |
Bianco JJ, Handelsman DJ, Pedersen JS, Risbridger GP (2002) Direct response of the murine prostate gland and seminal vesicles to estradiol. Endocrinology 143, 4922–4933.
| Direct response of the murine prostate gland and seminal vesicles to estradiol.Crossref | GoogleScholarGoogle Scholar | 12446620PubMed |
Brogden RN, Buckley MM, Ward A (1990) Buserelin. A review of its pharmacodynamic and pharmacokinetic properties, and clinical profile. Drugs 39, 399–437.
| Buserelin. A review of its pharmacodynamic and pharmacokinetic properties, and clinical profile.Crossref | GoogleScholarGoogle Scholar | 2109679PubMed |
Büchter D, Behre HM, Kliesch S, Nieschlag E (1998) Pulsatile GnRH or human chorionic gonadotropin/human menopausal gonadotropin as effective treatment for men with hypogonadotropic hypogonadism: a review of 42 cases. European Journal of Endocrinology 139, 298–303.
| Pulsatile GnRH or human chorionic gonadotropin/human menopausal gonadotropin as effective treatment for men with hypogonadotropic hypogonadism: a review of 42 cases.Crossref | GoogleScholarGoogle Scholar | 9758439PubMed |
Camela ESC, Nociti RP, Santos VJC, Macente BI, Murawski M, Vicente WRR, Bartlewski PM, Oliveira MEF (2019) Changes in testicular size, echotexture, and arterial blood flow associated with the attainment of puberty in Dorper rams raised in a subtropical climate. Reproduction in Domestic Animals 54, 131–137.
| Changes in testicular size, echotexture, and arterial blood flow associated with the attainment of puberty in Dorper rams raised in a subtropical climate.Crossref | GoogleScholarGoogle Scholar | 29989218PubMed |
CBRA (2013) ‘Manual para exame andrológico e avaliação de sêmen animal.’ (Colégio Brasileiro de Reprodução Animal: Belo Horizonte, MG, Brazil)
Cunha GR, Alarid ET, Turner T, Donjacour AA, Boutin EL, Foster BA (1992) Normal and abnormal development of the male urogenital tract. Role of androgens, mesenchymal-epithelial interactions, and growth factors. Journal of Andrology 13, 465–475.
| Normal and abnormal development of the male urogenital tract. Role of androgens, mesenchymal-epithelial interactions, and growth factors.Crossref | GoogleScholarGoogle Scholar | 1293128PubMed |
Delgadillo JA, Fitz-Rodríguez G, Duarte G, Véliz FG, Carrillo E, Flores JA, Vielma J, Hernandez H, Malpaux B (2004) Management of photoperiod to control caprine reproduction in the subtropics. Reproduction, Fertility and Development 16, 471–478.
| Management of photoperiod to control caprine reproduction in the subtropics.Crossref | GoogleScholarGoogle Scholar |
Elbaz HT, Razek EMA, Dawod A (2019) Ultrasound imaging of the testes and accessory sex glands in male goat treated with GnRH during non-breeding season. American Journal of Animal and Veterinary Sciences 14, 86–94.
| Ultrasound imaging of the testes and accessory sex glands in male goat treated with GnRH during non-breeding season.Crossref | GoogleScholarGoogle Scholar |
Fields MJ, Burns WC, Warnick AC (1979) Age, season and breed effects on testicular volume and semen traits in young beef bulls. Journal of Animal Science 48, 1299–1304.
| Age, season and breed effects on testicular volume and semen traits in young beef bulls.Crossref | GoogleScholarGoogle Scholar | 479029PubMed |
Flores-Gil VN, Millan de la Blanca MG, Velázquez R, Toledano-Díaz A, Santiago-Moreno J, López-Sebastián A (2020) Influence of testosterone administration at the end of the breeding season on sperm cryoresistance in rams (Ovis aries) and bucks (Capra hircus. Domestic Animal Endocrinology 72, 106425
| Influence of testosterone administration at the end of the breeding season on sperm cryoresistance in rams (Ovis aries) and bucks (Capra hircus.Crossref | GoogleScholarGoogle Scholar | 32278257PubMed |
Fraser HM, Lincoln GA (1980) Effects of chronic treatment with an LHRH agonist on the secretion of LH, FSH and testosterone in the ram. Biology of Reproduction 22, 269–276.
| Effects of chronic treatment with an LHRH agonist on the secretion of LH, FSH and testosterone in the ram.Crossref | GoogleScholarGoogle Scholar | 6769512PubMed |
Giriboni J, Gökdal Ö, Eren V, Yaralı E, Santiago-Moreno J, Ungerfeld R (2019) Daily administration of a GnRH analogue enhances sperm quality in bucks during the non-breeding season. Animal Reproduction Science 200, 43–50.
| Daily administration of a GnRH analogue enhances sperm quality in bucks during the non-breeding season.Crossref | GoogleScholarGoogle Scholar | 30473147PubMed |
Giriboni J, Lacuesta L, Santiago-Moreno J, Ungerfeld R (2020) Chronic use of a GnRH agonist (deslorelin) or immunization against GnRH: effects on testicular function and sperm quality of bucks. Domestic Animal Endocrinology 71, 106395
| Chronic use of a GnRH agonist (deslorelin) or immunization against GnRH: effects on testicular function and sperm quality of bucks.Crossref | GoogleScholarGoogle Scholar | 31731252PubMed |
Hafez ESE, Hafez B (2004) ‘Reprodução animal.’ 7th edn. (Manole: São Paulo, SP, Brazil)
Jeyendran RS, Van der Ven HH, Zaneveld LJ (1992) The hypoosmotic swelling test: an update. Archives of Andrology 29, 105–116.
| The hypoosmotic swelling test: an update.Crossref | GoogleScholarGoogle Scholar | 1456832PubMed |
Junaidi A, Williamson PE, Martin GB, Stanton PG, Blackberry MA, Cummins JM, Trigg TE (2007) Pituitary and testicular endocrine responses to exogenous gonadotrophin-releasing hormone (GnRH) and luteinising hormone in male dogs treated with GnRH agonist implants. Reproduction, Fertility and Development 19, 891–898.
| Pituitary and testicular endocrine responses to exogenous gonadotrophin-releasing hormone (GnRH) and luteinising hormone in male dogs treated with GnRH agonist implants.Crossref | GoogleScholarGoogle Scholar |
Lincoln GA, Peet MJ, Cunningham RA (1977) Seasonal and circadian changes in the episodic release of follicle-stimulating hormone, luteinizing hormone and testosterone in rams exposed to artificial photoperiods. Journal of Endocrinology 72, 337–349.
| Seasonal and circadian changes in the episodic release of follicle-stimulating hormone, luteinizing hormone and testosterone in rams exposed to artificial photoperiods.Crossref | GoogleScholarGoogle Scholar |
Pereira RG (2017) ‘Resposta a diferentes formas sintéticas de GnRH na espécie ovina.’ MSc thesis, Universidade do Estado de Santa Catarina, Chapecó, SC, Brazil.
Picard-Hagen N, Lhermie G, Florentin S, Merle D, Frein P, Gayrard V (2015) Effect of gonadorelin, lecirelin, and buserelin on LH surge, ovulation, and progesterone in cattle. Theriogenology 84, 177–183.
| Effect of gonadorelin, lecirelin, and buserelin on LH surge, ovulation, and progesterone in cattle.Crossref | GoogleScholarGoogle Scholar | 25890780PubMed |
Risbridger G, Wang H, Young P, Kurita T, Wang YZ, Lubahn D, Gustafsson JA, Cunha G, Wong YZ (2001) Evidence that epithelial and mesenchymal estrogen receptor-alpha mediates effects of estrogen on prostatic epithelium. Developmental Biology 229, 432–442.
| Evidence that epithelial and mesenchymal estrogen receptor-alpha mediates effects of estrogen on prostatic epithelium.Crossref | GoogleScholarGoogle Scholar | 11150243PubMed |
Robayo I, Montenegro V, Valdés C, Cox JF (2008) CASA assessment of kinematic parameters of ram spermatozoa and their relationship to migration efficiency in ruminant cervical mucus. Reproduction in Domestic Animals 43, 393–399.
| CASA assessment of kinematic parameters of ram spermatozoa and their relationship to migration efficiency in ruminant cervical mucus.Crossref | GoogleScholarGoogle Scholar | 18282216PubMed |
Rodríguez-Martínez H (2006) Can we increase the estimated value of semen assessment? Reproduction in Domestic Animals 41, 2–10.
| Can we increase the estimated value of semen assessment?Crossref | GoogleScholarGoogle Scholar | 16984464PubMed |
Rosa HJ, Juniper DT, Bryant MJ (2000) Effects of recent sexual experience and melatonin treatment of rams on plasma testosterone concentration, sexual behaviour and ability to induce ovulation in seasonally anoestrous ewes. Reproduction 120, 169–176.
| Effects of recent sexual experience and melatonin treatment of rams on plasma testosterone concentration, sexual behaviour and ability to induce ovulation in seasonally anoestrous ewes.Crossref | GoogleScholarGoogle Scholar |
Roy F, Combes B, Vaiman D, Cribiu EP, Pobel T, Delétang F, Combarnous Y, Guillou F, Maurel M-C (1999) Humoral immune response to equine chorionic gonadotropin in ewes: association with major histocompatibility complex and interference with subsequent fertility. Biology of Reproduction 61, 209–218.
| Humoral immune response to equine chorionic gonadotropin in ewes: association with major histocompatibility complex and interference with subsequent fertility.Crossref | GoogleScholarGoogle Scholar | 10377051PubMed |
Salamon S, Maxwell WMC (2000) Storage of ram semen. Animal Reproduction Science 62, 77–111.
| Storage of ram semen.Crossref | GoogleScholarGoogle Scholar | 10924821PubMed |
Sandow J, Fraser HM, Seidel H, Krauss B, Jerabeck-Sandow G, Von Rechenberg W (1987) Buserelin: pharmacokinetics, metabolism and mechanisms of action. British Journal of Clinical Practice 4, 6–13.
Schanbacher BD (1978) Fertility of rams chronically treated with gonadotropin releasing hormone during the nonbreeding season. Biology of Reproduction 19, 661–665.
| Fertility of rams chronically treated with gonadotropin releasing hormone during the nonbreeding season.Crossref | GoogleScholarGoogle Scholar | 363186PubMed |
Schanbacher BD, Lunstra DD (1977) Acute and chronic effects of gonadotropin releasing hormone on reproductive characteristics of rams during the nonbreeding season. Journal of Animal Science 44, 650–655.
| Acute and chronic effects of gonadotropin releasing hormone on reproductive characteristics of rams during the nonbreeding season.Crossref | GoogleScholarGoogle Scholar | 323207PubMed |
Skarin G, Nillius SJ, Wibell L, Wide L (1982) Chronic pulsatile low dose GnRH therapy for induction of testosterone production and spermatogenesis in a man with secondary hypogonadotropic hypogonadism. The Journal of Clinical Endocrinology & Metabolism 55, 723–726.
| Chronic pulsatile low dose GnRH therapy for induction of testosterone production and spermatogenesis in a man with secondary hypogonadotropic hypogonadism.Crossref | GoogleScholarGoogle Scholar |
Suarez SS, Pacey AA (2006) Sperm transport in the female reproductive tract. Human Reproduction Update 12, 23–37.
| Sperm transport in the female reproductive tract.Crossref | GoogleScholarGoogle Scholar | 16272225PubMed |
Suiter J (1994) Body condition scoring of sheep and goats. Farmnote 69–1994. Department of Agriculture and Food Western Australia, Perth, WA, Australia.
Tilbrook AJ, de Kretser DM, Cummins JT, Clarke IJ (1991) The negative feedback effects of testicular steroids are predominantly at the hypothalamus in the ram. Endocrinology 129, 3080–3092.
| The negative feedback effects of testicular steroids are predominantly at the hypothalamus in the ram.Crossref | GoogleScholarGoogle Scholar | 1954890PubMed |
Ungerfeld R, Clemente N, Bonjour L, Orihuela A (2014) Equine chorionic gonadotrophin administration to rams improves their effectiveness to stimulate anoestrous ewes (the ‘ram effect’). Animal Reproduction Science 149, 194–198.
| Equine chorionic gonadotrophin administration to rams improves their effectiveness to stimulate anoestrous ewes (the ‘ram effect’).Crossref | GoogleScholarGoogle Scholar | 25059200PubMed |
Ungerfeld R, Casuriaga D, Giriboni J, Freitas-de-Melo A, Silveira P, Brandão FZ (2018) Administration of cloprostenol and oxytocin before electroejaculation in goat bucks reduces the needed amount of electrical stimulation without affecting seminal quality. Theriogenology 107, 1–5.
| Administration of cloprostenol and oxytocin before electroejaculation in goat bucks reduces the needed amount of electrical stimulation without affecting seminal quality.Crossref | GoogleScholarGoogle Scholar | 29120706PubMed |
Verstegen J, Iguer-Ouada M, Onclin K (2002) Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology 57, 149–179.
| Computer assisted semen analyzers in andrology research and veterinary practice.Crossref | GoogleScholarGoogle Scholar | 11775967PubMed |
Vilanova XM, De Briyne N, Beaver B, Turner PV (2019) Horse welfare during equine chorionic gonadotropin (eCG) production. Animals 9, 1053
| Horse welfare during equine chorionic gonadotropin (eCG) production.Crossref | GoogleScholarGoogle Scholar |
Xue JL, Dial GD, Bartsh S, Kerkaert B, Squires EJ, Marsh WE, Ferre G (1994) Influence of a gonadotropin-releasing hormone agonist on circulating concentrations of luteinizing hormone and testosterone and tissue concentrations of compounds associated with boar taint. Journal of Animal Science 72, 1290–1298.
| Influence of a gonadotropin-releasing hormone agonist on circulating concentrations of luteinizing hormone and testosterone and tissue concentrations of compounds associated with boar taint.Crossref | GoogleScholarGoogle Scholar | 8056676PubMed |
Zhang L, Cai K, Wang Y, Ji W, Cheng Z, Chen G, Liao Z (2019) The pulsatile gonadorelin pump induces earlier spermatogenesis than cyclical gonadotropin therapy in congenital hypogonadotropic hypogonadism men. American Journal of Men’s Health 13, 1557988318818280
| The pulsatile gonadorelin pump induces earlier spermatogenesis than cyclical gonadotropin therapy in congenital hypogonadotropic hypogonadism men.Crossref | GoogleScholarGoogle Scholar | 30569789PubMed |