Physiological Anti-Müllerian Hormone Concentrations in Male and Female Dogs and Cats before and around Puberty
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animal and Blood Sample Collection
2.2. Hormone Analysis
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Jost, A. Problems of fetal endocrinology: The gonadal and hypophyseal hormones. Recent Prog. Horm. Res. 1953, 8, 379–418. [Google Scholar]
- Kitahara, G.; El-Sheikh Ali, H.; Sato, T.; Kobayashi, I.; Hemmi, K.; Shirao, Y.; Kamimura, S. Anti-Müllerian hormone (AMH) profiles as a novel biomarker to evaluate the existence of a functional chryptorchid testis in Japaniese black calves. J. Reprod. Dev. 2012, 58, 310–315. [Google Scholar] [CrossRef]
- Durlinger, A.L.; Gruijters, M.J.; Kramer, P.; Karels, B.; Ingraham, H.A.; Nachtigal, M.W.; Uilenbroek, J.T.J.; Grootegoed, J.A.; Themmen, A.P. Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002, 143, 1076–1084. [Google Scholar] [CrossRef]
- Sriraman, V.; Niu, E.; Matias, J.; Donahoe, P.; MacLaughlin, D.; Hardy, M.; Lee, M. Müllerian inhibiting substance inhibits testosterone synthesis in adult rats. J. Androl. 2001, 22, 750–758. [Google Scholar] [CrossRef] [PubMed]
- Silva, M.S.; Giacobini, P. New insights into anti-Müllerian hormone role in the hypothalamic–pituitary–gonadal axis and neuroendocrine development. Cell. Mol. Life Sci. 2021, 78, 1–16. [Google Scholar] [CrossRef]
- Place, N.J.; Hansen, B.S.; Cheraskin, J.-L.; Cudney, S.E.; Flanders, J.A.; Newmark, A.D.; Barry, B.; Scarlett, J.M. Measurement of serum anti-Müllerian hormone concentration in female dogs and cats before and after ovariohysterectomy. J. Vet. Diagn. Investig. 2011, 23, 524–527. [Google Scholar] [CrossRef]
- Themmen, A.P.; Kalra, B.; Visser, J.A.; Kumar, A.; Savjani, G.; de Gier, J.; Jaques, S. The use of anti-Müllerian hormone as diagnostic for gonadectomy status in dogs. Theriogenology 2016, 86, 1467–1474. [Google Scholar] [CrossRef]
- Axnér, E.; Holst, B.S. Concentrations of anti-Müllerian hormone in the domestic cat. Relation with spay or neuter status and serum estradiol. Theriogenology 2015, 83, 817–821. [Google Scholar] [CrossRef] [PubMed]
- Turna Yilmaz, Ö.; Toydemir, T.S.F.; Kirsan, I.; Gunay Ucmak, Z.; Caliskan Karacam, E. Anti-Müllerian hormone as a diagnostic tool for ovarian remnant syndrome in bitches. Vet. Res. Commun. 2015, 39, 159–162. [Google Scholar] [CrossRef] [PubMed]
- Place, N.J.; Cheraskin, J.-L.; Hansen, B.S. Evaluation of combined assessments of serum anti-Müllerian hormone and progesterone concentrations for the diagnosis of ovarian remnant syndrome in dogs. J. Am. Vet. Med. Assoc. 2019, 254, 1067–1072. [Google Scholar] [CrossRef]
- Flock, U.; Fischer, S.; Weeger, J.; Reese, S.; Walter, B. Anti-Müllerian hormone as a diagnostic tool to identify queens with ovarian remnant syndrome. J. Feline Med. Surg. 2022, 24, e168–e174. [Google Scholar] [CrossRef]
- Holst, B.S.; Dreimanis, U. Anti-Müllerian hormone: A potentially useful biomarker for the diagnosis of canine Sertoli cell tumours. BMC Vet. Res. 2015, 11, 166. [Google Scholar] [CrossRef]
- Walter, B.; Coelfen, A.; Jäger, K.; Reese, S.; Meyer-Lindenberg, A.; Aupperle-Lellbach, H. Anti-Muellerian hormone concentration in bitches with histopathologically diagnosed ovarian tumours and cysts. Reprod. Domest. Anim. 2018, 53, 784–792. [Google Scholar] [CrossRef]
- Hornakova, L.; Vrbovska, T.; Pavlak, M.; Valencakova-Agyagosova, A.; Halo, M.; Hajurka, J. The evaluation of blood concentrations of testosterone, 17β-oestradioland anti-Muellerian hormone in dogs with cryptorchidism and testicular tumours. Pol. J. Vet. Sci. 2017, 20, 677–685. [Google Scholar]
- Walter, B.; Flock, U.; Leykam, C.; Otzdorff, C.; Simmet, K.; Hecht, W.; Kempker, L.; Aupperle-Lellbach, H.; Reese, S. Serum anti-Müllerian hormone concentration as a diagnostic tool to identify testicular tissue in canine disorders of sexual development. Domest. Anim. Endocrinol. 2022, 78, 106654. [Google Scholar] [CrossRef]
- Balogh, O.; Somoskői, B.; Kollár, E.; Kowalewski, M.P.; Gram, A.; Reichler, I.M.; Klein, R.; Kawate, N.; Mester, L.; Walter, B. Anti-Müllerian hormone, testosterone, and insulin-like peptide 3 as biomarkers of Sertoli and Leydig cell function during deslorelin-induced testicular downregulation in the dog. Theriogenology 2021, 175, 100–110. [Google Scholar] [CrossRef]
- Nagashima, J.; Hansen, B.; Songsasen, N.; Travis, A.; Place, N. Anti-müllerian hormone in the domestic dog during the anestrus to oestrous transition. Reprod. Domest. Anim. 2016, 51, 158–164. [Google Scholar] [CrossRef]
- Flock, U.; Reese, S.; Otzdorff, C.; Klein, R.; Walter, B. Anti-Müllerian hormone concentrations in queens throughout the estrous cycle. Domest. Anim. Endocrinol. 2022, 81, 106749. [Google Scholar] [CrossRef]
- Lapuente, C.; Faya, M.; Blanco, P.; Grisolia-Romero, M.; Marchetti, C.; Gobello, C. Anti-Müllerian hormone in queens: Serum concentrations and total ovarian follicle population. Theriogenology 2023, 197, 111–115. [Google Scholar] [CrossRef]
- Hollinshead, F.; Walker, C.; Hanlon, D. Determination of the normal reference interval for anti-Müllerian hormone (AMH) in bitches and use of AMH as a potential predictor of litter size. Reprod. Domest. Anim. 2017, 52, 35–40. [Google Scholar] [CrossRef]
- Snoeck, F.; Sarrazin, S.; Wydooghe, E.; Van Soom, A. Age and anti-Müllerian hormone levels predict the success of in vitro maturation of cat oocytes. Reprod. Domest. Anim. 2017, 52, 98–102. [Google Scholar] [CrossRef]
- Ferré-Dolcet, L.; Ferro, S.; Contiero, B.; Andretta, F.; Cattai, A.; Fontaine, C.; Romagnoli, S. Resumption of ovarian activity following removal of a 4.7 mg deslorelin implant in queens. Reprod. Domest. Anim. 2022, 57, 3–9. [Google Scholar] [CrossRef]
- Hill, J.; Wilkinson, J.; Mallyon, J.; Anderson, S. Low sensitivity of a test for anti-Mullerian hormone to assess presence of ovaries in prepubertal bitches. Aust. Vet. J. 2018, 96, 356–359. [Google Scholar] [CrossRef]
- Karakas Alkan, K.; Ceylan, A.; Alkan, H.; Ozen, D.; Bayraktaroglu, A.G.; Kaymaz, M. Immunohistochemical and qPCR determination of the expression and serum level of anti-Müllerian hormone in pre-pubertal, intact and ovarian remnant syndrome detected bitches. Reprod. Domest. Anim. 2019, 54, 979–986. [Google Scholar] [CrossRef]
- Meyers-Wallen, V.; Palmer, V.; Maclaughlin, D.; Donahoe, P. Mullerian-inhibiting substance secretion is delayed in XX sex-reversed dog embryos. Mol. Reprod. Dev. 1994, 39, 1–7. [Google Scholar] [CrossRef]
- Banco, B.; Veronesi, M.; Giudice, C.; Rota, A.; Grieco, V. Immunohistochemical evaluation of the expression of anti-Müllerian hormone in mature, immature and neoplastic canine Sertoli cells. J. Comp. Pathol. 2012, 146, 18–23. [Google Scholar] [CrossRef]
- Ball, B.; Conley, A.; Grundy, S.; Sabeur, K.; Liu, I. Expression of anti-Müllerian hormone (AMH) in the equine testis. Theriogenology 2008, 69, 624–631. [Google Scholar] [CrossRef]
- Claes, A.; Ball, B.A.; Almeida, J.; Corbin, C.J.; Conley, A.J. Serum anti-Müllerian hormone concentrations in stallions: Developmental changes, seasonal variation, and differences between intact stallions, cryptorchid stallions, and geldings. Theriogenology 2013, 79, 1229–1235. [Google Scholar] [CrossRef]
- Grinspon, R.P.; Rey, R.A. Anti-müllerian hormone and sertoli cell function in paediatric male hypogonadism. Horm. Res. Paediatr. 2010, 73, 81–92. [Google Scholar] [CrossRef]
- Rey, R.; Lordereau-Richard, I.; Carel, J.C.; Barbet, P.; Cate, R.L.; Roger, M.; Chaussain, J.L.; Josso, N. Anti-müllerian hormone and testosterone serum levels are inversely during normal and precocious pubertal development. J. Clin. Endocrinol. Metab. 1993, 77, 1220–1226. [Google Scholar] [CrossRef] [PubMed]
- Pasqualini, T.; Chemes, H.; Rivarola, M. Testicular testosterone levels during puberty in cryptorchidism. Clin. Endocrinol. 1981, 15, 545–554. [Google Scholar] [CrossRef]
- Rey, R.; Lukas-Croisier, C.; Lasala, C.; Bedecarrás, P. AMH/MIS: What we know already about the gene, the protein and its regulation. Mol. Cell. Endocrinol. 2003, 211, 21–31. [Google Scholar] [CrossRef]
- Rota, A.; Cozzi, B.; Rey, R.; Ballarin, C. AMH plasma concentrations in bovine freemartins, a model of spontaneously occuring mammalian intersexes. Gen. Comp. Endocrinol. 2002, 129, 39–44. [Google Scholar] [CrossRef]
- Forest, M.G.; Sizonenko, P.C.; Cathiard, A.M.; Bertrand, J. Hypophyso-gonadal function in humans during the first year of life: I. Evidence for testicular activity in early infancy. J. Clin. Investig. 1974, 53, 819–828. [Google Scholar] [CrossRef]
- Donahoe, P.K.; Ito, Y.; Price, J.M.; Hendren, W.H., III. Müllerian Inhibiting Substance Activity in Bovine Fetal, Newborn and Prepubertal Testes1. Biol. Reprod. 1977, 16, 238–243. [Google Scholar] [CrossRef]
- Lee, M.M.; Donahoe, P.K. Mullerian Inhibiting Substance: A Gonadal Hormone with Multiple Functions*. Endocr. Rev. 1993, 14, 152–164. [Google Scholar] [CrossRef]
- Cazorla, O.; Seck, M.; Pisselet, C.; Perreau, C.; Saumande, J.; Fontaine, J.; de Reviers, M.; Hochereau-de Reviers, M.T. Anti-Müllerian hormone (AMH) secretion in prepubertal and adult rams. Reproduction 1998, 112, 259–266. [Google Scholar] [CrossRef]
- Fujisawa, M.; Yamasaki, T.; Okada, H.; Kamidono, S. The significance of anti-Müllerian hormone concentration in seminal plasma for spermatogenesis. Hum. Reprod. 2002, 17, 968–970. [Google Scholar] [CrossRef]
- Weenen, C.; Laven, J.S.E.; von Bergh, A.R.M.; Cranfield, M.; Groome, N.P.; Visser, J.A.; Kramer, P.; Fauser, B.C.J.M.; Themmen, A.P.N. Anti-Müllerian hormone expression pattern in the human ovary: Potential implications for initial and cyclic follicle recruitment. Mol. Hum. Reprod. 2004, 10, 77–83. [Google Scholar] [CrossRef] [PubMed]
- Lee, M.M.; Donahoe, P.K.; Hasegawa, T.; Silverman, B.; Crist, G.B.; Best, S.; Hasegawa, Y.; Noto, R.A.; Schoenfeld, D.; MacLaughlin, D.T. Mullerian inhibiting substance in humans: Normal levels from infancy to adulthood. J. Clin. Endocrinol. Metab. 1996, 81, 571–576. [Google Scholar] [CrossRef]
- Fong, I.; Valkenburg, O.; de Jong, F.H.; Visser, J.A.; Laven, J.S.E. The role of anti-Müllerian hormone in the classification of anovulatory infertility. Eur. J. Obstetrics Gynecol. Reprod. Biol. 2015, 186, 75–79. [Google Scholar] [CrossRef]
- Visser, J.A.; de Jong, F.H.; Laven, J.S.E.; Themmen, A.P.N. Anti-Müllerian hormone: A new marker for ovarian function. Reproduction 2006, 131, 1–9. [Google Scholar] [CrossRef]
- Bedaiwy, M.A.; Mahfouz, R.Z.; Kubaney, H.R.; Plautz, G.E.; Hurd, W.; Falcone, T. The role of anti-Müllerian hormone (AMH) in prepubertal gonadal reserve screening. Fertil. Steril. 2010, 94, S46. [Google Scholar] [CrossRef]
- El-Sheikh Ali, H.; Kitahara, G.; Takahashi, T.; Mido, S.; Sadawy, M.; Kobayashi, I.; Hemmi, K.; Osawa, T. Plasma anti-Müllerian hormone profile in heifers from birth through puberty and relationship with puberty onset. Biol. Reprod. 2017, 97, 153–161. [Google Scholar] [CrossRef]
- Claaßen, S.; Aurich, J.; Walter, I.; Gautier, C.; Aurich, C. Abundance of Anti-Muellerian hormone in cat ovaries and correlation of its plasma concentration with animal age, weight and stage of the estrous cycle. Theriogenology 2023, 212, 30–36. [Google Scholar] [CrossRef]
- La Marca, A.; Spada, E.; Grisendi, V.; Argento, C.; Papaleo, E.; Milani, S.; Volpe, A. Normal serum andi-Müllerian hormone levels in the general femlale Population and the relationship with reproductive history. Eur. J. Obstet. Gynecol. Reprod. Biol. 2012, 163, 180–184. [Google Scholar] [CrossRef]
- Claes, A.; Ball, B.A.; Scoggin, K.E.; Esteller-Vico, A.; Kalmar, J.J.; Conley, A.J.; Squires, E.L.; Troedsson, M.H.T. The interrelationship between anti-Müllerian hormone, ovarian follicular populations and age in mares. Equine Vet. J. 2015, 47, 537–541. [Google Scholar] [CrossRef]
- Scarlet, D.; Wulf, M.; Kuhl, J.; Köhne, M.; Ille, N.; Conley, A.J.; Aurich, C. Anti-Müllerian hormone profiling in prepubertal horses and its relationship with gonadal function. Theriogenology 2018, 117, 72–77. [Google Scholar] [CrossRef] [PubMed]
- Bergman, D.; Larsson, A.; Hansson-Hamlin, H.; Svensson, A.; Ström Holst, B. Prevalence of interfering antibodies in dogs and cats evaluated using a species-independent assay. Vet. Clin. Pathol. 2018, 47, 205–212. [Google Scholar] [CrossRef] [PubMed]
- Bergman, D.; Larsson, A.; Hansson-Hamlin, H.; Ström Holst, B. Investigation of interference from canine anti-mouse antibodies in hormone immunoassays. Vet. Clin. Pathol. 2019, 48, 59–69. [Google Scholar] [CrossRef] [PubMed]
- Lahoz, B.; Alabart, J.L.; Cocero, M.J.; Monniaux, D.; Echegoyen, E.; Sanchez, P.; Folch, J. Anti-Müllerian hormone concentration in sheep and its dependence of age and independence of BMP15 genotype: An endocrine predictor to select the best donors for embryo biotechnologies. Theriogenology 2014, 81, 347–354. [Google Scholar] [CrossRef] [PubMed]
- Hagen, C.P.; Mouritsen, A.; Mieritz, M.G.; Tinggaard, J.; Wohlfart-Veje, C.; Fallentin, E.; Brocks, V.; Sundberg, K.; Jensen, L.N.; Anderson, R.A.; et al. Circulating AMH Reflects Ovarian Morphology by Magnetic Resonance Imaging and 3D Ultrasound in 121 Healthy Girls. J. Clin. Endocrinol. Metab. 2015, 100, 880–890. [Google Scholar] [CrossRef] [PubMed]
- Rico, C.; Fabre, S.; Médigue, C.; Clemente, N.d.; Clément, F.; Bontoux, M.; Touzé, J.-L.; Dupont, M.; Briant, E.; Rémy, B.; et al. Anti-Müllerian Hormone Is an Endocrine Marker of Ovarian Gonadotropin-Responsive Follicles and Can Help to Predict Superovulatory Responses in the Cow1. Biol. Reprod. 2009, 80, 50–59. [Google Scholar] [CrossRef]
- Monniaux, D.; Baril, G.; Laine, A.-L.; Jarrier, P.; Poulin, N.; Cognié, J.; Fabre, S. Anti-Müllerian hormone as a predictive endocrine marker for embryo production in the goat. Reproduction 2011, 142, 845–854. [Google Scholar] [CrossRef] [PubMed]
Species | Gender | Age in Weeks and Size of Group | |||||
---|---|---|---|---|---|---|---|
Cats | Female | 2 to 6 8 animals | - | 6 to 12 8 animals | - | - | - |
Male | - | <8 8 animals | - | 8 to 16 8 animals | 16 to 24 8 animals | 24 to 48 8 animals | |
Dogs | Female | - | - | - | 8 to 16 8 animals | 16 to 24 8 animals | 24 to 48 8 animals |
Male | - | - | - | 8 to 16 8 animals | 16 to 24 8 animals | 24 to 48 8 animals |
Species | Gender | Age [Weeks] | AMH [ng/mL] | Testosterone [ng/mL] | ||||
---|---|---|---|---|---|---|---|---|
Median | Minimum | Maximum | Median | Minimum | Maximum | |||
Cats | Female | 2 to 6 | 0.4 | 0.12 | 1.22 | - | ||
6 to 12 | 20.71 | 0.87 | 22.96 | - | ||||
Male | <8 | 22.96 | 22.96 | 22.96 | - | |||
8 to 16 | 22.96 | 22.96 | 22.96 | - | ||||
16 to 24 | 22.96 | 22.96 | 22.96 | - | ||||
24 to 48 | 14.12 | 6.46 | 22.96 | 5.5 | <0.07 | 7.6 | ||
Dogs | Female | 8 to 16 | 0.01 | 0.01 | 0.01 | - | ||
16 to 24 | 0.035 | 0.01 | 0.1 | - | ||||
24 to 48 | 0.245 | 0.07 | 0.56 | - | ||||
Male | 8 to 16 | 22.96 | 22.96 | 22.96 | - | |||
16 to 24 | 22.96 | 22.96 | 22.96 | - | ||||
24 to 48 | 19.68 | 5.49 | 22.96 | 1.95 | 0.3 | 4.4 |
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Alexander, T.; Flock, U.; Klein, R.; Reese, S.; Meyer-Lindenberg, A.; Walter, B. Physiological Anti-Müllerian Hormone Concentrations in Male and Female Dogs and Cats before and around Puberty. Animals 2024, 14, 2561. https://doi.org/10.3390/ani14172561
Alexander T, Flock U, Klein R, Reese S, Meyer-Lindenberg A, Walter B. Physiological Anti-Müllerian Hormone Concentrations in Male and Female Dogs and Cats before and around Puberty. Animals. 2024; 14(17):2561. https://doi.org/10.3390/ani14172561
Chicago/Turabian StyleAlexander, Tanja, Ulrike Flock, Ruth Klein, Sven Reese, Andrea Meyer-Lindenberg, and Beate Walter. 2024. "Physiological Anti-Müllerian Hormone Concentrations in Male and Female Dogs and Cats before and around Puberty" Animals 14, no. 17: 2561. https://doi.org/10.3390/ani14172561
APA StyleAlexander, T., Flock, U., Klein, R., Reese, S., Meyer-Lindenberg, A., & Walter, B. (2024). Physiological Anti-Müllerian Hormone Concentrations in Male and Female Dogs and Cats before and around Puberty. Animals, 14(17), 2561. https://doi.org/10.3390/ani14172561