Dynamics of progesterone, estradiol, cortisol, triiodothyronine and indicators of adaptive immunity concentrations in female dogs during estrus

Authors

DOI:

https://doi.org/10.29329/JofBS.2023.501.02

Keywords:

Estrus, Phagocytic activity of neutrophils, Progesterone, Estradiol, Cortisol

Abstract

In different periods of postnatal ontogenesis in dogs, as well as in other animals, there are critical physiological periods, the adequacy of which depends on immunoendocrine homeostasis. The estrus in bitches is a critical period because it lasts longer than in other mammals and has specific endocrine and immune changes in the body. In this study authors demonstrated the dynamics of changes in hormone content and indicators of adaptive cellular immunity in bitches during the estrus. Determination of these indicators does not require expensive laboratory equipment and is available in veterinary practice. Taking into account the fact that estrus in dogs lasts long enough, it is not clear enough what indicators and in what terms should be determined for predicting possible dysfunctions of the reproductive system and, as a result, premature impossibility of reproduction in bitches. The peak concentration of progesterone occurs on the 20th day of estrus, the reaction of the immune system, which is manifested by the maximum decrease in the phagocytic activity of neutrophils, should be noted. An increase in the concentration of estradiol on the 5th day of estrus, in contrast to progesterone, had the opposite effect on phagocytic activity of neutrophils, namely, the ability of neutrophils to phagocytosis increased. Further, we conducted clinical animals’ observations for three months after estrus for the possibility of inflammatory processes in the reproductive system development. According to the obtained indicators, no complications were found.

References

Bartoskova, A., Ondrackova, P., Leva, L., Vitasek, R., Novotny, R., Janosovska, M., & Faldyna, M. (2014). The Effects of in Vitro Exposure to Progesterone and Estradiol-17β on the Activity of Canine Neutrophils. Veterinarni Medicina, 59(4), 202-209. https://doi.org/10.17221/7481-VETMED

Bukovsky, A., Indrapichate, K., Fujiwara, H., Cekanova, M., Ayala, M. E., Dominguez, R., Caudle, M. R., Wimalsena, J., Elder, R. F., Copas, P., Foster, J. S., Fernando, R. I., Henley, D. C., & Upadhyaya, N. B. (2003). Multiple Luteinizing Hormone Receptor (LHR) Protein Variants, Interspecies Reactivity of Anti-LHR mAb Clone 3B5, Subcellular Localization of LHR in Human Placenta, Pelvic Floor and Brain, and Possible Role for LHR in the Development of Abnormal Pregnancy, Pelvic Floor Disorders and Alzheimer's Disease. Reproductive Biology and Endocrinology, 1, 46. https://doi.org/10.1186/1477-7827-1-46

Bulmer, J., Longfellow, M., & Ritson, A. (1991). Leukocytes and Resident Blood Cells in Endometrium. Annals of the New York Academy of Sciences, 622(1), 57-68. https://doi.org/10.1111/j.1749-6632.1991.tb37850.x

Chastain C. B. (1990). Canine Pseudohypothyroidism and Covert Hypothyroidism. Problems in Veterinary Medicine, 2(4), 693-716.

Concannon P. W. (2009). Endocrinologic Control of Normal Canine Ovarian Function. Reproduction in Domestic Animals, 44(S2), 3-15. https://doi.org/10.1111/j.1439-0531.2009.01414.x

Concannon, P. W., Castracane, V. D., Temple, M., & Montanez, A. (2009). Endocrine Control of Ovarian Function in Dogs and Other Carnivores. Animal Reproduction, 6(1), 172-193.

Corder-Ramos, N. L. B., Flatland, B., Fry, M. M., Sun, X., Fecteau, K., & Giori, L. (2019). Cortisol, Progesterone, 17α-hydroxyprogesterone, and TSH Responses in Dogs Injected with Low-dose Lipopolysaccharide. PeerJ, 7, e7468. https://doi.org/10.7717/peerj.7468

Daminet, S., & Ferguson, D. C. (2003). Influence of Drugs on Thyroid Function in Dogs. Journal of Veterinary Internal Medicine, 17(4), 463-472. https://doi.org/10.1111/j.1939-1676.2003.tb02467.x

Detillion, C. E., Craft, T. K., Glasper, E. R., Prendergast, B. J., & DeVries, A. C. (2004). Social Facilitation of Wound Healing. Psychoneuroendocrinology, 29(8), 1004-1011. https://doi.org/10.1016/j.psyneuen.2003.10.003

Dhaliwal, G. K., England, G. C., & Noakes, D. E. (1999). The Influence of Exogenous Steroid Hormones on Steroid Receptors, Uterine Histological Structure and the Bacterial Flora of the Normal Bitch. Animal Reproduction Science, 56(3-4), 259-277. https://doi.org/10.1016/s0378-4320(99)00042-1

Directive (2010). Directive (EU) 2010/63 of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32010L0063

Faldyna, M., Laznicka, A., & Toman, M. (2001). Immunosuppression in Bitches with Pyometra. Journal of Small Animal Practice, 42(1), 5-10. https://doi.org/10.1111/j.1748-5827.2001.tb01976.x

Farstad, W., Mondain-Monval, M., Hyttel, P., Smith, A. J., & Markeng, D. (1989). Periovulatory Endocrinology and Oocyte Maturation in Unmated Mature Blue Fox Vixens (Alopex lagopus). Acta Veterinaria Scandinavica, 30(3), 313-319. https://doi.org/10.1186/BF03548037

Garcia, M. R., Patel, M. V., Shen, Z., Fahey, J. V., Biswas, N., Mestecky, J., & Wira, C. R. (2015). Mucosal Immunity in the Human Female Reproductive Tract. Mucosal Immunology, 2, 2097-2124. https://doi.org/10.1016/B978-0-12-415847-4.00108-7

Glaser, R., & Kiecolt-Glaser, J. K. (2005). Stress-induced Immune Dysfunction: Implications for Health. Nature Reviews Immunology, 5(3), 243-251. https://doi.org/10.1038/nri1571

Groppetti, D., Aralla, M., Bronzo, V., Bosi, G., Pecile, A., & Arrighi, S. (2015). Periovulatory Time in the Bitch: What's New to Know?: Comparison between Ovarian Histology and Clinical Features. Animal Reproduction Science, 152, 108-116. https://doi.org/10.1016/j.anireprosci.2014.11.008

Hall, O. J., & Klein, S. L. (2017). Progesterone-based Compounds Affect Immune Responses and Susceptibility to Infections at Diverse Mucosal Sites. Mucosal Immunology, 10(5), 1097-1107. https://doi.org/10.1038/mi.2017.35

Hostetter S. J. (2012). Neutrophil Function in Small Animals. Veterinary Clinics: Small Animal Practice, 42(1), 157-171. https://doi.org/10.1016/j.cvsm.2011.09.010

Jurczak, A., & Janowski, T. (2018). Arterial Ovarian Blood Flow in the Periovulatory Period of GnRH-Induced and Spontaneous Estrous Cycles of Bitches. Theriogenology, 119, 131-136. https://doi.org/10.1016/j.theriogenology.2018.06.014

Kazmirchuk, V. I., Kovalchuk, L. V., & Maltsiv, D .V. (2012). Klinichna Imunolohiia ta Alerholohiia z Vikovymy Osoblyvostiamy. Medytsyna, 521. (in Ukrainian)

Kemeny, M. E., & Schedlowski, M. (2007). Understanding the Interaction between Psychosocial Stress and Immune-related Diseases: A Stepwise Progression. Brain, Behavior, and Immunity, 21(8), 1009-1018. https://doi.org/10.1016/j.bbi.2007.07.010

Kutzler, M. A., Mohammed, H. O., Lamb, S. V., & Meyers-Wallen, V. N. (2003). Accuracy of Canine Parturition Date Prediction from the Initial Rise in Preovulatory Progesterone Concentration. Theriogenology, 60(6), 1187-1196. https://doi.org/10.1016/s0093-691x(03)00109-2

Ladyman S. R. (2008). Leptin Resistance During Pregnancy in the Rat. Journal of Neuroendocrinology, 20(2), 269-277. https://doi.org/10.1111/j.1365-2826.2007.01628.x

Law of Ukraine "On the Protection of Animals from Cruelty Treatment" № 5456-VI (2012). https://zakon.rada.gov.ua/laws/show/3447-15#Text

Lövebrant, J. (2013). Surgical Stress Response in Dogs Diagnosed with Pyometra Undergoing Ovariohysterectomy. Second Cycle, A2E. Uppsala: SLU, Dept. of Clinical Sciences. Retrieved January 12, 2023 from https://stud.epsilon.slu.se/5815/

Lovick, T. A., & Zangrossi Jr, H. (2021). Effect of Estrous Cycle on Behavior of Females in Rodent Tests of Anxiety. Frontiers in Psychiatry, 12, 711065. https://doi.org/10.3389/fpsyt.2021.711065

Markle, J. G., & Fish, E. N. (2014). SeXX Matters in Immunity. Trends in Immunology, 35(3), 97-104. https://doi.org/10.1016/j.it.2013.10.006

Menchetti, L., Andoni, E., Barbato, O., Canali, C., Quattrone, A., Vigo, D., Codini, M., Curone, G., & Brecchia, G. (2020). Energy Homeostasis in Rabbit Does During Pregnancy and Pseudopregnancy. Animal Reproduction Science, 218, 106505. https://doi.org/10.1016/j.anireprosci.2020.106505

Mold, J., & McCune, J. (2012) Immunological Tolerance During Fetal Development: From Mouse to Man. Advances in Immunology, 115, 73-111. https://doi.org/10.1016/B978-0-12-394299-9.00003-5

Nagashima, J. B., & Songsasen, N. (2021). Canid Reproductive Biology: Norm and Unique Aspects in Strategies and Mechanisms. Animals, 11(3), 653. https://doi.org/10.3390/ani11030653

Oakley, A. E., Breen, K. M., Clarke, I. J., Karsch, F. J., Wagenmaker, E. R., & Tilbrook, A. J. (2009). Cortisol Reduces Gonadotropin-releasing Hormone Pulse Frequency in Follicular Phase Ewes: Influence of Ovarian Steroids. Endocrinology, 150(1), 341-349. https://doi.org/10.1210/en.2008-0587

Offner, H., & Polanczyk, M. (2006). A Potential Role for Estrogen in Experimental Autoimmune Encephalomyelitis and Multiple Sclerosis. Annals of the New York Academy of Sciences, 1089, 343-372. https://doi.org/10.1196/annals.1386.021

Onclin, K., Murphy, B., & Verstegen, J. P. (2002). Comparisons of Estradiol, LH and FSH Patterns in Pregnant and Nonpregnant Beagle Bitches. Theriogenology, 57(8), 1957-1972. https://doi.org/10.1016/s0093-691x(02)00644-1

Polanczyk, M. J., Carson, B. D., Subramanian, S., Afentoulis, M., Vandenbark, A. A., Ziegler, S. F., & Offner, H. (2004). Cutting Edge: Estrogen Drives Expansion of the CD4+CD25+ Regulatory T Cell Compartment. Journal of Immunology, 173(4), 2227-2230. https://doi.org/10.4049/jimmunol.173.4.2227

Polanczyk, M., Zamora, A., Subramanian, S., Matejuk, A., Hess, D. L., Blankenhorn, E. P., Teuscher, C., Vandenbark, A. A., & Offner, H. (2003). The Protective Effect of 17β-Estradiol on Experimental Autoimmune Encephalomyelitis is Mediated through Estrogen Receptor-alpha. The American Journal of Pathology, 163(4), 1599-1605. https://doi.org/10.1016/s0002-9440(10)63516-x

Risvanli, A., Ocal, H., & Kalkan, C. (2016). Abnormalities in the sexual cycle of bitches. In H. A. E. Kaoud (Ed.), Canine Medicine (pp. 127-138). IntechOpen. https://doi.org/10.5772/64648

Robertson, S.A. (2000) Control of the Immunological Environment of the Uterus. Reviews of Reproduction, 5, 164–74. https://doi.org/10.1530/revreprod/5.3.164

Salem M. L. (2004). Estrogen, a Double-edged Sword: Modulation of TH1- and TH2-mediated Inflammations by Differential Regulation of TH1/TH2 Cytokine Production. Current Drug Targets-Inflammation & Allergy, 3(1), 97-104. https://doi.org/10.2174/1568010043483944

Salvetti, N. R., Panzani, C. G., Gimeno, E. J., Neme, L. G., Alfaro, N. S., & Ortega, H. H. (2009). An Imbalance between Apoptosis and Proliferation Contributes to Follicular Persistence in Polycystic Ovaries in Rats. Reproductive Biology and Endocrinology, 7, 68. https://doi.org/10.1186/1477-7827-7-68

Schlafer, D. H., & Foster, R. A. (2016). Female Genital System. Jubb, Kennedy & Palmer's Pathology of Domestic Animals, 3, 358-464.e1. https://doi.org/10.1016/B978-0-7020-5319-1.00015-3

Schumacher, A., Costa, S. D., & Zenclussen, A. C. (2014). Endocrine Factors Modulating Immune Responses in Pregnancy. Frontiers in Immunology, 5, 196. https://doi.org/10.3389/fimmu.2014.00196

Silva, J. F., Ocarino, N. M., & Serakides, R. (2018). Thyroid Hormones and Female Reproduction. Biology of Reproduction, 99(5), 907-921. https://doi.org/10.1093/biolre/ioy115

Steckler, D., Nöthling, J. O., & Harper, C. (2013). Prediction of the Optimal Time for Insemination using Frozen-thawed Semen in a Multi-sire Insemination Trial in Bitches. Animal Reproduction Science, 142(3-4), 191-197. https://doi.org/10.1016/j.anireprosci.2013.09.013

Stockham, S.L. & Scott, M.A. (2008) Fundamentals of Veterinary Clinical Pathology (2nd ed.). Blackwell.

Sugiura, K., Nishikawa, M., Ishiguro, K., Tajima, T., Inaba, M., Torii, R., Hatoya, S., Wijewardana, V., Kumagai, D., Tamada, H., Sawada, T., Ikehara, S., & Inaba, T. (2004). Effect of Ovarian Hormones on Periodical Changes in Immune Resistance associated with Estrous Cycle in the Beagle Bitch. Immunobiology, 209(8), 619-627. https://doi.org/10.1016/j.imbio.2004.09.003

Tavares Pereira, M., Nowaczyk, R., Payan-Carreira, R., Miranda, S., Aslan, S., Kaya, D., & Kowalewski, M. P. (2021). Selected Uterine Immune Events Associated With the Establishment of Pregnancy in the Dog. Frontiers in Veterinary Science, 7, 625921. https://doi.org/10.3389/fvets.2020.625921

Thomassen, R., Sanson, G., Krogenaes, A., Fougner, J. A., Berg, K. A., & Farstad, W. (2006). Artificial Insemination with Frozen Semen in Dogs: A Retrospective Study of 10 Years using a Non-surgical Approach. Theriogenology, 66(6-7), 1645-1650. https://doi.org/10.1016/j.theriogenology.2006.01.022

Thuróczy, J., Müller, L., Kollár, E., & Balogh, L. (2016). Thyroxin and Progesterone Concentrations in Pregnant, Nonpregnant Bitches, and Bitches during Abortion. Theriogenology, 85(6), 1186-1191. https://doi.org/10.1016/j.theriogenology.2015.11.035

Tonello, A., & Poli, G. (2007). Tubal Ectopic Pregnancy: Macrophages under the Microscope. Human Reproduction, 22(10), 2577-2584. https://doi.org/10.1093/humrep/dem246

Turner, M., Healey, G. & Sheldon, I. (2012). Immunity and Inflammation in the Uterus. Reproduction in Domestic Animals, 47, 402-409. https://doi.org/10.1111/j.1439-0531.2012.02104.x

Vitalo, A., Fricchione, J., Casali, M., Berdichevsky, Y., Hoge, E. A., Rauch, S. L., Berthiaume, F., Yarmush, M. L., Benson, H., Fricchione, G. L., & Levine, J. B. (2009). Nest Making and Oxytocin Comparably Promote Wound Healing in Isolation Reared Rats. PloS One, 4(5), e5523. https://doi.org/10.1371/journal.pone.0005523

Vlizlo, V. V., Fedoruk, R. S., & Ratych I. B. (2012). Laboratory research methods in biology, animal husbandry and veterinary medicine: A handbook. Lviv: Spolom. (in Ukrainian)

Wakim, A. N., Polizotto, S. L., Buffo, M. J., Marrero, M. A., & Burholt, D. R. (1993). Thyroid Hormones in Human Follicular Fluid and Thyroid Hormone Receptors in Human Granulosa Cells. Fertility and Sterility, 59(6), 1187-1190. https://doi.org/10.1016/s0015-0282(16)55974-3

WHO Chronicle (1985) International Guiding Principles for Biomedical Research Involving Animals, 39, 3-9. https://iris.paho.org/handle/10665.2/26848?show=full

Wildt, D. E., Chakraborty, P. K., Panko, W. B., & Seager, S. W. (1978). Relationship of Reproductive Behavior, Serum Luteinizing Hormone and Time of Ovulation in the Bitch. Biology of Reproduction, 18(4), 561-570. https://doi.org/10.1095/biolreprod18.4.561

Zeng, M. Y., Miralda, I., Armstrong, C. L., Uriarte, S. M., & Bagaitkar, J. (2019). The Roles of NADPH Oxidase in Modulating Neutrophil Effector Responses. Molecular Oral Microbiology, 34(2), 27-38. https://doi.org/10.1111/omi.12252

Zhang, S. S., Carrillo, A. J., & Darling, D. S. (1997). Expression of Multiple Thyroid Hormone receptor mRNAs in Human Oocytes, Cumulus Cells, and Granulosa Cells. Molecular Human Reproduction, 3(7), 555-562. https://doi.org/10.1093/molehr/3.7.555

Zhang, Y. M., Rao, C.hV., & Lei, Z. M. (2003). Macrophages in Human Reproductive Tissues Contain Luteinizing Hormone/Chorionic Gonadotropin Receptors. American Journal of Reproductive Immunology, 49(2), 93-100. https://doi.org/10.1034/j.1600-0897.2003.00013.x

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30-06-2023

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