Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Ovarian and uterine changes during the oestrous cycle in female dogs

Lena Lindh https://orcid.org/0000-0001-8381-789X A * , Mariusz P. Kowalewski B , Anne-Rose Günzel-Apel C , Sandra Goericke-Pesch C , Vesa Myllys D , Gerhard Schuler E , Merja Dahlbom A , Heli Lindeberg F and Olli A. T. Peltoniemi A
+ Author Affiliations
- Author Affiliations

A Department of Production Animal Medicine, University of Helsinki, Saarentaus FI-04920, Finland.

B University of Zürich, Institute of Veterinary Anatomy, Vetsuisse Faculty, Winterthurerstrasse 260, 8057 Zurich, Switzerland.

C Reproductive Unit – Clinic for Small Animals, University of Veterinary Medicine Hannover, Hannover, Germany.

D Vetcare Oy, Mäntsälä, Finland.

E Veterinary Clinic for Obstetrics, Gynecology and Andrology, Justus Liebig University, Giessen, Germany.

F Natural Resources Institute Finland (Luke), Production Systems, Halolantie 31 A, Maaninka FI-71750, Finland.

* Correspondence to: lena.lindh@helsinki.fi

Handling Editor: Graeme Martin

Reproduction, Fertility and Development 35(4) 321-337 https://doi.org/10.1071/RD22177
Published online: 23 December 2022

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

Abstract

Context: An accurate staging of sexual cycle is essential for the optimum timing of medical interventions.

Aims: Here, an updated insight into clinical, endocrinological and vagino-cytological parameters, and their correlation with histomorphology of ovarian and uterine tissue samples is presented.

Methods: Samples from 39 dogs were collected at various stages of the oestrous cycle: pro-oestrus (n = 8), oestrus (n = 12), dioestrus (n = 9) (luteal phase) and anoestrus (n = 10), according to clinical observations. Final allocation of samples was done after histomorphological evaluation of all tissues. Peripheral oestradiol-17ß (E2) and progesterone (P4) concentrations were measured, P4 by both chemiluminescent immunoassay (CLIA) and radioimmunoassay (RIA).

Key results: Differences were observed between determination of the stage of the oestrous cycle, either by clinical, endocrinological or histomorphological evaluation. Individuals considered to be in clinical and endocrinological oestrus, had entered the luteal phase according to histomorphology. P4 concentrations measured by two different assays differed, underlying the importance to understand that absolute P4 concentrations may deviate depending on the used assay. Comparison of E2 and P4 concentrations is suggested to be useful when defining the transition from early follicular phase to the time of ovulation.

Conclusions and implications: Based on parallel histomorphological observations, combined with clinical and endocrinological findings on the same individuals, the present study emphasises that an accurate classification of the stage of the cycle in female dogs based solely on clinical and endocrinological assessments can be difficult. The histomorphological findings presented herein provide new insights into the transitional phases between the different stages of the oestrous cycle in the dog.

Keywords: canine, determination of heat, endocrine changes, endometrial cycle, female dog, histomorphological changes, oestrous cycle, ovarian cycle.


References

Arlt, S (2018). Canine ovulation timing: a survey on methodology and an assessment on reliability of vaginal cytology. Reproduction in Domestic Animals 53, 53–62.
Canine ovulation timing: a survey on methodology and an assessment on reliability of vaginal cytology.Crossref | GoogleScholarGoogle Scholar |

Bartel, C, Tichy, A, and Walter, I (2014). Characterization of foamy epithelial surface cells in the canine endometrium. Anatomia, Histologia, Embryologia 43, 165–181.
Characterization of foamy epithelial surface cells in the canine endometrium.Crossref | GoogleScholarGoogle Scholar |

Concannon, PW (2011). Reproductive cycles of the domestic bitch. Animal Reproduction Science 124, 200–210.
Reproductive cycles of the domestic bitch.Crossref | GoogleScholarGoogle Scholar |

Concannon, PW, Hansel, W, and Visek, WJ (1975). The ovarian cycle of the bitch: plasma estrogen, LH and progesterone. Biology of Reproduction 13, 112–121.
The ovarian cycle of the bitch: plasma estrogen, LH and progesterone.Crossref | GoogleScholarGoogle Scholar |

Concannon, PW, McCann, JP, and Temple, M (1989). Biology and endocrinology of ovulation, pregnancy and parturition in the dog. Journal of Reproduction and Fertility. Supplement 39, 3–25.

Davidson, AP, and Baker, TW (2009). Reproductive ultrasound of the bitch and queen. Topics in Companion Animal Medicine 24, 55–63.
Reproductive ultrasound of the bitch and queen.Crossref | GoogleScholarGoogle Scholar |

Feldman EC, Nelson RW (2004) Ovarian cycle and vaginal cytology. In ‘Canine and feline endocrinology and reproduction’. (Eds EC Feldman, RW Nelson) pp.752–774. (Saunders)

Galabova, G, Egerbacher, M, Aurich, JE, Leitner, M, and Walter, I (2003). Morphological changes of the endometrial epithelium in the bitch during metoestrus and anoestrus. Reproduction in Domestic Animals 38, 415–420.
Morphological changes of the endometrial epithelium in the bitch during metoestrus and anoestrus.Crossref | GoogleScholarGoogle Scholar |

Gill, JL, and Hafs, HD (1971). Analysis of repeated measurements of animals. Journal of Animal Science 33, 331–336.
Analysis of repeated measurements of animals.Crossref | GoogleScholarGoogle Scholar |

Gloria, A, Contri, A, Carluccio, A, and Robbe, D (2018). Blood periovulatory progesterone quantification using different techniques in the dog. Animal Reproduction Science 192, 179–184.
Blood periovulatory progesterone quantification using different techniques in the dog.Crossref | GoogleScholarGoogle Scholar |

Hoffmann, B, Kyrein, HJ, and Ender, ML (1973). An efficient procedure for the determination of progesterone by radioimmunoassay applied to bovine peripheral plasma. Hormone Research 4, 302–310.
An efficient procedure for the determination of progesterone by radioimmunoassay applied to bovine peripheral plasma.Crossref | GoogleScholarGoogle Scholar |

Hoffmann, B, Höveler, R, Hasan, SH, and Failing, K (1992). Ovarian and pituitary function in dogs after hysterectomy. Journal of Reproduction and Fertility 96, 837–845.
Ovarian and pituitary function in dogs after hysterectomy.Crossref | GoogleScholarGoogle Scholar |

Hoffmann, B, Höveler, R, Nohr, B, and Hasan, SH (1994). Investigations on hormonal changes around parturition in the dog and the occurrence of pregnancy-specific non conjugated oestrogens. Experimental and Clinical Endocrinology & Diabetes 102, 185–189.
Investigations on hormonal changes around parturition in the dog and the occurrence of pregnancy-specific non conjugated oestrogens.Crossref | GoogleScholarGoogle Scholar |

Hoffmann, B, Büsges, F, Engel, E, Kowalewski, MP, and Papa, P (2004). Regulation of corpus luteum-function in the bitch. Reproduction in Domestic Animals 39, 232–240.
Regulation of corpus luteum-function in the bitch.Crossref | GoogleScholarGoogle Scholar |

Hollinshead, FK, and Hanlon, DW (2019). Normal progesterone profiles during estrus in the bitch: a prospective analysis of 1420 estrous cycles. Theriogenology 125, 37–42.
Normal progesterone profiles during estrus in the bitch: a prospective analysis of 1420 estrous cycles.Crossref | GoogleScholarGoogle Scholar |

Hori, T, Tsutsui, T, Amano, Y, and Concannon, PW (2012). Ovulation day after onset of vulval bleeding in a beagle colony. Reproduction in Domestic Animals 47, 47–51.
Ovulation day after onset of vulval bleeding in a beagle colony.Crossref | GoogleScholarGoogle Scholar |

Jöchle, W, and Andersen, AC (1977). The estrous cycle in the dog: a review. Theriogenology 7, 113–140.
The estrous cycle in the dog: a review.Crossref | GoogleScholarGoogle Scholar |

Jurczak, A, Janowski, T, Zdunczyk, S, Failing, K, Schuler, G, and Hoffmann, B (2020). Attempts to downregulate ovarian function in the bitch by applying a GnRH agonist implant in combination with a 3ß-hydroxysteroid-dehydrogenase blocker; a pilot study. Theriogenology 145, 176–180.
Attempts to downregulate ovarian function in the bitch by applying a GnRH agonist implant in combination with a 3ß-hydroxysteroid-dehydrogenase blocker; a pilot study.Crossref | GoogleScholarGoogle Scholar |

Klein, R, Schams, D, Failing, K, and Hoffmann, B (2003). Investigations on the re-establishment of the positive feedback of oestradiol during anoestrus in the bitch. Reproduction in Domestic Animals 38, 13–20.
Investigations on the re-establishment of the positive feedback of oestradiol during anoestrus in the bitch.Crossref | GoogleScholarGoogle Scholar |

Kowalewski, MP (2014). Luteal regression vs. prepartum luteolysis: regulatory mechanisms governing canine corpus luteum function. Reproductive Biology 14, 89–102.
Luteal regression vs. prepartum luteolysis: regulatory mechanisms governing canine corpus luteum function.Crossref | GoogleScholarGoogle Scholar |

Kowalewski MP (2017) Regulation of corpus luteum function in the domestic dog (Canis familiaris) and comparative aspects of luteal function in the domestic cat (Felis catus). In ‘The life cycle of the corpus luteum’. (Ed. R Meidan) pp. 133–157. (Springer International Publishing)

Kowalewski MP (2018) Selected comparative aspects of canine female reproductive physiology. In ‘Encyclopedia of reproduction’. (Ed. MK Skinner) pp. 682–691. (Elsevier) https://doi.org/10.1016/B978-0-12-809633-8.20527-X

Kowalewski, MP, Beceriklisoy, HB, Pfarrer, C, Aslan, S, Kindahl, H, Kücükaslan, I, and Hoffmann, B (2010). Canine placenta: a source of prepartal prostaglandins during normal and antiprogestin-induced parturition. Reproduction 139, 655–664.
Canine placenta: a source of prepartal prostaglandins during normal and antiprogestin-induced parturition.Crossref | GoogleScholarGoogle Scholar |

Kowalewski, MP, Ihle, S, Siemieniuch, MJ, Gram, A, Boos, A, Zduńczyk, S, Fingerhut, J, Hoffmann, B, Schuler, G, Jurczak, A, Domosławska, A, and Janowski, T (2015). Formation of the early canine CL and the role of prostaglandin E2 (PGE2) in regulation of its function: an in vivo approach. Theriogenology 83, 1038–1047.
Formation of the early canine CL and the role of prostaglandin E2 (PGE2) in regulation of its function: an in vivo approach.Crossref | GoogleScholarGoogle Scholar |

Kustritz, MVR (2006). Collection of tissue and culture samples from the canine reproductive tract. Theriogenology 66, 567–574.
Collection of tissue and culture samples from the canine reproductive tract.Crossref | GoogleScholarGoogle Scholar |

Kutzler, MA, Mohammed, HO, Lamb, SV, and Meyers-Wallen, VN (2003). Accuracy of canine parturition date prediction from the initial rise in preovulatory progesterone concentration. Theriogenology 60, 1187–1196.
Accuracy of canine parturition date prediction from the initial rise in preovulatory progesterone concentration.Crossref | GoogleScholarGoogle Scholar |

Lévy, X (2016). Videovaginoscopy of the canine vagina. Reproduction in Domestic Animals 51, 31–36.
Videovaginoscopy of the canine vagina.Crossref | GoogleScholarGoogle Scholar |

McLean, AC, Valenzuela, N, Fai, S, and Bennett, SAL (2012). Performing vaginal lavage, crystal violet staining, and vaginal cytological evaluation for mouse estrous cycle staging identification. Journal of Visualized Experiments , e4389.
Performing vaginal lavage, crystal violet staining, and vaginal cytological evaluation for mouse estrous cycle staging identification.Crossref | GoogleScholarGoogle Scholar |

Moxon, R, Copley, D, and England, GCW (2010). Quality assurance of canine vaginal cytology: a preliminary study. Theriogenology 74, 479–485.
Quality assurance of canine vaginal cytology: a preliminary study.Crossref | GoogleScholarGoogle Scholar |

Nöthling, JO, and De Cramer, KGM (2019). Comparison of progesterone assay by chemiluminescence or radioimmunoassay for clinical decision-making in canine reproduction. Journal of the South African Veterinary Association 90, a1730.
Comparison of progesterone assay by chemiluminescence or radioimmunoassay for clinical decision-making in canine reproduction.Crossref | GoogleScholarGoogle Scholar |

Onclin, K, Murphy, B, and Verstegen, JP (2002). Comparisons of estradiol, LH and FSH patterns in pregnant and nonpregnant beagle bitches. Theriogenology 57, 1957–1972.
Comparisons of estradiol, LH and FSH patterns in pregnant and nonpregnant beagle bitches.Crossref | GoogleScholarGoogle Scholar |

Reckers, F, Klopfleisch, R, Belik, V, and Arlt, S (2022). Canine vaginal cytology: a revised definition of exfoliated vaginal cells. Frontiers in Veterinary Science 9, 834031.
Canine vaginal cytology: a revised definition of exfoliated vaginal cells.Crossref | GoogleScholarGoogle Scholar |

Rehm, S, Stanislaus, DJ, and Williams, AM (2007). Estrous cycle-dependent histology and review of sex steroid receptor expression in dog reproductive tissues and mammary gland and associated hormone levels. Birth Defects Research Part B. Developmental and Reproductive Toxicology 80, 233–245.
Estrous cycle-dependent histology and review of sex steroid receptor expression in dog reproductive tissues and mammary gland and associated hormone levels.Crossref | GoogleScholarGoogle Scholar |

Reynaud, K, Saint-Dizier, M, Tahir, MZ, Havard, T, Harichaux, G, Labas, V, Thoumire, S, Fontbonne, A, Grimard, B, and Chastant-Maillard, S (2015). Progesterone plays a critical role in canine oocyte maturation and fertilization. Biology of Reproduction 93, 1–9.
Progesterone plays a critical role in canine oocyte maturation and fertilization.Crossref | GoogleScholarGoogle Scholar |

Schmicke, M, Urhausen, C, Wolf, K, Schmidt, S, and Günzel-Apel, A-R (2016). Evaluation of the blood progesterone concentration in the bitch measured by chemiluminescence immunoassay at the day of ovulation. Tierarztl Prax Ausg K Kleintiere Heimtiere 44, 317–322.
Evaluation of the blood progesterone concentration in the bitch measured by chemiluminescence immunoassay at the day of ovulation.Crossref | GoogleScholarGoogle Scholar |

Sonnack M (2009) Investigations of the formation, regression and functionality of the Corpus luteum in the non pregnant bitch; morphological and biochemical aspects. PhD Thesis, Justus-Liebig-University, Giessen, Germany.