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Aetiology and Pathogenesis of Cystic Ovarian Follicles in Dairy Cattle: a Review Tom Vanholder, Geert Opsomer, Aart De Kruif

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Aetiology and Pathogenesis of Cystic Ovarian Follicles in Dairy Cattle: a Review Tom Vanholder, Geert Opsomer, Aart De Kruif Aetiology and pathogenesis of cystic ovarian follicles in dairy cattle: a review Tom Vanholder, Geert Opsomer, Aart de Kruif To cite this version: Tom Vanholder, Geert Opsomer, Aart de Kruif. Aetiology and pathogenesis of cystic ovarian follicles in dairy cattle: a review. Reproduction Nutrition Development, EDP Sciences, 2006, 46 (2), pp.105-119. 10.1051/rnd:2006003. hal-00900607 HAL Id: hal-00900607 https://hal.archives-ouvertes.fr/hal-00900607 Submitted on 1 Jan 2006 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Reprod. Nutr. Dev. 46 (2006) 105–119 105 © INRA, EDP Sciences, 2006 DOI: 10.1051/rnd:2006003 Review Aetiology and pathogenesis of cystic ovarian follicles in dairy cattle: a review Tom VANHOLDER, Geert OPSOMER*, Aart DE KRUIF Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium (Received 23 August 2005; accepted 5 December 2005) Abstract – Cystic ovarian follicles (COF) are an important ovarian dysfunction and a major cause of reproductive failure in dairy cattle. Due to the complexity of the disorder and the heterogeneity of the clinical signs, a clear definition is lacking. A follicle becomes cystic when it fails to ovulate and persists on the ovary. Despite an abundance of literature on the subject, the exact pathogenesis of COF is unclear. It is generally accepted that disruption of the hypothalamo-pituitary-gonadal axis, by endogenous and/or exogenous factors, causes cyst formation. Secretion of GnRH/LH from the hypothalamus-pituitary is aberrant, which is attributed to insensitivity of the hypothalamus-pituitary to the positive feedback effect of oestrogens. In addition, several factors can influence GnRH/LH release at the hypothalamo-pituitary level. At the ovarian level, cellular and molecular changes in the growing follicle may contribute to anovulation and cyst formation, but studying follicular changes prior to cyst formation remains extremely difficult. Differences in receptor expression between COF and dominant follicles may be an indication of the pathways involved in cyst formation. The genotypic and phenotypic link of COF with milk yield may be attributed to negative energy balance and the associated metabolic and hormonal adaptations. Altered metabolite and hormone concentrations may influence follicle growth and cyst development, both at the level of the hypothalamus-pituitary and the ovarian level. cystic ovarian follicles / pathogenesis / hypothalamus-pituitary / ovary / negative energy balance 1. INTRODUCTION In the 1940’s, the presence of cystic folli- cles on the ovaries was mainly associated Cystic ovarian follicles (COF) are an with nymphomania and a bull-like appear- important cause of subfertility in dairy cat- ance in cows [4, 5], which are clear clinical tle, since they extend the calving interval signs of a state of “disease”. Over the past [1–3]. Prolongation of the calving interval decades, dairy herd management and eco- and treatment costs of COF result in eco- nomics have evolved to a situation in which nomic loss for the dairy farmer. In most of fertility in the postpartum period is utterly the literature, COF are referred to as Cystic important. During this period, cystic folli- Ovarian Disease (COD). However, this ter- cles are rather common, and generally occur minology should be revised since the empha- without obvious clinical signs. Normal sis on cystic follicles has shifted over time. ovarian cyclicity is, however, delayed and * Corresponding author: [email protected] Article published by EDP Sciences and available at http://www.edpsciences.org/rnd or http://dx.doi.org/10.1051/rnd:2006003 106 T. Vanholder et al. these cysts should therefore be regarded as tunity to perform a second examination of COD, despite the absence of previously an animal ten days after the initial diagnosis “classical” signs of disease in the majority of COF to fulfill all the terms of the defini- of cases. In addition, after a variable period tion. The absence of a corpus luteum is of time, cysts can become non-steroido- another requirement, which is not always genic and then they no longer interfere with fulfilled [21]. Non-steroidogenic cysts which cyclicity [6, 7]. Consequently, at the time are hormonally inactive do not influence the non-steroidogenic cyst is observed, no the normal oestrous cycle, so they can occur other clinical abnormalities are present. together with a corpus luteum. Therefore, In present-day dairy herd health pro- recent research articles define COF differ- grammes, “cysts” are often diagnosed in the ently and perhaps more logically [16, 22–24], absence of clear clinical signs. Therefore the although a generally accepted definition is term “Cystic Ovarian Disease” no longer still lacking, which can also be attributed to seems appropriate and should be replaced the heterogeneity (type of cyst, time of occur- by the term “Cystic Ovarian Follicle(s)” rence, clinical signs) of the cysts. which does not necessarily implicate a state Based on the current knowledge and of disease. In this review, we will therefore recent literature, COF may be defined as fol- use COF instead of COD. We prefer to use licles with a diameter of at least 2 cm that are COF instead of “ovarian cysts”, because the present on one or both ovaries in the absence former term indicates that it is the ovarian of any active luteal tissue and that clearly follicle(s) and not any other ovarian tissue interfere with normal ovarian cyclicity. that becomes cystic. Macroscopically, cysts can be subdivided into follicular and luteal cysts, which are considered to be different forms of the same 2. DEFINITION disorder [25]. Luteal cysts are believed to Cystic ovarian follicles develop when one be follicular cysts in later stages [26]. Deter- or more follicles fail to ovulate and subse- mination of progesterone concentrations in quently do not regress but maintain growth blood plasma, milk or milk fat can help to and steroidogenesis. They are defined as make a distinction between the two types. follicle-like structures, present on one or both Follicular cysts secrete little or no proges- ovaries, with a diameter of at least 2.5 cm terone while luteal cysts clearly do [26]. for a minimum of ten days in the absence However, the threshold values used in the of luteal tissue [8–11]. It has become clear literature differ a lot [27–31], which makes though that this definition needs to be it difficult to set a concentration threshold. revised. First, the size limit is rather artifi- In addition, the many intermediate forms cial since follicles might already become with limited or extensive luteinisation do cystic at a smaller size, and dominant folli- not allow for a clear identification of cyst cles ovulate on average at a size of 1.6 to type. So classification is not easy and is sub- 1.9 cm in dairy cows [12–14]. Moreover, ject to personal interpretation. Ultrasound many researchers showed that COF are actu- can be useful in supplying extra information. ally dynamic structures, which can regress Follicular cysts have a thin wall (≤ 3mm) and be replaced by new cysts [15–18]. The and the follicular fluid is uniformly anecho- factors that determine whether a cyst will genic, while luteal cysts have a thicker wall regress or not, remain unknown [19, 20], (> 3 mm), which is visible as an echogenic although changes in mean LH concentra- rim. Also, the latter often have echogenic tion seem to be involved [16]. So the spots and web-like structures in the follic- required individual persistency of ten days ular fluid [32, 33]. Luteal cysts should not is questionable. In addition, in practice, vet- be confused with hollow corpora lutea, erinarians generally do not have the oppor- which are not pathological at all [26]. Cystic ovarian follicles in dairy cattle 107 Hollow corpora lutea are just young cor- common, especially during the postpartum pora lutea with an antrum [34]. Ultrasound period [9]. Irregular oestrus intervals, nym- examination of the ovaries is useful in mak- phomania, relaxation of the broad pelvic ing a distinction between a luteal cyst and ligaments and development of masculine a cystic corpus luteum [32, 35]. physical traits are other signs which may be Follicular cysts initially continue to pro- present, especially later during lactation duce oestrogens in the absence of other fol- [11, 55]. licles > 5 mm on ultrasound [36]. After a variable period of time oestrogen production may cease. The cyst becomes non-steroidog- 4. PATHOGENESIS OF OVARIAN enic without luteinising, thereby allowing a CYSTS new follicular wave to emerge and follicles to grow beyond 5 mm [6, 7]. Ovarian dysfunctions like cysts occur most often during the early postpartum period when there is a transition from the non- 3. INCIDENCE AND SIGNS cyclic condition during pregnancy to the establishment of regular cyclicity. It is gen- Cystic ovarian follicles can occur at dif- erally accepted that cystic follicles develop ferent times throughout lactation. The inci- due to a dysfunction of the hypothalamic- dence varies between 6 and 30% [9, 11, 37– pituitary-ovarian axis. This dysfunction has 43]. The diagnosis of COF is most often a multifactorial etiology, in which genetic, made during the first 60 days post partum phenotypic and environmental factors are [8, 9, 38, 44], mainly because of the close involved [9, 19, 26]. When discussing the monitoring of cow fertility during this pathogenesis of COF, a distinction may be period.
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