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Ultrasound and Folliculogenesis 1Fernando Bonilla-Musoles, 2Newton Osborne, 1Francisco Raga, 1Francisco JB Bartret

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Ultrasound and Folliculogenesis 1Fernando Bonilla-Musoles, 2Newton Osborne, 1Francisco Raga, 1Francisco JB Bartret DSJUOG Fernando Bonilla-Musoles et al. 10.5005/jp-journals-10009-1577 REVIEW ARTICLE Ultrasound and Folliculogenesis 1Fernando Bonilla-Musoles, 2Newton Osborne, 1Francisco Raga, 1Francisco JB Bartret ABSTRACT In spite of these advances, a review of the literature Ultrasound as well as gynecologic endocrinology are two major leads us to raise more questions: advances which enabled revolution in assisted reproduction • How can an evaluation of folliculogenesis be technology (ART). Today it is impossible to imagine ART without improved? ultrasound. • How can we better evaluate existing antral follicles Keywords: Assisted reproduction technology, Gynecologic (AF)? endocrinology, Ultrasound. • How can we know the best moment to administer How to cite this article: Bonilla-Musoles F, Osborne N, Raga F, hCG for the induction of ovulation? Bartret FJB. Ultrasound and Folliculogenesis. Donald School J • What is the effect of the dominant follicle luteinization Ultrasound Obstet Gynecol 2018;12(4):282-299. on growing follicles that remain? Source of support: Nil • When should a luteal body be considered active, Conflict of interest: None regressive, or luteinized and not broken? Lastly, discussions related to ultrasound characteris- INTRODUCTION tics of the endometrium (thickness, morphology, vascu- larization, delimitation, and volume) are so ample that No one disagrees that ultrasounds along with gyneco- it is no simple matter to develop a protocol that guides logic Endocrinology have been two major advances in to adequate evaluation of the concept of endometrial our specialty and that they have been the fundamental receptivity. enablers of the revolution that has occurred in ART.1,2 Commentary about the value of color Doppler and Without ultrasound, ART as we now know it would be Doppler energy along with the recent advances in the inconceivable. The main steps in this “revolution” were: varied modes of 3D/4D visualization (Figs 1 to 3) will • Introduction of vaginal probes by Kratochwil in Vienna. merit a separate chapter. • Description of endometrial changes, folliculogen- esis, and the diverse types of the endometrium by ULTRASONOGRAPHIC NOTIONS FOR Hackelöer in Hamburg. FOLLICULOGENESIS CONTROL • The disappearance of laparoscopic follicular aspira- tion because of the introduction of ultrasound-guided Among the available means for adequate control of fol- transvaginal aspiration, developed by Feichtinger, liculogenesis, only ultrasound is capable of showing the also in Vienna. evolution of follicular growth over short time spans. • Three- (3D) and four-dimentional (4D) ultrasound Folliculogenesis starts 70–74 days before ovulation. That have improved and eased folliculogenesis control. is two and a half cycles before its ovulatory cycle. Four-dimensional (4D) enables us to capture new planes About 400–500 primordial and primary follicles of vision, improves image quality, and introduces initiate growth in a different ovarian area each time, new ultrasound modes (HDlive and silhouette, AVC, with the mechanisms that control each area are still VOCAL, inverse mode, etc.) that allows great resolution unknown. and evaluation of pelvic organs. • Why in this area? In recent years, the spectacular advances with 4D • Why in this specific ovary? ultrasonography have generated a new revolution in ART. These events take place independently of the action of hormones from the hypophysis (Figs 1 to 3). 1,2Professor Although the mechanism by which these cells start 1Department of Obstetrics and Gynaecology, School of their growth is not known, it is known that there is an Medicine, Valencia, Spain increase in local growth factors and an increase in fol- 2Department of Obstetrics and Gynaecology, Obaidia Hospital, licular microvasculature. Furthermore, it is known that School of Medicine David, Panamá the layer of granulosa cells is functional and remains Corresponding Author: Fernando Bonilla-Musoles, Professor, intact. The larger the number of cells in the granulosa Department of Obstetrics and Gynaecology, School of Medicine, layer will result in a greater number of gonadotropin Valencia, Spain, e-mail: [email protected] (FSH and LH) receptors, and as a consequence, with a 282 DSJUOG Ultrasound and Folliculogenesis Fig. 1: (Top) Nowadays used new US modes for follicle genesis monitoring which are more definitive than the 2D vaginal ultrasound used today. Above and left the three-orthogonal planes and histogram doing the total ovarian volume calculation which is of interest when looking to the ovarian reserve.To the right Doppler energy and tomography ovarian cuts. This modes increases the findings by using only color Doppler. (Below) 2D in orthogonal planes and AVC from the existing antral follicles. Each follicle is shown in a different color. It is easy to count and measure each follicle. The dominant follicle is clearly depicted in blue color greater probability of follicular. Ovarian folliculogenesis They must wait several days to notice size and color has three well-established phases (Fig.4). changes that indicate when picking must be done. It The end of the vast majority of antral and preantral is the same with follicles. It is advisable to have the follicles will be their atresia by apoptosis (Fig. 4). first ultrasound evaluation on the second or third day of the cycle. Subsequent evaluations in induced ANTRAL FOLLICLES cycles will be done six days after the administration of gonadotropins or four to five days after administra- There are two basic exploratory ultrasound applica- tion of clomiphene. tions during these events: visualization and antral We are of the opinion that ultrasound evaluation follicle (AF) count in the basal state. is sufficient for adequate folliculogenesis control in The number of existing antral follicles in basic ultra- natural cycles as well as in ART cycles. Additional sound and, although in lesser magnitude, the ovarian evaluation of estradiol concentrations has not proven volume, is of great importance for knowledge about to add additional information that is crucial for the ovarian reserve. To develop an evaluation proto- adequate control of ovarian stimulation cycles for col, it is agreed that the count of antral follicles must IVF/ICSI. In the vast majority of cases, ultrasound is be done during the first days of the menstrual cycle. enough. In this way laboratory, overwork and unnec- Nevertheless, antral follicle count can be carried out at any phase of the menstrual cycle. Small follicles (2–3 essary additional charges are avoided. mm) can be seen and measured with vaginal probes. Visualization is much simpler using the different 3D FOLLICULOGENESIS IN NATURAL CYCLE modes: inverse, AVC, VOCAL, and silhouette (Figs 5 Folliculogenesis varies depending on whether it is and 6). spontaneous or induced. As mentioned above, the first (or basal) ultrasound should be performed on the FOLLICULOGENESIS CONTROL second or third day of the cycle. This would provide Vaginal 2D or 3D ultrasound allows optimal evalua- approximate knowledge of ovarian reserve. tion (daily or at short intervals) of follicular growth. Follicles between 2 mm and 9 mm are part of the When farmers want to determine the best time to pick cohort of small antral follicles that are starting the their oranges they do not need to check on them daily. process of maturation. Shortly after, a dominant follicle, Donald School Journal of Ultrasound in Obstetrics and Gynecology, October-December 2018;12(4):282-299 283 Fernando Bonilla-Musoles et al. Fig. 3: Spontaneous folliculogenesis. The new US mode “silhouette” shows a better delimitation of the structure profile and allow a clear delimitation of each antral follicle distinguished by greater size and faster growth, will appear. The remaining antral follicles will cease to grow or become atretic. It is from this moment that, if so desired, hormonal determinations and ultrasound controls every 48 hours can be done. Follicle growth and 17b-estradiol production occur in parallel. The follicle is considered to be mature when it produces ~ 250 pg/mL of 17 b-estradiol. Since in natural cycles the relation of follicular Fig. 2: Follicle genesis. Vascular image around each follicle obtained growth to estradiol production occurs in a linear manner with 3D angiography and color power Doppler. It is clearly depicted up to the tenth day of the cycle, these determinations that only preovulatory follicles dispose of a great vascularity located around the whole follicle which will allow fluid transvasation to the can be avoided. Follicle growth after the tenth day is follicular fluid without increasing its internal fluid pressure. It can not linear, but exponential. The closest the follicle gets be observed that only antral preovulatory follicles dispose of this to ovulation, the fastest is its growth. The follicle grows enormous perifollicular vascularization. In the above picture, the between 1 mm and 1.2 mm/day up to the tenth day same follicles observed with AVC mode and a mean growth of 1.8 mm/day at the end of the proliferative phase. Before ovulation the dominant follicle measures 22–25 mm (occasionally, between 18 and 36 mm), and this growth is the only marker that will predict with certainty ovulation (Figs 7 to 10). A very approximated summary would be (Table 1). There are other US images that predict an approaching ovulation, but they are not always visible. VISUALIZATION OF THE CUMULUS OOPHORUS The cumulus oophorus can be seen 20% of the times with transvaginal ultrasound. However,
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