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Ultrasound Obstet Gynecol. Writer manuscript; available in PMC 2010 Jun 25.

Published in final edited form equally:

PMCID: PMC2891966

CAMSID: CAMS594

Endometrial development in association with ovarian follicular waves during the menstrual cycle

Abstract

Objectives

Waves of ovarian follicular development during the menstrual cycle have recently been documented in our laboratory. The objective of this written report was to test the hypothesis that ultrasonographically detectable changes in the endometrium during the menstrual cycle would differ betwixt women with two vs. iii waves of ovarian follicular development and among women with different major and pocket-size wave patterns of follicle growth.

Methods

50 women of reproductive age (mean age ± SD, 28.0 ± 6.nine years) underwent daily transvaginal ultrasonography for one interovulatory interval (IOI). Ultrasonographic images of the endometrium were obtained each day, and measurements of endometrial surface area and perimeter (based on the shape of an ellipse, in the transverse airplane) and thickness and pattern (in the sagittal plane) were recorded. Endometrial area, perimeter, thickness and design were compared betwixt women with ii and three waves of follicle development and amongst women with dissimilar minor and major moving ridge patterns of follicular growth during the IOI.

Results

Endometrial area, perimeter, thickness and blueprint increased earlier during the follicular phase in women with two vs. three waves of follicular development. In women with two follicle waves, endometrial area and perimeter increased earlier in those with major major vs. minor major follicle wave patterns.

Conclusions

Ultrasonographically detectable changes in the endometrium occurred in association with follicle wave dynamics in women. Before development of the endometrium during the follicular stage in women with two vs. three follicle waves was attributed to an earlier increment in dominant follicle estradiol production.

Keywords: endometrium, follicular waves, menstrual cycle, ovary

INTRODUCTION

Endometrial development during the human menstrual wheel is closely associated with changes in ovarian function. Granulosa cells of developing ovarian follicles in the follicular phase of the bicycle produce estradiol, which stimulates the development of the endometrial lining^ane–three. In the few days before ovulation, progesterone levels brainstorm to ascent². The source of the preovulatory rising in progesterone levels is not fully known, but is believed to be the theca, granulosa or interstitial cells^2,4–6. After ovulation, progesterone produced past the corpus luteum is believed to maintain the estrogen-primed endometrium and stimulate endometrial glandular development to provide an surround conducive to implantation^1–3. Several growth factors have as well been shown to regulate endometrial development (due east.grand. prostaglandins, interleukins, insulin-similar growth factors); withal, their precise roles are not fully elucidated^7–11. Communication between the ovaries and uterus is required for reproductive success. It is therefore plausible that abnormal signaling mechanisms between the ovary and uterus are associated with abnormal endometrial development, infertility and recurrent embryonic loss.

Transvaginal ultrasonography (TVS) has go an invaluable tool for evaluating the endometrium during natural menstrual cycles and the handling for infertility^12–xvi. Ultrasonographically detectable changes in the endometrium occur throughout the menstrual bike in association with changes in concentrations of serum estradiol and progesterone^17,18. The endometrium is comprised of two layers: the stratum basalis, which lies next to the myometrium, and the stratum functionalis, which lines the endometrial cavity¹⁹. The thickness of the endometrium and relative echotexture (i.e. reflectivity) of the stratum functionalis compared to the myometrium are measurements used to assess the endometrium ultrasonographically. Endometrial thickness is measured equally the distance betwixt the anterior stratum basalis and posterior stratum basalis layers in the sagittal plane^twenty,21. Endometrial thickness has been reported to increase during the follicular phase of the menstrual cycle, peak prior to ovulation, plateau during the early on luteal stage and then decline prior to menstruation^xiv–18. The increase in endometrial thickness during the follicular phase is associated with an increase in serum estradiol levels^17,18,22.

The endometrium appears ultrasonographically equally a thin, simple hyperechogenic single stripe immediately post-obit menses (A pattern). The statum functionalis and basalis layers can be visually differentiated as the endometrium develops during the mid–belatedly follicular phase (B blueprint). A pronounced triple-line echotextural pattern, reflective of the separation of the stratum basalis and functionalis layers, is observed in the periovulatory period in association with rising estradiol levels (C pattern). The triple-line design disappears after ovulation. A more homogeneous, hyperechogenic endometrium is observed equally endometrial glands branch and expand under the influence of luteal progesterone production in the secretory phase (D design). Visualization of agile menstrual flow is indicative of flow (One thousand blueprint)^{14,18,twenty,22–24}.

The use of ultrasonographic assessment of the endometrium to predict success following controlled ovarian hyperstimulation and in-vitro fertilization (IVF) has been studied. In many reports, a thick endometrium and/or triple-line echogenic pattern of the endometrium around the fourth dimension of follicle aspiration was associated with favorable IVF outcomes^25–35. By contrast, other researchers reported no associations betwixt the ultrasonographic appearance of the endometrium and success following assisted reproduction^13,36–xl, and recommended that farther research exist performed before any definitive conclusions are made.

Limited research has been performed to evaluate the endometrium ultrasonographically during spontaneous menstrual cycles. The electric current country of knowledge on endometrial growth during the menstrual bicycle has been based on previously held notions that dominant ovarian follicles developed just during the follicular phase, followed by follicular quiescence during the luteal phase^41–48. However, it is now known that waves of ovarian follicular development occur during the menstrual bike^49,50. A total of 34/l (68%) women exhibited two follicular waves, and the remaining 32% exhibited three waves during an interovulatory interval (IOI)⁴⁹. A follicular wave was defined every bit the synchronous growth of a grouping of follicles. Only the last follicular wave was ovulatory, while all preceding waves were anovulatory. Follicular waves were characterized every bit major or modest waves^l. Major waves were those in which one follicle was selected to become dominant over other follicles of the moving ridge, while minor waves were those in which selection of a ascendant follicle was not detected. Ascendant follicles were selected for preferential growth at a diameter of approximately 10 mm^l. In women with 2 follicle waves, minor major (−+) and major major (++) patterns of follicle wave dynamics were observed^fifty. In women with three follicle waves, small-scale pocket-sized major blueprint (−−+), minor major major design (−++) and major major major (+++) patterns were observed^l.

It is non known whether ultrasonographically detectable changes in the endometrium differ between women with ii vs. three follicle waves and amongst women with major and modest patterns of follicular wave dynamics. This information would increment our understanding about the cyclic changes in ovarian and endometrial function that occur in women. Studies performed thus for have involved the assessment of small numbers of women using transabdominal ultrasonography sometimes in combination with endometrial biopsy and/or histological assessment^14–18. Serial evaluations of the endometrium during the menstrual wheel using high-resolution TVS in big samples of women have not yet been performed. The objective of this report was to characterize changes in the endometrium every twenty-four hours during ane IOI using high-resolution TVS. The research hypothesis tested was that endometrial development (every bit adamant by measurements of endometrial area, perimeter, thickness and echotextural blueprint) would differ between women with two vs. three follicular waves and among women with different follicle wave patterns.

METHODS

Fifty women participated in a report designed to characterize ovarian follicular wave dynamics during the menstrual cycle^49,l. Information collected from the 50 women were evaluated to elucidate associations between patterns of follicle wave dynamics and endometrial development. Participants were assessed, by history and physical examination, to exist healthy women of reproductive historic period (mean age ± SD, 28.0 ± vi.9 (range, 19–43) years). Women who smoked, had been pregnant or lactating 6 months prior to initiating report procedures, had used hormonal contraception within 3 months of enrolling, had a history of irregular menstrual cycles, were taking medication(due south) known or suspected to interfere with reproductive function, or were planning surgery during the study menses were non eligible to participate. Informed consent was obtained from all women prior to initiating study procedures. Study protocol was canonical by the Institutional Review Board of the University of Saskatchewan.

Each participant underwent daily TVS evaluation of her ovarian and uterine status for one IOI. Scans were initiated 12 days after catamenia (i.due east. earlier the first ovulation) and were continued until 3 days afterwards the second ovulation. High-resolution Ultramark nine and ATL HDI 5000 ultrasound machines (Advanced Technologies Laboratories, Bothell, WA, USA) with 5–nine-MHz multifrequency convex array transducers were used to acquire imaging data. Approximately 90% of the examinations were performed by a unmarried sonographer (A.R.B.). A second sonographer (R.A.P.) was available when the chief sonographer was not nowadays.

The area, perimeter and thickness of the endometrium were measured during each ultrasound examination. Endometrial area and perimeter measurements were based on the shape of an ellipse, in the transverse plane (Figure 1). Endometrial thickness was measured as the distance from the inductive stratum basalis–myometrial junction to the posterior stratum basalis–myometrial junction, in the mid-sagittal plane. The transverse and sagittal planes of department that represented the largest dimensions of the fundal aspect of the endometrium were used for all measurements. Endometrial echotexture was assessed each day equally either an M, A, B, C or D pattern. The criteria used to determine endometrial pattern are shown in Table ane ²⁰. Plus and minus values of endometrial blueprint were used to further refine endometrial pattern scores and minimize intraobserver variability. A plus symbol indicated that the endometrium exhibited ultrasonographic features of both the letter pattern noted and the pattern above. A minus symbol indicated an endometrium that exhibited ultrasonographic features of both the alphabetic character value noted and the value below.

Ultrasonographic images of the endometrium in maximal transverse aeroplane. The outer stratum basalis layer, inner functionalis layer and uterine lumen are shown (a). Measurements of the long axis, short axis, perimeter and expanse of the endometrium are shown in the bottom left corner (b). Dotted lines depict the perimeter measurement of the endometrium (b).

Table 1

Characteristics for determining endometrial blueprint

Blueprint	Criteria
Chiliad	Active menstrual flow observed
A	Postmenstrual; thin; single line; no detectable differentiation of stratum functionalis and basalis
B	Early follicular phase; triple line; some differentiation of the stratum functionalis and basalis
C	Periovulatory; thick; pronounced triple line; pronounced differentiation of the stratum functionalis and basalis
D	Luteal phase; thick; homogeneous echogenicity

Hateful endometrial area, perimeter, thickness and design during the IOI were plotted, irrespective of follicle wave condition. Endometrial information were and so plotted separately for women with 2- or three-moving ridge cycles, as previously adamant⁴⁹. In women with two follicle waves, endometrial information were further partitioned into −+ and ++ follicle wave patterns, as previously determined^l. In women with three follicle waves, information were further categorized into −−+, −++ and +++ follicle moving ridge patterns, equally previously determined⁵⁰. For graphical purposes, information were normalized to the hateful IOI for women with ii (27.4 ± 0.iv days) and three (29.4 ± 0.half-dozen days) follicle waves. Repeated measures ANOVA (PROC MIXED, SAS/STAT Software, 2001, SAS Institute Inc., Cary, NC, Us) were used to assess changes in the area, perimeter, thickness and pattern of the endometrium during the IOI to decide if differences could exist detected between women with ii vs. three follicular waves and among women with different follicle wave patterns.

RESULTS

The hateful area, perimeter, thickness and pattern of the endometrium, irrespective of follicle moving ridge dynamics (i.e. earlier partitioning data into women with 2 vs. three follicular waves and major and minor patterns of follicular development), remained abiding during the early on to mid-luteal phase, decreased approximately 10 days later ovulation (i.e. the late luteal phase) so increased during the follicular phase. Endometrial area reached peak values of 281.seven ± eleven.9 mm² on the mean solar day of the first ovulation, declined to a nadir of 106.viii mm² 3 days subsequently menstruum began and reached a peak level again of 253.0 ± xiv.2 mm^two immediately prior to the 2nd ovulation. Endometrial perimeter reached a pinnacle level of 75.9 ± two mm 10 days afterward ovulation, decreased to 55.3 ± one.8 mm 1 day after menses began and then increased to 66.6 ± 2.1 mm prior to the 2d ovulation. Endometrial thickness reached a peak of 10.iv ± 0.3 mm on the 24-hour interval of the starting time ovulation, decreased to 4.4 ± 0.2 mm 1 day after catamenia began and then increased to 9.2 ± 0.iv mm in the late follicular phase before the second ovulation. The endometrium was a D pattern 1 day following the first ovulation, an A pattern two days after menstruum began and a C pattern in the belatedly follicular phase prior to the second ovulation. Ultrasonographic characterizations of endometrial design in one woman during the IOI are shown in Figure 2.

Ultrasonographic images of the endometrium illustrating the M design (a: 24-hour interval 3 of menstruum; active catamenia visualized), A pattern (b: early follicular stage), B blueprint (c: mid-follicular phase), C pattern (d: periovulatory flow) and D pattern (e: mid-luteal stage) of echogenicity. The endometrium is shown in sagittal section. Arrows demarcate the anterior and posterior borders of the endometrium.

Changes in the endometrium during the IOI for women with two vs. three follicular waves are illustrated in Figure 3. Endometrial area (Effigy 3a) during the follicular stage of the bike (i.eastward. days 17–30) increased before in women with ii vs. three follicular waves (day effect: P < 0.0001; moving ridge effect: 0.88; twenty-four hours * wave result = 0.008). Endometrial perimeter (Figure 3b) during the follicular stage increased before in women with two vs. iii follicle waves (day effect: P < 0.0001; wave effect: P = 0.28; day * wave effect: P = 0.008). Endometrial thickness (Figure 3c) during the follicular stage increased earlier in women with 2 vs. three follicle waves (day consequence: P < 0.0001; wave effect: P = 0.01; day * moving ridge consequence: P = 0.08). Likewise, endometrial blueprint (Figure 3d) during the follicular phase increased before in women with ii vs. three follicular waves (24-hour interval effect: P < 0.0001; wave event: P = 0.02; 24-hour interval * moving ridge effect: P < 0.0001). No differences in endometrial development were detected between women with 2 vs. three waves during the luteal phase (P > 0.05).

Endometrial expanse (a), perimeter (b), thickness (c) and blueprint (d) normalized to the mean interovulatory interval for women with 2 (○; 27.4 ± 0.4 days) and 3 (●; 29.4 ± 0.6 days) waves of follicle development. Mean ± standard error is shown. ov, ovulation.

Changes in the endometrium during the IOI for women with major and pocket-size wave patterns of follicle development are shown in Figure iv. In women with two follicle waves, endometrial area (twenty-four hours effect: P < 0.0001; pattern issue: P = 0.15; day * design effect: P = 0.002) and perimeter (mean solar day result: P < 0.0001; pattern issue: P = 0.003; mean solar day * blueprint consequence: P = 0.69) during the follicular stage appeared to increment earlier in those with ++ vs. −+ wave patterns of follicle growth. In women with three follicle waves, no differences in endometrial development were detected among −−+, −++ and +++ follicle wave patterns (day effect: P < 0.0001; pattern effect: P > 0.05; 24-hour interval * pattern effect: P > 0.05).

Endometrial area (a), perimeter (b), thickness (c) and design (d) normalized to the hateful interovulatory interval for women with −+ (■; 27.4 ± 0.4 days), ++ (▲; 27.ii ± 1.0 days), −−+ (●; 28.8 ± 0.7 days), −++ (○; 30.7 ± 1.0 days) and +++ (□; 30.0 ± i.0 days) patterns of follicle wave dynamics. Mean ± standard error is shown. ov, ovulation.

DISCUSSION

Series examinations of the endometrium using high-resolution TVS supported the results of previous studies in which changes in endometrial thickness and echotexture during the menstrual wheel were documented^{14,18,xx,22–24}. Endometrial expanse, perimeter and thickness reached a plateau afterward ovulation, declined at the end of the luteal stage earlier period, and then increased sharply during the follicular stage of the IOI. Endometrial echotexture was represented by a D blueprint in the luteal phase, M pattern during menstruum, A pattern in the early follicular phase and C pattern in the late follicular phase of the IOI.

The results of the present report supported the hypothesis that endometrial development would differ among women in association with differences in ovarian follicular moving ridge dynamics. Ultrasonographically detectable differences in endometrial evolution during the menstrual cycle were observed in women with ii vs. three waves of ovarian follicular development. Endometrial surface area, perimeter, thickness and pattern measurements increased earlier during the follicular stage in women with two compared with iii waves of follicular development. The earlier development of the endometrium during the follicular phase in women with two follicle waves occurred in association with an before rise in serum estradiol levels, as previously described in our laboratory^l. The earlier increment in estradiol levels was believed to occur equally a result of the earlier emergence of the dominant ovulatory follicle in women with two vs. three follicle waves⁵⁰. The preovulatory estradiol, follicle-stimulating hormone and luteinizing hormone surges were previously documented to occur 1 twenty-four hours earlier, in clan with a shorter IOI, in women with ii vs. three follicle waves^l. Nosotros therefore concluded that the earlier emergence of the dominant ovulatory follicle in women with 2 vs. three follicle waves was associated with earlier dominant follicle estradiol production, endometrial development and preovulatory hormonal surge.

Major and minor waves of follicle development occur during the follicular and luteal phases of the menstrual cycle in healthy women of reproductive historic period⁵⁰. Differences in endometrial growth, as determined ultrasonographically, were detected in women with minor and major wave patterns of follicle evolution. In women with two follicle waves, endometrial area and perimeter during the follicular stage appeared to rise earlier in women with ++ vs. −+ moving ridge patterns of follicular growth. In women with three moving ridge patterns of follicle growth (−−+, −++ and +++ patterns) no differences in endometrial growth were observed. Major waves were those in which a dominant follicle was selected for preferential growth, while minor waves were those in which dominance was not manifest⁵⁰. There was no departure in the solar day of emergence of the second follicle wave (14 days after the first ovulation) in women with both ++ and −+ patterns of follicular growth⁵⁰. Therefore, we believe the earlier development of the endometrium in women with ++ vs. −+ wave patterns to be inconclusive. Categorization of the data into subgroups of women with unlike patterns of follicular wave dynamics resulted in pocket-size sample sizes. Resolution of this puzzler will require farther analyses on a larger sample population.

The results of the present study accept increased our understanding of the basic physiological mechanisms underlying ovarian and uterine function during the menstrual cycle and provide rationale for the notion that endometrial development is closely related to ovarian follicle wave dynamics. The noesis that the endometrium develops before during the follicular phase in women with ii vs. 3 follicle waves may help to explicate the variability in endometrial thickness and echotexture that has been reported in women undergoing assisted reproductive technologies. In addition, we believe that the cognition about variability in endometrial growth and follicle moving ridge dynamics during the menstrual bicycle may provide insight into the elucidation of uterine factors which may exist associated with infertility and/or recurrent pregnancy loss.

Acknowledgments

Appreciation is expressed to the inquiry volunteers, whose participation was invaluable for the completion of this written report. Funding for this project was provided by the Canadian Institutes of Health Research, Saskatoon, Saskatchewan, Canada.

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