Department of Obstetrics and Gynecology, Clnica Universitaria de Navarra, University of Navarra, Pamplona, Spain
Three-dimensional ultrasound (3D US) is a new imaging modality, which is being introduced into clinical practice. Although this technique will not probably replace two-dimensional ultrasound, it is being increasingly used. It has been reported that 3D US is a very high reproducible technique. The endometrium has been paid special attention when using this technique. The aim of this paper is to address some technical aspects of 3D US and to review critically its current status in evaluating endometrial function with special focus in its role in predicting pregnancy in assisted reproductive techniques. In spontaneous cycles endometrial volume grows during follicular phase remaining constant through the luteal phase. Endometrial vascularization increases during follicular phase peaking 2–3 days before ovulation, decreasing thereafter and increasing again during mid and late luteal phase. Data from studies analysing the role of 3D US for predicting IVF outcome are controversial. An explanation for these controversial findings might be different design of reported studies, specially the timing of ultrasound evaluation.
Endometrial receptivity is a crucial fact in human reproduction. Endometrial assessment has been performed usually by endometrial biopsy1. However, such as invasive method is not acceptable when evaluating endometrial receptivity in order not to damage the endometrium. Therefore, endometrial receptivity should be ideally evaluated before implantation by a non-invasive method.
Transvaginal ultrasonography may represent, theoretically, such an ideal non-invasive technique. Several parameters have been proposed for assessing endometrial receptivity, including endometrial thickness, endometrial pattern and endometrial and subendometrial blood flow2-7. These parameters may identify patients with low implantation potential. However, their positive predictive value is low8,9.
Recently, three-dimensional ultrasound (3D US) has become available10-13. With this technology any desired plane through an organ can be obtained. With 3D US a volume of a region of interest (ROI) can be acquired and stored. This volume can be further analysed in several ways, such as navigation, multiplanar display, and surface rendering or volume calculation. This technique also allows a whole assessment of the endometrial and subendometrial vascularization14,15.
In this review I shall address current state-of-the-art of 3D US in assessing the endometrium throughout the menstrual cycle and its possible role in predicting endometrial receptivity in assisted reproductive techniques (ARTs). A Medline search (1995–2006) was performed using the following key words: "three-dimensional ultrasound", "angiography", "power Doppler", "endometrium", "endometrial", "receptivity". A total of 27 articles were identified. Twenty-three were clinical studies and were selected for review, whereas 4 papers were reviews and were excluded.
Several published papers deal in detail the technical aspects of 3D US and an extensive description of these technical aspects is beyond the scope of this review16-19. Notwithstanding, I shall explain briefly some basic considerations.
3D US images can be obtained by two methods: freehand and automated. The freehand method requires manual movement of the transducer through the ROI. The automated method acquires the images using dedicated 3D transducers. When these probes are activated, the transducer elements automatically sweep through the ROI selected by the operator (the so-called "volume box") while the probe is held stationary. This provides more accuracy to this method as compared with the freehand systems, in which speed of sweep is more difficult to maintain constant manually by the operator.
The digitally stored volume data can be manipulated and presented in various displays: multiplanar display, "niche" mode or surface rendering mode. Probably, the most used and useful display is multiplanar display, which simultaneously shows three perpendicular planes (axial, sagital and coronal), allowing navigation through these three planes with the possibility of switch over any desired plane (Figure 1).
Another important ability of 3D US is volume calculation, even in irregularly shaped structures, using the Virtual Organ Computer-aided AnaLysis (VOCAL) (Figure 2). This is a rotational method, based on rotations in given steps (6°, 9°, 15°, 30°) on a given orthogonal plane (A, B or C). This method has been demonstrated to be more accurate than 2D-volume estimation, with an error estimation of 7% for 3D US as compared of 22% for 2D US17.
Vascularization of tissues within the ROI can be also assessed using 3D Power-Doppler ultrasound (3D-PDA) and the VOCAL program18. Using this method, three vascular indexes can be calculated: the Vascularization Index (VI), expressed as percentage, measures the number of colour voxels in the studied volume, representing the blood vessels within the tissue. The Flow Index (FI) is the average colour value of all colour voxels, representing average colour intensity. And the Vascular-Flow Index (VFI) is the average colour value of all grey and colour voxels, which represents both blood flow and vascularization (Figure 3). Using the "shell" function it is possible to calculate a volume at different thickness around the predetermined endometrium and estimate the vascularization in this "shell". This allows the assessment of the so-called "subendometrial region" (Figures 4 and 5).
3D US has a very low inter-observer and intra-observer variability for calculating endometrial volume, with intraclass correlation coefficients ≥ 0.9714,20-22. However, this depends on the technique used, being the VOCAL method the most reproducible23. This technique has been also found to be highly reproducible for estimating ovarian and endometrial vascularization using 3D PD with intraclass correlation coefficients ≥ 0.99 for all indexes15,24,25.
Correlation of endometrial ultrasound and histology
Several studies have assessed the correlation between some endometrial sonographic parameters and histologic dating of the endometrium.
Li et al, using transabdominal ultrasonographic measurement of endometrial thickness prior to endometrial sampling in regularly cycling women found that endometrial histology was likely to be proliferative if the thickness was < 8 mm and likely to be secretory if endometrial thickness was ≥ 9 mm. However, for a given endometrial thickness, the stage of endometrial development appeared to vary widely, suggesting that ultrasonographic measurement of endometrial thickness cannot accurately predict histological dating26. These results have been confirmed by other studies27,28.
Endometrial pattern, however, has been found to correlate with histologic dating of the endometrium29-31. Thus, a three-layered endometrium use to be present in the proliferative phase and an echogenic endometrium use to be present in the secretory phase29.
Most studies evaluating the correlation of Doppler ultrasonographic assessment of uterine arteries and endometrial hisologic dating found that Doppler ultrasound cannot predict histologic dating28-32.
To the best of my knowledge, no study has been published correlating 3D ultrasonographic data and histologic dating of the endometrium.
Angiogenesis in the endometrium during the menstrual cycle and implantation
Controversy exists regarding angiogenesis, vascular density and expression of VEGF in the endometrium during normal menstrual cycle.
Some investigators have shown a significant increase in the vascular surface area, diameter and total number of capillaries in the secretory phase as compared with the proliferative phase33. Others have noted a peak in stromal VEGF expression in the proliferative phase with a peak glandular VEGF expression during the secretory phase34.
Au and Rogers reported that angiogenesis was weakest during menstrual phase, followed by a rapid increase during the early proliferative phase to peak in mid-cycle before a gradually decrease towards cycle end35.
Torry and Torry detected a significant increase in VEGF mRNA throughout the endometrial cycle in the non-pregnant patient with its expression increasing 3 to 5 times from the early proliferative phase to the late secretory phase36.
On the contrary, some investigators have found that endometrial VEGF expression during the menstrual cycle is inconsistent37 and others have reported no modifications in vascular density in different phases of the endometrial cycle38 or that endothelial cell proliferation does not show a consistent pattern across the menstrual cycle39.
Implantation is a progressive and versatile process in which the blastocyst apposes, attaches and invades the underlying endometrial surface. Angiogenesis is a crucial step fro embryo implantation. Several studies have demonstrated that VEGF and its receptors are markedly increased post ovulation and around peri-implantation period40,41.
In summary, in spite of some controversial data, it seems that changes related to angiogenesis of reproduction are ovulatory-related and serve to prepare a receptive nidation site or the blastocyst/embryo42-44.
Three-dimensional evaluation of the endometrium in spontaneous menstrual cycles
Lee et al45 first reported endometrial volume changes during spontaneous menstrual cycles assessed by 3D US. These authors reported on 18 nullipara regularly menstruating women, mean age 31 years. They performed a longitudinal study at 3–6 days interval during a single menstrual period, measuring the endometrial and uterine volume using the multi-slice technique and calculating the "uterus-endometrium" ratio. Mean endometrial volume was 1.23 cm3 (SD: 0.98), ranging from 0.25 cm3 to 5.5 cm3. They found that this ratio decreased throughout the menstrual cycle reaching a nadir around the 20th cycle's day, reflecting that endometrial volume was highest at mid luteal phase (R2 = 0.4318).
Raine-Fenning analysed the endometrial volume longitudinally in a series of 30 "apparently fertile" women, having regular menstrual cycle and no history of gynaecological disease46. Study design was an ultrasound examination n an alternate-day basis until ovulation, confirmed by ultrasound, and then every four days until next menstrual period. In this study the authors used the rotational method (plane C, rotation step 9°). This technique has been proven to be more precise and reproducible than multi-slice method for volume calculation24. They found a steady increase of the endometrial volume throughout the follicular phase until ovulation occurs and the remained relatively constant through luteal phase. As could be expected endometrial thickness was significantly correlated with endometrial volume (R2 = 0.7671).
These findings would be in agreement with histological data in which endometrial growth is restricted to the follicular phase of the menstrual cycle when expansion of the stratum functionalis of the endometrium occurs, which in turns is directly related to the increase of serum estradiol levels. In this study endometrial volume was found to be greater in parous women. No relationship was found smoking or age.
This same group evaluated endometrial and subendometrial blood flow by 3D-PDA47. Subendometrial region was considered as an area within 5 mm of the originally defined myometrial-endometrial contour, using the "shell" software's facility. They found that both VI and VFI increased from mid-follicular phase, peaking 3 days prior to ovulation. Thereafter, there was a decrease in both of these indices, reaching a nadir 5 days postovulation, before a gradual increase during the transition from early to mid-luteal phase. FI showed a similar pattern but with a more pronounced nadir in late follicular phase. These changes in VI; FI and VFI were closely correlated with estradiol levels during the follicular phase but this relationship was lost after ovulation. All three indices began to rise when serum progesterone levels increased during luteal phase.
These findings were rather conflicting with data obtained from conventional pulsed Doppler studies in which uterine blood flow showed a steady increase throughout the menstrual cycle peaking in mid-luteal phase48,49. Most of these studies assume that blood flow within the uterine arteries is representative of the whole uterine and endometrial perfusion. However, power Doppler is more sensitive to lower velocity and combined with 3D US provides information from a specific region of the uterus (endometrial and subendometrial area). On the other hand, preovulatory reduction in 3D-PDA indices might be explained by a physical vessel obstruction induces by an increase in myometrial contractility50.
More recently, Jokubkiene et al have reported similar findings on a group of 16 regular menstruating healthy women51. These researchers performed a prospective longitudinal assessment through the menstrual cycle on a daily basis from day 2, 3 or 4 until follicular rupture and then on days 1, 2, 5, 7 and 12 after ovulation. They used the VOCAL program (plane A, 30° rotation step). Subendometrial region was defined as 2 mm shell within the defined endometrial contour. Regarding endometrial volume their findings were identical to those from Raine-Fenning47, an increase during the follicular phase and then plateaued throughout the luteal phase. In terms of vascularization, VI and VFI increased during the follicular phase reaching a maximum 2 days before ovulation, then decreased to reach a nadir 2 days after ovulation and then rose again progressively during the luteal phase. Changes in FI were similar but less clear, reaching the nadir 5 days after ovulation. However, these authors did not find a correlation between VI; FI and VFI in endometrial and subendometrial regions and progesterone levels on day +7 after ovulation or LH levels on days -1 or +1.
Different study design and methodology could explain differences between these two studies. Notwithstanding, in spite of these differences, both studies clearly show that changes in endometrial and subendometrial vascularization are ovulatory-related and would be in agreement with those previously mentioned studies that evaluated VEGF expression34,36.
These studies are summarized in table 1.
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Reproductive Biology and Endocrinology 2006, 4:56 doi:10.1186/1477-7827-4-56
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