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48
E. H. Y. Ng
a
b
Fig. 3.2 (a, b) Endometrial volume and blood ow measured by 3D Doppler ultrasound
3 Two-Dimensional andThree-Dimensional Doppler inReproductive Medicine
a
49
b
Fig. 3.3 (a, b) Subendometrial volume and blood ow measured by 3D Doppler ultrasound
50
Table 3.3 Summary of studies of endometrial and subendometrial blood ow by 3D power Doppler ultrasound
Study IVF cycles Inclusion/exclusion criteria USS day Results Schild etal.
(2000) [26]
Kupesic etal. (2001) [18]
Wu etal. (2003) [27]
Dorn etal. (2004) [28]
Järvelä etal. (2005) [29]
Ng etal. (2006) [30]
Ng etal. (2006) [33]
Mercè etal. (2008) [35]
Ng etal. (2009) [40]
USS ultrasound, VI vascularization index, FI ow index, VFI vascularization ow index, OR oocyte retrieval, ET embryo transfer
75cycles using a long protocol ET 2days after TUGOR Subendometrial FI is the strongest
89cycles using a long protocol Blastocyst transfer 5days after TUGOR 54cycles; rst cycles only (details of ovarian stimulation and ET not given) 42cycles using a long protocol
35cycles using a long protocol ET 2days after TUGOR
451cycles using a long protocol; rst cycle only ET 2days after TUGOR 193cycles Frozen-thawed embryo transfer cycles 80cycles using a long protocol
293cycles using a long protocol ET 2days after OR
Inclusion criteria Downregulation conrmed
(endometrium <5mm; no ovarian cyst of >2.5cm; serum oestradiol <60pg/ ml)
Inclusion criteria Serum FSH<10IU/L No broid, ovarian cysts
and ovarian endometriosis
Inclusion criteria Age<38years Normal uterine cavity Serum FSH <15IU/L ≥2 good quality embryos Exclusion criteria Polycystic ovary syndrome Endometrium <6mm Gynaecological surgery Exclusion criteria Uterine broids Endometriosis Single ovary Previous operation on the
uterus or salpingectomy Inclusion criteria Normal uterine cavity on
scanning
Inclusion criteria Normal uterine cavity
Inclusion criteria First cycle Normal uterine cavity Serum FSH <10IU/L Regular cycles Non-smokers Inclusion criteria First cycle Normal uterine cavity
Before stimulation
ET (hCG +7)
hCG Subendometrial VFI higher in
OR No difference in subendometrial
After stimulation and OR
OR Endometrial VI and VFI lower in
LH+1 No difference in endometrial and
hCG Higher endometrial VI, FI and
OR and ET No difference in endometrial and
Subendometrial VI, FI and VFI lower in pregnant than non­pregnant cycles
predictive factor for IVF in logistic regression analysis Higher subendometrial FI in pregnant cycles
pregnant cycles
VI, FI and VFI between pregnant and non-pregnant cycles
No difference in endometrial and subendometrial VI between pregnant and non-pregnant cycles on both days
pregnant cycles
subendometrial 3D Doppler ow indices between pregnant and non-pregnant cycles
VFI in pregnant cycles
subendometrial 3D Doppler ow indices on the 2days and changes in these indices between pregnant and non-pregnant cycles
E. H. Y. Ng
The age of women, their smoking habits, their types of infertility and parity and causes of subfer­tility had no effect on all endometrial and subendo­metrial 3D Doppler ow indices [31]. Endometrial blood ow was negatively affected by serum oes-
tradiol concentration on the day of hCG. Indeed, endometrial and subendometrial 3D Doppler ow indices in the stimulated cycles were signicantly lower than those in the natural cycles of the same patients undergoing IVF treatment [32].
3 Two-Dimensional andThree-Dimensional Doppler inReproductive Medicine
51
Uterine PI, uterine RI and endometrial and subendometrial 3D Doppler ow indices were comparable between the non-pregnant and preg­nant groups in frozen-thawed embryo transfer cycles using natural or clomiphene-induced cycles [33]. On the other hand, endometrial and subendometrial blood ow was signicantly higher in pregnant patients with livebirth follow­ing IVF and frozen-thawed embryo transfer treat­ment [34].
Mercè et al. [35] found that endometrial 3D power Doppler ow indices were statistically sig­nicantly higher in the pregnant group. The area under ROC curve was statistically signicant for endometrial VI, FI and VFI when no grade 1 embryos or only one was transferred but not when two or three grade 1 embryos were transferred.
The pregnancy outcomes of women who had 3D power Doppler study of the endometrial and subendometrial regions on the day of oocyte retrieval in stimulated IVF cycles or on luteiniz­ing hormone surge +1 day in frozen-thawed embryo transfer cycles were compared. Women in the pregnancy-induced hypertension (PIH) or small for gestational age (SGA) foetuses group had signicantly lower endometrial VI (0.504 vs
1.051; P = 0.023) and VFI (0.121 vs 0.253; P=0.023) than those in the non-PIH/SGA group [36]. The endometrial blood ow may have an impact on the placental development when preg­nant and gives insight into a potential novel screening tool for assessing the risk of PIH or SGA in women undergoing IVF.
Changes inEndometrial andSubendometrial Blood Flow
Ultrasound examination was performed on the day of hCG [27, 35], oocyte retrieval [28–30] and blastocyst transfer [18]. There is no consensus when the ultrasound examination for assessing endometrial receptivity in IVF treatment should be done. The day of the ultrasound examination in these studies was chosen for logistic reasons.
Raine-Fenning et al. [37] showed that endo­metrial and subendometrial blood ow by 3D ultrasound increased during the proliferative
phase, peaking around 3days prior to ovulation before decreasing to a nadir 5days post- ovulation. Hypoxia in the endometrium plays a benecial role for implantation as the expression of vascu­lar endothelial growth factor is upregulated by hypoxia [38], and relatively low oxygen tension was present around the blastocyst during the time of implantation [39].
Endometrial and subendometrial blood ow was measured on the days of hCG and ET [40]. Patients in non-pregnant and pregnant groups had comparable 3D Doppler ow indices of endome­trial and subendometrial regions measured on either day. Percentage changes in endometrial and subendometrial 3D Doppler ow indices between these 2 days were also similar. Again, none of the ultrasound parameters was predictive of pregnancy in a multiple logistic regression analysis and the ROC curve analysis.
Prediction ofOvarian Response toGonadotrophin
The development of multiple follicles in response to ovarian stimulation is the key factor leading to a successful outcome of IVF treatment. Poor ovarian response is associated with lower preg­nancy rates, while exaggerated ovarian response leads to an increased risk of ovarian hyperstimu­lation syndrome. Prediction of ovarian responses prior to gonadotrophin stimulation is useful in counselling patients and helpful in tailoring the dosage of gonadotrophin to individual patients.
A number of ultrasound parameters have been examined to predict the ovarian response to gonadotrophins, including ovarian volume, antral follicle count (AFC) and ovarian stromal blood ow [15, 41–44].
Folliculogenesis in the human ovary is a com­plex process regulated by a variety of endocrine and paracrine signals [45]. It has been suggested that the availability of an adequate vascular sup­ply to provide endocrine and paracrine signals may play a key role in the regulation of follicle growth [46]. Increased ovarian stromal blood ow may lead to a greater delivery of gonadotro­phins to the granulosa cells of the developing follicles.
52
E. H. Y. Ng

Ovarian Stromal Blood Flow by 2D Doppler

Ovarian stromal blood ow can be assessed by colour Doppler and power Doppler ultrasound. Power Doppler is better suited to the study of the ovarian stromal blood ow as it is more sensitive to lower velocities and essentially angle­independent [11, 47]. Flow velocity waveforms were obtained from stromal blood vessels away from the ovarian capsule, if present. The ‘gate’ of the Doppler was positioned when the vessel with good colour signals was identied on the screen. PI, RI and peak systolic blood ow velocity (PSV) of stromal vessels were calculated elec­tronically when three similar, consecutive wave­forms of good quality were obtained.
Zaidi et al. [48] showed that mean ovarian stromal PSV prior to pituitary downregulation was signicantly correlated with the number of follicles, after controlling for patients’ age. Patients with >6 follicles at retrieval had signi­cantly higher velocity than those with <6 follicles (10.2 ± 5.8 cm/s vs 5.2 ± 4.2 cm/s). Similarly, Engmann et al. [41] demonstrated that ovarian stromal PSV after pituitary downregulation was the most important independent predictor of the number of oocytes obtained in patients with nor­mal basal FSH concentration, when compared with age of women, basal FSH concentration, E2 concentration or FSH/LH ratio. Bassil etal. [49] reported that women with RI of ovarian blood ow >0.56 had a signicantly longer stimulation and a signicantly lower mean number of oocytes retrieved. Both BMI and AFC were not included in these three studies.
Popovic-Todorovic etal. [44] evaluated ovar­ian stromal blood by 2D power Doppler ultra­sound, and a semi-quantitative score was allocated to each ovary according to the number and area of the power Doppler signals. Total Doppler score was the sum of scores for each ovary: score 1 for poor ow, score 2 for moderate ow and score 3 for good ow. The number of oocytes was predicted by AFC, total Doppler score, serum testosterone concentration and smoking status.
In a prospective study, 136 women aged <40years with basal FSH concentration <10IU/L received a standard regimen of ovarian stimulation in their rst IVF cycle [50]. The ovarian stromal blood ow measured by 2D power Doppler was compared to age of women, body mass index, basal FSH concentration and AFC in the predic­tion of the ovarian response. Basal FSH concentra­tion achieved the best predictive value in relation to the number of oocytes obtained, followed by AFC and BMI.AFC was the only predictive factor of serum oestradiol concentration on the day of HCG, while BMI was predictive of the gonadotro­phin dosage. Ovarian stromal blood ow indices measured by power Doppler ultrasound had no predictive value for the ovarian response.

Ovarian Stromal Blood Flow by 3D Doppler

I further evaluated the role of ovarian stromal blood ow by 3D power Doppler. Age of women, BMI, basal FSH concentration, AFC and ovarian stromal vascularity indices measured by 3D power Doppler were compared in 111 women aged <40years old with basal FSH concentration <10IU/L in their rst IVF cycle [51]. The results indicated that AFC achieved the best predictive value in relation to the number of oocytes obtained, followed by age of women and BMI.Basal FSH concentration was the only pre­dictive factor for the duration and dosage of gonadotrophin used. Mean ovarian 3D power Doppler ow indices were not predictive of preg­nancy in a multiple logistic regression analysis.
Therefore, ovarian stromal blood ow mea­sured after pituitary downregulation by both 2D and 3D power Doppler was not predictive of the ovarian response in terms of the number of oocytes obtained, the duration and dose of FSH used and maximum serum E2 concentrations. These results were in line with those of previous studies assessing ovarian stromal blood ow in fertile Chinese women [52, 53]. There was no effect of age on mean PSV of ovarian stromal blood vessels determined by 2D colour Doppler
3 Two-Dimensional andThree-Dimensional Doppler inReproductive Medicine
53
ultrasound. Using 3D Doppler ultrasound, ovar­ian stromal vascularity was signicantly lower in fertile Chinese women aged ≥41years, and the rate of decline of total ovarian vascularity index was only 0.18% per year [53]. These data strongly suggest that reduction in ovarian stromal blood ow with increasing age is a relatively late phe­nomenon and ovarian stromal blood ow is unlikely an early marker for ovarian response.

Conclusion

Ultrasound examination is a noninvasive method to evaluate the endometrium during IVF.Doppler ow of uterine vessels measured by 2D ultrasound has a high negative predictive value and sensitivity (in the ranges of 88–100% and 96–100%, respec­tively) and a relatively higher range of positive predictive value and specicity (44–56% and 13–35%, respectively) when compared with endo­metrial thickness and pattern. Doppler study of uterine arteries measured by 2D ultrasound does not reect the blood ow to the endometrium mea­sured by 3D ultrasound with power Doppler. Conicting results are reported with regard to their role in the prediction of pregnancy in IVF.
Furthermore, endometrial and subendometrial blood ow measured by 3D ultrasound on the days of hCG and embryo transfer and the per­centage change in these parameters between these 2days were not predictive of pregnancy in IVF. On the other hand, the endometrial blood ow may give insight into a potential novel screening tool for assessing the risk of pregnancy induced hypertension or small for gestational age in women undergoing IVF. Ovarian stromal blood ow measured by 2D and 3D power Doppler ultrasound had no predictive value for the ovarian response during IVF.

References

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16. Yuval Y, Lipitz S, Dor J, Achiron R.The relationship between endometrial thickness, and blood ow and pregnancy rates in in-vitro fertilization. Hum Reprod. 1999;14:1067–71.
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23. Pairleitner H, Steiner H, Hasenoehrl G, Staudach A. Three-dimensional power Doppler sonography: imaging and quantifying blood ow and vasculariza­tion. Ultrasound Obstet Gynecol. 1999;14:139–43.
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26. Schild RL, Holthanus S, Alquen JD, Fimmers R, Dorn C, van der Ven H, Hansmann M.Quantitative assessment of subendometrial blood ow by three­dimensional- ultrasound is an important predictive factor of implantation in an in-vitro fertilization pro­gramme. Hum Reprod. 2000;15:89–94.
27. Wu HM, Chiang CH, Huang HY, Chao AS, Wang HS, Soong YK.Detection of the subendometrial vascular­ization ow index by three-dimensional ultrasound may be useful for predicting the pregnancy rate for
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28. Dorn C, Reinsberg J, Willeke C, Wendt A, van der Ven H, Schild RL.Three-dimensional power Doppler ultrasound of the subendometrial blood ow under the administration of a contrast agent (Levovist). Arch Gynecol Obstet. 2004;270:94–8.
29. Järvelä IY, Sladkevicius P, Kelly S, Ojha K, Campbell S, Nargund G.Evaluation of endometrial receptivity during in-vitro fertilization using three- dimensional power Doppler ultrasound. Ultrasound Obstet Gynecol. 2005;26:765–9.
30. Ng EHY, Chan CCW, Tang OS, Yeung WSB, Ho PC. The role of endometrial and subendometrial blood ow measured by three-dimensional power Doppler ultrasound in the prediction of pregnancy during in vitro fertilization treatment. Hum Reprod. 2006;21:164–70.
31. Ng EHY, Chan CCW, Tang OS, Yeung WSB, Ho PC.Factors affecting endometrial and subendometrial blood ow measured by three-dimensional power Doppler ultrasound during invitro fertilization treat­ment. Hum Reprod. 2006;21:1062–9.
32. Ng EHY, Chan CCW, Tang OS, Yeung WSB, Ho PC. Comparison of endometrial and subendome­trial blood ow measured by three-dimensional power Doppler ultrasound between stimulated and natural cycles in the same patients. Hum Reprod. 2004;19:2385–90.
33. Ng EHY, Chan CCW, Tang OS, Yeung WSB, Ho PC. The role of endometrial and subendometrial vascularity measured by three-dimensional power Doppler ultrasound in the prediction of pregnancy during frozen-thawed embryo transfer cycles. Hum Reprod. 2006;21:1612–7.
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Part III
Ultrasound of the Ovary
The Normal Ovary: Changes intheMenstrual Cycle
RenatoBauman andUrsulaResMuravec
4

Transabdominal Ultrasound

The ovaries can be displayed along with the uter­ine body in transverse plane if they are not too distant from the uterus. According to the position of the ovaries that in normal circumstances can be variable, there is a real possibility that both ovaries could not be seen on the scan in the same time/image. In this situation in order to detect the second ovary, the examiner should move the probe cranially or caudally. If the ovary is located more cranially and near the pelvic wall, there is a realistic possibility that this ovary could be cov­ered by the intestine, and so it could not be visu­alized and examined. The same is the situation with small postmenopausal ovaries that due to the size often cannot be distinguished from the intestines.
Full bowel loops can be misdiagnosed as an ovary, but if the examiner is patient enough to wait the peristaltic wave, it will solve the prob­lem; otherwise the examiner has to verify the position of the iliac vessels in order to longitudi­nally nd the position of the ovary.
R. Bauman (*) Rotunda IVF, The National Fertility Centre, The Rotunda Hospital, Dublin, Ireland
U. R. Muravec Medical Center Dravlje, Department for Infertility, Ljubljana, Slovenia

Transvaginal Ultrasound

Alfred Kratochwil is considered to be the father of transvaginal ultrasound. He described in 1969 his experience with the new endovaginal sonography technique using the probe attached to the colposcope [1]. Due to the low quality of the obtained images, the technique was abandoned until the mid-1980s when the rst endovaginal probe with the visible angle of 240° that allowed panoramic view of the genital organs was put in market. The rst meeting about endovaginal ultrasound was organized in Hamburg, Germany, in 1985, by L. Popp [2]. First accepted with skepticism, the new technique was quickly adopted in the majority of sonography cen­ters, rst in Germany and then all over the world. Because of numerous advantages in pelvic sonogra­phy, the endovaginal technique today is essential for quality examination of the female pelvis.
Ovaries can be visualized with the probe moved laterally of the uterus toward the pelvic wall in the longitudinal or sagittal section. Ovaries have ellipsoid shape, with relatively hypoecho­genic structure and homogenic echotexture, and often are positioned near the iliac blood vessels (Fig. 4.1). Using probes with the wide angle of insonation, it is possible to visualize in the same frontal section of both ovaries if they are posi­tioned in the same plane. Regularly each ovary is visualized separately. In order to compare the ovaries, it is useful to divide the image in two parts and then visualize both ovaries (Fig.4.2).
© Springer Nature Switzerland AG 2019 L. A. Stadtmauer, I. Tur-Kaspa (eds.), Ultrasound Imaging in Reproductive Medicine,
https://doi.org/10.1007/978-3-030-16699-1_4
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