Scholarly article on topic 'The usefulness of endometrial thickness, morphology and vasculature by 2D Doppler ultrasound in prediction of pregnancy in IVF/ICSI cycles'

The usefulness of endometrial thickness, morphology and vasculature by 2D Doppler ultrasound in prediction of pregnancy in IVF/ICSI cycles Academic research paper on "Veterinary science"

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{Doppler / "Endometrial thickness" / Morphology / Vasculature / IVF/ICSI}

Abstract of research paper on Veterinary science, author of scientific article — Moustafa Abdel Kader, Ayman Abdelmeged, Ahmad Mahran, Manal F. Abu Samra, Haitham Bahaa

Abstract Objective The aim of this study was to assess the predictive value of endometrial thickness, morphology and vasculature using two-dimensional (2D) Doppler ultrasound on the IVF/ICSI cycle outcome. Subjects and methods Endometrial thickness, morphology and subendometrial blood flow were assessed using transvaginal ultrasound on the day of hCG in 100 patients undergoing IVF/ICSI treatment in the period between June 2013 and January 2015. Statistical analysis was done. Results There was no difference in the demographic features or details of ovarian stimulation between pregnant and non-pregnant women. Overall, 40 patients conceived; 23 (57.5%) of them had blood flow in zone III and 15 (37.5%) in zone II. All patients achieved pregnancy had endometrial thickness >8mm. Using the ROC curve, the cutoff endometrial thickness for non-achieving pregnancy was 7mm with a sensitivity and specificity of 100%. There was no significant difference in Doppler indices between pregnant and non-pregnant women. Conclusion When the endometrial thickness is <8mm, and if there are non-triple endometrial line and non-favorable blood flow zone on day of hCG in IVF/ICSI cycles, pregnancy is unlikely and embryo transfer should be canceled with freezing of all embryos for future transfer to increase the success rate.

Academic research paper on topic "The usefulness of endometrial thickness, morphology and vasculature by 2D Doppler ultrasound in prediction of pregnancy in IVF/ICSI cycles"

The Egyptian Journal of Radiology and Nuclear Medicine (2015) xxx, xxx-xxx

Egyptian Society of Radiology and Nuclear Medicine The Egyptian Journal of Radiology and Nuclear Medicine

www.elsevier.com/locate/ejrnm www.sciencedirect.com

ORIGINAL ARTICLE

The usefulness of endometrial thickness, morphology and vasculature by 2D Doppler ultrasound in prediction of pregnancy in IVF/ICSI cycles

Moustafa Abdel Kader a,% Ayman Abdelmegedb, Ahmad Mahranb, Manal F. Abu Samraa, Haitham Bahaab

a Radiodiagnosis Department, Faculty of Medicine, El-Minia University, Egypt b Obstetrics and Gynaecology Department, Faculty of Medicine, El-Minia University, Egypt

Received 30 July 2015; accepted 24 August 2015 Available online xxxx

KEYWORDS

Doppler;

Endometrial thickness; Morphology; Vasculature; IVF/ICSI

Abstract Objective: The aim of this study was to assess the predictive value of endometrial thickness, morphology and vasculature using two-dimensional (2D) Doppler ultrasound on the IVF/ICSI cycle outcome.

Subjects and methods: Endometrial thickness, morphology and subendometrial blood flow were assessed using transvaginal ultrasound on the day of hCG in 100 patients undergoing IVF/ICSI treatment in the period between June 2013 and January 2015. Statistical analysis was done. Results: There was no difference in the demographic features or details of ovarian stimulation between pregnant and non-pregnant women. Overall, 40 patients conceived; 23 (57.5%) of them had blood flow in zone III and 15 (37.5%) in zone II. All patients achieved pregnancy had endometrial thickness >8 mm. Using the ROC curve, the cutoff endometrial thickness for non-achieving pregnancy was 7 mm with a sensitivity and specificity of 100%. There was no significant difference in Doppler indices between pregnant and non-pregnant women.

Conclusion: When the endometrial thickness is <8 mm, and if there are non-triple endometrial line and non-favorable blood flow zone on day of hCG in IVF/ICSI cycles, pregnancy is unlikely and embryo transfer should be canceled with freezing of all embryos for future transfer to increase the success rate.

© 2015 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-

nd/4.0/).

* Corresponding author at: El-Minia University, El Minia, Egypt. Tel.: +20 01123850453.

E-mail address: Moustafa18_1970@yahoo.com (M. Abdel Kader). Peer review under responsibility of Egyptian Society of Radiology and Nuclear Medicine.

1. Introduction

Successful implantation requires good harmony between the endometrium and blastocyst (1). Ultrasound examination of

http://dx.doi.org/10.1016/j.ejrnm.2015.08.014

0378-603X © 2015 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

the endometrium is a commonly used non-invasive tool to assess endometrial receptivity during IVF treatment. A good blood supply to the endometrium is an essential requirement for implantation and assessment of endometrial blood flow in IVF treatment has attracted a lot of attention in recent years (2).

Doppler study of uterine arteries does not reflect the actual blood flow to the endometrium. Endometrial and sub-endometrial blood flows can be more objectively and reliably measured with three-dimensional power Doppler ultrasound. However, their role in the prediction of pregnancy in IVF treatment reported a conflicting result (3,4).

The study of endometrial thickness, pattern, volume, Dop-pler and sub-endometrial blood flow by ultrasound has been used to assess endometrial receptivity during IVF treatment. The measurement of endometrial blood flow as a physiologic dimension in addition to the anatomic parameters gained by the ultrasound had played an important role in the expectation of pregnancy outcome in IVF/ICSI cycles (1,4,5). So, endome-trial receptivity is essential to implantation of an embryo and ultrasound has been developed as a valuable method in evaluation of endometrial preparation before embryo transfer in fresh IVF cycles (6).

This study aimed to assess the role of measurement of the endometrial thickness, morphology and sub-endometrial blood flows by 2D power Doppler ultrasound in prediction of pregnancy in IVF/ICSI cycles.

2. Patients and methods

This study is a prospective observational study including 100 women undergoing IVF/ICSI treatment at a University based IVF center. The ethical approval for the study was obtained from the institute's ethical committee. All the patients gave a written informed consent before enrollment in the study. The inclusion criteria of the study were as follow: (a) age between 20 and 39 years and (b) IVF/ICSI treatment due to many factors including tubal, male, PCOS or other unexplained factors. We excluded (a) patients under 20 years or above 39 years and (b) patients who were unable to give a written informed consent.

The down-regulation protocol and the dose of gonadotro-phin used were determined by patient's age, ovarian reserve tests and prior response to ovarian stimulation as per unit protocol. Folliculometry was performed using transvaginal ultrasound scan starting from day six of stimulation and every other day afterwards till the day of hCG.

One expert radiologist evaluated each patient on day of hCG using 2D transvaginal ultrasound machine (Logiq P5, GE Medical Systems, Korea) with 7.5-9 MHz-convex array transducer as follows:

1. We use the gray scale function of the ultrasound machine to study and measure the endometrial thickness as the thickest part of the endometrium between the highly reflective echo-genic lines in the true longitudinal scan of the uterus.

2. In this true longitudinal scan of the uterus, we note the endometrial pattern as either triple-line (described as hypoechoic endometrium surrounded by hyperechoic zones) or non-triple-line.

3. After then, we activate the Doppler function of the ultrasound machine to evaluate the endo-subendometrial blood flow or vascularization and is either, zone I in which the

blood flow reached only subendometrial region, zone II in which the blood flow reached the outer hyper-echoic region or zone III in which the blood flow reached the inner hypo-echoic zone. 4. To evaluate the Doppler indices of the endometrial vascu-lature, we activate the pulsed power Doppler function of the machine and applied the Doppler gate over the appropriate color area then tried to have five or more consecutive waveforms for the study to be satisfactory (each wave represented maximum Doppler shift). Then we measure the resistive index = Peak systolic velocities - Peak diastolic velocities/Peak systolic velocities and standard of deviation ratio (S/D ratio) was calculated on three consecutive uniform waveforms.

Then we give 10,000 hCG IU intramuscular when there were minimum of three mature follicles measuring 17-18 mm in dimensions and after 36 h the ovum was picked up under intra-venous sedation. Two or three embryos were placed inside the uterine cavity of the patient on days 4-5 after the retrieval and good quality embryos were frozen. On the luteal phase we gave 800 microgram of micronized progesterone vaginally from day of embryo-transfer (ET) till 12 weeks of pregnancy. A serum pregnancy test was done two weeks after embryo transfer.

2.1. Study outcome

The primary outcome of the study was clinical pregnancy rate that defined as the presence of one or more gestational sac by ultrasound scan two weeks after a positive serum pregnancy test.

- The secondary outcome of the study was endometrial thickness and sub-endometrial blood flow.

2.2. Statistical analysis

Statistical analysis was performed using the Statistical Package for Social Science (SPSS Inc, Chicago) version 21 for Microsoft Windows. Data were described in terms of mean ± SEM (standard error of the mean) for continuous variables and frequencies (number of cases) and percentages for categorical data. Independent Student's t-test was used to compare quantitative variables and Chi square test was used to compare categorical data. A P value <0.05% was considered significant. The receptor operating characteristic (ROC) curve analysis was performed to determine the best predictive values.

3. Results

The current study included 100 patients who underwent IVF/ ICSI treatment. Pregnancy was achieved in forty patients. There was no difference in the demographic features, hormonal milieu, and ovarian response between pregnant and non-pregnant women as shown in Table 1.

There was no statistically significant difference in the Doppler indices of the sub-endometrial blood vessels between pregnant and non-pregnant women as shown in Table 2.

Table 1 Demographic characteristics and details of controlled stimulation cycles in the pregnant and non-pregnant women.

Pregnant Non-pregnant P

(n = 40) (n = 60) value

Age (years) 30.6 ± 2.1 28.2 ± 1.8 0.9

BMI (kg/m2) 29.2 ± 0.5 28.8 ± 0.4 0.5

Duration of infertility (years) 9.1 ± 1.3 8.5 ± 0.7 0.7

Cause of infertility 0.8

Male factor 17 (42.5%) 24 (40%)

Tubal factor 8 (20%) 11 (18.3%)

Endometriosis 2 (5%) 4 (6.7%)

Unexplained 10 (25%) 16(26.7%)

Anovulation 2 (5%) 3 (5%)

Combined 1 (2.5%) 2 (3.3%)

Basal FSH (IU/L) 6.7 ± 0.5 6.4 ± 0.5 0.6

Basal LH (IU/L) 4.2 ± 0.3 4.7 ± 0.5 0.7

Basal AMH (ng/ml) 2.3 ± 0.3 2.9 ± 0.3 0.9

AFC 12.8 ± 1.1 13.9 ± 1.1 0.5

Down-regulation protocol 0.9

Long protocol (%) 21 (52.5%) 32 (78%)

Short protocol (%) 16 40%) 15 (25%)

Antagonist (%) 3 (7.5%) 3 (2%)

Total HMG dose (IU) 3365.4 ± 147 341.3 ± 186.7 0.8

Duration of stimulation 11.3 ± 0.8 11.1 ± 0.9 0.9

(days)

Pre-ovulatory follicle (n) 13.1 ± 2.6 13.3 ± 2.5 0.9

Retrieved oocytes (n) 12.9 ± 1.6 11.6 ± 1.6 0.8

Mature oocytes (n) 10.5 ± 0.7 10.2 ± 0.8 0.5

Total no. of embryos 8.9 ± 1.3 8.8 ± 1.5 0.7

Embryo transferred (n) 2.5 ± 0.5 2.5 ± 0.6 0.5

Grade A embryo transferred 2.3 ± 0.4 2.4 ± 0.4 0.6

Fertilization rate (%) 84.7 ± 2.5 86.3 ± 4.6 0.7

Cleavage rate (%) 94.5 ± 0.6 94.7 ± 0.5 0.9

Data are presented as mean ± SEM or number (%). FSH = follicle stimulating hormone, LH = luteinizing hormone, AMH = anti-MUllerian hormone, AFC = antral follicle count.

Table 2 Doppler indices and pregnancies.

Pregnant Non-pregnant P

(n = 40) (n = 60) value

Resistance index 0.93 ± 0.69 0.93 ± 0.86 0.2 (RI)

Pulsatility index 1.06 ± 0.54 1.06 ± 0.99 0.1 (PI)

S/D ratio 18.4 ± 6.2 9.9 ± 4.3 0.7

Table 3 Endometrial blood flow zone and pregnancies.

Endometrial No. of cases No. of pregnancies Percentage blood flow (n = 100) (n = 40) (%)

Zone I 21 2 5

Zone II 37 15 37.5

Zone III 42 23 57.5

Table 4 Endometrial thickness and number of pregnancies.

Endometrial No. of cases No. of pregnancies Percentage

thickness (n = = 100) (n = 40) (%)

<8 mm 4 0 0

8-10 mm 41 20 50

10-12 mm 25 10 25

12-14 mm 20 9 22.5

>14 mm 10 1 2.5

ROC Curve

o.o H-S-1-1-1-

0.0 0.2 0.4 0.6 0.8 1.0

1 - Specificity

Diagonal segments are produced by ties.

Fig. 1 A receiver operating characteristic (ROC) curve for pregnancy in relation to endometrial thickness. The cutoff endometrial thickness for no pregnancy in IVF/ICSI was 7 mm. Area under the curve = 0.516.

There was a direct correlation between endometrial blood flow and IVF/ICSI cycle outcome as more pregnancies were achieved when endometrial blood flow was in zone III (57.5%) as compared with 37.5% and 5% when the blood flow was in zone II and zone I respectively. These results are shown in Table 3.

Endometrial thickness was found to be strongly correlated with successful pregnancy in IVF/ICSI cycles. No pregnancies were achieved when endometrial thickness was less than 8 mm (Table 4). Regarding endometrial morphology, all cases who achieved pregnancies had a triple-line pattern of the endome-

trium on day of hCG. In eight cases, there was gapping between the endometrium and fluid inside. None of these cases achieved pregnancy.

The receiver operating characteristic (ROC) curve was used to determine the cutoff endometrial thickness for no pregnancy in IVF/ICSI cycle. Using a cutoff level of 7 mm the sensitivity and specificity achieved 100% (Fig. 1).

4. Discussion

The assessment of the endometrial receptivity is mandatory for the success of all IVF/ICSI procedures. Angiogenesis plays important role in various female reproductive processes as maturation of dominant follicle, endometrial growth and implantation process (7-9). Here, there was no difference in the demographic features or details of ovarian stimulation between pregnant and non-pregnant women.

In this study, there were no statistically significant differences in the Doppler indices of sub-endometrial blood vessels between pregnant and non-pregnant women. Raine-Fenning et al. (2004a) stated that endometrial and subendometrial blood flows by ultrasound increased during the proliferative phase, peaking around 3 days prior to ovulation then decreased 5 days post-ovulation. Therefore, there was a period of relatively reduced perfusion in the immediate post-ovulatory period, extending to the implantation period in spontaneous cycles (10). Ernest Hung et al. (2006) concluded

that endometrial and sub-endometrial blood flows were not good predictors of pregnancy if they were measured at one time-point during IVF treatment (5). This debate suggests that further longitudinal studies in the late follicular phase and early luteal phase are needed to reach a firm conclusion. So, we suggest that the endometrial and subendometrial S/D, RI and PI could not be used alone to predict endometrial receptivity.

In this study, the endometrial thickness was found to be strongly correlated with successful pregnancy in IVF/ICSI cycles. The most suitable endometrial thickness for pregnancy was 8-10 mm (50% of them achieved pregnancy), followed by endometrial thickness of 10-12 mm (25% of them achieved pregnancy). The least of them is when the endometrial thickness is more than 14 mm (only 2.5% of them achieved pregnancy). No pregnancies were achieved when endometrial thickness was less than 8 mm. According to the ROC curve results, a cutoff value for non-occurrence of pregnancy was 7 mm. Singh et al. (2011) reported that, largest number of pregnancies occurred when the endometrial thickness is 810 mm. He also, postulated that no pregnancies reported when endometrial thickness is less than 5.8 mm (1). Weissman et al. (1999) reported the lowest percentage of conception when endometrial thickness is more than 14 mm (11) (Fig. 1).

Fig. 3 Represented the Doppler ultrasound of the endometrial-subendometrial vessels that reached zone II in a non-fertile female (A) and zone III in a fertile female (B). The arrow in A and B referred to the inner extension of the Doppler flow.

Fig. 2 29-year old female with primary infertility underwent ovarian stimulation protocol revealed the following: (A) the endometrial and sub-endometrial blood flow reached zone III; (B) Represented the Doppler ultrasound velocimetry of the endome-trial vessels in a fertile female.

In our research, all cases who achieved pregnancy had a triple-line pattern of the endometrium on day of hCG. In eight cases, there was gapping between the endometrium and fluid inside, and none of these cases achieved pregnancy. El-Zenneni et al. (2014) stated that the triple layer endometrial pattern was the most suitable for conception (12). Singh et al. (2011) proved that the triple layer endometrium was good prognostic factor for occurrence of pregnancy (1). Jarvela et al. (2005) considered the endometrial thickness and morphology correlated to IVF/ET outcomes, as 44.8% of their patients with triple line pattern before hCG injection achieved pregnancy; 80% of patients with triple-line pattern on the day of ovum collection achieved pregnancy (13). Contrary to our research results, Ng et al. (2006), reported, no relationship between endometrial thickness, morphology and pregnancy outcomes (14) (Fig. 4).

Regarding the endometrial blood flow zones, in this study, 57.5% of the pregnant women had zone III of endometrial blood flow, 37.5% had zone II of blood flow while only 5% of the pregnant women had zone I of blood flow. Ng et al. (2006) found that the endometrial and subendometrial blood flow was not a good predictor of pregnancy (15). In this study, the clinical pregnancy rate reached 40%. Other investigators stated that the clinical pregnancy rate was 26.73% and noted a higher pregnancy rate when the blood flow to the endome-

trium was in zone III (51.8%) compared to (14.8%) when in zone I (16,17). Dechaud et al. (2008), considered that, the endometrial pattern, thickness and end-diastolic blood flow were shown to be the most effective combination for the evaluation of uterine receptivity (18) (Figs. 2 and 3).

Wang et al. (2010) and Nygren et al. (2011), had suggested positive correlation of the endometrial and subendometrial blood flows to the outcome of IVF/ET (19,20) while Aghahoseini et al. (2008) had suggested negative correlation (21).

Divya Sardana et al. (2014), suggested that a combination of endometrial thickness and Doppler analysis of endometrial blood flow was a simple and effective tool to improve the outcome of IVF/ET and should be incorporated into routine clinical practice (22). This was suggested by our study results in addition to the endometrial pattern.

5. Conclusion

With endometrial thickness less than 8 mm and no-triple-line pattern on hCG day in IVF/ICSI cycles, there is a poor chance of achieving pregnancy. Average endometrial line thickness of 8-12 mm and triple line (good morphologic texture) are good prognostic values if good quality embryos are transferred. The

Fig. 4 This figure represented different endometrial patterns and responding ovary, (A): Represented the triple-line pattern (arrows). (B): Showed the non-triple-line endometrial pattern in 30-year old non-fertile female (star). (C): Represented a fluid within the endometrial cavity in 29-year-old female with secondary infertility. (D): Showed the enlarged ovary with multiple mature follicles and related pelvic collection (star) in a fertile female.

endometrial blood flow is used as a predictor for implantation rate in IVF/ICSI cycles.

Conflict of interest

All authors have materially participated in the research preparation and agreed for the submission.

We have no conflict of interest to declare.

Disclosure of funding

No disclosure of funding received for this work from any organization.

All authors have appraised the article and actively contributed to the work.

Moustafa Abdel Kader: Data collection, revision and final editing.

Ayman Abdelmeged: Data collection and revision.

Ahmad Mahran: Data collection, statistical performance and revision.

Manal F. Abu Samra: Final editing and revision.

Haitham Bahaa: Data collection and follow-up.

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