Investigating the Effect of Endometrial Thickness Changes and Compaction on the Fertility Rate of Patients Undergoing ART: A Prospective Study

Background Today, the thickness of the endometrium as a key factor plays an important role in pregnancy outcomes of infertile patients. Based on this, it has been shown that endometrial compaction affects fertility success in patients. In this study, the impact of endometrial compaction on pregnancy outcomes (assisted reproductive technology) has been evaluated.

This prospective cohort study included 253 patients undergoing embryo transfer, who referred to the infertility center of Shariati Hospital in Tehran during 2021–2022. They were examined from the point of relationship between endometrial thickness changes and fertility rate in frozen embryo transfer and fresh cycles. After preparing the endometrium, the thickness was evaluated using ultrasound.

The results showed that the percentage of chemical and clinical pregnancy in the compact group was higher compared to the non-compact one, which was statistically significant (p < 0.05). The rate of pregnancy in four groups of 5, 10, 15, and %20 compaction was 77(30.4%), 49(19.4%), 28(11.1%), and 14(5.5%), respectively.

Finally, endometrial compaction can be associated with an increase in chemical and clinical pregnancy rate in infertile patients. In addition, secondary thickness has predictive value for clinical pregnancy.

Endometrial thickness, Fertility rate, Assisted reproductive technology

Infertility is one of the disorders that affects many couples of the reproductive age. Today, the use of assisted reproductive technology (ART) to treat infertile patients has expanded [1]. In order to increase the success rate of ART, many researches are being conducted. Endometrial characteristics are one of the main factors that can affect the ART success. Previous studies have been shown that there is a direct relationship between the thickness of the endometrium and the fertility rate using ART [2, 3]. Based on this, an endometrium thickness of less than 7 mm is considered a thin endometrium, which can be associated with adverse perinatal outcomes, miscarriage, or abnormal placentation. Currently, most studies have observed that thin endometrium has an adverse effect on pregnancy outcome during in vitro fertilization (IVF) treatment, even though its specific mechanism is not well understood [4–6]. The results of published studies that evaluated the effect of endometrial thickness on the favorable outcomes of ART patients are completely heterogeneous. Some studies have observed a decrease in pregnancy and live birth rate in relation to low endometrial thickness [7–11]. But other studies have not observed any similar relationships [12]. There are only a few studies that have evaluated the effect of endometrial thickness on frozen embryo transfer (FET) cycles. Therefore, this study was designed according to the mentioned points and many uncertainties. The present study also investigates the relationship between the thickness of the endometrium and its compaction with the fertility rate after embryo transfer; we hope that our findings help to remove obstacles to successful reproduction and increase the chance of live birth in patients using assisted reproduction methods.

and Method The studied population in this prospective cohort was 253 patients undergoing embryo transfer, who referred to the infertility center of Shariati Hospital in Tehran during 2021–2022. They were examined from the point of relationship between endometrial thickness changes and fertility rates in FET and fresh cycles. All referred patients were entered into the study, provided they met the entry criteria, and consented to participate until the desired sample size was reached. Inclusion and Exclusion Criteria Inclusion criteria were patient satisfaction, the age range of 18–40 years, individuals with single blastocyst transfer, the endometrial pattern of A/B on the day of progesterone administration, and pattern C on the day of embryo transfer. Exclusion criteria included the mother suffering from high blood pressure, diabetes, and anatomical problems of the uterus and the impossibility of measuring the thickness of the endometrium in ultrasound evaluation, low-quality embryos (blastocyst score less than 3 BC according to the Gardner system) [13], and patients with thin endometrial thickness (< 7 mm per day of progesterone administration). Primary Outcome Ongoing pregnancy was defined as the live birth or the activity of the fetal heart in transvaginal ultrasound at or after 12 weeks of gestation. Endometrial Preparation and Patient Follow-Up Endometrial preparation included administration of estrogen/progesterone (EP) and natural cycle (NC). In patients under hormone therapy, the protocol started with exogenous E2 on day 2–3 of the normal cycle, or GnRH agonist was started in the previous luteal phase and exogenous E2 on day 2–3 of the next cycle. Patients with endometriosis were generally treated with depot leuprolide acetate with estrogen and progesterone for at least 2 months before embryo transfer (ET). In all cases, patients were given oral or vaginal administration (as determined by the physician) of 2 mg of micronized E2 twice daily, which was increased to 4 mg twice daily after 5 days [13]. Ultrasound measurement of endometrial thickness was done 10 days after the start of E2 to measure the thickness and pattern of the endometrium. A higher thickness equal to 7 mm and a trilaminar pattern of the endometrium were considered sufficient to start progesterone administration. If it was insufficient, estrogen administration was continued and serial ultrasound evaluation was performed until the adequate endometrium was observed. Patients with endometrial thickness less than 7 mm were canceled and excluded from the analysis. The patients started progesterone injection (50 mg daily intramuscularly) or vaginal progesterone inside the body (for patients in normal cycle, injectable progesterone (40 mg) was prescribed on the day of ovulation) when the thickness of the endometrium reached greater than or equal to 7 mm. The measured thickness of the endometrium was recorded on this day, and then, the embryos were weighed and transferred on day 6 of progesterone administration [13]. On the day of embryo transfer under ultrasound guidance, the ultrasound technician measured the thickness of the endometrium vaginally and recorded the endometrial images. All blastocysts were evaluated before embryo transfer by an experienced embryologist using the grading system proposed by Gardner [14]. Each embryo was also graded according to the Society for Assisted Reproductive Technology simplified grading system proposed by Heitmann et al. [15]. To measure the thickness of the endometrium on the day of embryo transfer, the ultrasound images taken by the ultrasound technician were retrieved using the imaging software, and the best image showing the longitudinal section of the endometrium including the cervical canal was measured. In cases where the image did not include the cervical canal or the measurement could not be accurately performed, the patient was excluded from the data analysis. Serum β-hCG levels were assessed for all patients 14 to 16 days after ET to confirm the biochemical pregnancy [16]. If pregnancy was achieved, progesterone support continued until the end of the 12th week of pregnancy. Also, clinical pregnancy was confirmed by ultrasound (fetal poles and fetal heart rate) in 5 weeks. Patients were divided into two groups based on the calculation of the difference in endometrial thickness measurement between the day of embryo transfer and the last ultrasound during progesterone administration: (1) those whose endometrial thickness at the time of embryo transfer compared to the first day of progesterone administration, 5%, 10%, 15%, or 20% reduction, and (2) those who had an increase in endometrial thickness or a decrease in thickness of less than 5%, 10%, or 15%. Statistical Analysis and Sample Size Continuous variables were reported as mean ± standard deviation (SD). Categorical variables were expressed as absolute frequency and frequency percentage. Shapiro–Wilk test was used to check the normal distribution of quantitative variables. Based on this, Student’s t test or Mann–Whitney U test was performed for quantitative variables and the chi-square test for qualitative ones. ROC curve analysis was used to estimate the discriminating potential of ET between the groups of studied subjects. Youden’s method was also used to identify the optimal threshold. For this purpose, MedCalc v19.7 software was used. All statistical analyses were performed in SPSS software version 24, and a P value of less than 0.05 was considered significant for all statistical tests. The sample size in this study was estimated to be 234 based on the 95% power, type one error (alpha) = 0.05, the anticipated incidence of a given outcome for group 1 = 45.2%, and for group 2 = 23.1% [17]. Considering the possibility of patients dropping out, 253 cases were considered.

General Characteristics of Patients In the present study, uterine thickness on the first day of progesterone administration (primary thickness) and ET day (secondary thickness) was evaluated by vaginal ultrasound in 253 women who underwent FET or fresh cycles. The presence or absence of compaction and compaction of 5, 10, 15, and 20% were evaluated in these patients. The basic and clinical characteristics of patients with or without compaction are given in Table 1. The comparison of demographic and clinical characteristics of patients between these two groups did not show any significant difference. Table 1. | parameter | Total (N = 253) | Compact (N = 93) | No compaction (N = 160) | P value | | | Embryo | Frozen–thaw | 193(76.3) | 73(78.5) | 120(75) | 0.64 | | Fresh | 60(23.7) | 20(21.5) | 40(25) | || | Etiologies | PCD | 53(20.9) | 18(19.6) | 35(21.9) | 0.62 | | Male factor | 59(23.3) | 26(28) | 33(20.6) | || | Tubal factor | 13(5.1) | 3(3.2) | 10(6.3) | || | Septum | 3(1.2) | 1(1.1) | 2(1.3) | || | Endometriosis | 27(10.7) | 12(12.9) | 15(9.4) | || | Amenorrhea | 3(1.2) | 1(1.1) | 2(1.3) | || | Low ovarian reserve | 68(26.9) | 20(21.5) | 48(30) | || | Salpingectomy | 5(2) | 3(3.2) | 2(1.3) | || | Unknown | 22(8.7) | 9(9.7) | 13(8.1) | || | ART.Hx | IUI | 76(30) | 28(30.1) | 48(30) | 0.97 | | IVF | 75(29.6) | 29(31.2) | 46(28.8) | || | Other | 29(11.5) | 10(10.8) | 19(11.9) | || | No.Hx | 73(28.9) | 26(28) | 47(29.4) | || | Medical.Hx | Hypothyroidism | 51(20.2) | 25(26.9) | 26(16.3) | 0.23 | | Thrombophilia | 3(1.2) | 1(1.1) | 2(1.3) | || | DM | 4(1.6) | 0(0) | 4(2.5) | || | Myomectomy | 2(0.8) | 1(1.1) | 1(0.6) | || | Cardiovascular | 1(0.4) | 0(0) | 1(0.6) | || | No.Hx | 192(75.9) | 66(71) | 126(78.8) | || | Menses | Regular | 206(81.4) | 74(79.6) | 132(82.5) | 0.81 | | Irregular | 47(18.6) | 19(20.4) | 28(17.5) | || | HSG findings | Normal | 224(88.5) | 81(87.1) | 143(89.4) | 0.68 | | Abnormal | 29(11.5) | 12(12.9) | 17(10.6) | || | Female age(year) | 33.02 ± 5.92 | 33.11 ± 5.83 | 32.96 ± 6 | 0.84 | | | Male age(year) | 37.26 ± 6.46 | 37.51 ± 7.69 | 37.12 ± 5.64 | 0.66 | | | Female height(cm) | 162.16 ± 6.72 | 162.34 ± 6.28 | 162.06 ± 6.98 | 0.74 | | | Female weight(Kg) | 69.18 ± 13.21 | 67.9 ± 10.61 | 69.93 ± 14.49 | 0.2 | | | Female BMI(Kg/m2) | 26.33 ± 5.01 | 25.8 ± 4.02 | 26.65 ± 5.49 | 0.16 | | | FSH(mIU/mL) | 7.82 ± 4.86 | 7.65 ± 3.71 | 7.91 ± 5.43 | 0.66 | | | AMH(ng/ml) | 3.85 ± 4.36 | 4.1 ± 4.1 | 3.7 ± 4.5 | 0.5 | | | LH(IU/mL) | 6.63 ± 4.88 | 6.14 ± 3.62 | 6.92 ± 5.49 | 0.21 | | | Estradiol(pg/mL) | 61.44 ± 48.98 | 66.97 ± 47.47 | 57.51 ± 50.01 | 0.3 | | | TSH(mIU/L) | 2.08 ± 1.15 | 2.06 ± 1.16 | 2.1 ± 1.15 | 0.79 | | | prolactin(µg/L) | 139.77 ± 212.2 | 163.56 ± 205.9 | 126.56 ± 218.3 | 0.58 | | | primary endometrial thickness(mm) | 9.69 ± 1.64 | 9.51 ± 1.57 | 10 ± 1.71 | 0.02 | | | secondary endometrial thickness(mm) | 10.24 ± 2.15 | 8.76 ± 1.62 | 11.10 ± 1.95 | 0.0001 | *Qualitative parameters are given as number (%), and quantitative parameters are given as mean ± standard deviation Association of Endometrial Compaction with Chemical and Clinical Pregnancy Rate In this part of the study, the association between the presence or absence of endometrial compaction with the rate of chemical pregnancy and clinical pregnancy was investigated. The chemical pregnancy rate was 99 (39.13%), 21(35%) of fresh embryos, and 78(40%) of FETs, and the clinical pregnancy rate was 71 (28.06%). The results showed that both chemical and clinical pregnancy have a significant association with compact endometrium. Table 2 shows the incidence rate of pregnancy in two groups. Table 2. | Parameter | Compact (N = 93) | No compaction (N = 160) | P value | |---|---|---|---| | Chemical pregnancy | ||| | Positive | 51(54.8%) | 48(30%) | 0.0001 | | Negative | 42(45.2%) | 112(70%) | | | Clinical pregnancy | ||| | Positive | 37(39.8%) | 34(21.3%) | 0.001 | | Negative | 56(60.2%) | 126(78.8%) | Association of Endometrial Compaction Percentage with Chemical and Clinical Pregnancy In this part of the study, the association of the percentage of endometrial compaction with the rate of chemical and clinical pregnancy was evaluated. Based on analysis, all the percentages of compaction have a significant association with the occurrence of chemical and clinical pregnancy (Table 3). Table 3. | parameter | Chemical pregnancy | Clinical pregnancy | P value (Chemical) (Clinical) | || |---|---|---|---|---|---| | Positive | Negative | Positive | Negative | || | 5 percent compaction | ||||| | Yes(N = 77) | 44(44.4%) | 33(21.4%) | 37(52.1%) | 40(22%) | 0.0001 | | No(N = 176) | 55(55.6%) | 121(78.6%) | 34(47.9%) | 142(78%) | 0.0001 | | 10 percent compaction | ||||| | Yes(N = 49) | 35(35.4%) | 14(9.1%) | 32(45.1%) | 17(9.3%) | 0.0001 | | No(N = 204) | 64(64.4%) | 140(90.9%) | 39(54.9%) | 165(90.7%) | 0.0001 | | 15 percent compaction | ||||| | Yes(N = 28) | 23(23.2%) | 5(3.2%) | 22(31%) | 6(3.3%) | 0.0001 | | No(N = 225) | 76(76.8%) | 149(96.8%) | 49(69%) | 176(96.7%) | 0.0001 | | 20 percent compaction | ||||| | Yes(N = 14) | 13(13.1) | 1(0.6) | 13(18.3) | 1(0.5) | 0.0001 | | No(N = 239) | 86(86.9) | 153(99.4) | 58(81.7) | 181(99.5) | 0.0001 | Association of Primary and Secondary Endometrial Thickness with Chemical and Clinical Pregnancy and ROC Curve Analysis In this part of the study, primary and secondary endometrial thickness was compared between people with and without chemical and clinical pregnancy separately. The results showed that only secondary thickness (thickness measured on the day of embryo transfer) had a significant difference between people with positive and negative clinical pregnancies. So, in people with positive clinical pregnancy, the thickness of the endometrium was less (Table 4, Fig. 1). Table 4. | Chemical pregnancy | Mean ± SD | P value | | |---|---|---|---| | Primary endometrial thickness | Positive(N = 99) | 9.79 ± 1.63 | 0.16 | | Negative(N = 154) | 9.49 ± 1.64 | || | Secondary endometrial thickness | Positive(N = 99) | 10.09 ± 2.03 | 0.14 | | Negative(N = 154) | 10.51 ± 2.35 | | Clinical pregnancy | Mean ± SD | P value | | |---|---|---|---| | Primary endometrial thickness | Positive(N = 71) | 9.79 ± 1.63 | 0.25 | | Negative(N = 182) | 9.55 ± 1.64 | || | Secondary endometrial thickness | Positive(N = 71) | 9.92 ± 1.97 | 0.006 | | Negative(N = 182) | 10.67 ± 2.33 | Also, the predictive power of secondary endometrial thickness was evaluated in clinical pregnancy prediction; it has an acceptable power in predicting clinical pregnancy. Figure 2 shows the area under the curve (AUC) in this regard (AUC = 0.59, P value = 0.01).

Today, the thickness of the endometrium as a key factor affects the pregnancy outcomes in infertile patients. It has been shown that endometrial compaction can affect the fertility increment success in patients [8]. In the present study, the results showed that the percentage of chemical and clinical pregnancy was higher in the compacted group compared to the non-compacted one, which was statistically significant. In terms of chemical and clinical pregnancy, 74.2% were positive in the compacted group and 60% in the non-compacted group. In addition, in terms of clinical pregnancy, 48.8% were positive in the non-compacted cases. Youngster and his colleagues showed that the ratio of clinical and ongoing pregnancy was higher in the compacted group, which was consistent with the present study [18]. Also, Ju et al. reported higher percentage of clinical pregnancy in the compacted group. In this study, clinical pregnancy evaluation was done in patients undergoing frozen–thaw embryo transfer (FET) cycle [19]. Another study reported that live birth is directly related to endometrial compaction, so that the incidence of live birth has been higher in the compacted group [20]. During the menstrual cycle, in the follicular phase, the secretion of estrogen causes the growth and proliferation of endometrial cells, as well as the formation of blood vessels. Following ovulation, the secretion of progesterone stops the endometrial volume increment. However, it does not stop the thickening of the endometrium, and the growth of blood vessels continues [21]. Several studies have shown that pregnancy outcomes are affected by the percentage of endometrial compaction [22]. In the present study, the amount of endometrial compaction was evaluated in percentages of 5, 10, 15, and 20. The rate of pregnancy in four groups of %5, %10, %15, and %20 compaction was 77(30.4%), 49(19.4%), 28(11.1%), and 14(5.5%), respectively. Haas et al. showed that with the increment of endometrial compaction from 5 to 10%, the rate of clinical and ongoing pregnancy increased [17]. Youngster and his colleagues showed that the clinical and chemical pregnancy rate was higher in the compacted group with 10 and 15% compared to 5%. Further investigations showed that an increase of more than 10% compaction does not have much effect on the clinical and chemical pregnancy rate [18]. Their results were not consistent with the present study. This inconsistency can be due to the number of patients examined and the days of measurement after embryo transfer. On the other hand, in the present study only secondary thickness has predictive value for clinical pregnancy. Meanwhile, various studies measured the thickness of the endometrium on different days after embryo transfer and reported its different effects on pregnancy outcomes. This study also had a series of limitations, one of which was not evaluating the thickness of the endometrium on different days after embryo transfer. On the other hand, more studies should be done in the bigger populations in the future.

According to the main results of this study, endometrial compaction has a significant effect on the rate of chemical and clinical pregnancy. Although in this study all the percentages of compaction had a significant association with pregnancy, no significant superiority was observed in a particular percentage of compaction. On the other hand, the results showed that the thickness of the endometrium on the day of embryo transfer, regardless of compaction, had a definite effect on pregnancy success; it is also a valuable predictive factor. Acknowledgments We wish to thank all our colleagues at Tehran University of Medical Science. Author Contributions Marzieh Aghahosseini, Ashraf Aleyassin, and Sedigheh Hosseinimousa designed the manuscript. Atoosa Etezadi, Ayda Najafian, and Fatemeh Sarvi wrote the manuscript. Maryam Shabani Nashtaee analyzed the data. Funding None. Data Availability Data availability is corresponding author responsibility. Declarations Conflict of interest The authors declare that they have no conflict of interest. Ethical Approval All the procedures performed in the studies involving human participants were in accordance with the ethical standards of the local ethics committee of Tehran University of Medical Science (IR.TUMS.SHARIATI.REC.1401.013), as well as the 1964 Helsinki Declaration. Consent for Publication Not applicable. Footnotes Atoosa Etezadi, Assistant Professor; Marzieh Aghahosseini, Professor; Ashraf Aleyassin, Professor; Sedigheh Hosseinimousa, Assistant Professor; Ayda Najafian, Associate Professor; Fatemeh Sarvi, Associate Professor; Maryam Shabani Nashtaee, Assistant Professor. Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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