Ultrasound evaluation of endometrial receptivity to predict the clinical pregnancy outcome of IVF-ET: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

YU Zhen ^1,2 ,  TANG Ying ^1,2 , LONG Youlin ³ , QIN Xiyu ^1,2 , YANG Jie ^1,2 , YANG Haibo ^1,2

1. Department of Ultrasound, West China Second Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. Key Laboratory of Obstetric & Gynecologic and Pediatric Disease and Birth Defects, Ministry of Education, Chengdu 610041, P. R. China;
3. Chinese Evidence-based Medicine, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

TANG Ying, Email: tangy_cd@163.com

Keywords：

Endometrial receptivity; IVF-ET; Ultrasonography; Pregnancy outcome; Meta-analysis

DOI：

10.7507/1672-2531.202111125

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Objective To systematically review the endometrial receptivity evaluated by transvaginal ultrasound and predict the clinical pregnancy outcome of in vitro fertilization-embryo transfer (IVF-ET). Methods PubMed, The Cochrane Library, EMbase, Web of Science, CNKI, WanFang Data and VIP databases were electronically searched to collect studies on transvaginal ultrasound evaluation of endometrial receptivity to predict the clinical pregnancy outcome of IVF-ET from inception to December 1^st, 2021. Two researchers independently screened literature, extracted data and evaluated the risk of bias of the included studies. RevMan 5.4 software and Stata 16.0 software were used to perform meta-analysis. Results A total of 24 cohort studies and 1 case-control study were included. The total sample size was 6 632 cases, including 3 340 in non-pregnancy group and 3 292 in pregnancy group. The results of meta-analysis showed that there was no difference in endometrial volume (MD=−0.11, 95%CI −0.33 to 0.11, P=0.34) or uterine artery S/D (MD= −0.04, 95%CI −0.17 to 0.09, P=0.55) between the two groups. The endometrial thickness measured on human chorionic gonadotrophin (HCG) day in the non-pregnant group (MD=−0.48, 95%CI −0.77 to −0.18, P=0.001) was thinner than that in the pregnant group. On embryo transfer (ET) day, uterine artery pulsatility index (PI) (MD=0.08, 95%CI 0.02 to 0.15, P=0.01) and resistance index (RI) (MD=0.01, 95%CI 0.01 to 0.01, P<0.000 01) were higher than those in the pregnancy group. Conclusion Endometrial volume and uterine artery S/D measured during IVF-ET were not correlated with clinical pregnancy outcome, while endometrial thickness measured on HCG day and uterine artery PI and RI measured on ET day were correlated with clinical pregnancy outcome. Transvaginal ultrasound evaluation of endometrial receptivity has a certain predictive value for clinical pregnancy outcome of IVF-ET. Due to the limited quality and quantity of included studies, more high-quality studies are needed to verify the above conclusion.

Citation： YU Zhen, TANG Ying, LONG Youlin, QIN Xiyu, YANG Jie, YANG Haibo. Ultrasound evaluation of endometrial receptivity to predict the clinical pregnancy outcome of IVF-ET: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2022, 22(3): 284-290. doi: 10.7507/1672-2531.202111125 Copy

1.	卜晓萌, 贾婵维, 王树玉. 子宫内膜微生态与不孕症及IVF-ET结局的相关性研究. 中国优生与遗传杂志, 2021, 29(4): 590-592.
2.	刘耘利, 许伟标, 刘琼珠, 等. 经阴道三维超声对体外受精-胚胎移植患者子宫内膜容受性的评估及对妊娠结局的预测价值. 中国临床医学影像杂志, 2021, 32(6): 426-431.
3.	Wang J, Xia F, Zhou Y, et al. Association between endometrial/subendometrial vasculature and embryo transfer outcome: a meta-analysis and subgroup analysis. J Ultrasound Med, 2018, 37(1): 149-163.
4.	蒋振林, 朱泽静, 唐丽. 超声监测子宫内膜对IVF-ET妊娠结局的预测价值. 中国计划生育学杂志, 2021, 29(10): 2126-2128.
5.	杨彬, 王薇, 苟永贤, 等. 阴道三维超声评估子宫内膜容受性预测体外受精-胚胎移植后妊娠结局的临床价值. 临床医学研究与实践, 2020, 5(29): 135-136.
6.	李芷舒, 鲁海鸥, 张宇明, 等. 不孕患者移植当日子宫内膜容受性评估对临床妊娠率影响研究. 中国实用妇科与产科杂志, 2020, 36(3): 264-266.
7.	陈慧佳, 吴艺佳, 张觇宇, 等. 彩色多普勒超声检查预测冻融胚胎解冻移植妊娠结局的价值. 检验医学与临床, 2019, 16(13): 1819-1822.
8.	杨文秀. 经阴道三维超声评价冻融胚胎移植周期子宫内膜容受性的研究. 济南: 山东大学, 2017.
9.	姚丽婷, 黄枢, 闫建平, 等. 子宫内膜容积和内膜下血流对子宫内膜容受性影响的比较. 临床军医杂志, 2015, 43(4): 388-390,396.
10.	Prasad S, Goyal R, Kumar Y, et al. The relationship between uterine artery two-dimensional color Doppler measurement and pregnancy outcome: a prospective observational study. J Reprod Infertil, 2017, 18(2): 251-256.
11.	Nandi A, Martins WP, Jayaprakasan K, et al. Assessment of endometrial and subendometrial blood flow in women undergoing frozen embryo transfer cycles. Reprod Biomed Online, 2014, 28(3): 343-351.
12.	刘灿华, 孔凤贝, 王晓萍, 等. 经阴道彩色多普勒超声对IVF-ET中子宫内膜容受性的评估价值. 南昌大学学报(医学版), 2014, 54(4): 38-40,44.
13.	Son JB, Jeong JE, Joo JK, et al. Measurement of endometrial and uterine vascularity by transvaginal ultrasonography in predicting pregnancy outcome during frozen-thawed embryo transfer cycles. J Obstet Gynaecol Res, 2014, 40(6): 1661-1667.
14.	Zhao J, Zhang Q, Wang Y, et al. Endometrial pattern, thickness and growth in predicting pregnancy outcome following 3319 IVF cycle. Reprod Biomed Online, 2014, 29(3): 291-298.
15.	李江涛, 曹金丽, 程传生, 等. 经阴道三维超声在冻融胚胎解冻移植时机选择中的运用价值. 中华临床医师杂志(电子版), 2013, (9): 3782-3785.
16.	王晓红. 彩色多普勒超声检测子宫内膜参数在预测IVF-ET结局的作用. 太原: 山西医科大学, 2012.
17.	王丽娜, 苏雪松, 乔杰, 等. 子宫内膜内及子宫内膜下血流对胚胎解冻移植周期妊娠结局的影响. 中国微创外科杂志, 2012, 12(3): 245-249.
18.	屈文娟, 姜宏, 罗福成, 等. 经阴道彩色多普勒超声在IVF-ET中对子宫内膜容受性的评估价值. 中国超声医学杂志, 2011, 27(11): 1027-1030.
19.	Engels V, Sanfrutos L, Pérez-Medina T, et al. Evaluation of endometrial and subendometrial vascularization and endometrial volume by 3-D power Doppler ultrasound and its relationship with age and pregnancy in intrauterine insemination cycles. Gynecol Obstet Invest, 2011, 72(2): 117-122.
20.	Yilmaz N, Kilic S, Madendag Y, et al. Endometrial parameters in IVF and IUI administration on elderly women. Turk J Med Sci, 2010, 40(3): 343-348.
21.	Zácková T, Järvelä IY, Tapanainen JS, et al. Assessment of endometrial and ovarian characteristics using three dimensional power Doppler ultrasound to predict response in frozen embryo transfer cycles. Reprod Biol Endocrinol, 2009, 7: 151.
22.	Mercé LT, Barco MJ, Bau S, et al. Are endometrial parameters by three-dimensional ultrasound and power Doppler angiography related to in vitro fertilization/embryo transfer outcome. Fertil Steril, 2008, 89(1): 111-117.
23.	张清学, 邢卫杰, 文艳玲, 等. 彩色超声多普勒评价子宫内膜容受性的价值. 中国超声医学杂志, 2006, 22(5): 375-377.
24.	刘红梅, 邢福祺, 陈士岭. 经阴道超声对体外受精-胚胎移植中子宫内膜容受性的评价. 中国超声医学杂志, 2005, (11): 66-68.
25.	张宜生, 周馥贞, 应伟雯. 三维超声测定子宫内膜容积预测IVFET结局. 实用妇产科杂志, 2005, 21(6): 375-377.
26.	Chien LW, Lee WS, Au HK, et al. Assessment of changes in utero-ovarian arterial impedance during the peri-implantation period by Doppler sonography in women undergoing assisted reproduction. Ultrasound Obstet Gynecol, 2004, 23(5): 496-500.
27.	Wu HM, Chiang CH, Huang HY, et al. Detection of the subendometrial vascularization flow index by three-dimensional ultrasound may be useful for predicting the pregnancy rate for patients undergoing in vitro fertilization-embryo transfer. Fertil Steril, 2003, 79(3): 507-511.
28.	Cacciatore B, Simberg N, Fusaro P, et al. Transvaginal Doppler study of uterine artery blood flow in in vitro fertilization-embryo transfer cycles. Fertil Steril, 1996, 66(1): 130-134.
29.	裴红, 姜宏, 张文香, 等. 体外受精-胚胎移植中子宫内膜超声参数与妊娠率的相关性. 生殖医学杂志, 2009, 18(4): 390-392.
30.	Schild RL, Knobloch C, Dorn C, et al. Endometrial receptivity in an in vitro fertilization program as assessed by spiral artery blood flow, endometrial thickness, endometrial volume, and uterine artery blood flow. Fertil Steril, 2001, 75(2): 361-366.
31.	唐志霞, 洪名云, 张玲, 等. 子宫动脉及子宫内膜血流对体外受精-胚胎移植结局的影响. 中国计划生育和妇产科, 2015, 7(7): 15-17.
32.	Sun Y, Huang J, Kong HF. Spontaneous rupture of unscarred uterus in the third trimester after in vitro fertilization-embryo transfer because of bilateral salpingectomy: A case report. Medicine (Baltimore), 2019, 98(48): e18182.
33.	Shang J, Peng R, Zheng J, et al. The indicator of clinical outcomes for patients with heterotopic pregnancy following in-vitro fertilization with embryo transfer. Taiwan J Obstet Gynecol, 2019, 58(6): 827-832.

1. 卜晓萌, 贾婵维, 王树玉. 子宫内膜微生态与不孕症及IVF-ET结局的相关性研究. 中国优生与遗传杂志, 2021, 29(4): 590-592.
2. 刘耘利, 许伟标, 刘琼珠, 等. 经阴道三维超声对体外受精-胚胎移植患者子宫内膜容受性的评估及对妊娠结局的预测价值. 中国临床医学影像杂志, 2021, 32(6): 426-431.
3. Wang J, Xia F, Zhou Y, et al. Association between endometrial/subendometrial vasculature and embryo transfer outcome: a meta-analysis and subgroup analysis. J Ultrasound Med, 2018, 37(1): 149-163.
4. 蒋振林, 朱泽静, 唐丽. 超声监测子宫内膜对IVF-ET妊娠结局的预测价值. 中国计划生育学杂志, 2021, 29(10): 2126-2128.
5. 杨彬, 王薇, 苟永贤, 等. 阴道三维超声评估子宫内膜容受性预测体外受精-胚胎移植后妊娠结局的临床价值. 临床医学研究与实践, 2020, 5(29): 135-136.
6. 李芷舒, 鲁海鸥, 张宇明, 等. 不孕患者移植当日子宫内膜容受性评估对临床妊娠率影响研究. 中国实用妇科与产科杂志, 2020, 36(3): 264-266.
7. 陈慧佳, 吴艺佳, 张觇宇, 等. 彩色多普勒超声检查预测冻融胚胎解冻移植妊娠结局的价值. 检验医学与临床, 2019, 16(13): 1819-1822.
8. 杨文秀. 经阴道三维超声评价冻融胚胎移植周期子宫内膜容受性的研究. 济南: 山东大学, 2017.
9. 姚丽婷, 黄枢, 闫建平, 等. 子宫内膜容积和内膜下血流对子宫内膜容受性影响的比较. 临床军医杂志, 2015, 43(4): 388-390,396.
10. Prasad S, Goyal R, Kumar Y, et al. The relationship between uterine artery two-dimensional color Doppler measurement and pregnancy outcome: a prospective observational study. J Reprod Infertil, 2017, 18(2): 251-256.
11. Nandi A, Martins WP, Jayaprakasan K, et al. Assessment of endometrial and subendometrial blood flow in women undergoing frozen embryo transfer cycles. Reprod Biomed Online, 2014, 28(3): 343-351.
12. 刘灿华, 孔凤贝, 王晓萍, 等. 经阴道彩色多普勒超声对IVF-ET中子宫内膜容受性的评估价值. 南昌大学学报(医学版), 2014, 54(4): 38-40,44.
13. Son JB, Jeong JE, Joo JK, et al. Measurement of endometrial and uterine vascularity by transvaginal ultrasonography in predicting pregnancy outcome during frozen-thawed embryo transfer cycles. J Obstet Gynaecol Res, 2014, 40(6): 1661-1667.
14. Zhao J, Zhang Q, Wang Y, et al. Endometrial pattern, thickness and growth in predicting pregnancy outcome following 3319 IVF cycle. Reprod Biomed Online, 2014, 29(3): 291-298.
15. 李江涛, 曹金丽, 程传生, 等. 经阴道三维超声在冻融胚胎解冻移植时机选择中的运用价值. 中华临床医师杂志(电子版), 2013, (9): 3782-3785.
16. 王晓红. 彩色多普勒超声检测子宫内膜参数在预测IVF-ET结局的作用. 太原: 山西医科大学, 2012.
17. 王丽娜, 苏雪松, 乔杰, 等. 子宫内膜内及子宫内膜下血流对胚胎解冻移植周期妊娠结局的影响. 中国微创外科杂志, 2012, 12(3): 245-249.
18. 屈文娟, 姜宏, 罗福成, 等. 经阴道彩色多普勒超声在IVF-ET中对子宫内膜容受性的评估价值. 中国超声医学杂志, 2011, 27(11): 1027-1030.
19. Engels V, Sanfrutos L, Pérez-Medina T, et al. Evaluation of endometrial and subendometrial vascularization and endometrial volume by 3-D power Doppler ultrasound and its relationship with age and pregnancy in intrauterine insemination cycles. Gynecol Obstet Invest, 2011, 72(2): 117-122.
20. Yilmaz N, Kilic S, Madendag Y, et al. Endometrial parameters in IVF and IUI administration on elderly women. Turk J Med Sci, 2010, 40(3): 343-348.
21. Zácková T, Järvelä IY, Tapanainen JS, et al. Assessment of endometrial and ovarian characteristics using three dimensional power Doppler ultrasound to predict response in frozen embryo transfer cycles. Reprod Biol Endocrinol, 2009, 7: 151.
22. Mercé LT, Barco MJ, Bau S, et al. Are endometrial parameters by three-dimensional ultrasound and power Doppler angiography related to in vitro fertilization/embryo transfer outcome. Fertil Steril, 2008, 89(1): 111-117.
23. 张清学, 邢卫杰, 文艳玲, 等. 彩色超声多普勒评价子宫内膜容受性的价值. 中国超声医学杂志, 2006, 22(5): 375-377.
24. 刘红梅, 邢福祺, 陈士岭. 经阴道超声对体外受精-胚胎移植中子宫内膜容受性的评价. 中国超声医学杂志, 2005, (11): 66-68.
25. 张宜生, 周馥贞, 应伟雯. 三维超声测定子宫内膜容积预测IVFET结局. 实用妇产科杂志, 2005, 21(6): 375-377.
26. Chien LW, Lee WS, Au HK, et al. Assessment of changes in utero-ovarian arterial impedance during the peri-implantation period by Doppler sonography in women undergoing assisted reproduction. Ultrasound Obstet Gynecol, 2004, 23(5): 496-500.
27. Wu HM, Chiang CH, Huang HY, et al. Detection of the subendometrial vascularization flow index by three-dimensional ultrasound may be useful for predicting the pregnancy rate for patients undergoing in vitro fertilization-embryo transfer. Fertil Steril, 2003, 79(3): 507-511.
28. Cacciatore B, Simberg N, Fusaro P, et al. Transvaginal Doppler study of uterine artery blood flow in in vitro fertilization-embryo transfer cycles. Fertil Steril, 1996, 66(1): 130-134.
29. 裴红, 姜宏, 张文香, 等. 体外受精-胚胎移植中子宫内膜超声参数与妊娠率的相关性. 生殖医学杂志, 2009, 18(4): 390-392.
30. Schild RL, Knobloch C, Dorn C, et al. Endometrial receptivity in an in vitro fertilization program as assessed by spiral artery blood flow, endometrial thickness, endometrial volume, and uterine artery blood flow. Fertil Steril, 2001, 75(2): 361-366.
31. 唐志霞, 洪名云, 张玲, 等. 子宫动脉及子宫内膜血流对体外受精-胚胎移植结局的影响. 中国计划生育和妇产科, 2015, 7(7): 15-17.
32. Sun Y, Huang J, Kong HF. Spontaneous rupture of unscarred uterus in the third trimester after in vitro fertilization-embryo transfer because of bilateral salpingectomy: A case report. Medicine (Baltimore), 2019, 98(48): e18182.
33. Shang J, Peng R, Zheng J, et al. The indicator of clinical outcomes for patients with heterotopic pregnancy following in-vitro fertilization with embryo transfer. Taiwan J Obstet Gynecol, 2019, 58(6): 827-832.

Chinese Journal of Evidence-Based Medicine

Ultrasound evaluation of endometrial receptivity to predict the clinical pregnancy outcome of IVF-ET: a meta-analysis

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