Miscarriage on Endometriosis and Adenomyosis in Women by Assisted Reproductive Technology or with Spontaneous Conception: A Systematic Review and Meta-Analysis

Yangxue Huang, Xianhong Zhao, Yiyuan Chen, Jie Wang, Weilin Zheng, Lixing Cao, Yangxue Huang, Xianhong Zhao, Yiyuan Chen, Jie Wang, Weilin Zheng, Lixing Cao

Abstract

Background: In the past several years, there has been an increasing concern on miscarriage caused by endometriosis or adenomyosis. However, the results reported by different studies remain controversial. The present study is aimed at assessing the impact of endometriosis and adenomyosis on miscarriage.

Materials and methods: Searches were carried out in PubMed, Embase, and the Cochrane library for studies published from inception until February 29, 2020. The investigators included studies that evaluated miscarriage risk in pregnant women with endometriosis or adenomyosis by assisted reproductive technology (ART), or with spontaneous conception (SC). Miscarriage (<28 weeks) was the primary outcome. The secondary outcomes were antepartum hemorrhage (APH), postpartum hemorrhage (PPH), preterm birth, low birthweight, placenta praevia, placental abruption, ectopic pregnancy, stillbirth, gestational diabetes, preeclampsia, and intrauterine growth restriction (IUGR). Endnote was used for the study collection, and the data analyses were carried out by two authors using Review Manager version 5.2.

Results: Thirty-nine studies, which is comprised of 697,984 women, were included in the present study. Miscarriage risk increased in women with endometriosis in SC (OR: 1.81, 95% CI: 1.44-2.28, I 2 = 96%) compared with those without endometriosis, while women with endometriosis who underwent ART had a similar miscarriage risk, when compared to those with tubal infertility (OR: 1.03, 95% CI: 0.92-1.14, I 2 = 0%). Compared with those without adenomyosis, women with adenomyosis had an augmented miscarriage risk in ART (OR: 2.81, 95% CI: 1.44-5.47, I 2 = 64%). Compared with those without endometriosis, women with endometriosis had higher odds of APH, PPH, preterm birth, stillbirth, and placenta praevia. No difference was observed in the incidence of ectopic pregnancy, placental abruption, pre-eclampsia, gestational diabetes, low birthweight, and IUGR.

Conclusion: Women with endometriosis had an augmented miscarriage risk in SC and a similar miscarriage risk during ART. Adenomyosis was associated with miscarriage in pregnant women using ART.

Conflict of interest statement

All authors declare no conflict of interest.

Copyright © 2020 Yangxue Huang et al.

Figures

Figure 1
Figure 1
Flow chart of the literature selection.
Figure 2
Figure 2
Miscarriage risk in pregnant women with EMS in SC or using ART.
Figure 3
Figure 3
Miscarriage risk in pregnant women with AD in ART.
Figure 4
Figure 4
Sensitivity analysis of miscarriage risk in pregnant women with AD.
Figure 5
Figure 5
Miscarriage risk in women with EMS in retrospective cohort studies and prospective cohort studies in SC.
Figure 6
Figure 6
Miscarriage risk in women with EMS in retrospective cohort studies and prospective cohort studies during ART.
Figure 7
Figure 7
Miscarriage risk in women with AD in retrospective cohort studies during ART.
Figure 8
Figure 8
Miscarriage risk in women with EMS diagnosed by laparoscopy.
Figure 9
Figure 9
Miscarriage risk in women with resected OMA, unresected OMA, DIE, and SUP.
Figure 10
Figure 10
Miscarriage risk in EMS I/II and EMS III/IV.
Figure 11
Figure 11
Early abortion and late abortion in women with EMS.
Figure 12
Figure 12
Funnel plot of miscarriage risk in women with EMS.
Figure 13
Figure 13
Low birthweight, preeclampsia, IUGR, and placental abruption in women with EMS.
Figure 14
Figure 14
APH, PPH, and preterm birth in women with EMS.
Figure 15
Figure 15
Ectopic pregnancy, stillbirth, gestational diabetes, and placenta praevia in women with EMS.

References

    1. Parasar P., Ozcan P., Terry K. L. Endometriosis: epidemiology, diagnosis and clinical management. Current Obstetrics and Gynecology Reports. 2017;6(1):34–41. doi: 10.1007/s13669-017-0187-1.
    1. Macer M. L., Taylor H. S. Endometriosis and infertility: a review of the pathogenesis and treatment of endometriosis-associated infertility. Obstetrics and Gynecology Clinics of North America. 2012;39(4):535–549. doi: 10.1016/j.ogc.2012.10.002.
    1. Benagiano G., Brosens I., Habiba M. Structural and molecular features of the endomyometrium in endometriosis and adenomyosis. Human Reproduction Update. 2014;20(3):386–402. doi: 10.1093/humupd/dmt052.
    1. Naftalin J., Hoo W., Pateman K., Mavrelos D., Holland T., Jurkovic D. How common is adenomyosis? A prospective study of prevalence using transvaginal ultrasound in a gynaecology clinic. Human Reproduction (Oxford, England) 2012;27(12):3432–3439. doi: 10.1093/humrep/des332.
    1. Horton J., Sterrenburg M., Lane S., Maheshwari A., Li T. C., Cheong Y. Reproductive, obstetric, and perinatal outcomes of women with adenomyosis and endometriosis: a systematic review and meta-analysis. Human Reproduction Update. 2019;25(5):592–632. doi: 10.1093/humupd/dmz012.
    1. Hamdan M., Omar S. Z., Dunselman G., Cheong Y. Influence of endometriosis on assisted reproductive technology outcomes: a systematic review and meta-analysis. Obstetrics and Gynecology. 2015;125(1):79–88. doi: 10.1097/AOG.0000000000000592.
    1. Higgins JPT GSe. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [Updated March 2011] The Cochrane Collaboration; 2011. .
    1. DerSimonian R., Laird N. Meta-analysis in clinical trials. Controlled Clinical Trials. 1986;7(3):177–188. doi: 10.1016/0197-2456(86)90046-2.
    1. Egger M., Smith G. D., Schneider M., Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–634. doi: 10.1136/bmj.315.7109.629.
    1. Moher D., Liberati A., Tetzlaff J., Altman D. G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. International Journal of Surgery. 2010;8(5):336–341. doi: 10.1016/j.ijsu.2010.02.007.
    1. Pittaway D. E., Vernon C., Fayez J. A. Spontaneous abortions in women with endometriosis. Fertility and Sterility. 1988;50(5):711–715. doi: 10.1016/S0015-0282(16)60303-5.
    1. Curtis P., Jackson A., Bernard A., Shaw R. W. Pretreatment with gonadotrophin releasing hormone (GnRH) analogue prior to in vitro fertilisation for patients with endometriosis. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 1993;52(3):211–216. doi: 10.1016/0028-2243(93)90074-M.
    1. Geber S., Paraschos T., Atkinson G., Margara R., Winston R. M. L. Results of IVF in patients with endometriosis: the severity of the disease does not affect outcome, or the incidence of miscarriage. Human Reproduction (Oxford, England) 1995;10(6):1507–1511. doi: 10.1093/HUMREP/10.6.1507.
    1. Olivennes F., Feldberg D., Liu H. C., Cohen J., Moy F., Rosenwaks Z. Endometriosis: a stage by stage analysis--the role of in vitro fertilization. Fertility and Sterility. 1995;64(2):392–398. doi: 10.1016/S0015-0282(16)57740-1.
    1. Arici A., Oral E., Bukulmez O., Duleba A., Olive D. L., Jones E. E. The effect of endometriosis on implantation: results from the Yale University in vitro fertilization and embryo transfer program. Fertility and Sterility. 1996;65(3):603–607. doi: 10.1016/S0015-0282(16)58162-X.
    1. Pabuccu R., Onalan G., Goktolga U., Kucuk T., Orhon E., Ceyhan T. Aspiration of ovarian endometriomas before intracytoplasmic sperm injection. Fertility and Sterility. 2004;82(3):705–711. doi: 10.1016/j.fertnstert.2004.02.117.
    1. Bahceci M., Ulug U. Does underlying infertility aetiology impact on first trimester miscarriage rate following ICSI? A preliminary report from 1244 singleton gestations. Human Reproduction (Oxford, England) 2005;20(3):717–721. doi: 10.1093/humrep/deh681.
    1. Kuivasaari P., Hippeläinen M., Anttila M., Heinonen S. Effect of endometriosis on IVF/ICSI outcome: stage III/IV endometriosis worsens cumulative pregnancy and live-born rates. Human Reproduction (Oxford, England) 2005;20(11):3130–3135. doi: 10.1093/humrep/dei176.
    1. Omland A. K., Åbyholm T., Fedorcsák P., et al. Pregnancy outcome after IVF and ICSI in unexplained, endometriosis-associated and tubal factor infertility. Human Reproduction (Oxford, England) 2005;20(3):722–727. doi: 10.1093/humrep/deh664.
    1. Esinler I., Bozdag G., Aybar F., Bayar U., Yarali H. Outcome of in vitro fertilization/intracytoplasmic sperm injection after laparoscopic cystectomy for endometriomas. Fertility and Sterility. 2006;85(6):1730–1735. doi: 10.1016/j.fertnstert.2005.10.076.
    1. Matalliotakis I. M., Cakmak H., Mahutte N., Fragouli Y., Arici A., Sakkas D. Women with advanced-stage endometriosis and previous surgery respond less well to gonadotropin stimulation, but have similar IVF implantation and delivery rates compared with women with tubal factor infertility. Fertility and Sterility. 2007;88(6):1568–1572. doi: 10.1016/j.fertnstert.2007.01.037.
    1. Kuroda K., Kitade M., Kikuchi I., et al. The impact of endometriosis, endometrioma and ovarian cystectomy on assisted reproductive technology. Reproductive Medicine and Biology. 2009;8(3):113–118. doi: 10.1007/s12522-009-0021-1.
    1. Mathieu d'Argent E., Coutant C., Ballester M., et al. Results of first in vitro fertilization cycle in women with colorectal endometriosis compared with those with tubal or male factor infertility. Fertility and Sterility. 2010;94(6):2441–2443. doi: 10.1016/j.fertnstert.2010.03.033.
    1. Costello M. F., Lindsay K., McNally G. The effect of adenomyosis on in vitro fertilisation and intra-cytoplasmic sperm injection treatment outcome. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2011;158(2):229–234. doi: 10.1016/j.ejogrb.2011.04.030.
    1. Kim C. H., Ahn J. W., Kim S. H., Chae H. D., Kang B. M. Effects on in vitro fertilization-embryo transfer outcomes of vascular endothelial growth factor receptor-1, -2 and -3 in eutopic endometrial tissue of women with endometriosis. The Journal of Obstetrics and Gynaecology Research. 2011;37(11):1631–1637. doi: 10.1111/j.1447-0756.2011.01588.x.
    1. Martínez-Conejero J. A., Morgan M., Montesinos M., et al. Adenomyosis does not affect implantation, but is associated with miscarriage in patients undergoing oocyte donation. Fertility and Sterility. 2011;96(4):943–950.e1. doi: 10.1016/j.fertnstert.2011.07.1088.
    1. Opøien H. K., Fedorcsak P., Omland A. K., et al. In vitro fertilization is a successful treatment in endometriosis-associated infertility. Fertility and Sterility. 2012;97(4):912–918. doi: 10.1016/j.fertnstert.2012.01.112.
    1. Salim R., Riris S., Saab W., Abramov B., Khadum I., Serhal P. Adenomyosis reduces pregnancy rates in infertile women undergoing IVF. Reproductive Biomedicine Online. 2012;25(3):273–277. doi: 10.1016/j.rbmo.2012.05.003.
    1. Benaglia L., Cardellicchio L., Leonardi M., et al. Asymptomatic adenomyosis and embryo implantation in IVF cycles. Reproductive Biomedicine Online. 2014;29(5):606–611. doi: 10.1016/j.rbmo.2014.07.021.
    1. Hjordt Hansen M. V., Dalsgaard T., Hartwell D., Skovlund C. W., Lidegaard Ø. Reproductive prognosis in endometriosis. A national cohort study. Acta Obstetricia et Gynecologica Scandinavica. 2014;93(5):483–489. doi: 10.1111/aogs.12373.
    1. Mekaru K., Masamoto H., Sugiyama H., et al. Endometriosis and pregnancy outcome: are pregnancies complicated by endometriosis a high-risk group? European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2014;172:36–39. doi: 10.1016/j.ejogrb.2013.10.024.
    1. Polat M., Boynukalın F. K., Yaralı İ., Esinler İ., Yaralı H. Endometriosis is not associated with inferior pregnancy rates in in vitro fertilization: an analysis of 616 patients. Gynecologic and Obstetric Investigation. 2014;78(1):59–64. doi: 10.1159/000360607.
    1. Pop-Trajkovic S., Kopitovic V., Popovic J., Antic V., Radovic D., Zivadinovic R. In vitro fertilization outcome in women with endometriosis &amp; previous ovarian surgery. The Indian Journal of Medical Research. 2014;140(3):387–391.
    1. Yan L., Ding L., Tang R., Chen Z. J. Effect of adenomyosis on in vitro fertilization/intracytoplasmic sperm injection outcomes in infertile women: a retrospective cohort study. Gynecologic and Obstetric Investigation. 2014;77(1):14–18. doi: 10.1159/000355101.
    1. Guo H., Wang Y., Chen Q., Chai W., Lv Q., Kuang Y. Effect of natural cycle endometrial preparation for frozen-thawed embryo transfer in patients with advanced endometriosis. Medical Science Monitor. 2016;22:4596–4603. doi: 10.12659/MSM.898044.
    1. Santulli P., Marcellin L., Menard S., et al. Increased rate of spontaneous miscarriages in endometriosis-affected women. Human Reproduction (Oxford, England) 2016;31(5):1014–1023. doi: 10.1093/humrep/dew035.
    1. Senapati S., Sammel M. D., Morse C., Barnhart K. T. Impact of endometriosis on in vitro fertilization outcomes: an evaluation of the Society for Assisted Reproductive Technologies Database. Fertility and Sterility. 2016;106(1):164–71.e1. doi: 10.1016/j.fertnstert.2016.03.037.
    1. Singh A. K., Chattopadhyay R., Chakravarty B., Chaudhury K. Altered circulating levels of matrix metalloproteinases 2 and 9 and their inhibitors and effect of progesterone supplementation in women with endometriosis undergoing in vitro fertilization. Fertility and Sterility. 2013;100(1):127–34.e1. doi: 10.1016/j.fertnstert.2013.03.006.
    1. Queiroz Vaz G., Evangelista A. V., Almeida Cardoso M. C., Gallo P., Erthal M. C., Pinho Oliveira M. A. Frozen embryo transfer cycles in women with deep endometriosis. Gynecological Endocrinology. 2017;33(7):540–543. doi: 10.1080/09513590.2017.1296945.
    1. Saraswat L., Ayansina D. T., Cooper K. G., et al. Pregnancy outcomes in women with endometriosis: a national record linkage study. BJOG: An International Journal of Obstetrics & Gynaecology. 2016;124(3):444–452. doi: 10.1111/1471-0528.13920.
    1. Hashimoto A., Iriyama T., Sayama S., et al. Adenomyosis and adverse perinatal outcomes: increased risk of second trimester miscarriage, preeclampsia, and placental malposition. The Journal of Maternal-Fetal & Neonatal Medicine. 2018;31(3):364–369. doi: 10.1080/14767058.2017.1285895.
    1. Farland L. V., Prescott J., Sasamoto N., et al. Endometriosis and risk of adverse pregnancy outcomes. Obstetrics and Gynecology. 2019;134(3):527–536. doi: 10.1097/AOG.0000000000003410.
    1. Sharma S., Bathwal S., Agarwal N., Chattopadhyay R., Saha I., Chakravarty B. Does presence of adenomyosis affect reproductive outcome in IVF cycles? A retrospective analysis of 973 patients. Reproductive Biomedicine Online. 2019;38(1):13–21. doi: 10.1016/j.rbmo.2018.09.014.
    1. Porpora M. G., Tomao F., Ticino A., et al. Endometriosis and pregnancy: a single institution experience. International Journal of Environmental Research and Public Health. 2020;17(2):p. 401. doi: 10.3390/ijerph17020401.
    1. Sharma S., RoyChoudhury S., Bathwal S., et al. Pregnancy and live birth rates are comparable in young infertile women presenting with severe endometriosis and tubal infertility. Reproductive Sciences. 2020;27(6):1340–1349. doi: 10.1007/s43032-020-00158-x.
    1. Bergendal A., Naffah S., Nagy C., Bergqvist A., Sjöblom P., Hillensjö T. Outcome of IVF in patients with endometriosis in comparison with tubal-factor infertility. Journal of Assisted Reproduction and Genetics. 1998;15(9):530–534. doi: 10.1023/A:1022526002421.
    1. Kohl Schwartz A. S., Wölfler M. M., Mitter V., et al. Endometriosis, especially mild disease: a risk factor for miscarriages. Fertility and Sterility. 2017;108(5):806–814.e2. doi: 10.1016/j.fertnstert.2017.08.025.
    1. Youm H. S., Choi Y. S., Han H. D. In vitro fertilization and embryo transfer outcomes in relation to myometrial thickness. Journal of Assisted Reproduction and Genetics. 2011;28(11):1135–1140. doi: 10.1007/s10815-011-9640-7.
    1. Thalluri V., Tremellen K. P. Ultrasound diagnosed adenomyosis has a negative impact on successful implantation following GnRH antagonist IVF treatment. Human Reproduction (Oxford, England) 2012;27(12):3487–3492. doi: 10.1093/humrep/des305.
    1. Zullo F., Spagnolo E., Saccone G., et al. Endometriosis and obstetrics complications: a systematic review and meta-analysis. Fertility and Sterility. 2017;108(4):667–72.e5. doi: 10.1016/j.fertnstert.2017.07.019.
    1. Younes G., Tulandi T. Effects of adenomyosis on in vitro fertilization treatment outcomes: a meta-analysis. Fertility and Sterility. 2017;108(3):483–90.e3. doi: 10.1016/j.fertnstert.2017.06.025.
    1. Barbosa M. A., Teixeira D. M., Navarro P. A., Ferriani R. A., Nastri C. O., Martins W. P. Impact of endometriosis and its staging on assisted reproduction outcome: systematic review and meta-analysis. Ultrasound in Obstetrics & Gynecology. 2014;44(3):261–278. doi: 10.1002/uog.13366.
    1. Parazzini F., Ferraroni M., Fedele L., Bocciolone L., Rubessa S., Riccardi A. Pelvic endometriosis: reproductive and menstrual risk factors at different stages in Lombardy, northern Italy. Journal of Epidemiology and Community Health. 1995;49(1):61–64. doi: 10.1136/jech.49.1.61.
    1. Wu C. Q., Albert A., Alfaraj S., et al. Live birth rate after surgical and expectant management of endometriomas after in vitro fertilization: a systematic review, meta-analysis, and critical appraisal of current guidelines and previous meta-analyses. Journal of Minimally Invasive Gynecology. 2019;26(2):299–311.e3. doi: 10.1016/j.jmig.2018.08.029.
    1. Leone Roberti Maggiore U., Scala C., Tafi E., et al. Spontaneous fertility after expectant or surgical management of rectovaginal endometriosis in women with or without ovarian endometrioma: a retrospective analysis. Fertility and Sterility. 2017;107(4):969–976.e5. doi: 10.1016/j.fertnstert.2017.02.106.
    1. Mounsambote L., Cohen J., Bendifallah S., et al. Deep infiltrative endometriosis without digestive involvement, what is the impact of surgery on in vitro fertilization outcomes? A retrospective study. Gynécologie Obstétrique Fertilité & Sénologie. 2017;45(1):15–21. doi: 10.1016/j.gofs.2016.12.008.
    1. Boujenah J., Cedrin-Durnerin I., Herbemont C., Sifer C., Poncelet C. Non-ART pregnancy predictive factors in infertile patients with peritoneal superficial endometriosis. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2017;211:182–187. doi: 10.1016/j.ejogrb.2017.03.008.
    1. Palomba S., Homburg R., Santagni S., la Sala G. B., Orvieto R. Risk of adverse pregnancy and perinatal outcomes after high technology infertility treatment: a comprehensive systematic review. Reproductive Biology and Endocrinology. 2016;14(1):p. 76. doi: 10.1186/s12958-016-0211-8.
    1. Groll M. Endometriosis and spontaneous abortion. Fertility and Sterility. 1984;41(6):933–935. doi: 10.1016/S0015-0282(16)47911-2.
    1. Maheshwari A., Gurunath S., Fatima F., Bhattacharya S. Adenomyosis and subfertility: a systematic review of prevalence, diagnosis, treatment and fertility outcomes. Human Reproduction Update. 2012;18(4):374–392. doi: 10.1093/humupd/dms006.
    1. Asghari S., Valizadeh A., Aghebati-Maleki L., Nouri M., Yousefi M. Endometriosis: perspective, lights, and shadows of etiology. Biomedicine & Pharmacotherapy. 2018;106:163–174. doi: 10.1016/j.biopha.2018.06.109.
    1. Greene A. D., Lang S. A., Kendziorski J. A., Sroga-Rios J. M., Herzog T. J., Burns K. A. Endometriosis: where are we and where are we going? Reproduction. 2016;152(3):R63–R78. doi: 10.1530/REP-16-0052.
    1. Tomassetti C., Meuleman C., Pexsters A., et al. Endometriosis, recurrent miscarriage and implantation failure: is there an immunological link? Reproductive Biomedicine Online. 2006;13(1):58–64. doi: 10.1016/S1472-6483(10)62016-0.
    1. Chen X., Man G. C. W., Liu Y., et al. Physiological and pathological angiogenesis in endometrium at the time of embryo implantation. American Journal of Reproductive Immunology. 2017;78(2, article e12693) doi: 10.1111/aji.12693.
    1. Vannuccini S., Petraglia F. Recent advances in understanding and managing adenomyosis. F1000Research. 2019;8 doi: 10.12688/f1000research.17242.1.
    1. Campo S., Campo V., Benagiano G. Infertility and adenomyosis. Obstetrics and Gynecology International. 2012;2012:8. doi: 10.1155/2012/786132.786132
    1. Laschke M. W., Menger M. D. Basic mechanisms of vascularization in endometriosis and their clinical implications. Human Reproduction Update. 2018;24(2):207–224. doi: 10.1093/humupd/dmy001.
    1. Gonzales M., de Matos L. A., da Costa Gonçalves M. O., et al. Patients with adenomyosis are more likely to have deep endometriosis. Gynecological Surgery. 2012;9(3):259–264. doi: 10.1007/s10397-012-0746-4.
    1. Naphatthalung W., Cheewadhanaraks S. Prevalence of endometriosis among patients with adenomyosis and/or myoma uteri scheduled for a hysterectomy. Journal of the Medical Association of Thailand. 2012;95(9):1136–1140.
    1. Vannuccini S., Clifton V. L., Fraser I. S., et al. Infertility and reproductive disorders: impact of hormonal and inflammatory mechanisms on pregnancy outcome. Human Reproduction Update. 2016;22(1):104–115. doi: 10.1093/humupd/dmv044.
    1. Lalani S., Choudhry A. J., Firth B., et al. Endometriosis and adverse maternal, fetal and neonatal outcomes, a systematic review and meta-analysis. Human Reproduction (Oxford, England) 2018;33(10):1854–1865. doi: 10.1093/humrep/dey269.

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir