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Systematic review of pregnancy outcomes after fertility-preserving treatment of uterine fibroids

Published:January 09, 2020DOI:https://doi.org/10.1016/j.rbmo.2020.01.003

      HIGHLIGHTS

      • Myomectomy is the gold standard to preserve fertility with the best pregnancy outcome
      • Fibroid ablation may be offered to women where there are contraindications to surgery
      • Uterine artery embolisation is associated with poor pregnancy outcomes.
      • There are too few reported pregnancies after ulipristal acetate to assess.

      Abstract

      The aim of this study was to compare pregnancy outcomes after medical (ulipristal acetate [UPA]), surgical (myomectomy) and radiological (uterine artery embolization [UAE] or thermal ablation) therapy for fibroids in women. A systematic review was conducted and ScienceDirect, PubMed, Web of Science and Cochrane Library databases were thoroughly searched from 2000 to 2018. Only primary research was included with independent extraction of articles by two reviewers, using a standardized form. Data were available on 12 pregnancies after treatment with UPA, 1575 after myomectomy, 424 after UAE and 420 after fibroid ablation. Results after UPA therapy were not included in the statistical analysis owing to the limited number of cases; most were ongoing pregnancies. High rates of successful pregnancy were seen after myomectomy (75.6%) and fibroid ablation (70.5%), whereas pregnancies after UAE had the lowest live birth rates (60.6%) and highest miscarriage rates (27.4%) (both P < 0.001 versus other treatments). In conclusion, myomectomy is associated with better pregnancy outcomes than other fertility-preserving treatments for fibroids. At present, UPA is the only medical treatment for fibroids; however, the evidence on pregnancy outcome is limited. In the absence of randomized controlled trials, these data may be of benefit in advising patients about future pregnancy.

      KEYWORDS

      Introduction

      Fibroids (leiomyomata) are the most common benign tumours of the pelvis in women of reproductive age group and are more commonly seen in African–American women (
      • Verkauf B.S.
      Myomectomy for fertility enhancement and preservation.
      ). In addition to pain and abnormal uterine bleeding, fibroids have been associated with infertility and a higher risk of miscarriage, placenta praevia, fetal malpresentation, preterm labour, the need for caesarean section and peripartum haemorrhage (
      • Klatsky P.C.
      • Tran N.D.
      • Caughey A.B.
      • Fujimoto V.Y.
      Fibroids and reproductive outcomes: a systematic literature review from conception to delivery.
      ). Present evidence indicates that submucosal fibroids of any size and intramural fibroids wider than 4 cm in diameter significantly impair fertility and results of assisted reproductive therapy (
      • Zepiridis L.I.
      • Grimbizis G.F.
      • Tarlatzis B.C.
      Infertility and uterine fibroids.
      ).
      The appropriate approach for the treatment of fibroids depends on multiple factors, including age, fertility wishes, the severity of symptoms and clinical presentation, the type and size of the fibroids, and the woman's overall health, with an emphasis on medical and surgical history or ongoing treatments (
      Society of Obstetricians & Gynaecologists of Canada
      SOGC clinical practice guidelines. Uterine fibroid embolization (UFE).
      ;
      • Flynn M.
      • Jamison M.
      • Datta S.
      • Myers E.
      Health care resource use for uterine fibroid tumors in the United States.
      ;
      • Marret H.
      • Fritel X.
      • Ouldamer L.
      • Bendifallah S.
      • Brun J.L.
      • De Jesus I.
      • Derrien J.
      • Giraudet G.
      • Kahn V.
      • Koskas M.
      • Legendre G.
      • Lucot J.P.
      • Niro J.
      • Panel P.
      • Pelage J.P.
      • Fernandez H.
      Cngof
      Therapeutic management of uterine fibroid tumors: updated French guidelines.
      ;
      • van der Kooij S.M.
      • Ankum W.M.
      • Hehenkamp W.J.
      Review of nonsurgical/minimally invasive treatments for uterine fibroids.
      ). As fibroids are benign, choice of treatment methods should aim to minimize risk and morbidity.
      At present, the management of fibroids in women who wish to preserve their uterus and fertility remains a challenge. The gold standard is myomectomy (
      • Verkauf B.S.
      Myomectomy for fertility enhancement and preservation.
      ;
      • Flynn M.
      • Jamison M.
      • Datta S.
      • Myers E.
      Health care resource use for uterine fibroid tumors in the United States.
      ;
      • Flyckt R.
      • Coyne K.
      • Falcone T.
      Minimally Invasive Myomectomy.
      ), which can be carried out by hysteroscopy, laparoscopy, laparotomy or robotic-assisted, each having their pros and cons (
      • Cinar M.
      • Aksoy R.T.
      • Guzel A.I.
      • Tokmak A.
      • Yenicesu O.
      • Sarikaya E.
      • Evliyaoglu O.
      The association between clinical parameters and uterine fibroid size in patients who underwent abdominal myomectomy.
      ;
      • Adesina K.T.
      • Owolabi B.O.
      • Raji H.O.
      • Olarinoye A.O.
      Abdominal myomectomy: A retrospective review of determinants and outcomes of complications at the University of Ilorin Teaching Hospital, Ilorin, Nigeria.
      ;
      • Bean E.M.
      • Cutner A.
      • Holland T.
      • Vashisht A.
      • Jurkovic D.
      • Saridogan E.
      Laparoscopic Myomectomy: A Single-center Retrospective Review of 514 Patients.
      ;
      • Choi E.J.
      • Rho A.M.
      • Lee S.R.
      • Jeong K.
      • Moon H.S.
      Robotic Single-Site Myomectomy: Clinical Analysis of 61 Consecutive Cases.
      ;
      • Lonnerfors C.
      Robot-assisted myomectomy.
      ). The type of myomectomy used is greatly influenced by the clinical presentation, size, number and location of the fibroids (
      • Cinar M.
      • Aksoy R.T.
      • Guzel A.I.
      • Tokmak A.
      • Yenicesu O.
      • Sarikaya E.
      • Evliyaoglu O.
      The association between clinical parameters and uterine fibroid size in patients who underwent abdominal myomectomy.
      ;
      • Martinez M.E.G.
      • Domingo M.V.C.
      Size, Type, and Location of Myoma as Predictors for Successful Laparoscopic Myomectomy: A Tertiary Government Hospital Experience.
      ).
      Alternative medical treatment with ulipristal acetate (UPA) and radiological procedures, including uterine artery embolization (UAE) and fibroid thermal ablation, have been evaluated. Ulipristal acetate is a selective progesterone receptor modulator that has antiproliferative effects on the leiomyoma and endometrium (
      • Vilos G.A.
      • Allaire C.
      • Laberge P.-Y.
      • Leyland N.
      • Vilos A.G.
      • Murji A.
      • Chen I.
      The Management of Uterine Leiomyomas.
      ). It also induces apoptosis and suppresses angiogenic factors, such as vascular endothelial growth factor and adrenomedullin (
      • Xu Q.
      • Ohara N.
      • Chen W.
      • Liu J.
      • Sasaki H.
      • Morikawa A.
      • Sitruk-Ware R.
      • Johansson E.D.
      • Maruo T.
      Progesterone receptor modulator CDB-2914 down-regulates vascular endothelial growth factor, adrenomedullin and their receptors and modulates progesterone receptor content in cultured human uterine leiomyoma cells.
      ;
      • Yoshida S.
      • Ohara N.
      • Xu Q.
      • Chen W.
      • Wang J.
      • Nakabayashi K.
      • Sasaki H.
      • Morikawa A.
      • Maruo T.
      Cell-type specific actions of progesterone receptor modulators in the regulation of uterine leiomyoma growth.
      ). On the other hand, UAE involves selective cannulation of uterine arteries with injection of emboli to occlude blood supply to the leiomyoma (
      • Viswanathan M.
      • Hartmann K.
      • McKoy N.
      • Stuart G.
      • Rankins N.
      • Thieda P.
      • Lux L.J.
      • Lohr K.N.
      Management of uterine fibroids: an update of the evidence.
      ). It is, however, associated with potential complications, such as premature ovarian insufficiency and pelvic infection, and has a high re-intervention rate (
      • Freed M.M.
      • Spies J.B.
      Uterine artery embolization for fibroids: a review of current outcomes.
      ;
      • Torre A.
      • Paillusson B.
      • Fain V.
      • Labauge P.
      • Pelage J.P.
      • Fauconnier A.
      Uterine artery embolization for severe symptomatic fibroids: effects on fertility and symptoms.
      ). In addition, UAE is relatively contraindicated in women desiring future pregnancies as its effect on fertility has not been clearly defined (
      American College of Obstetricians & Gynecologists
      ACOG practice bulletin. Alternatives to hysterectomy in the management of leiomyomas.
      ;
      • Stokes L.S.
      • Wallace M.J.
      • Godwin R.B.
      • Kundu S.
      • Cardella J.F.
      Society of Interventional Radiology Standards of Practice C
      Quality improvement guidelines for uterine artery embolization for symptomatic leiomyomas.
      ). Fibroid thermal ablation techniques include radiofrequency volumetric thermal ablation and high-intensity focused ultrasound, magnetic resonance imaging or laparoscopy (
      • Hesley G.K.
      • Gorny K.R.
      • Henrichsen T.L.
      • Woodrum D.A.
      • Brown D.L.
      A clinical review of focused ultrasound ablation with magnetic resonance guidance: an option for treating uterine fibroids.
      ;
      • Chudnoff S.G.
      • Berman J.M.
      • Levine D.J.
      • Harris M.
      • Guido R.S.
      • Banks E.
      Outpatient procedure for the treatment and relief of symptomatic uterine myomas.
      ;
      • Vilos G.A.
      • Allaire C.
      • Laberge P.-Y.
      • Leyland N.
      • Vilos A.G.
      • Murji A.
      • Chen I.
      The Management of Uterine Leiomyomas.
      ); these induce targeted necrosis in the fibroid. These treatment methods are primarily indicated for women who are unable to undergo surgery for symptomatic fibroids (
      Society of Obstetricians & Gynaecologists of Canada
      SOGC clinical practice guidelines. Uterine fibroid embolization (UFE).
      ;
      • Marret H.
      • Fritel X.
      • Ouldamer L.
      • Bendifallah S.
      • Brun J.L.
      • De Jesus I.
      • Derrien J.
      • Giraudet G.
      • Kahn V.
      • Koskas M.
      • Legendre G.
      • Lucot J.P.
      • Niro J.
      • Panel P.
      • Pelage J.P.
      • Fernandez H.
      Cngof
      Therapeutic management of uterine fibroid tumors: updated French guidelines.
      ).
      Women who undergo myomectomy or UAE seem to be at higher risk during pregnancy as complications with abnormal placentation and a higher risk of the fetus being small for gestational age have been recorded (
      • Pron G.
      • Mocarski E.
      • Bennett J.
      • Vilos G.
      • Common A.
      • Vanderburgh L.
      Ontario U.F.E.C.G
      Pregnancy after uterine artery embolization for leiomyomata: the Ontario multicenter trial.
      ;
      • Dutton S.
      • Hirst A.
      • McPherson K.
      • Nicholson T.
      • Maresh M.
      A UK multicentre retrospective cohort study comparing hysterectomy and uterine artery embolisation for the treatment of symptomatic uterine fibroids (HOPEFUL study): main results on medium-term safety and efficacy.
      ;
      • Marret H.
      • Fritel X.
      • Ouldamer L.
      • Bendifallah S.
      • Brun J.L.
      • De Jesus I.
      • Derrien J.
      • Giraudet G.
      • Kahn V.
      • Koskas M.
      • Legendre G.
      • Lucot J.P.
      • Niro J.
      • Panel P.
      • Pelage J.P.
      • Fernandez H.
      Cngof
      Therapeutic management of uterine fibroid tumors: updated French guidelines.
      ). Uterine rupture is of further major concern (
      • Hortu I.
      • Akdemir A.
      • Sendag F.
      • Oztekin M.K.
      Uterine rupture in pregnancy after robotic myomectomy.
      ;
      • Pakniat H.
      • Soofizadeh N.
      • Khezri M.B.
      Spontaneous uterine rupture after abdominal myomectomy at the gestational age of 20 weeks in pregnancy: A case report.
      ;
      • Cho H.
      Rupture of a myomectomy site in the third trimester of pregnancy after myomectomy, septoplasty and cesarean section: A case report.
      ).
      It is unclear whether the risks to a subsequent pregnancy from conservative approaches to treatment of fibroids differ from surgical myomectomy. Hence, the purpose of this review is to evaluate and compare pregnancy outcomes resulting from currently used therapeutic modalities.

      Materials and methods

      The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) approach was used for this study. ScienceDirect, PubMed, Web of Science and Cochrane Library databases were thoroughly searched using the following key words: ulipristal acetate, myomectomy, uterine artery embolism, ablation, reduction, fibroid, leiomyoma, leiomyomata, pregnancy, infertility, pregnancy loss and IVF. The articles reviewed were inclusive of primary research, such as randomized controlled trials, cohort studies, prospective studies, retrospective studies, case control studies, case reports and case series from year 2000 to 2018. Additional studies were searched for in the references of all identified publications, including previous narrative reviews and meta-analyses.

      Selection criteria

      Only studies published as full-length articles were included. Pregnancy outcomes were assessed by rates of live birth, miscarriage, stillbirth, ectopic pregnancy, premature delivery and cases of uterine rupture. The exclusion criteria were women treated for indications other than fibroids and studies that used more than one treatment method.

      Data extraction

      All identified publications were then independently reviewed by two reviewers (SCK and ZZW). The data were independently extracted using a standardized form, and study design, patient demographics, intervention, time taken to conceive, number of pregnancies, pregnancy outcomes and complications were recorded. Discrepancies were subsequently resolved through consensus. The selection process according to PRISMA is presented in Figure 1.
      Figure 1
      Figure 1Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Flowchart.

      Statistical analysis

      Pregnancy outcomes after UPA, myomectomy, UAE or thermal ablation were compared. Statistical software SPSS Version 24.0.0.2 (IBM Corp., USA) was used to analyse the dataset. A chi-squared test of independence was conducted to examine the relationship between treatment modality and pregnancy outcomes. The time taken to conceive was expressed as mean and range. P < 0.05 was regarded as statistically significant.
      Ethics Review Board approval was not required as all data were abstracted from previously published studies. No funding was received for this study.

      Results

      The initial literature search retrieved 1805 articles after duplicates were removed. One study was removed from the analysis as it only presented post-hysteroscopic myomectomy data, and therefore has significant differences in techniques used and post-myomectomy risks compared with other studies (
      • Bernard G.
      • Darai E.
      • Poncelet C.
      • Benifla J.L.
      • Madelenat P.
      Fertility after hysteroscopic myomectomy: effect of intramural myomas associated.
      ). Some articles were excluded for more than one criterion, in which case the first criterion according to the order methodology, intervention and insufficient results is reported. After exclusion, four randomized controlled trials, three cohort studies, 15 prospective studies, 19 retrospective studies, 11 case series and 16 case reports were included; the PRISMA flowchart is presented in Figure 1. Details of the study type included for each treatment modality is presented in Figure 2. Overall, data were available from 12 pregnancies after treatment with UPA, 1575 after myomectomy, 424 after UAE and 420 after ablation (Figure 2).
      Figure 2
      Figure 2Studies included by conservative treatment modality.

      Ulipristal acetate

      The nine reports reviewed included women with fibroids that were intramural or submucosal, ranging from 20 mm to 100 mm in diameter (
      • Wdowiak A.
      Pre-treatment with ulipristal acetate before ICSI procedure: a.
      ;
      • Luyckx M.
      • Squifflet J.L.
      • Jadoul P.
      • Votino R.
      • Dolmans M.M.
      • Donnez J.
      First series of 18 pregnancies after ulipristal acetate treatment for uterine fibroids.
      ;
      • Monleon J.
      • Martinez-Varea A.
      • Galliano D.
      • Pellicer A.
      Successful pregnancy after treatment with ulipristal acetate for uterine fibroids.
      ;
      • Romer T.
      Case report: successful pregnancy after combined preoperative pretreatment with ulipristal acetate and laparoscopic myoma enucleation in deep-seated cervical posterior wall myoma and desire to have children.
      ;
      • Tikhomirov A.L.
      Successful pregnancy after gigantic uterine fibroids treatment with the help of ulipristal acetate.
      ;
      • Luyckx M.
      • Pirard C.
      • Fellah L.
      • Dereume A.
      • Mhallem M.
      • Debieve F.
      • Squifflet J.
      Long-term nonsurgical control with ulipristal acetate of multiple uterine fibroids, enabling pregnancy.
      ;
      • Murad K.
      Spontaneous Pregnancy Following Ulipristal Acetate Treatment in a Woman with a Symptomatic Uterine Fibroid.
      ;
      • Kale A.R.
      Ulipristal acetate (UPA) for fibroids–IVF outcomes following treatment with UPA after IVF failure: series of 2 case reports.
      ;
      • Hrgovic Z.
      • Habek D.
      • Cerkez Habek J.
      • Hrgovic I.
      • Jerkovic Gulin S.
      • Gulin D.
      Spontaneous pregnancy during ulipristal acetate treatment of giant uterine leiomyoma.
      ). Of the 12 pregnancies (Table 1), six (50.0%) resulted in live birth, four (33.3%) were ongoing and two (17.7%) ended in miscarriage. Of the six livebirths, two babies were delivered prematurely at 34 and 36 weeks, respectively (
      • Monleon J.
      • Martinez-Varea A.
      • Galliano D.
      • Pellicer A.
      Successful pregnancy after treatment with ulipristal acetate for uterine fibroids.
      ;
      • Hrgovic Z.
      • Habek D.
      • Cerkez Habek J.
      • Hrgovic I.
      • Jerkovic Gulin S.
      • Gulin D.
      Spontaneous pregnancy during ulipristal acetate treatment of giant uterine leiomyoma.
      ), whereas the others were delivered at term. No cases of intrauterine growth retardation or congenital malformation were recorded. The time to conception after UPA was reported in seven cases, and ranged from 1–3.5 months (
      • Wdowiak A.
      Pre-treatment with ulipristal acetate before ICSI procedure: a.
      ;
      • Monleon J.
      • Martinez-Varea A.
      • Galliano D.
      • Pellicer A.
      Successful pregnancy after treatment with ulipristal acetate for uterine fibroids.
      ;
      • Tikhomirov A.L.
      Successful pregnancy after gigantic uterine fibroids treatment with the help of ulipristal acetate.
      ;
      • Luyckx M.
      • Pirard C.
      • Fellah L.
      • Dereume A.
      • Mhallem M.
      • Debieve F.
      • Squifflet J.
      Long-term nonsurgical control with ulipristal acetate of multiple uterine fibroids, enabling pregnancy.
      ;
      • Murad K.
      Spontaneous Pregnancy Following Ulipristal Acetate Treatment in a Woman with a Symptomatic Uterine Fibroid.
      ;
      • Kale A.R.
      Ulipristal acetate (UPA) for fibroids–IVF outcomes following treatment with UPA after IVF failure: series of 2 case reports.
      ;
      • Hrgovic Z.
      • Habek D.
      • Cerkez Habek J.
      • Hrgovic I.
      • Jerkovic Gulin S.
      • Gulin D.
      Spontaneous pregnancy during ulipristal acetate treatment of giant uterine leiomyoma.
      ).
      Table 1Pregnancy outcomes after ulipristal acetate therapy
      Study, yearStudy designMean age, yearsTotal number of womenNumber of pregnant womenPregnanciesPregnancy outcomesTime to conception, monthsMode of delivery
      Live birthOngoing pregnancyMiscarriagesGestation at delivery, weeks
      • Luyckx M.
      • Squifflet J.L.
      • Jadoul P.
      • Votino R.
      • Dolmans M.M.
      • Donnez J.
      First series of 18 pregnancies after ulipristal acetate treatment for uterine fibroids.
      Case series36.422312NR
      • Hrgovic Z.
      • Habek D.
      • Cerkez Habek J.
      • Hrgovic I.
      • Jerkovic Gulin S.
      • Gulin D.
      Spontaneous pregnancy during ulipristal acetate treatment of giant uterine leiomyoma.
      Case report33111136 + 33CS
      • Kale A.R.
      Ulipristal acetate (UPA) for fibroids–IVF outcomes following treatment with UPA after IVF failure: series of 2 case reports.
      Case report28.522223NR
      • Murad K.
      Spontaneous Pregnancy Following Ulipristal Acetate Treatment in a Woman with a Symptomatic Uterine Fibroid.
      Case report351111382VD
      • Luyckx M.
      • Pirard C.
      • Fellah L.
      • Dereume A.
      • Mhallem M.
      • Debieve F.
      • Squifflet J.
      Long-term nonsurgical control with ulipristal acetate of multiple uterine fibroids, enabling pregnancy.
      Case report391111393.5CS
      • Romer T.
      Case report: successful pregnancy after combined preoperative pretreatment with ulipristal acetate and laparoscopic myoma enucleation in deep-seated cervical posterior wall myoma and desire to have children.
      Case report411111TermNRVD
      • Tikhomirov A.L.
      Successful pregnancy after gigantic uterine fibroids treatment with the help of ulipristal acetate.
      Case report361111383CS
      • Monleon J.
      • Martinez-Varea A.
      • Galliano D.
      • Pellicer A.
      Successful pregnancy after treatment with ulipristal acetate for uterine fibroids.
      Case report371111343CS
      • Wdowiak A.
      Pre-treatment with ulipristal acetate before ICSI procedure: a.
      Case report3511111
      Total1111126 (50.0%)4 (33.3%)2 (17.7%)
      CS, caesarean section; NR not reported; VD, vaginal delivery; –, not-applicable.

      Myomectomy

      A total of 1575 pregnancies after myomectomy were identified. The surgical approach was reported in 1449 women: 1047 women underwent laparoscopic myomectomy, 107 operations were robotic assisted, 51 were open surgeries or laparotomies, 26 were mini-laparotomies, whereas 218 cases were not clearly stated (Table 2). These pregnancies resulted in 1191 live births (75.6%), 42 ongoing pregnancies (2.7%), 299 miscarriages (19.0%), 24 ectopic pregnancies (1.5%) and two stillbirths. Of the 17 pregnancies that were terminated (1.1%), three were caused by fetal anomaly, one was caused by chromosomal abnormalities, whereas the remaining terminations were for either social or maternal medical reasons (
      • Dessolle L.
      • Soriano D.
      • Poncelet C.
      • Benifla J.L.
      • Madelenat P.
      • Darai E.
      Determinants of pregnancy rate and obstetric outcome after laparoscopic myomectomy for infertility.
      ;
      • Soriano D.
      • Dessolle L.
      • Poncelet C.
      • Benifla J.L.
      • Madelenat P.
      • Darai E.
      Pregnancy outcome after laparoscopic and laparoconverted myomectomy.
      ;
      • Kumakiri J.
      • Takeuchi H.
      • Kitade M.
      • Kikuchi I.
      • Shimanuki H.
      • Itoh S.
      • Kinoshita K.
      Pregnancy and delivery after laparoscopic myomectomy.
      ;
      • Paul P.G.
      • Koshy A.K.
      • Thomas T.
      Pregnancy outcomes following laparoscopic myomectomy and single-layer myometrial closure.
      ;
      • Seracchioli R.
      • Manuzzi L.
      • Vianello F.
      • Gualerzi B.
      • Savelli L.
      • Paradisi R.
      • Venturoli S.
      Obstetric and delivery outcome of pregnancies achieved after laparoscopic myomectomy.
      ;
      • Mara M.
      • Maskova J.
      • Fucikova Z.
      • Kuzel D.
      • Belsan T.
      • Sosna O.
      Midterm Clinical and First Reproductive Results of a Randomized Controlled Trial Comparing Uterine Fibroid Embolization and Myomectomy.
      ;
      • Bernardi T.S.
      • Radosa M.P.
      • Weisheit A.
      • Diebolder H.
      • Schneider U.
      • Schleussner E.
      • Runnebaum I.B.
      Laparoscopic myomectomy: a 6-year follow-up single-center cohort analysis of fertility and obstetric outcome measures.
      ;
      • Borja de Mozota D.
      • Kadhel P.
      • Janky E.
      Fertility, pregnancy outcomes and deliveries following myomectomy: experience of a French Caribbean University Hospital.
      ;
      • Sangha R.
      • Strickler R.
      • Dahlman M.
      • Havstad S.
      • Wegienka G.
      Myomectomy to Conserve Fertility: Seven-Year Follow-Up.
      ). A total of six placental abnormalities were reported (four placenta previa, one placenta accreta and one placenta percreta (
      • Dubuisson J.B.
      • Chapron C.
      • Fauconnier A.
      • Babaki-Fard K.
      Laparoscopic myomectomy fertility results.
      ;
      • Paul P.G.
      • Koshy A.K.
      • Thomas T.
      Pregnancy outcomes following laparoscopic myomectomy and single-layer myometrial closure.
      ;
      • Tinelli A.
      • Hurst B.S.
      • Hudelist G.
      • Tsin D.A.
      • Stark M.
      • Mettler L.
      • Guido M.
      • Malvasi A.
      Laparoscopic myomectomy focusing on the myoma pseudocapsule: technical and outcome reports.
      ;
      • Pitter M.C.
      • Gargiulo A.R.
      • Bonaventura L.M.
      • Lehman J.S.
      • Srouji S.S.
      Pregnancy outcomes following robot-assisted myomectomy.
      ). Sixty-three preterm deliveries (5.3%) were reported, in which eight were of extreme prematurity of less than 34 weeks with one case at 24 weeks. Overall, 60.8% were delivered by caesarean section versus 39.2% delivered vaginally.
      Table 2Pregnancy outcomes after myomectomy
      Twenty-four ectopic pregnancies, 17 terminations and two stillbirths.
      Study, yearStudy designMean age, yearsManagementTotal number of womenNumber of pregnant womenPregnanciesPregnancy outcomesMean time to conception (months)Mode of delivery
      Live birthOngoing pregnancyMiscarriageGestation at delivery Gestation, n
      Gestationn
      • Mara M.
      • Maskova J.
      • Fucikova Z.
      • Kuzel D.
      • Belsan T.
      • Sosna O.
      Midterm Clinical and First Reproductive Results of a Randomized Controlled Trial Comparing Uterine Fibroid Embolization and Myomectomy.
      Randomized controlled trial32LM and OM4031321956Preterm513NR
      • Palomba S.
      • Zupi E.
      • Falbo A.
      • Russo T.
      • Marconi D.
      • Tolino A.
      • Manguso F.
      • Mattei A.
      • Zullo F.
      A multicenter randomized, controlled study comparing laparoscopic versus minilaparotomic myomectomy: reproductive outcomes.
      Randomized controlled trial26LM and ML13662625408Preterm25VD (31%); LSCS (69%)
      • Seracchioli R.
      • Rossi S.
      • Govoni F.
      • Rossi E.
      • Venturoli S.
      • Bulletti C.
      • Flamigni C.
      Fertility and obstetric outcome after laparoscopic myomectomy of large myomata: a randomized comparison with abdominal myomectomy.
      Randomized controlled trial34LM and OM115636347510Preterm3NRVD (28%); LSCS (72%)
      • Bernardi T.S.
      • Radosa M.P.
      • Weisheit A.
      • Diebolder H.
      • Schneider U.
      • Schleussner E.
      • Runnebaum I.B.
      Laparoscopic myomectomy: a 6-year follow-up single-center cohort analysis of fertility and obstetric outcome measures.
      Prospective observational study33LM59445538013Preterm523.2VD (24%); LSCS (76%)
      • Tinelli A.
      • Hurst B.S.
      • Hudelist G.
      • Tsin D.A.
      • Stark M.
      • Mettler L.
      • Guido M.
      • Malvasi A.
      Laparoscopic myomectomy focusing on the myoma pseudocapsule: technical and outcome reports.
      Prospective observational study36.5LM235
      Includes those who did not intend pregnancy. CS, caesarean section; HM, hysteroscopic myomectomy; LM, laparoscopic myomectomy; LSCS, lower segment caesarean section; ML, mini-laparotomy; NR, not reported; OM, open/laparotomic myomectomy; RM, robot-assisted myomectomy; VD, vaginal delivery.
      97979700Term10–24 (range)SVD (42.2%); LCSC (32.9%); vacuum (24.8%)
      • Sizzi O.
      • Rossetti A.
      • Malzoni M.
      • Minelli L.
      • La Grotta F.
      • Soranna L.
      • Panunzi S.
      • Spagnolo R.
      • Imperato F.
      • Landi S.
      • Fiaccamento A.
      • Stola E.
      Italian multicenter study on complications of laparoscopic myomectomy.
      Prospective observational study36.1LM1683
      Includes those who did not intend pregnancy. CS, caesarean section; HM, hysteroscopic myomectomy; LM, laparoscopic myomectomy; LSCS, lower segment caesarean section; ML, mini-laparotomy; NR, not reported; OM, open/laparotomic myomectomy; RM, robot-assisted myomectomy; VD, vaginal delivery.
      386386309077Preterm9NRVD (22%); CS (78%)
      • Campo S.
      • Campo V.
      • Gambadauro P.
      Reproductive outcome before and after laparoscopic or abdominal myomectomy for subserous or intramural myomas.
      Prospective observational study32.4LM and OM4125292504TermNRNR
      • Dubuisson J.B.
      • Chapron C.
      • Fauconnier A.
      • Babaki-Fard K.
      Laparoscopic myomectomy fertility results.
      Prospective observational study33.2LM9143513749NR16NR
      • Shue S.
      • Radeva M.
      • Falcone T.
      Comparison of Long-Term Fertility Outcomes after Myomectomy: Relationship with Number of Myomas Removed.
      Retrospective observational study35.7RM, LM, OM144797963014Preterm4NRCS (100%)
      • Sangha R.
      • Strickler R.
      • Dahlman M.
      • Havstad S.
      • Wegienka G.
      Myomectomy to Conserve Fertility: Seven-Year Follow-Up.
      Retrospective observational studyNRLM and OM124545431614Preterm4NRVD (94%); CS (6%)
      • Borja de Mozota D.
      • Kadhel P.
      • Janky E.
      Fertility, pregnancy outcomes and deliveries following myomectomy: experience of a French Caribbean University Hospital.
      Retrospective observational study36.2Myomectomy220546639717Preterm720.7VD (72%); CS (28%)
      • Pitter M.C.
      • Gargiulo A.R.
      • Bonaventura L.M.
      • Lehman J.S.
      • Srouji S.S.
      Pregnancy outcomes following robot-assisted myomectomy.
      Retrospective observational Study34.8RM872
      Includes those who did not intend pregnancy. CS, caesarean section; HM, hysteroscopic myomectomy; LM, laparoscopic myomectomy; LSCS, lower segment caesarean section; ML, mini-laparotomy; NR, not reported; OM, open/laparotomic myomectomy; RM, robot-assisted myomectomy; VD, vaginal delivery.
      10712792924Preterm1612.9VD (4.3%); LSCS (95.7%)
      • Paul P.G.
      • Koshy A.K.
      • Thomas T.
      Pregnancy outcomes following laparoscopic myomectomy and single-layer myometrial closure.
      Retrospective observational study30LM217
      Includes those who did not intend pregnancy. CS, caesarean section; HM, hysteroscopic myomectomy; LM, laparoscopic myomectomy; LSCS, lower segment caesarean section; ML, mini-laparotomy; NR, not reported; OM, open/laparotomic myomectomy; RM, robot-assisted myomectomy; VD, vaginal delivery.
      115141106028Preterm38.9VD (18%); LSCS (82%)
      • Seracchioli R.
      • Manuzzi L.
      • Vianello F.
      • Gualerzi B.
      • Savelli L.
      • Paradisi R.
      • Venturoli S.
      Obstetric and delivery outcome of pregnancies achieved after laparoscopic myomectomy.
      Retrospective observational study33.7LM233127158106343Preterm217.8VD (25.5%); LSCS (74.5%)
      • Kumakiri J.
      • Takeuchi H.
      • Kitade M.
      • Kikuchi I.
      • Shimanuki H.
      • Itoh S.
      • Kinoshita K.
      Pregnancy and delivery after laparoscopic myomectomy.
      Retrospective observational study35.5LM108404732111Preterm113VD (59%); LSCS (41%)
      • Seracchioli R.
      Laparoscopic myomectomy for fibroids penetrating the uterine cavity: is it a safe procedure?.
      Retrospective observational study34.9LM3299702TermNRVD (14%); LSCS (86%)
      • Soriano D.
      • Dessolle L.
      • Poncelet C.
      • Benifla J.L.
      • Madelenat P.
      • Darai E.
      Pregnancy outcome after laparoscopic and laparoconverted myomectomy.
      Retrospective Observational Study35.9LM and OM10652544009Preterm111.3VD (74%); LSCS (26%)
      • Dessolle L.
      • Soriano D.
      • Poncelet C.
      • Benifla J.L.
      • Madelenat P.
      • Darai E.
      Determinants of pregnancy rate and obstetric outcome after laparoscopic myomectomy for infertility.
      Retrospective observational study36.1LM10342443406NR7.5VD (68%); LSCS (32%)
      • Rossetti A.
      • Sizzi O.
      • Soranna L.
      • Mancuso S.
      • Lanzone A.
      Fertility outcome: long-term results after laparoscopic myomectomy.
      Retrospective observational study36LM2919211524Preterm37.1VD (26.6%) LSCS (73.4%)
      Total4588144915751191 (75.6%)42 (2.7%)299 (19.0%)
      a Twenty-four ectopic pregnancies, 17 terminations and two stillbirths.
      b Includes those who did not intend pregnancy.CS, caesarean section; HM, hysteroscopic myomectomy; LM, laparoscopic myomectomy; LSCS, lower segment caesarean section; ML, mini-laparotomy; NR, not reported; OM, open/laparotomic myomectomy; RM, robot-assisted myomectomy; VD, vaginal delivery.
      A total of 10 cases (0.6%) of uterine rupture occurred with one resulting in intrauterine death (
      • Dubuisson J.B.
      • Chapron C.
      • Fauconnier A.
      • Babaki-Fard K.
      Laparoscopic myomectomy fertility results.
      ;
      • Sizzi O.
      • Rossetti A.
      • Malzoni M.
      • Minelli L.
      • La Grotta F.
      • Soranna L.
      • Panunzi S.
      • Spagnolo R.
      • Imperato F.
      • Landi S.
      • Fiaccamento A.
      • Stola E.
      Italian multicenter study on complications of laparoscopic myomectomy.
      ;
      • Pitter M.C.
      • Gargiulo A.R.
      • Bonaventura L.M.
      • Lehman J.S.
      • Srouji S.S.
      Pregnancy outcomes following robot-assisted myomectomy.
      ;
      • Bernardi T.S.
      • Radosa M.P.
      • Weisheit A.
      • Diebolder H.
      • Schneider U.
      • Schleussner E.
      • Runnebaum I.B.
      Laparoscopic myomectomy: a 6-year follow-up single-center cohort analysis of fertility and obstetric outcome measures.
      ;
      • Sangha R.
      • Strickler R.
      • Dahlman M.
      • Havstad S.
      • Wegienka G.
      Myomectomy to Conserve Fertility: Seven-Year Follow-Up.
      ). One out of 10 woman had undergone open myomectomy, one had undergone robotic-assisted myomectomy and the remaining eight had undergone laparoscopic myomectomy. Two of the women treated with laparoscopic myomectomy had undergone an additional laparotomy for myomectomy and for corneal reanastomosis afterwards. One uterine rupture occurred after a road traffic accident at 24 weeks in a twin pregnancy. Three cases occurred at term, whereas six cases occurred before 35 weeks (range 24–34). The myomectomy-to-conception interval was only reported in four cases, with one patient conceiving 18 weeks after surgery. The other three women conceived more than 12 months from surgery, at 14, 18 and 36 months (
      • Dubuisson J.B.
      • Fauconnier A.
      • Deffarges J.V.
      • Norgaard C.
      • Kreiker G.
      • Chapron C.
      Pregnancy outcome and deliveries following laparoscopic myomectomy.
      ;
      • Dubuisson J.B.
      • Chapron C.
      • Fauconnier A.
      • Babaki-Fard K.
      Laparoscopic myomectomy fertility results.
      ;
      • Pitter M.C.
      • Gargiulo A.R.
      • Bonaventura L.M.
      • Lehman J.S.
      • Srouji S.S.
      Pregnancy outcomes following robot-assisted myomectomy.
      ). Uterine rupture occurred in two women in whom the uterine cavity had been breached and five women in whom the uterine cavity was not entered, although two of them had undergone repeat laparotomy. The remaining three cases did not indicate whether the uterine cavity was breached (
      • Sizzi O.
      • Rossetti A.
      • Malzoni M.
      • Minelli L.
      • La Grotta F.
      • Soranna L.
      • Panunzi S.
      • Spagnolo R.
      • Imperato F.
      • Landi S.
      • Fiaccamento A.
      • Stola E.
      Italian multicenter study on complications of laparoscopic myomectomy.
      ;
      • Pitter M.C.
      • Gargiulo A.R.
      • Bonaventura L.M.
      • Lehman J.S.
      • Srouji S.S.
      Pregnancy outcomes following robot-assisted myomectomy.
      ;
      • Sangha R.
      • Strickler R.
      • Dahlman M.
      • Havstad S.
      • Wegienka G.
      Myomectomy to Conserve Fertility: Seven-Year Follow-Up.
      ).
      Overall, the average time from surgery to pregnancy was 13.0 months (range 5–24 months). This contrasts with the only case series of pregnancy after hysteroscopic myomectomy, the time to pregnancy was shorter in women with no intramural fibroids at 3.1 months (range 2–5 months) compared with 4.8 months in those with intramural fibroids (P = 0.05) (
      • Bernard G.
      • Darai E.
      • Poncelet C.
      • Benifla J.L.
      • Madelenat P.
      Fertility after hysteroscopic myomectomy: effect of intramural myomas associated.
      ).

      Uterine artery embolization

      From the 19 studies of 424 pregnancies (Table 3), the overall live birth rate, ongoing pregnancy rate and miscarriage rate were 60.6% (257/424), 4.0% (17/424) and 27.4% (116/424), respectively. Ten (2.4%) ectopic pregnancies and three (0.7%) stillbirths were reported, whereas the remaining 21 (5%) pregnancies were terminated (
      • Ravina J.H.
      • Vigneron N.C.
      • Aymard A.
      • Le Dref O.
      • Merland J.J.
      Pregnancy after embolization of uterine myoma: report of 12 cases.
      ;
      • McLucas B.
      • Reed R.A.
      • Goodwin S.
      • Rappaport A.
      • Adler L.
      • Perrella R.
      • Dalrymple J.
      Outcomes following unilateral uterine artery embolisation.
      ;
      • Walker W.J.
      • Pelage J.P.
      Uterine artery embolisation for symptomatic fibroids: clinical results in 400 women with imaging follow up.
      ;
      • Carpenter T.T.
      • Walker W.J.
      Pregnancy following uterine artery embolisation for symptomatic fibroids: a series of 26 completed pregnancies.
      ;
      • Pron G.
      • Mocarski E.
      • Bennett J.
      • Vilos G.
      • Common A.
      • Vanderburgh L.
      Ontario U.F.E.C.G
      Pregnancy after uterine artery embolization for leiomyomata: the Ontario multicenter trial.
      ;
      • Walker W.J.
      • McDowell S.J.
      Pregnancy after uterine artery embolization for leiomyomata: a series of 56 completed pregnancies.
      ;
      • Dutton S.
      • Hirst A.
      • McPherson K.
      • Nicholson T.
      • Maresh M.
      A UK multicentre retrospective cohort study comparing hysterectomy and uterine artery embolisation for the treatment of symptomatic uterine fibroids (HOPEFUL study): main results on medium-term safety and efficacy.
      ;
      • Holub Z.
      • Mara M.
      • Eim J.
      Laparoscopic uterine artery occlusion versus uterine fibroid embolization.
      ;
      • Mara M.
      • Maskova J.
      • Fucikova Z.
      • Kuzel D.
      • Belsan T.
      • Sosna O.
      Midterm Clinical and First Reproductive Results of a Randomized Controlled Trial Comparing Uterine Fibroid Embolization and Myomectomy.
      ;
      • Holub Z.
      • Mara M.
      • Kuzel D.
      • Jabor A.
      • Maskova J.
      • Eim J.
      Pregnancy outcomes after uterine artery occlusion: prospective multicentric study.
      ;
      • Kim H.S.
      • Paxton B.E.
      • Lee J.M.
      Long-term efficacy and safety of uterine artery embolization in young patients with and without uteroovarian anastomoses.
      ;
      • Pinto Pabon I.
      • Magret J.P.
      • Unzurrunzaga E.A.
      • Garcia I.M.
      • Catalan I.B.
      • Cano Vieco M.L.
      Pregnancy after uterine fibroid embolization: follow-up of 100 patients embolized using tris-acryl gelatin microspheres.
      ;
      • Firouznia K.
      • Ghanaati H.
      • Sanaati M.
      • Jalali A.H.
      • Shakiba M.
      Pregnancy after uterine artery embolization for symptomatic fibroids: a series of 15 pregnancies.
      ;
      • Bonduki C.E.
      • Feldner J.P.C.
      • Silva J.D.
      • Castro R.A.
      • Sartori M.G.F.
      • Girão M.J.B.C.
      Pregnancy after uterine arterial embolization.
      ;
      • Pisco J.M.
      • Duarte M.
      • Bilhim T.
      • Cirurgiao F.
      • Oliveira A.G.
      Pregnancy after uterine fibroid embolization.
      ;
      • Mara M.
      • Kubinova K.
      • Maskova J.
      • Horak P.
      • Belsan T.
      • Kuzel D.
      Uterine artery embolization versus laparoscopic uterine artery occlusion: the outcomes of a prospective, nonrandomized clinical trial.
      ;
      • Redecha Jr., M.
      • Mizickova M.
      • Javorka V.
      • Redecha Sr., M.
      • Kurimska S.
      • Holoman K.
      Pregnancy after uterine artery embolization for the treatment of myomas: a case series.
      ;
      • McLucas B.
      • Voorhees 3rd, W.D.
      Results of UAE in women under 40 years of age.
      ;
      • Torre A.
      • Paillusson B.
      • Fain V.
      • Labauge P.
      • Pelage J.P.
      • Fauconnier A.
      Uterine artery embolization for severe symptomatic fibroids: effects on fertility and symptoms.
      ). Overall, 27 premature deliveries were reported, whereas the rest were at term. Most deliveries were by caesarean section (63.5%) compared with 36.5% by vaginal delivery. In 17 reports of placenta abnormalities in 424 pregnancies after UAE, five cases of placenta praevia were reported, four placenta accreta, one placenta membranacea, one placental abruption, and the others were uncategorized (
      • McLucas B.
      • Reed R.A.
      • Goodwin S.
      • Rappaport A.
      • Adler L.
      • Perrella R.
      • Dalrymple J.
      Outcomes following unilateral uterine artery embolisation.
      ;
      • Carpenter T.T.
      • Walker W.J.
      Pregnancy following uterine artery embolisation for symptomatic fibroids: a series of 26 completed pregnancies.
      ;
      • Pron G.
      • Mocarski E.
      • Bennett J.
      • Vilos G.
      • Common A.
      • Vanderburgh L.
      Ontario U.F.E.C.G
      Pregnancy after uterine artery embolization for leiomyomata: the Ontario multicenter trial.
      ;
      • Walker W.J.
      • McDowell S.J.
      Pregnancy after uterine artery embolization for leiomyomata: a series of 56 completed pregnancies.
      ;
      • Mara M.
      • Maskova J.
      • Fucikova Z.
      • Kuzel D.
      • Belsan T.
      • Sosna O.
      Midterm Clinical and First Reproductive Results of a Randomized Controlled Trial Comparing Uterine Fibroid Embolization and Myomectomy.
      ;
      • Firouznia K.
      • Ghanaati H.
      • Sanaati M.
      • Jalali A.H.
      • Shakiba M.
      Pregnancy after uterine artery embolization for symptomatic fibroids: a series of 15 pregnancies.
      ;
      • Bonduki C.E.
      • Feldner J.P.C.
      • Silva J.D.
      • Castro R.A.
      • Sartori M.G.F.
      • Girão M.J.B.C.
      Pregnancy after uterine arterial embolization.
      ;
      • Mara M.
      • Kubinova K.
      • Maskova J.
      • Horak P.
      • Belsan T.
      • Kuzel D.
      Uterine artery embolization versus laparoscopic uterine artery occlusion: the outcomes of a prospective, nonrandomized clinical trial.
      ). No cases of uterine rupture or intrauterine growth restriction were reported. The average time taken for women to conceive after UAE was 15 months (range 9–36 months) (
      • Ravina J.H.
      • Vigneron N.C.
      • Aymard A.
      • Le Dref O.
      • Merland J.J.
      Pregnancy after embolization of uterine myoma: report of 12 cases.
      ;
      • Carpenter T.T.
      • Walker W.J.
      Pregnancy following uterine artery embolisation for symptomatic fibroids: a series of 26 completed pregnancies.
      ;
      • Pron G.
      • Mocarski E.
      • Bennett J.
      • Vilos G.
      • Common A.
      • Vanderburgh L.
      Ontario U.F.E.C.G
      Pregnancy after uterine artery embolization for leiomyomata: the Ontario multicenter trial.
      ;
      • Dutton S.
      • Hirst A.
      • McPherson K.
      • Nicholson T.
      • Maresh M.
      A UK multicentre retrospective cohort study comparing hysterectomy and uterine artery embolisation for the treatment of symptomatic uterine fibroids (HOPEFUL study): main results on medium-term safety and efficacy.
      ;
      • Holub Z.
      • Mara M.
      • Eim J.
      Laparoscopic uterine artery occlusion versus uterine fibroid embolization.
      ;
      • Mara M.
      • Maskova J.
      • Fucikova Z.
      • Kuzel D.
      • Belsan T.
      • Sosna O.
      Midterm Clinical and First Reproductive Results of a Randomized Controlled Trial Comparing Uterine Fibroid Embolization and Myomectomy.
      ;
      • Holub Z.
      • Mara M.
      • Kuzel D.
      • Jabor A.
      • Maskova J.
      • Eim J.
      Pregnancy outcomes after uterine artery occlusion: prospective multicentric study.
      ;
      • Pinto Pabon I.
      • Magret J.P.
      • Unzurrunzaga E.A.
      • Garcia I.M.
      • Catalan I.B.
      • Cano Vieco M.L.
      Pregnancy after uterine fibroid embolization: follow-up of 100 patients embolized using tris-acryl gelatin microspheres.
      ;
      • Firouznia K.
      • Ghanaati H.
      • Sanaati M.
      • Jalali A.H.
      • Shakiba M.
      Pregnancy after uterine artery embolization for symptomatic fibroids: a series of 15 pregnancies.
      ;
      • Bonduki C.E.
      • Feldner J.P.C.
      • Silva J.D.
      • Castro R.A.
      • Sartori M.G.F.
      • Girão M.J.B.C.
      Pregnancy after uterine arterial embolization.
      ;
      • Pisco J.M.
      • Duarte M.
      • Bilhim T.
      • Cirurgiao F.
      • Oliveira A.G.
      Pregnancy after uterine fibroid embolization.
      ;
      • Mara M.
      • Kubinova K.
      • Maskova J.
      • Horak P.
      • Belsan T.
      • Kuzel D.
      Uterine artery embolization versus laparoscopic uterine artery occlusion: the outcomes of a prospective, nonrandomized clinical trial.
      ;
      • Redecha Jr., M.
      • Mizickova M.
      • Javorka V.
      • Redecha Sr., M.
      • Kurimska S.
      • Holoman K.
      Pregnancy after uterine artery embolization for the treatment of myomas: a case series.
      ;
      • Torre A.
      • Paillusson B.
      • Fain V.
      • Labauge P.
      • Pelage J.P.
      • Fauconnier A.
      Uterine artery embolization for severe symptomatic fibroids: effects on fertility and symptoms.
      ).
      Table 3Pregnancy outcomes after uterine artery embolization therapy
      Ten ectopic pregnancies and three stillbirths.
      Study, yearStudy designMean age, yearsTotal number of womenNumber of pregnant womenPregnanciesPregnancy outcomesMean time to conception (months)Mode of delivery
      Live birthOngoing pregnancyMiscarriageGestation at delivery, weeks
      Gestationn
      • Mara M.
      • Maskova J.
      • Fucikova Z.
      • Kuzel D.
      • Belsan T.
      • Sosna O.
      Midterm Clinical and First Reproductive Results of a Randomized Controlled Trial Comparing Uterine Fibroid Embolization and Myomectomy.
      Randomized controlled trial32.8261317519Term18VD (40%); CS (60%)
      • Mara M.
      • Kubinova K.
      • Maskova J.
      • Horak P.
      • Belsan T.
      • Kuzel D.
      Uterine artery embolization versus laparoscopic uterine artery occlusion: the outcomes of a prospective, nonrandomized clinical trial.
      Cohort study33.142294223213Preterm126.7NR
      • Holub Z.
      • Mara M.
      • Kuzel D.
      • Jabor A.
      • Maskova J.
      • Eim J.
      Pregnancy outcomes after uterine artery occlusion: prospective multicentric study.
      Cohort study32.3112202810114Preterm29.1VD (20%); CS (80%)
      • Holub Z.
      • Mara M.
      • Eim J.
      Laparoscopic uterine artery occlusion versus uterine fibroid embolization.
      Cohort study31.9271417817Preterm19VD (25%); CS (75%)
      • Torre A.
      • Paillusson B.
      • Fain V.
      • Labauge P.
      • Pelage J.P.
      • Fauconnier A.
      Uterine artery embolization for severe symptomatic fibroids: effects on fertility and symptoms.
      Prospective observational study37.36611010Term14NR
      • Redecha Jr., M.
      • Mizickova M.
      • Javorka V.
      • Redecha Sr., M.
      • Kurimska S.
      • Holoman K.
      Pregnancy after uterine artery embolization for the treatment of myomas: a case series.
      Prospective observational study34.42177700Term13.14VD (87.5%); CS (12.5%)
      • Firouznia K.
      • Ghanaati H.
      • Sanaati M.
      • Jalali A.H.
      • Shakiba M.
      Pregnancy after uterine artery embolization for symptomatic fibroids: a series of 15 pregnancies.
      Prospective observational study33.82314151302Term30.5CS (100%)
      • Pinto Pabon I.
      • Magret J.P.
      • Unzurrunzaga E.A.
      • Garcia I.M.
      • Catalan I.B.
      • Cano Vieco M.L.
      Pregnancy after uterine fibroid embolization: follow-up of 100 patients embolized using tris-acryl gelatin microspheres.
      Prospective observational study35571011803Preterm115VD (50%); CS (50%)
      • Kim H.S.
      • Paxton B.E.
      • Lee J.M.
      Long-term efficacy and safety of uterine artery embolization in young patients with and without uteroovarian anastomoses.
      Prospective observational study36.6191215603TermNRVD (17%); CS (83%)
      • Pron G.
      • Mocarski E.
      • Bennett J.
      • Vilos G.
      • Common A.
      • Vanderburgh L.
      Ontario U.F.E.C.G
      Pregnancy after uterine artery embolization for leiomyomata: the Ontario multicenter trial.
      Prospective observational study34555
      Includes those who did not intend pregnancy.
      21241804Preterm415VD (50%); CS (50%)
      • Walker W.J.
      • Pelage J.P.
      Uterine artery embolisation for symptomatic fibroids: clinical results in 400 women with imaging follow up.
      Prospective observational study3624 + 3
      Indicates patients who did not intend pregnancy but became pregnant. CS, caesarean section; NR, not reported; VD, vaginal delivery.
      1213902Preterm1NRVD (89%); CS (11%)
      • McLucas B.
      • Reed R.A.
      • Goodwin S.
      • Rappaport A.
      • Adler L.
      • Perrella R.
      • Dalrymple J.
      Outcomes following unilateral uterine artery embolisation.
      Prospective Observational Study<4013914171025Preterm1NRVD (30%); CS (70%)
      • Ravina J.H.
      • Vigneron N.C.
      • Aymard A.
      • Le Dref O.
      • Merland J.J.
      Pregnancy after embolization of uterine myoma: report of 12 cases.
      Prospective observational study36184
      Includes those who did not intend pregnancy.
      912705Preterm29VD (75%;) CS (25%)
      • McLucas B.
      • Voorhees 3rd, W.D.
      Results of UAE in women under 40 years of age.
      Retrospective observational study3310223271926NRNRNR
      • Pisco J.M.
      • Duarte M.
      • Bilhim T.
      • Cirurgiao F.
      • Oliveira A.G.
      Pregnancy after uterine fibroid embolization.
      Retrospective observational study367444443354Preterm210.8VD (41%); CS (59%)
      • Bonduki C.E.
      • Feldner J.P.C.
      • Silva J.D.
      • Castro R.A.
      • Sartori M.G.F.
      • Girão M.J.B.C.
      Pregnancy after uterine arterial embolization.
      Retrospective observational study34.47515151320Preterm123.8CS (100%)
      • Dutton S.
      • Hirst A.
      • McPherson K.
      • Nicholson T.
      • Maresh M.
      A UK multicentre retrospective cohort study comparing hysterectomy and uterine artery embolisation for the treatment of symptomatic uterine fibroids (HOPEFUL study): main results on medium-term safety and efficacy.
      Retrospective observational study38187273719015Term36VD (21%); CS (79%)
      • Walker W.J.
      • McDowell S.J.
      Pregnancy after uterine artery embolization for leiomyomata: a series of 56 completed pregnancies.
      Retrospective observational study37108335633017Preterm6NRVD (27%); CS (73%)
      • Carpenter T.T.
      • Walker W.J.
      Pregnancy following uterine artery embolisation for symptomatic fibroids: a series of 26 completed pregnancies.
      Retrospective observational study377926261607Preterm520VD (12%); CS (88%)
      Total1923344424257 (60.6%)17 (4.0%)116 (27.4%)
      a Ten ectopic pregnancies and three stillbirths.
      b Includes those who did not intend pregnancy.
      c Indicates patients who did not intend pregnancy but became pregnant.CS, caesarean section; NR, not reported; VD, vaginal delivery.

      Fibroid ablation

      A total of 420 pregnancies were reported after fibroid ablation, resulting in 296 live births (70.5%), 50 miscarriages (11.9%), 39 terminations (9.3%) and 35 ongoing pregnancies (8.3%) (Table 4). All terminations were elective and none were stated to be caused by fetal abnormality (
      • Rabinovici J.
      • David M.
      • Fukunishi H.
      • Morita Y.
      • Gostout B.S.
      • Stewart E.A.
      • Group M.R.S.
      Pregnancy outcome after magnetic resonance-guided focused ultrasound surgery (MRgFUS) for conservative treatment of uterine fibroids.
      ;
      • Qin J.
      • Chen J.Y.
      • Zhao W.P.
      • Hu L.
      • Chen W.Z.
      • Wang Z.B.
      Outcome of unintended pregnancy after ultrasound-guided high-intensity focused ultrasound ablation of uterine fibroids.
      ;
      • Bing-song Z.
      • Jing Z.
      • Zhi-Yu H.
      • Chang-tao X.
      • Rui-fang X.
      • Xiu-mei L.
      • Hui L.
      Unplanned pregnancy after ultrasound-guided percutaneous microwave ablation of uterine fibroids: A follow-up study.
      ;
      • Li J.S.
      • Wang Y.
      • Chen J.Y.
      • Chen W.Z.
      Pregnancy outcomes in nulliparous women after ultrasound ablation of uterine fibroids: A single-central retrospective study.
      ;
      • Zou M.
      • Chen L.
      • Wu C.
      • Hu C.
      • Xiong Y.
      Pregnancy outcomes in patients with uterine fibroids treated with ultrasound-guided high-intensity focused ultrasound.
      ;
      • Liu X.
      • Xue L.
      • Wang Y.
      • Wang W.
      • Tang J.
      Vaginal delivery outcomes of pregnancies following ultrasound-guided high-intensity focused ultrasound ablation treatment for uterine fibroids.
      ), although one woman terminated her pregnancy owing to concerns about the potential effects of fibroid ablation on the fetus (
      • Qin J.
      • Chen J.Y.
      • Zhao W.P.
      • Hu L.
      • Chen W.Z.
      • Wang Z.B.
      Outcome of unintended pregnancy after ultrasound-guided high-intensity focused ultrasound ablation of uterine fibroids.
      ). Eight successful cases of placental abnormalities were reported (seven placenta praevia and one placental insufficiency) and no cases of stillbirth or ectopic pregnancy (
      • Rabinovici J.
      • David M.
      • Fukunishi H.
      • Morita Y.
      • Gostout B.S.
      • Stewart E.A.
      • Group M.R.S.
      Pregnancy outcome after magnetic resonance-guided focused ultrasound surgery (MRgFUS) for conservative treatment of uterine fibroids.
      ;
      • Li J.S.
      • Wang Y.
      • Chen J.Y.
      • Chen W.Z.
      Pregnancy outcomes in nulliparous women after ultrasound ablation of uterine fibroids: A single-central retrospective study.
      ). A total of 15 preterm deliveries were reported. Most pregnancies were delivered vaginally (61.6%), with the remaining 38.4% by caesarean section. No cases of uterine rupture were reported (
      • Gavrilova-Jordan L.P.
      • Rose C.H.
      • Traynor K.D.
      • Brost B.C.
      • Gostout B.S.
      Successful term pregnancy following MR-guided focused ultrasound treatment of uterine leiomyoma.
      ;
      • Hanstede M.M.
      • Tempany C.M.
      • Stewart E.A.
      Focused ultrasound surgery of intramural leiomyomas may facilitate fertility: a case report.
      ;
      • Morita Y.
      • Ito N.
      • Hikida H.
      • Takeuchi S.
      • Nakamura K.
      • Ohashi H.
      Non-invasive magnetic resonance imaging-guided focused ultrasound treatment for uterine fibroids - early experience.
      ;
      • Funaki K.
      • Fukunishi H.
      • Sawada K.
      Clinical outcomes of magnetic resonance-guided focused ultrasound surgery for uterine myomas: 24-month follow-up.
      ;
      • Rabinovici J.
      • David M.
      • Fukunishi H.
      • Morita Y.
      • Gostout B.S.
      • Stewart E.A.
      • Group M.R.S.
      Pregnancy outcome after magnetic resonance-guided focused ultrasound surgery (MRgFUS) for conservative treatment of uterine fibroids.
      ;
      • Yoon S.W.
      • Kim K.A.
      • Kim S.H.
      • Ha D.H.
      • Lee C.
      • Lee S.Y.
      • Jung S.G.
      • Kim S.J.
      Pregnancy and natural delivery following magnetic resonance imaging-guided focused ultrasound surgery of uterine myomas.
      ;
      • Zaher S.
      • Lyons D.
      • Regan L.
      Uncomplicated term vaginal delivery following magnetic resonance-guided focused ultrasound surgery for uterine fibroids.
      ;
      • Bouwsma E.V.
      • Gorny K.R.
      • Hesley G.K.
      • Jensen J.R.
      • Peterson L.G.
      • Stewart E.A.
      Magnetic resonance-guided focused ultrasound surgery for leiomyoma-associated infertility.
      ;
      • Kim C.H.
      • Kim S.R.
      • Lee H.A.
      • Kim S.H.
      • Chae H.D.
      • Kang B.M.
      Transvaginal ultrasound-guided radiofrequency myolysis for uterine myomas.
      ;
      • Zaher S.
      • Lyons D.
      • Regan L.
      Successful in vitro fertilization pregnancy following magnetic resonance-guided focused ultrasound surgery for uterine fibroids.
      ;
      • Qin J.
      • Chen J.Y.
      • Zhao W.P.
      • Hu L.
      • Chen W.Z.
      • Wang Z.B.
      Outcome of unintended pregnancy after ultrasound-guided high-intensity focused ultrasound ablation of uterine fibroids.
      ;
      • Froeling V.
      • Meckelburg K.
      • Schreiter N.F.
      • Scheurig-Muenkler C.
      • Kamp J.
      • Maurer M.H.
      • Beck A.
      • Hamm B.
      • Kroencke T.J.
      Outcome of uterine artery embolization versus MR-guided high-intensity focused ultrasound treatment for uterine fibroids: long-term results.
      ;
      • Yoon S.W.
      • Cha S.H.
      • Ji Y.G.
      • Kim H.C.
      • Lee M.H.
      • Cho J.H.
      Magnetic resonance imaging-guided focused ultrasound surgery for symptomatic uterine fibroids: estimation of treatment efficacy using thermal dose calculations.
      ;
      • Garza-Leal J.G.
      • León I.H.
      • Toub D.
      Pregnancy after transcervical radiofrequency ablation guided by intrauterine sonography: case report.
      ;
      • Hahn M.
      • Brucker S.
      • Kraemer D.
      • Wallwiener M.
      • Taran F.A.
      • Wallwiener C.W.
      • Kramer B.
      Radiofrequency Volumetric Thermal Ablation of Fibroids and Laparoscopic Myomectomy: Long-Term Follow-up From a Randomized Trial.
      ;
      • Thiburce A.C.
      • Frulio N.
      • Hocquelet A.
      • Maire F.
      • Salut C.
      • Balageas P.
      • Bouzgarrou M.
      • Hocke C.
      • Trillaud H.
      Magnetic resonance-guided high-intensity focused ultrasound for uterine fibroids: Mid-term outcomes of 36 patients treated with the Sonalleve system.
      ;
      • Bing-song Z.
      • Jing Z.
      • Zhi-Yu H.
      • Chang-tao X.
      • Rui-fang X.
      • Xiu-mei L.
      • Hui L.
      Unplanned pregnancy after ultrasound-guided percutaneous microwave ablation of uterine fibroids: A follow-up study.
      ;
      • Li J.S.
      • Wang Y.
      • Chen J.Y.
      • Chen W.Z.
      Pregnancy outcomes in nulliparous women after ultrasound ablation of uterine fibroids: A single-central retrospective study.
      ;
      • Zou M.
      • Chen L.
      • Wu C.
      • Hu C.
      • Xiong Y.
      Pregnancy outcomes in patients with uterine fibroids treated with ultrasound-guided high-intensity focused ultrasound.
      ;
      • Bends R.
      • Toub D.B.
      • Romer T.
      Normal spontaneous vaginal delivery after transcervical radiofrequency ablation of uterine fibroids: a case report.
      ;
      • Liu X.
      • Xue L.
      • Wang Y.
      • Wang W.
      • Tang J.
      Vaginal delivery outcomes of pregnancies following ultrasound-guided high-intensity focused ultrasound ablation treatment for uterine fibroids.
      ). The average time taken for women to conceive after thermal ablation was 10 months (range 3–33 months) (
      • Hanstede M.M.
      • Tempany C.M.
      • Stewart E.A.
      Focused ultrasound surgery of intramural leiomyomas may facilitate fertility: a case report.
      ;
      • Morita Y.
      • Ito N.
      • Hikida H.
      • Takeuchi S.
      • Nakamura K.
      • Ohashi H.
      Non-invasive magnetic resonance imaging-guided focused ultrasound treatment for uterine fibroids - early experience.
      ;
      • Funaki K.
      • Fukunishi H.
      • Sawada K.
      Clinical outcomes of magnetic resonance-guided focused ultrasound surgery for uterine myomas: 24-month follow-up.
      ;
      • Rabinovici J.
      • David M.
      • Fukunishi H.
      • Morita Y.
      • Gostout B.S.
      • Stewart E.A.
      • Group M.R.S.
      Pregnancy outcome after magnetic resonance-guided focused ultrasound surgery (MRgFUS) for conservative treatment of uterine fibroids.
      ;
      • Yoon S.W.
      • Kim K.A.
      • Kim S.H.
      • Ha D.H.
      • Lee C.
      • Lee S.Y.
      • Jung S.G.
      • Kim S.J.
      Pregnancy and natural delivery following magnetic resonance imaging-guided focused ultrasound surgery of uterine myomas.
      ;
      • Zaher S.
      • Lyons D.
      • Regan L.
      Uncomplicated term vaginal delivery following magnetic resonance-guided focused ultrasound surgery for uterine fibroids.
      ;
      • Bouwsma E.V.
      • Hesley G.K.
      • Woodrum D.A.
      • Weaver A.L.
      • Leppert P.C.
      • Peterson L.G.
      • Stewart E.A.
      Comparing focused ultrasound and uterine artery embolization for uterine fibroids-rationale and design of the Fibroid Interventions: reducing symptoms today and tomorrow (FIRSTT) trial.
      ;
      • Zaher S.
      • Lyons D.
      • Regan L.
      Successful in vitro fertilization pregnancy following magnetic resonance-guided focused ultrasound surgery for uterine fibroids.
      ;
      • Froeling V.
      • Meckelburg K.
      • Schreiter N.F.
      • Scheurig-Muenkler C.
      • Kamp J.
      • Maurer M.H.
      • Beck A.
      • Hamm B.
      • Kroencke T.J.
      Outcome of uterine artery embolization versus MR-guided high-intensity focused ultrasound treatment for uterine fibroids: long-term results.
      ;
      • Yoon S.W.
      • Cha S.H.
      • Ji Y.G.
      • Kim H.C.
      • Lee M.H.
      • Cho J.H.
      Magnetic resonance imaging-guided focused ultrasound surgery for symptomatic uterine fibroids: estimation of treatment efficacy using thermal dose calculations.
      ;
      • Garza-Leal J.G.
      • León I.H.
      • Toub D.
      Pregnancy after transcervical radiofrequency ablation guided by intrauterine sonography: case report.
      ;
      • Hahn M.
      • Brucker S.
      • Kraemer D.
      • Wallwiener M.
      • Taran F.A.
      • Wallwiener C.W.
      • Kramer B.
      Radiofrequency Volumetric Thermal Ablation of Fibroids and Laparoscopic Myomectomy: Long-Term Follow-up From a Randomized Trial.
      ;
      • Thiburce A.C.
      • Frulio N.
      • Hocquelet A.
      • Maire F.
      • Salut C.
      • Balageas P.
      • Bouzgarrou M.
      • Hocke C.
      • Trillaud H.
      Magnetic resonance-guided high-intensity focused ultrasound for uterine fibroids: Mid-term outcomes of 36 patients treated with the Sonalleve system.
      ;
      • Bing-song Z.
      • Jing Z.
      • Zhi-Yu H.
      • Chang-tao X.
      • Rui-fang X.
      • Xiu-mei L.
      • Hui L.
      Unplanned pregnancy after ultrasound-guided percutaneous microwave ablation of uterine fibroids: A follow-up study.
      ;
      • Li J.S.
      • Wang Y.
      • Chen J.Y.
      • Chen W.Z.
      Pregnancy outcomes in nulliparous women after ultrasound ablation of uterine fibroids: A single-central retrospective study.
      ;
      • Zou M.
      • Chen L.
      • Wu C.
      • Hu C.
      • Xiong Y.
      Pregnancy outcomes in patients with uterine fibroids treated with ultrasound-guided high-intensity focused ultrasound.
      ;
      • Bends R.
      • Toub D.B.
      • Romer T.
      Normal spontaneous vaginal delivery after transcervical radiofrequency ablation of uterine fibroids: a case report.
      ;
      • Liu X.
      • Xue L.
      • Wang Y.
      • Wang W.
      • Tang J.
      Vaginal delivery outcomes of pregnancies following ultrasound-guided high-intensity focused ultrasound ablation treatment for uterine fibroids.
      ).
      Table 4Pregnancy outcomes after fibroid ablation.
      Thirty-nine terminations.
      Study, yearStudy designMean ageTotal number of womenNumber of pregnant womenPregnanciesPregnancy outcomesMean time to conception (months)Mode of delivery
      Live birth rateOngoing pregnancyMiscarriageGestation at delivery, weeks
      Gestationn
      • Liu X.
      • Xue L.
      • Wang Y.
      • Wang W.
      • Tang J.
      Vaginal delivery outcomes of pregnancies following ultrasound-guided high-intensity focused ultrasound ablation treatment for uterine fibroids.
      Prospective observational study31.117481887409Preterm523.1Elective LSCS (72% [53/7]); VD (28% [21/74]).
      • Zou M.
      • Chen L.
      • Wu C.
      • Hu C.
      • Xiong Y.
      Pregnancy outcomes in patients with uterine fibroids treated with ultrasound-guided high-intensity focused ultrasound.
      Retrospective observational Study34.540678807153Preterm35.6LSCS (79% [56/71]); VD (21% [15/71])
      • Li J.S.
      • Wang Y.
      • Chen J.Y.
      • Chen W.Z.
      Pregnancy outcomes in nulliparous women after ultrasound ablation of uterine fibroids: A single-central retrospective study.
      Retrospective observational study30.3189131133931917Preterm612.3VD (28% [26/93]); LSCS (72% [67/93])
      • Bing-song Z.
      • Jing Z.
      • Zhi-Yu H.
      • Chang-tao X.
      • Rui-fang X.
      • Xiu-mei L.
      • Hui L.
      Unplanned pregnancy after ultrasound-guided percutaneous microwave ablation of uterine fibroids: A follow-up study.
      Case series34.2169
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      910300Term12.7LSCS (100% [3/3])
      • Thiburce A.C.
      • Frulio N.
      • Hocquelet A.
      • Maire F.
      • Salut C.
      • Balageas P.
      • Bouzgarrou M.
      • Hocke C.
      • Trillaud H.
      Magnetic resonance-guided high-intensity focused ultrasound for uterine fibroids: Mid-term outcomes of 36 patients treated with the Sonalleve system.
      Case series45
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      22200Term18VD (100% [2/2])
      • Hahn M.
      • Brucker S.
      • Kraemer D.
      • Wallwiener M.
      • Taran F.A.
      • Wallwiener C.W.
      • Kramer B.
      Radiofrequency Volumetric Thermal Ablation of Fibroids and Laparoscopic Myomectomy: Long-Term Follow-up From a Randomized Trial.
      Case series3125
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      22200Term7.6VD (100% [2/2])
      • Garza-Leal J.G.
      • León I.H.
      • Toub D.
      Pregnancy after transcervical radiofrequency ablation guided by intrauterine sonography: case report.
      Case series41111100Term3.5LSCS (100% [1/1])
      • Yoon S.W.
      • Cha S.H.
      • Ji Y.G.
      • Kim H.C.
      • Lee M.H.
      • Cho J.H.
      Magnetic resonance imaging-guided focused ultrasound surgery for symptomatic uterine fibroids: estimation of treatment efficacy using thermal dose calculations.
      Case series60
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      11100Term4NR
      • Froeling V.
      • Meckelburg K.
      • Schreiter N.F.
      • Scheurig-Muenkler C.
      • Kamp J.
      • Maurer M.H.
      • Beck A.
      • Hamm B.
      • Kroencke T.J.
      Outcome of uterine artery embolization versus MR-guided high-intensity focused ultrasound treatment for uterine fibroids: long-term results.
      Case series36.236
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      910703Term16.1NR
      • Qin J.
      • Chen J.Y.
      • Zhao W.P.
      • Hu L.
      • Chen W.Z.
      • Wang Z.B.
      Outcome of unintended pregnancy after ultrasound-guided high-intensity focused ultrasound ablation of uterine fibroids.
      Case series34.5435
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      2424702Term<12LSCS (100% [7/7])
      • Kim C.H.
      • Kim S.R.
      • Lee H.A.
      • Kim S.H.
      • Chae H.D.
      • Kang B.M.
      Transvaginal ultrasound-guided radiofrequency myolysis for uterine myomas.
      Case series39.869
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      33300Term<12LSCS (33% [1/3]); VD (67% [2/3])
      • Rabinovici J.
      • David M.
      • Fukunishi H.
      • Morita Y.
      • Gostout B.S.
      • Stewart E.A.
      • Group M.R.S.
      Pregnancy outcome after magnetic resonance-guided focused ultrasound surgery (MRgFUS) for conservative treatment of uterine fibroids.
      Case series37.2515154221114Preterm18VD 64% [14/22]); LSCS (36% [8/22])
      • Funaki K.
      • Fukunishi H.
      • Sawada K.
      Clinical outcomes of magnetic resonance-guided focused ultrasound surgery for uterine myomas: 24-month follow-up.
      Case series91
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      44202Term12.8NR
      • Bends R.
      • Toub D.B.
      • Romer T.
      Normal spontaneous vaginal delivery after transcervical radiofrequency ablation of uterine fibroids: a case report.
      Case report33111100Term33VD
      • Bouwsma E.V.
      • Gorny K.R.
      • Hesley G.K.
      • Jensen J.R.
      • Peterson L.G.
      • Stewart E.A.
      Magnetic resonance-guided focused ultrasound surgery for leiomyoma-associated infertility.
      Case report37111100Term3VD
      • Zaher S.
      • Lyons D.
      • Regan L.
      Successful in vitro fertilization pregnancy following magnetic resonance-guided focused ultrasound surgery for uterine fibroids.
      Case report35111100Term10Emergency LSCS
      • Zaher S.
      • Lyons D.
      • Regan L.
      Uncomplicated term vaginal delivery following magnetic resonance-guided focused ultrasound surgery for uterine fibroids.
      Case report39111100Term10VD
      • Yoon S.W.
      • Kim K.A.
      • Kim S.H.
      • Ha D.H.
      • Lee C.
      • Lee S.Y.
      • Jung S.G.
      • Kim S.J.
      Pregnancy and natural delivery following magnetic resonance imaging-guided focused ultrasound surgery of uterine myomas.
      Case report31111100Term4VD
      • Gavrilova-Jordan L.P.
      • Rose C.H.
      • Traynor K.D.
      • Brost B.C.
      • Gostout B.S.
      Successful term pregnancy following MR-guided focused ultrasound treatment of uterine leiomyoma.
      Case report38111100TermNRVD
      • Hanstede M.M.
      • Tempany C.M.
      • Stewart E.A.
      Focused ultrasound surgery of intramural leiomyomas may facilitate fertility: a case report.
      Case report40111100Term18VD
      • Morita Y.
      • Ito N.
      • Hikida H.
      • Takeuchi S.
      • Nakamura K.
      • Ohashi H.
      Non-invasive magnetic resonance imaging-guided focused ultrasound treatment for uterine fibroids - early experience.
      Case report3048
      Includes those who did not intend pregnancy. LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.
      11100Term4VD
      Total1806404420296 (70.5%)35 (8.3%)50 (11.9%)
      a Thirty-nine terminations.
      b Includes those who did not intend pregnancy.LSCS, lower segment caesarean section; NR, not reported; VD, vaginal delivery.

      Comparison of pregnancy outcomes

      As only 12 pregnancies after UPA treatment were reported, it was not included in the statistical analysis. No significant difference was observed in the percentage of live birth in women who received myomectomy or ablation (75.6% versus 70.5%; P > 0.05). After UAE, however, the live birth rate was significantly lower at 60.6% (P < 0.001) compared with both myomectomy and ablation groups. Pregnancies after UAE also showed the highest rate of miscarriage (27.4%), followed by myomectomy (19.9%) and ablation (11.9%) (P < 0.001).
      Five cases of stillbirth were reported, three after UAE and two after myomectomy (
      • Seracchioli R.
      • Manuzzi L.
      • Vianello F.
      • Gualerzi B.
      • Savelli L.
      • Paradisi R.
      • Venturoli S.
      Obstetric and delivery outcome of pregnancies achieved after laparoscopic myomectomy.
      ;
      • Walker W.J.
      • McDowell S.J.
      Pregnancy after uterine artery embolization for leiomyomata: a series of 56 completed pregnancies.
      ;
      • Pisco J.M.
      • Duarte M.
      • Bilhim T.
      • Cirurgiao F.
      • Oliveira A.G.
      Pregnancy after uterine fibroid embolization.
      ;
      • Bernardi T.S.
      • Radosa M.P.
      • Weisheit A.
      • Diebolder H.
      • Schneider U.
      • Schleussner E.
      • Runnebaum I.B.
      Laparoscopic myomectomy: a 6-year follow-up single-center cohort analysis of fertility and obstetric outcome measures.
      ). Abnormal placentation was more common after UAE at 4% (n = 17) than after myomectomy (0.38%; n = 6) or after ablation (1.9%; n = 8; P < 0.001). No placental abnormalities were reported in women who underwent UPA therapy. Ten cases of uterine rupture were recorded after myomectomy and none after UPA, UAE or ablation therapy (
      • Dubuisson J.B.
      • Chapron C.
      • Fauconnier A.
      • Babaki-Fard K.
      Laparoscopic myomectomy fertility results.
      ;
      • Sizzi O.
      • Rossetti A.
      • Malzoni M.
      • Minelli L.
      • La Grotta F.
      • Soranna L.
      • Panunzi S.
      • Spagnolo R.
      • Imperato F.
      • Landi S.
      • Fiaccamento A.
      • Stola E.
      Italian multicenter study on complications of laparoscopic myomectomy.
      ;
      • Pitter M.C.
      • Gargiulo A.R.
      • Bonaventura L.M.
      • Lehman J.S.
      • Srouji S.S.
      Pregnancy outcomes following robot-assisted myomectomy.
      ;
      • Bernardi T.S.
      • Radosa M.P.
      • Weisheit A.
      • Diebolder H.
      • Schneider U.
      • Schleussner E.
      • Runnebaum I.B.
      Laparoscopic myomectomy: a 6-year follow-up single-center cohort analysis of fertility and obstetric outcome measures.
      ;
      • Sangha R.
      • Strickler R.
      • Dahlman M.
      • Havstad S.
      • Wegienka G.
      Myomectomy to Conserve Fertility: Seven-Year Follow-Up.
      ).

      Discussion

      This is the first review of pregnancy outcomes comparing medical, radiological and surgical conservative treatment of uterine fibroids, and is limited by the quality of the evidence available, with significant risk of bias. It seems, however, that the live birth rate is highest after myomectomy (75.6%) and ablation (70.5%). Pregnancies after UAE had the lowest live birth rate of 60.6% and the highest rate of miscarriage, at 27.4%, compared with the general population rate of 10–20% (
      • Stirrat G.M.
      Recurrent miscarriage.
      ;
      • Regan L.
      • Rai R.
      Epidemiology and the medical causes of miscarriage.
      ;
      • Weeks A.
      • Danielsson K.G.
      Spontaneous miscarriage in the first trimester.
      ). Live birth rates after UPA were excluded from the statistical analysis owing to the limited number of cases. The stillbirth rates were low (range: 0–3%) with all treatments and are similar to the global average stillbirth rate of 2% (
      • Blencowe H.
      • Cousens S.
      • Jassir F.B.
      • Say L.
      • Chou D.
      • Mathers C.
      • Hogan D.
      • Shiekh S.
      • Qureshi Z.U.
      • You D.
      • Lawn J.E.
      Lancet Stillbirth Epidemiology Investigator G
      National, regional, and worldwide estimates of stillbirth rates in 2015, with trends from 2000: a systematic analysis.
      ).
      At present, myomectomy is the gold-standard fertility preservation treatment for fibroids and seems to have an advantage over UPA, UAE or ablation for pregnancy outcomes. Surgical complications, such as major haemorrhage requiring transfusion and infections, do occur (
      • Holzer A.
      • Jirecek S.T.
      • Illievich U.M.
      • Huber J.
      • Wenzl R.J.
      Laparoscopic versus open myomectomy: a double-blind study to evaluate postoperative pain.
      ;
      American College of Obstetricians & Gynecologists
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      ;
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      ;
      • Yang W.
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      ), and a risk of uterine rupture during pregnancy and labour, of which 10 cases were identified (
      • Dubuisson J.B.
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      • Fauconnier A.
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      Laparoscopic myomectomy fertility results.
      ;
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      Obstetric and delivery outcome of pregnancies achieved after laparoscopic myomectomy.
      ;
      • Sizzi O.
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      • Malzoni M.
      • Minelli L.
      • La Grotta F.
      • Soranna L.
      • Panunzi S.
      • Spagnolo R.
      • Imperato F.
      • Landi S.
      • Fiaccamento A.
      • Stola E.
      Italian multicenter study on complications of laparoscopic myomectomy.
      ;
      • Kumakiri J.
      • Takeuchi H.
      • Itoh S.
      • Kitade M.
      • Kikuchi I.
      • Shimanuki H.
      • Kumakiri Y.
      • Kuroda K.
      • Takeda S.
      Prospective evaluation for the feasibility and safety of vaginal birth after laparoscopic myomectomy.
      ;
      • Gyamfi-Bannerman C.
      • Gilbert S.
      • Landon M.B.
      • Spong C.Y.
      • Rouse D.J.
      • Varner M.W.
      • Caritis S.N.
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      • Sorokin Y.
      • Carpenter M.
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      • O'Sullivan M.J.
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      • Ramin S.M.
      • Mercer B.M.
      Eunice Kennedy Shriver National Institute of Child HHuman Development Maternal-Fetal Medicine Units N
      Risk of uterine rupture and placenta accreta with prior uterine surgery outside of the lower segment.
      ;
      • Kim M.S.
      • Uhm Y.K.
      • Kim J.Y.
      • Jee B.C.
      • Kim Y.B.
      Obstetric outcomes after uterine myomectomy: Laparoscopic versus laparotomic approach.
      ;
      • Pitter M.C.
      • Gargiulo A.R.
      • Bonaventura L.M.
      • Lehman J.S.
      • Srouji S.S.
      Pregnancy outcomes following robot-assisted myomectomy.
      ;
      • Bernardi T.S.
      • Radosa M.P.
      • Weisheit A.
      • Diebolder H.
      • Schneider U.
      • Schleussner E.
      • Runnebaum I.B.
      Laparoscopic myomectomy: a 6-year follow-up single-center cohort analysis of fertility and obstetric outcome measures.
      ;
      • Koo Y.J.
      • Lee J.K.
      • Lee Y.K.
      • Kwak D.W.
      • Lee I.H.
      • Lim K.T.
      • Lee K.H.
      • Kim T.J.
      Pregnancy Outcomes and Risk Factors for Uterine Rupture After Laparoscopic Myomectomy: A Single-Center Experience and Literature Review.
      ;
      • Kim H.S.
      • Oh S.Y.
      • Choi S.J.
      • Park H.S.
      • Cho G.J.
      • Chung J.H.
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      • Hwang H.S.
      Uterine rupture in pregnancies following myomectomy: A multicenter case series.
      ;
      • Chao A.S.
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      • Chao A.
      • Chang W.Y.
      • Su S.Y.
      • Wang C.J.
      Laparoscopic uterine surgery as a risk factor for uterine rupture during pregnancy.
      ). Myomectomy also contributes to postpartum complications by increasing the incidence of placenta praevia and placenta accreta, but the rate of placental abnormalities identified here was only 0.25% (
      • Campo S.
      • Campo V.
      • Gambadauro P.
      Reproductive outcome before and after laparoscopic or abdominal myomectomy for subserous or intramural myomas.
      ;
      • Pron G.
      • Mocarski E.
      • Bennett J.
      • Vilos G.
      • Common A.
      • Vanderburgh L.
      Ontario U.F.E.C.G
      Pregnancy after uterine artery embolization for leiomyomata: the Ontario multicenter trial.
      ;
      • Dutton S.
      • Hirst A.
      • McPherson K.
      • Nicholson T.
      • Maresh M.
      A UK multicentre retrospective cohort study comparing hysterectomy and uterine artery embolisation for the treatment of symptomatic uterine fibroids (HOPEFUL study): main results on medium-term safety and efficacy.
      ;
      • Gyamfi-Bannerman C.
      • Gilbert S.
      • Landon M.B.
      • Spong C.Y.
      • Rouse D.J.
      • Varner M.W.
      • Caritis S.N.
      • Meis P.J.
      • Wapner R.J.
      • Sorokin Y.
      • Carpenter M.
      • Peaceman A.M.
      • O'Sullivan M.J.
      • Sibai B.M.
      • Thorp J.M.
      • Ramin S.M.
      • Mercer B.M.
      Eunice Kennedy Shriver National Institute of Child HHuman Development Maternal-Fetal Medicine Units N
      Risk of uterine rupture and placenta accreta with prior uterine surgery outside of the lower segment.
      ;
      • Lutomski J.E.
      • Byrne B.M.
      • Devane D.
      • Greene R.A.
      Increasing trends in atonic postpartum haemorrhage in Ireland: an 11-year population-based cohort study.
      ;
      • Kramer M.S.
      • Berg C.
      • Abenhaim H.
      • Dahhou M.
      • Rouleau J.
      • Mehrabadi A.
      • Joseph K.S.
      Incidence, risk factors, and temporal trends in severe postpartum hemorrhage.
      ;
      • Pitter M.C.
      • Gargiulo A.R.
      • Bonaventura L.M.
      • Lehman J.S.
      • Srouji S.S.
      Pregnancy outcomes following robot-assisted myomectomy.
      ;
      • Bernardi T.S.
      • Radosa M.P.
      • Weisheit A.
      • Diebolder H.
      • Schneider U.
      • Schleussner E.
      • Runnebaum I.B.
      Laparoscopic myomectomy: a 6-year follow-up single-center cohort analysis of fertility and obstetric outcome measures.
      ;
      • Sheldon W.R.
      • Blum J.
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      ;
      • Tanaka M.
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      ). Although pregnancy outcomes after myomectomy seem to be better than with other conservative treatments for fibroids, it remains unclear whether myomectomy has a benefit for fertility (
      • Metwally M.
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      ;
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      ).
      Fibroid ablation using either ultrasonography or magnetic resonance guided focused ultrasound  minimizes the damage to surrounding tissue by focusing on the area within the fibroid; however, cases of skin burns and bowel perforation have been reported (
      • Zupi E.
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      Myolysis of uterine fibroids: is there a role?.
      ;
      • Bouwsma E.V.
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      • Peterson L.G.
      • Stewart E.A.
      Magnetic resonance-guided focused ultrasound surgery for leiomyoma-associated infertility.
      ;
      • Bouwsma E.V.
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      • Woodrum D.A.
      • Weaver A.L.
      • Leppert P.C.
      • Peterson L.G.
      • Stewart E.A.
      Comparing focused ultrasound and uterine artery embolization for uterine fibroids-rationale and design of the Fibroid Interventions: reducing symptoms today and tomorrow (FIRSTT) trial.
      ;
      • Chodankar R.
      • Allison J.
      New Horizons in Fibroid Management.
      ). It is mostly limited to centrally situated fibroids, whereas fibroids usually grow peripherally. To maintain a certain safety margin, its use is limited to fibroids wider than 4 cm. Also, because of the long duration of the procedure, each treatment session is focused on a single fibroid only (
      • Vilos G.A.
      • Allaire C.
      • Laberge P.-Y.
      • Leyland N.
      • Vilos A.G.
      • Murji A.
      • Chen I.
      The Management of Uterine Leiomyomas.
      ;
      • Chodankar R.
      • Allison J.
      New Horizons in Fibroid Management.
      ). Radiofrequency volumetric thermal ablation has shown great potential by allowing a higher number of fibroids to be treated, with less intraoperative blood loss and a faster recovery compared with laparoscopic myomectomy (
      • Brucker S.Y.
      • Hahn M.
      • Kraemer D.
      • Taran F.A.
      • Isaacson K.B.
      • Kramer B.
      Laparoscopic radiofrequency volumetric thermal ablation of fibroids versus laparoscopic myomectomy.
      ). In this analysis, fibroid ablation had comparable pregnancy outcomes to myomectomy, with similar live birth rates (70.5% versus 75.6%) and low miscarriage rates (11.9% versus 19.0%). No cases of uterine rupture were reported, and it was not associated with higher risk of placental abnormalities. Although promising, fibroid ablation through a focused energy delivery system is relatively new and more controlled trials are required to evaluate its potential for the treatment of fibroids in women who intend pregnancy (
      • Vilos G.A.
      • Allaire C.
      • Laberge P.-Y.
      • Leyland N.
      • Vilos A.G.
      • Murji A.
      • Chen I.
      The Management of Uterine Leiomyomas.
      ;
      • Chodankar R.
      • Allison J.
      New Horizons in Fibroid Management.
      ).
      After UAE treatment, the disruption of normal uterine blood supply to the endometrium and placental blood supply may explain the suboptimal pregnancy outcomes after UAE compared with myomectomy, UPA and ablation therapy (
      • Tropeano G.
      • Litwicka K.
      • Di Stasi C.
      • Romano D.
      • Mancuso S.
      Permanent amenorrhea associated with endometrial atrophy after uterine artery embolization for symptomatic uterine fibroids.
      ;
      • Bulletti C.
      • de Ziegler D.
      Uterine contractility and embryo implantation.
      ;
      • Czuczwar P.
      • Stepniak A.
      • Wrona W.
      • Wozniak S.
      • Milart P.
      • Paszkowski T.
      The influence of uterine artery embolisation on ovarian reserve, fertility, and pregnancy outcomes - a review of literature.
      ). For these reasons, UAE has often only been offered to women who did not want to retain their fertility. In a prospective cohort (
      • Torre A.
      • Paillusson B.
      • Fain V.
      • Labauge P.
      • Pelage J.P.
      • Fauconnier A.
      Uterine artery embolization for severe symptomatic fibroids: effects on fertility and symptoms.
      ), women who had fibroids and intended to conceive yet were unable to undergo myomectomy were offered UAE. Only one out of 31 women who were actively trying for pregnancy after UAE succeeded, but the pregnancy ended in miscarriage. This analysis confirms that UAE should not be considered as first-line conservative management of fibroids for women with fertility wishes. As for UPA and ablation therapy, no controlled trials were conducted on pregnancy outcomes. Therefore, more studies need to establish whether UPA or ablation therapy are indeed associated with a lower live birth rate compared with myomectomy. Both UPA and ablation therapy, however, seem promising in women with leiomyomata who intend to have a subsequent pregnancy.
      This analysis is unable to assess pregnancy rates and time taken to achieve pregnancy owing to the limited and potentially selective nature of the data, and the lack of a denominator of women who wished and tried to conceive. Research includes mostly cohort studies or cases series, and pregnancy was not a primary outcome of the randomized controlled trials that were included. In addition, women being advised to wait after surgery before conceiving may also have an effect (
      • Dicle O.
      • Kucukler C.
      • Pirnar T.
      • Erata Y.
      • Posaci C.
      Magnetic resonance imaging evaluation of incision healing after cesarean sections.
      ), which may also apply to treatment with ablation or UAE. The lack of direct comparisons of different fibroid treatment within studies where pregnancy is desired by a significant proportion of women is, however, the most important limitation to this analysis, as systematic differences may exist in the characteristics of women offered the various treatments in the studies reported.
      In conclusion, myomectomy seems to be the treatment modality of choice for women wishing conservative management of fibroids with a view to subsequent pregnancy, although infrequent but specific risks of uterine rupture and abnormal placentation occur. Pregnancy outcomes were similar after fibroid ablation but were worse after UAE, and too few pregnancies have been reported after UPA treatment to allow analysis. In view of this, UAE is perhaps limited to women who have contraindications for other conservative approaches. Until large comparative randomized controlled trials or prospective cohort studies focusing on pregnancy outcomes are carried out, these data may allow more accurate counselling and decision making.

      Acknowledgements

      We would like to express our utmost gratitude to Mr Zhen Zhe Wong for taking up the role of the second reviewer and Ms Donna Watson for analytical resources and research methodology advice.

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