Obstetrics & Gynecology:
Pregnancy After Uterine Artery Embolization for Leiomyomata:: The Ontario Multicenter Trial
Pron, Gaylene PhD*; Mocarski, Eva MD†; Bennett, John MD‡; Vilos, George MD§; Common, Andrew MD¶; Vanderburgh, Leslie MD∥; Ontario UFE Collaborative Group
From the Departments of *Public Health Sciences, University of Toronto, Toronto, Ontario; †Obstetrics and Gynecology, St. Michael's Hospital, Toronto, Ontario; ‡Radiology, St. Joseph's Health Care, London, Ontario; §Obstetrics and Gynecology, St. Joseph's Health Care, London, Ontario; ¶Medical Imaging, St. Michael's Hospital, Toronto, Ontario; and ∥Radiology, William Osler Health Center, Brampton, Ontario, Canada.
Funded in part by the Boston Scientific Corporation.
Address reprint requests to: Dr. Gaylene Pron, Department Public Health Sciences, Faculty of Medicine, University of Toronto, 12 Queens Park Crescent West, Rm. 7 McMurich Building, Toronto, Ontario M5S 1A8, Canada; e-mail: email@example.com.
Received June 9, 2004. Received in revised form September 23, 2004. Accepted September 29, 2004.
OBJECTIVE: To report on pregnancies and deliveries occurring in a large cohort of women who underwent uterine artery embolization instead of surgery for symptomatic leiomyomata.
METHODS: A total of 555 women underwent uterine embolization in a multicenter clinical trial. The primary embolic agent was 355–500 μm polyvinyl alcohol particles with treatment end-point as bilateral stasis in the uterine arteries. Women desiring pregnancy were informed of the uncertain effect of embolization on fertility and pregnancy. Average age at embolization was 43 years (range 18–59 years). Thirty-one percent were younger than age 40 years. Women were followed up prospectively by telephone, and obstetric records of the women who conceived were reviewed.
RESULTS: Twenty-one women of average age 34 years (range 27–42 years) conceived, (3 of these twice), and 13 women were nulliparous. Twenty-three of the 24 pregnancies were conceived spontaneously (1 woman had in vitro fertilization). There were 4 spontaneous abortions (16.7%, 95% confidence interval 5.4–41.9%) and 2 elective pregnancy terminations. Fourteen of the 18 live births were full term and 4 were preterm. There were 9 vaginal deliveries and 9 cesarean deliveries, 4 of which were elective. Abnormal placentation occurred in 3 cases, all nulliparas (12.5% 95% confidence interval 3.1–36.3%). Two cases developed placenta previa (1 had a clinical partial accreta) and the third developed a placenta membranacea with accreta resulting in cesarean hysterectomy. Three postpartum hemorrhages all secondary to placental abnormalities occurred. Four newborns were small for gestational age (≤ 5th percentile); 2 of these pregnancies were complicated by gestational hypertension.
CONCLUSION: Women are able to achieve pregnancies after uterine artery embolization, and most resulted in term deliveries and appropriately grown newborns. Close monitoring of placental status, however, is recommended.
LEVEL OF EVIDENCE: II-3
Uterine artery embolization has now been shown in several large cohort studies to be an effective treatment for symptomatic uterine leiomyomata.1–7 The therapeutic effect of uterine embolization is thought to result from unrecoverable postembolic ischemic change within the leiomyomata leading to leiomyoma necrosis and volume reduction with subsequent improvement in menorrhagia, bulk (pressure) symptoms, and dysmenorrhea. Many patients with large symptomatic leiomyomata opting for uterine embolization also desire to maintain their fertility.
The efficacy of uterine embolization in the management of pelvic hemorrhage, both obstetric and gynecologic has been well documented8–10. Successful pregnancy outcomes have been reported after embolization for obstetric hemorrhage,11,12 gestational trophoblastic tumors,13 arteriovenous anomalies of the uterus,14,15 and cervical ectopic pregnancy.16–18
There is little published on the effect of uterine embolization for symptomatic leiomyomata on fertility and pregnancy. In addition to this study there have been only 4 case reports19–22 and 5 clinical studies,23–28 involving a total of 58 pregnancies in women undergoing uterine embolization for symptomatic leiomyomata. Uterine embolization continues to be offered primarily as a treatment alternative to hysterectomy to women with symptomatic leiomyomata. The use of embolization for fertility preservation, however, is rapidly becoming an issue, as more women of child-bearing age elect for transcatheter management of their symptomatic leiomyomata. To date, most centers have advocated a cautious approach in dealing with these patients and have generally advised against uterine embolization until more is known.
This study evaluated the pregnancies occurring in a large cohort of women undergoing uterine embolization as an alternative to hysterectomy for symptomatic leiomyomata in a prospective multicenter clinical study (the Ontario Uterine Fibroid Embolization Trial).7 The objectives of that study were to evaluate the safety, effectiveness, and durability of embolization. The desire for fertility was not an exclusion criterion for the study, and pregnancies were identified during our ongoing prospective follow-up interviews. These patients formed the basis of this study.
MATERIALS AND METHODS
Patients underwent uterine artery embolization in a prospective multicenter single-arm clinical treatment trial encompassing the practices of 11 interventional radiologists in 8 Ontario hospitals. Between November 1998 and November 2000, 555 women underwent uterine embolization for symptomatic leiomyomata and were enrolled in the study. Institutional Review Board approval for the study was obtained at all sites, and informed consent was obtained from patients before treatment. The average age of women in our study was 43 years (range 18–59 years). Thirty-one percent were aged less than 40 years, and 50% were nulliparous. The desire for fertility retention was not an exclusion criterion, and women were informed about the lack of information about the safety of undertaking pregnancy after uterine embolization. More complete details of the characteristics of the Ontario cohort have been reported elsewhere.29
Uterine artery embolization was performed with polyvinyl alcohol particles sized 355–500 μm as the primary embolic agent, with an embolization endpoint of complete stasis in the uterine arteries. Bilateral embolization was performed in 97% of the cases. Complete technical details on the procedure have been reported elsewhere.30
Patients were followed up with telephone interviews and ultrasonography at 2 weeks, 3 months, 6 months, and planned annually for 5 years. At the end of the study period, the 1-year and 2-year follow-up interview rates for the entire cohort were 91% and 84%. At telephone follow-up interviews, patients were asked whether they had been trying to achieve pregnancy and whether they had been successful. Women reporting pregnancies were sent additional consent forms for release of their obstetric records from physician offices and hospitals.
Because the study was not originally designed to evaluate fertility or pregnancy outcomes, we did not obtain detailed reproductive histories, investigate infertility factors, or measure gonadotropin levels. Maternal age, parity, prior myomectomy, and duration (months) from embolization to conception were noted, along with antepartum complications. Pregnancy details included management setting (teaching or community hospital), attending physician (obstetrician, family doctor), planned and actual mode of delivery, and indications for cesarean delivery. Peripartum complications were noted.
Neonatal outcome measurements included gestational age (preterm < 37 weeks), sex, birth weight, Apgar scores, and birth weight percentiles for gestational age. Low birth weight (LBW) was defined as less than 2,500 g, and very low birth weight (VLBW) was defined as less than 1,500 g.31 Percentiles for birth weights were determined by linear interpolation using birth weight gestational age charts for male and female singletons based on the Canadian population.32 Small for gestational age (SGA) was conservatively defined as those birth weights at or below the 5th birth weight percentile for gestational age. Exact confidence intervals (CI) for proportions based on number of women achieving pregnancy were calculated using StatXact software (Cytel Software, Cambridge, MA).
During our follow-up period after embolization, 24 pregnancies occurred in 21 women (Table 1). Three patients became pregnant twice. Average age at embolization of this group was 34 years (range 31–42 years). Eleven patients were white, 7 were African American, and 3 were Asian. Thirteen were nulliparous and 6 were nulligravida. Twelve patients had prior spontaneous abortions, and 2 had histories of recurrent miscarriages (4 and 9 spontaneous abortions, respectively).
Three patients (all nulliparous) had prior myomectomies and 1 of these (gravida 2, para 0) had 2 prior myomectomies. At embolization, all patients had dominant transmural leiomyomata, and all except for 1 measured 5 cm or greater in diameter (range 3–12 cm) (Table 2). The average number of leiomyomata per uterus was 3. The average uterine volume was 426 mL (standard deviation 320). Postembolization leiomyoma volume reduction averaged 46% (standard deviation 22%). No patients underwent magnetic resonance imaging before pregnancy to evaluate the integrity of the uterine wall. After embolization, menstruation resumed at the first cycle in all but 2 patients, whose menstruation resumed at the second cycle.
Twenty-three pregnancies were spontaneous and 1 (in a patient who had had 2 previous myomectomies) was achieved by in vitro fertilization. The pregnancies resulted in 18 live births, 4 spontaneous abortions (16.7%, 95% CI 5.4– 41.9%) and 2 elective terminations (1 for Trisomy 18 and 1 for an unplanned pregnancy). Of the 18 births, 14 were term and 4 were preterm (1 woman had 2 preterm deliveries). The average time from embolization to conception was 15 months (range 2–42 months). Ten occurred within the first year, 7 within the second year, 5 within the third, and 2 within the fourth year after embolization. The spontaneous abortions occurring in 4 patients 7, 12, 30, and 35 months after embolization, did not seem to be related to the duration to conception after embolization. The ages and (parity) of these patients were 34 (gravida 0, para 0), 37 (gravida 0, para 0), 38 (gravida 2, para 0), and 39 (gravida 0, para 0) years.
Twenty-one pregnancies were managed by obstetricians and 3 by family doctors. Care was more likely to be provided in a community hospital (n = 16) than a teaching hospital (n = 8). Pregnancies were uneventful except for 2 patients who required admission early in the third trimester for antepartum hemorrhage secondary to placenta previa. There were no complications related to leiomyoma growth or ischemic degeneration or breakdown. One patient in our study had a pregnancy before embolization complicated by red (ischemic) degeneration that resulted in the patient being hospitalized for several months to manage pain. Her pregnancy after embolization, like the others in our study group, was uneventful. Four patients in the group developed gestational hypertension, and 2 were delivered preterm.
The average age at delivery was 36 years (range 29–42 years). A trial of labor planned for 14 of the pregnancies resulted in 9 vaginal deliveries (7 spontaneous and 2 induced) and 5 cesarean deliveries (Fig. 1). The 2 labor inductions were for a postdate pregnancy and gestational hypertension. The indications for the 5 cesarean deliveries after a trial of labor were nonreassuring fetal heart rate tracing (n = 3), failure to progress (n = 1), and failed induction of labor (n = 1). The indications for the 4 elective cesarean deliveries involved prior myomectomy (n = 1), repeat cesarean delivery (n = 1), and antepartum hemorrhage (n = 2), both secondary to placenta previa.
Overall 3 pregnancies (12.5%, 95% CI 3.1–36.3%), all nulliparas, were complicated by abnormal placentation. Two patients aged 35 and 36 years had complete placenta previa. Neither had undergone prior myomectomy. Both were admitted and delivered early in the third trimester because of antepartum hemorrhage. Clinically, 1 of these patients (pregnancy 9) had a small area of placenta accreta in the vicinity of the cervix. The placenta was left in situ on this area. The other patient (pregnancy 8) underwent an inverted T incision due to lower segment leiomyomata with a breech delivery. Both deliveries resulted in postpartum hemorrhage, although neither delivery necessitated transfusion.
The third case (pregnancy 10) involved an African-American, 34-year-old women who conceived 3 years after embolization and had an uneventful pregnancy. A cesarean delivery was performed for failed induction of labor at 41 weeks gestation. At surgery, dilated superficial vessels were identified running over the external surface of the entire uterus. The infant (3,800 g) was delivered through a lower segment incision. The placenta occupied the entire uterine cavity and extended into the lower segment. The patient began to bleed heavily as traction was placed on the cord. The placenta did not separate and a clinical diagnosis of placenta increta or accreta was made. A cesarean hysterectomy was carried out. The patient lost 5 L of blood and received 7 units of packed red cells. The pathology report confirmed placenta accreta. The placental cake measured 2 cm in thickness, in keeping with a placenta membranacea.
The neonatal outcomes are summarized in Table 3. Five infants had LBWs (3 of whom were preterm) and 1 (also preterm) had a VLBW of 1,055 g. Delivery of the VLBW infant preterm at 31 weeks was the result of antepartum hemorrhage secondary to a placenta previa. Of the 18 infants, 12 were appropriate weight for gestational age. Of the 4 infants SGA (≤ 5th percentile), 3 were delivered at term. Two were born to women with gestational hypertension. All of these women conceived within 12 months of embolization.
Uterine artery embolization has only recently become a treatment option for symptomatic leiomyomata. The literature on pregnancies after uterine embolization is limited to case reports or clinical studies investigating the safety and effectiveness for leiomyoma reduction and symptom relief.
Because our study was also not designed to evaluate fertility, the denominator of women attempting to achieve pregnancy was not optimally defined. Although 164 women reported a desire for future pregnancy before embolization, only 35 women reported that they were trying to conceive at the 1-year follow-up telephone interview. Although age and past reproductive histories of many of the patients in this cohort suggests a level of subfertility before their embolization, most conceived spontaneously. One patient in our study achieved a pregnancy with in vitro fertilization, and at least 1 other successful pregnancy has been reported after embolization with in vitro fertilization.26 The efficacy of in vitro fertilization in women having undergone embolization is also an emerging consideration for both infertile women with leiomyomata and physicians providing these treatments
Potential effects of embolization on ovarian function are an important consideration if fertility preservation is desired. Few studies, however, have reported on gonadotropin levels. Of the 5 case studies33–37 reviewing gonadotrophin levels after embolization, the largest involved 66 cases,33 and follow-up was short term, to 6 months or 12 months.37 Clearly, the evidence is far too limited to make conclusive statements on premature menopause or ovarian failure after embolization.
Initially it was not known whether an embolized uterus could sustain a pregnancy, and it was thought that fetal losses could be high. Interpreting spontaneous abortion rates after embolization is difficult because of confounding factors such as advanced maternal age and the large leiomyoma burden present in most embolization study cohorts. Our study patients were older (an average of 42 years) and were generally more comparable in age to patients undergoing hysterectomy. Patients in our cohort also had multiple leiomyomata and long standing symptoms. Half were nulliparous, and many had prior spontaneous abortions.
Spontaneous abortions are known to increase with maternal age, ranging from 18% in the late 30s to 34% in the early 40s in the general population.38 The 16.7% spontaneous abortion rate in our study, although based on a small sample, does not seem to be higher than the general population rates. Our rate was also similar to the 20% rate reported in the British embolization cohort,28 but lower than the 35% and 29% reported in the French24,25 and American26 studies. Because embolic techniques with respect to angiographic endpoints were similar in these studies, patient differences and variability due to small samples are likely to account for these discrepancies. The high rate in the French study could be accounted for to some extent by the use of smaller embolic particles (150 –300 μm) and the advanced maternal age of the women (all older than 40 years of age). Based on these initial reports, although the numbers of pregnancies are small, uterine embolization does not seem to confer an obvious increased risk of pregnancy wastage.
Uterine embolization causes irreversible ischemia leading to leiomyoma degeneration, volume reduction, and symptom relief (particularly for menorrhagia). Because embolization cannot target exclusively the leiomyoma vascular supply, there is a concern for potential effects on the myometrium. Leiomyomata, however, are thought to be generally more susceptible to ischemia than the normal myometrium, which has an extensive collateral vascular system that is protective. Fortunately, endometrial and uterine infarction after uterine artery embolization is rare.39,40 Our own experience is 2 cases (0.36%) of uterine infarction in the cohort of 555 women.41
Although the integrity and strength of the myometrium after uterine embolization is not known, results from histopathologic studies of failed embolization have concluded that the adjacent myometrium is generally spared.40 It does seem possible, however, that a uterus having substantial areas that underwent ischemic or hyaline degeneration may be weak and could potentially rupture. Recently in one of our centers, but after our study enrollment was completed, a uterus ruptured during pregnancy after embolization. The woman, however, had 2 myomectomies as well as an embolization (personal communication, Wendy Whittle, March 24, 2004). Although pregnancies occurring after embolization are too few to make definitive comments on risk of uterine rupture, the use of multiple uterine interventions in women with leiomyomata hoping to achieve pregnancy does have increased risks.
Little is known about the optimal time to achieve pregnancy after embolization. Leiomyomata in most cases gradually shrink, and although most reductions are achieved within 6 months to a year,26the extent and timing of uterine healing associated with these changes are unknown. In our study patients intending to conceive after embolization were advised to wait several months, in keeping with the advice given women after myomectomy.42
The observation in our study of 3 cases of abnormal placentation was unexpected. Although ours is a small study, the number of cases of abnormal placentation seems unusually elevated. The incidence of placenta previa at delivery varies in published studies from 3 to 6 per 1,000 pregnancies.43 Placenta accreta, occurring when there is a focal or diffuse absence of the decidua basalis resulting in a poorly formed decidua that leads to deeper trophoblast invasion is also a rare complication.44 The incidence has been reported to range widely from 1 in 540 to 1 in 70,000.45 An increasing incidence of placenta accreta (1 in 14,780 deliveries in 1960–1970 to 1 in 7,270 deliveries in 1970 –1980)46 has been attributed to an increasing cesarean delivery rate.45,46 The risk of accreta when placenta previa is present is approximately 5% without a previous uterine surgery and can be as high as 30% with a prior cesarean delivery.47 Placenta membranacea, a variant wherein a thin placenta covers the entire uterine cavity and observed in 1 of our cases, is also a rare event (1 in 21,500 deliveries).48 It is thought to result from a developmental abnormality affecting the trophoblastic shell of the early placenta, resulting in villi covering the entire amnion.44
The known risk factors for abnormal placentations include advanced maternal age (older than 35 years), multiparity, smoking, and prior cesarean delivery.44,46–48 In a population-based record linkage study49 involving birth records and hospital discharge records, leiomyomata were not found to be associated with placenta previa (odds ratio 1.76, 95% CI 0.76–4.05), but they were found to be significantly associated with abruptio placentae (odds ratio 3.87, 95% CI 1.63–9.17). The 3 women in our study with placental anomalies, although older (34, 35, and 36 years), were nulliparous, and none had prior myomectomy.
It is uncertain whether abnormal placentas observed in our pregnancies are directly related to embolization. It is possible that during embolization endometrial perfusion could be compromised, leading to a focal or total absence of the decidua basalis. The fact that menstruation resumed after embolization in all of these women, however, suggests that the effects on the endometrium must have been more limited or focal. Denudation of endometrium after embolization has recently been described.50 In that case report, an atrophic endometrial cavity was found after a hysteroscopic investigation for persistent amenorrhea 6 months postembolization. Biopsy results confirmed atrophic endometrium. The patients in our study were very aggressively embolized to no flow in the uterine arteries, and adverse effects on the endometrium are possible.
Abnormal placentas have also been reported in pregnancies after endometrial resection or ablation. In a recent review51 of pregnancy occurring after these procedures, although half (49%; 22/45) were terminated at maternal request, 6 of the 17 pregnancies that progressed beyond 20 weeks had abnormally adherent placentas. Three of the placentas were very adherent, 2 were accretas (1 requiring a cesarean hysterectomy), and 1 was increta in which the uterus was preserved. The authors advised hysteroscopy after these procedures to demonstrate endometrial integrity before attempting pregnancy. Given the abnormal placentations occurring in our study, women contemplating pregnancy after uterine embolization might be advised to undergo diagnostic hysteroscopy to determine endometrial integrity.
Leiomyomata have been reported to be associated with higher complication rates during pregnancy, labor and delivery.49,52–54 We did not have a protocol for managing pregnancies in our study and because women only had routine obstetric ultrasonography, we are unable to comment directly on the behavior of leiomyomata in the gravid uterus after embolization. Although there were no leiomyoma-related complications in our study such as red degeneration, the number of pregnancies is too small to conclude that embolization might be protective for this complication. Pregnancies were uneventful except for 2 cases of placenta previa that had to be admitted and delivered early in the third trimester because of antepartum hemorrhage. The majority of patients in our study group labored at term. Uterine leiomyomata can lead to abnormal fetal lie, and breech rates as high as 13% have been reported.49 Only 1 infant presented as breech in our study, but the patient also had placenta previa (another risk factor for abnormal fetal lie).
Leiomyomata are also thought to be associated with a higher incidence of dystocia (poor contractility),52,53 and there may be further concerns regarding the contractility of myometrium of the embolized uterus. However, the majority of vaginal deliveries in our study were spontaneous. Although many deliveries in our study were managed by a trial of labor resulting in spontaneous vaginal delivery, an equal number of deliveries involved either elective or cesarean deliveries during labor. The number of deliveries in our study is too small to allow us to make recommendations on delivery management. However it would seem prudent to follow these pregnancies with at least the same assumed risk as after transmural myomectomy or cesarean delivery until more is known about pregnancy after embolization.
Women with leiomyomata have been reported to be twice as likely as women without leiomyomata to deliver a term, LBW infant.49 Neonatal outcomes in our study, however, were generally favorable. All infants were born live, and none of the fetuses required delivery in the mid trimester. Four infants, however, were SGA using a definition of 5th percentile or less for birth weight for gestational age, and 2 of these were below the 3rd percentile. The number of LBW babies is difficult to interpret, because 2 of the mothers also had gestational hypertension (another risk factor for LBW). The infant having a VLBW (1,055 g) SGA (4th percentile) was delivered at 31 weeks because of antepartum hemorrhage secondary to placenta previa.
Our report shows that women, many of them nulliparous with previous miscarriages are able to achieve successful pregnancies after uterine embolization. These outcomes do provide some hope to women who otherwise would have had a hysterectomy or are unsuitable for myomectomy. Larger prospective studies, however, are needed to learn more about fertility and outcomes of these pregnancies. In the interim, pregnancies occurring after embolization should be managed conservatively despite the uneventful pregnancies and successful trial of labors in our study until more is known about delivery outcomes. These patients would also benefit from an evaluation of their placental status during pregnancy to facilitate appropriate transfer of care if abnormalities are detected.
1. Ravina JH, Ciraru-Vigneron N, Aymard A, Ferrand J, Merland JJ. Uterine artery embolization for fibroid disease: results of a 6 year study. Min Invas Ther Allied Technol 1999;8:441–7.
2. Pelage JP, Soyer P, LeDref O, Dahan H, Coumbaras J, Kardache M, et al. Uterine arteries: bilateral catheterization with a single femoral approach and a single 5-F catheter—technical note. Radiology 1999;210:573–575.
3. Hutchins FL, Worthington-Kirsch R, Berkowitz RP. Selective uterine artery embolization as primary treatment for symptomatic leiomyomata uteri. J Am Assoc Gynecol Laparosc 1999;6:279–84.
4. McLucas B, Adler L, Perrella R. Uterine fibroid embolization: nonsurgical treatment for symptomatic fibroids. J Am Coll Surg 2001;192:95–105.
5. Spies JB, Spector A, Roth AR, Baker CM, Mauro L, Murphy-Skrynarz K. Complications after uterine artery embolization for leiomyomas. Obstet Gynecol 2002;100:873–80.
6. Walker WJ, Pelage JP. Uterine artery embolization for symptomatic fibroids: clinical results in 400 women with imaging follow up. BJOG 2002;109:1262–72.
7. Pron G, Bennett J, Common A, Wall J., Asch M, Sniderman K, et al. The Ontario Uterine Fibroid Embolization Trial. Part 2. Uterine fibroid reduction and symptom relief after uterine artery embolization for fibroids. Fertil Steril 2003;79:120–7.
8. Stancato-Pasik A, Mitty HA, Richard HM, Eshkar N. Obstetric embolotherapy: effect on menses and pregnancy. Radiology 1997;204:791–3.
9. Vedantham S, Goodwin S, McLucas B, Mohr G. Uterine artery embolization: an underused method of controlling pelvic hemorrhage. Am J Obstet Gynecol 1997;176:938–48.
10. Pelage JP, Le Dref O, Jacob D, Soyer P, Herbreteau D, Rymer R. Selective arterial embolization of the uterine arteries in the management of intractable post-partum hemorrhage. Acta Obstet Gynecol Scand 1999;78:698–703.
11. Ornan D, White R, Pollak J, Tal M. Pelvic embolization for intractable postpartum hemorrhage: long-term follow-up and implications for fertility. Obstet Gynecol 2003;102:904–10.
12. Wang H, Garmel S. Successful term pregnancy after bilateral uterine artery embolization for postpartum hemorrhage. Obstet Gynecol 2003;102:603–4.
13. McIvor J, Cameron EW. Pregnancy after uterine artery embolization to control hemorrhage from gestational trophoblastic tumor. Br J Radiol 1996;69:624–9.
14. Chow TW, Nwosc EC, Gould DA, Richmond DH. Pregnancy following successful embolization of a uterine vascular malformation. BJOG 1995;102:166–8.
15. Poppe W, Van Ascher FA, Wilms G, Favril A, Baert A. Pregnancy after transcatheter embolization of a uterine arteriovenous malformation. Am J Obstet Gynecol 1987;156:1179–80.
16. Frates MC, Benson CB, Doubilet PM, DiSalvo DN, Brown DL, Laing FL, et al. Cervical ectopic pregnancy: results of conservative treatment. Radiology 1994;191:773–5.
17. Marston LM, Dotters DJ, Katz VL. Methotrexate and angiographic embolization for conservative treatment of cervical pregnancy. South Med J 1996;89:246–8.
18. Pattinson HA, Dunphy BC, Wood S, Wood S, Saliken J Cervical pregnancy following in vitro fertilization: evacuation after uterine artery embolization with subsequent successful intrauterine pregnancy. Aust N Z J Obstet Gynaecol 1994;34:492–3.
19. Vashisht A, Smith JR, Thorpe-Beeston G, McCall J. Pregnancy subsequent to uterine artery embolization. Fertil Steril 2001;75:1246–7.
20. Kovacs P, Stangel JJ, Santoro NF, Lieman H. Successful pregnancy after transient ovarian failure following treatment of symptomatic leiomyomata. Fertil Steril 2002;77:1292–5.
21. Goldberg J, Pereira L, Berghella V. Pregnancy after uterine artery embolization. Obstet Gynecol 2002;100:869–72.
22. D'Angelo AD, Amso NN, Wood A. Spontaneous multiple pregnancy after uterine artery embolization for uterine fibroid: a case report. Eur J Obstet Gynecol Reprod Biol 2003;110:245–6.
23. Forman RG, Reidy J, Nott V, Braude P. Fibroids and fertility. Min Invas Ther Allied Technol 1999;8:415–9.
24. Ravina JH, Ciraru-Vigneron N, Aymard A, LeDref O, Merland JJ. Pregnancy after embolization of uterine myoma: report of 12 cases. Fertil Steril 2000;73:1241–3.
25. Ciraru-Vigneron N, Ravina JH. Pregnancy subsequent to uterine artery embolization. Fertil Steril 2001;75:1247–8.
26. McLucas B, Goodwin S, Adler L, Rappaport A, Reed R, Perrella R. Pregnancy following uterine fibroid embolization. Int J Gynaecol Obstet 2001;74:1–7.
27. Anderson PE, Lund N, Justesen P, Munk T, Elle B, Floridon C. Uterine artery embolization of symptomatic uterine fibroids: initial success and short-term results. Acta Radiol 2001;42:234–8.
28. Walker WJ, Pelage JP. Uterine artery embolisation for symptomatic fibroids: clinical results in 400 women with imaging follow up. BJOG 2002;109:1262–72.
29. Pron G, Cohen M, Soucie J, Garvin G, Vanderburgh L, Bell S. The Ontario uterine fibroid embolization trial. Part 1. Baseline patient characteristics, fibroid burden, and impact on life. Fertil Steril 2003;79:112–9.
30. Pron G, Bennett J, Common A, Sniderman K, Asch M, Bell S, et al. Technical results and effects of operator experience on uterine artery embolization for fibroids: the Ontario uterine fibroid embolization trial. J Vasc Interv Radiol 2003;14:545–54.
31. Arbuckle TE, Wilkins R, Sherman G. Birth weight percentiles by gestational age in Canada. Obstet Gynecol 1993;81:39–48.
32. Kramer MS, Platt RW, Wen SW, Joseph KS, Allan A, Abrahamowicz M, et al. A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics 2001;108:1–7.
33. Chrisman HB, Saker MB, Ryu RK, Nemcek AA, Gerbie MV, Milad MP, et al. The impact of uterine fibroid embolization on resumption of menses and ovarian function. J Vasc Interv Radiol 2000;11:699–703.
34. Spies JB, Roth AR, Gonsalves SM, Murphy-Skrzniarz KM. Ovarian function after uterine artery embolization of leiomyomata: assessment with use of serum follicle stimulating hormone assay. J Vasc Interv Radiol 2001;12:437–42.
35. Tulandi T, Sammour A, Valenti D, Child TJ, Seti L Tan SL. Ovarian reserve after uterine artery embolization for leiomyomata. Fertil Steril 2002;78:197-8.
36. Ahmad A, Qadan L, Hassan N, Najarian K. Uterine artery embolization treatment of uterine fibroids: effect on ovarian function in younger women. J Vasc Interv Radiol 2002;13:1017–20.
37. Tropeano G, Di Stasi C, Litwicka K, Romano D, Draisci G, Mancuso S. Uterine artery embolization for fibroids does not have adverse effects on ovarian reserve in regularly cycling women younger than 40 years. Fertil Steril 2004;81:1055–61.
38. Warburton D, Kline J, Stein A, Strobino B. Cytogenetic abnormalities in spontaneous abortions of recognized conceptions. In: Porter IH, editor. Perinatal genetics, diagnosis and treatment. New York (NY): Academic Press; 1986. p. 133.
39. McCluggageWG, Ellis PK, McClure N, Walker WJ, Jackson PA, Manek S. Pathologic features of uterine leiomyomas following uterine artery embolization. Int J Gynecol Pathol 2000;19:342-7.
40. Colgan TJ, Pron G, Mocarski EJM, Bennet J, Asch M, Common A. Pathologic features of uteri and leiomyomas following uterine artery embolization for leiomyomas. Am J Surg Pathol 2003;27:167–77.
41. Pron G, Mocarski E, Cohen M, Colgan T, Bennett J, Common A, et al. Hysterectomy for complications after uterine artery embolization for leiomyoma: results of a Canadian multicenter clinical trial. J Am Assoc Gynecol Laparosc 2003;10:99–106.
42. Thompson JD, Rock JA. Leiomyomata uteri and myomectomy. In: Thompson JD, Rock JA, editors. Te Linde's operative gynecology. 8th ed. Philadelphia (PA): Lippincott-Raven; 1997. p. 731–70.
43. Ananth CV, Demissie K, Smulian JC, Vintzileos AM. The effect of placenta previa on neonatal mortality: a population based study in the United States, 1989 through 1997. Am J Obstet Gynecol 2003;188:1299–304.
44. American Institute of Ultrasound in Medicine. Ultrasonography of the placenta—a review. Laurel (MD): American Institute Ultrasound in Medicine; 1994.
45. Miller DA, Chollet JA, Goodwin TM. Clinical risk factors for placenta previa–placenta accreta. Am J Obstet Gynecol 1997;177:210–4.
46. Read JA, Cotton DB, Miller FC. Placenta accreta: changing clinical aspects and outcome. Obstet Gynecol 1980;56:31–4.
47. Clark SL, Koonings PP, Phelan JP. Placenta previa/accreta and prior cesarean section. Obstet Gynecol 1985;66:89–92.
48. Hurley VA, Beischer NA. Placenta membranacea: case reports. BJOG 1987;94:798–802.
49. Coronado GD, Marshall LM, Schwartz SM. Complications in pregnancy, labor and delivery with uterine leiomyomas: a population-based study. Obstet Gynecol 2000;95:764–9.
50. 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. Fertil Steril 2003;79:132–5.
51. Cook JR, Seman EI. Pregnancy following endometrial ablation: case history and literature review. Obstet Gynecol Surv 2003;58:551–6.
52. Davis JL, Ray-Mazumder S, Hobel CJ, Baley K, Sassoon D. Uterine leiomyomas in pregnancy: a prospective study. Obstet Gynecol 1990;75:41–4.
53. Vergani P, Ghidini A, Strobelt N, Roncaglia N, Locatelli A, Lapinski RH, et al. Do uterine leiomyomas influence pregnancy outcome? Am J Perinatol 1994;11:356–8.
54. Rice JP, Kay HH, Mahoney BS. The clinical significance of uterine leiomyomas in pregnancy. Am J Obstet Gynecol 1989;160:1212–6.
The following physicians assisted in the clinical follow-up of the patients:
Dr. Kofi Amankwah, Sunnybrook and Women's College Health Sciences Center, Toronto, Ontario; Dr. Jon Barrett, Sunnybrook and Women's College Health Sciences Center, Toronto, Ontario; Dr. Sam Batarseh, Toronto East General Hospital, Toronto, Ontario; Dr. Barbara Brennan, McMaster University Medical Center, Hamilton, Ontario; Dr. Adrian Brown, North York General Hospital, North York, Ontario; Dr. Henry Cheng, William Osler Health Center, Brampton, Ontario; Dr. Anna Davenport, Headwaters Health Center, Orangeville, Ontario; Dr. Fraser Fellows, St. Joseph's Health Center, London, Ontario; Dr. Jeffrey Gilmour, Scarborough Grace Hospital, Scarborough, Ontario; Dr. Mathias Gysler, Credit Valley Hospital, Mississauga, Ontario; Dr. Peter Hawrylyshyn, Mount Sinai Hospital, Toronto, Ontario; Dr. Susan Hayward, William Osler Health Center, Brampton, Ontario; Dr. Linda Kapusta, Credit Valley Hospital, Mississauga, Ontario; Dr. David Langlois, Credit Valley Hospital, Mississauga, Ontario; Dr. Edith Linkenheil, Markham Stouffville Health Center, Markham, Ontario; Dr. Robert Nowicki, St. Catharines General, St. Catharines, Ontario; Dr. Titus Owolabi, North York General Hospital, North York, Ontario; Dr. Gareth Seaward, Mount Sinai Hospital, Toronto, Ontario; Dr. Oluyomi Adetokumbo Sobowale, Peterborough Regional Hospital, Peterborough, Ontario; and Dr. Michael Sved, Mount Sinai Hospital, Toronto, Ontario, Canada.
This article has been cited 89 time(s).
Ultrasound in Obstetrics & GynecologyMorbidly adherent placenta: evaluation of ultrasound diagnostic criteria and differentiation of placenta accreta from percretaUltrasound in Obstetrics & Gynecology
Obstetrics and Gynecology Clinics of North AmericaPlacenta Accreta, Increta, and PercretaObstetrics and Gynecology Clinics of North America
Journal of PerinatologyPlacenta accreta in a patient with a history of uterine artery embolization for postpartum hemorrhageJournal of Perinatology
Gynecologie Obstetrique & FertilitePlacenta accreta: Screening, management and complicationsGynecologie Obstetrique & Fertilite
Minimally Invasive Therapy & Allied TechnologiesPregnancy following uterine artery embolization: An updateMinimally Invasive Therapy & Allied Technologies
Minimally Invasive Therapy & Allied TechnologiesOvarian reserve following uterine artery embolization in women of reproductive age: A preliminary reportMinimally Invasive Therapy & Allied Technologies
Obstetrics and Gynecology Clinics of North AmericaThe Impact and Management of Fibroids for Fertility An Evidence-Based ApproachObstetrics and Gynecology Clinics of North America
Archives of Gynecology and ObstetricsPregnancy after uterine artery embolization for the treatment of myomas: a case seriesArchives of Gynecology and Obstetrics
Gynecological EndocrinologyAssisted reproductive technique increases the risk of placental polypGynecological Endocrinology
Cardiovascular and Interventional RadiologySuccessful pregnancy with a full-term vaginal delivery one year after n-butyl cyanoacrylate embolization of a uterine arteriovenous malformationCardiovascular and Interventional Radiology
Journal of Vascular and Interventional RadiologyUterine artery embolization and future fertilityJournal of Vascular and Interventional Radiology
New England Journal of Medicine
Treatment of uterine fibroids - Is surgery obsolete?
New England Journal of Medicine, 356(4):
Journal of Vascular and Interventional RadiologyUterine artery embolization for control of life-threatening hemorrhage at menarche: Brief reportJournal of Vascular and Interventional Radiology
Canadian Family Physician
Uterine fibroid embolization - CME update for family physicians
Canadian Family Physician, 53():
Seminars in PerinatologyAbnormal PlacentationSeminars in Perinatology
Ultrasound in Obstetrics & GynecologyUterine fibroid embolization: where are we and where should we go?Ultrasound in Obstetrics & Gynecology
Journal of Minimally Invasive GynecologyClinical update of smooth muscle tumors of the uterusJournal of Minimally Invasive Gynecology
Clinics in PerinatologyPlacenta Accreta and Cesarean Scar Pregnancy: Overlooked Costs of the Rising Cesarean Section RateClinics in Perinatology
Journal of Minimally Invasive GynecologyEvaluation and Treatment of Menorrhagia in an Adolescent PopulationJournal of Minimally Invasive Gynecology
American Journal of RoentgenologyHistory of Uterine Artery Occlusion and Subsequent PregnancyAmerican Journal of Roentgenology
European Journal of RadiologyThe role of interventional radiology in obstetric and gynaecology practiceEuropean Journal of Radiology
International Journal of Obstetric AnesthesiaBloodless trilogy? Anesthesia, obstetrics and interventional radiology for cesarean deliveryInternational Journal of Obstetric Anesthesia
Genes Chromosomes & CancerA micro-RNA signature associated with race, tumor size, and target gene activity in human uterine leiomyomasGenes Chromosomes & Cancer
Human Reproduction UpdateNon-surgical management of uterine fibroidsHuman Reproduction Update
Fertility and SterilityPregnancy outcomes after uterine artery occlusion: prospective multicentric studyFertility and Sterility
Fertility and SterilityRecanalization and particle exclusion after embolization of uterine arteries in sheep: a long-term studyFertility and Sterility
American Journal of Obstetrics and GynecologyUterine fibroid embolization: a viable alternative to hysterectomyAmerican Journal of Obstetrics and Gynecology
Bjog-An International Journal of Obstetrics and GynaecologyLong-term follow up of uterine artery embolisation - an effective alternative in the treatment of fibroidsBjog-An International Journal of Obstetrics and Gynaecology
Human Reproduction UpdateFibroids and female reproduction: a critical analysis of the evidenceHuman Reproduction Update
Best Practice & Research in Clinical Obstetrics & GynaecologyEndoscopic management of uterine fibroidsBest Practice & Research in Clinical Obstetrics & Gynaecology
Best Practice & Research in Clinical Obstetrics & GynaecologyRadiological treatment of symptomatic uterine fibroidsBest Practice & Research in Clinical Obstetrics & Gynaecology
New England Journal of Medicine
Uterine Fibroid Embolization
New England Journal of Medicine, 361(7):
International Journal of Gynecology & ObstetricsCell-free placental mRNA in maternal plasma to predict placental invasion in patients with placenta accretaInternational Journal of Gynecology & Obstetrics
Canadian Association of Radiologists Journal-Journal De L Association Canadienne Des Radiologistes
Survey of Gynecologists' and Interventional Radiologists' Opinions of Uterine Fibroid Embolization
Canadian Association of Radiologists Journal-Journal De L Association Canadienne Des Radiologistes, 57(3):
Medical Letter on Drugs and Therapeutics
Uterine artery embolization for fibroids
Medical Letter on Drugs and Therapeutics, 47():
Obstetrics and Gynecology Clinics of North AmericaUterine artery embolization as a treatment option for uterine myomasObstetrics and Gynecology Clinics of North America
Journal of Vascular and Interventional RadiologyDevelopment of a research agenda for uterine artery embolization: Proceedings from a multidisciplinary research consensus panel - CommentaryJournal of Vascular and Interventional Radiology
Journal of Obstetrics and Gynaecology ResearchUterine artery embolization should not be recommended without careful consideration in the treatment of symptomatic uterine fibroidsJournal of Obstetrics and Gynaecology Research
Fertility and SterilityMyomas and reproductive functionFertility and Sterility
European Journal of Gynaecological Oncology
Metastatic leiomyosarcoma diagnosed after uterine artery embolization
European Journal of Gynaecological Oncology, 30(2):
Fertility and SterilityPregnancy outcome after magnetic resonance-guided focused ultrasound surgery (MRgFUS) for conservative treatment of uterine fibroidsFertility and Sterility
Fertility and SterilityPregnancy after uterine fibroid embolization: follow-up of 100 patients embolized using tris-acryl gelatin microspheresFertility and Sterility
Human ImmunologyLeukocyte density and composition in human cycling endometrium with uterine fibroidsHuman Immunology
Cardiovascular and Interventional RadiologyPregnancy following uterine artery embolization with polyvinyl alcohol particles for patients with uterine fibroid or adenomyosisCardiovascular and Interventional Radiology
American Journal of Obstetrics and GynecologyPregnancy after uterine artery embolization for leiomyomata: A series of 56 completed pregnanciesAmerican Journal of Obstetrics and Gynecology
Journal of Vascular and Interventional RadiologyFocal myometrial defect and partial placenta accreta in a pregnancy following bilateral uterine artery embolizationJournal of Vascular and Interventional Radiology
Seminars in PerinatologyPostpartum hemorrhage: A recurring pregnancy complicationSeminars in Perinatology
Seminars in Reproductive MedicineThe effect of uterine fibroids on embryo implantationSeminars in Reproductive Medicine
Geburtshilfe Und FrauenheilkundeTreatment options for uterine leiomyoma - New aspects in 2008Geburtshilfe Und Frauenheilkunde
American Journal of Obstetrics and GynecologyIntraabdominal adhesions after uterine artery embolizationAmerican Journal of Obstetrics and Gynecology
Journal De Gynecologie Obstetrique Et Biologie De La Reproduction
Guidelines for the management of menometrorrhagia, in women with and without pregnancy intention: hierarchy of therapies
Journal De Gynecologie Obstetrique Et Biologie De La Reproduction, 37(8):
Clinical and Experimental Obstetrics & Gynecology
The development of placenta increta following pelvic transcatheter artery embolization for postpartum hemorrhage
Clinical and Experimental Obstetrics & Gynecology, 36(1):
ContraceptionUterine artery embolization to treat hemorrhage following second-trimester abortion by dilatation and surgical evacuationContraception
Archives of Gynecology and ObstetricsTreatment of fibroids via uterine artery occlusion (uterine artery embolization and Doppler-guided uterine artery occlusion): potential role in today's armamentariumArchives of Gynecology and Obstetrics
Journal of Vascular and Interventional RadiologyEffects of utero-ovarian anastomoses on basal follicle-stimulating hormone level change after uterine artery embolization with tris-acryl gelatin microspheresJournal of Vascular and Interventional Radiology
Journal of Obstetrics and Gynaecology ResearchHysteroscopy after uterine fibroid embolization in women of fertile ageJournal of Obstetrics and Gynaecology Research
Fertility and SterilityUterine myomas: managementFertility and Sterility
Journal De Gynecologie Obstetrique Et Biologie De La ReproductionPregnancy after uterine-artery embolization for symptomatic fibroids: A case of placenta accreta with uterine ruptureJournal De Gynecologie Obstetrique Et Biologie De La Reproduction
American Journal of RoentgenologyPregnancy After Uterine Artery Embolization for Symptomatic Fibroids: A Series of 15 PregnanciesAmerican Journal of Roentgenology
Journal of Minimally Invasive GynecologyUnmet Therapeutic Needs for Uterine MyomasJournal of Minimally Invasive Gynecology
Fertility and SterilityUterine artery embolization for fibroids is associated with an increased risk of miscarriageFertility and Sterility
International Journal of Gynecology & ObstetricsLaparoscopic uterine artery occlusion versus uterine fibroid embolizationInternational Journal of Gynecology & Obstetrics
Journal of Psychosomatic ResearchHysterectomy and loss of fertility: Implications for women's mental healthJournal of Psychosomatic Research
Bjog-An International Journal of Obstetrics and GynaecologyA 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 efficacyBjog-An International Journal of Obstetrics and Gynaecology
Fertility and SterilityFertility after bilateral uterine artery embolization in a sheep modelFertility and Sterility
American Journal of RoentgenologyLong-Term Quality of Life Assessment Among Patients Undergoing Uterine Fibroid EmbolizationAmerican Journal of Roentgenology
Bjog-An International Journal of Obstetrics and GynaecologyThromboembolism of the leg following prophylactic balloon occlusion of the uterine arteriesBjog-An International Journal of Obstetrics and Gynaecology
Journal of Minimally Invasive GynecologyRole of laparoscopic uterine artery coagulation in management of symptomatic myomas: A prospective study using ultrasound and magnetic resonance imagingJournal of Minimally Invasive Gynecology
American Journal of Obstetrics and GynecologyFibroids and reproductive outcomes: a systematic literature review from conception to deliveryAmerican Journal of Obstetrics and Gynecology
Best Practice & Research in Clinical Obstetrics & GynaecologyMolecular genetics and racial disparities of uterine leiomyomasBest Practice & Research in Clinical Obstetrics & Gynaecology
Minimally Invasive Therapy & Allied TechnologiesMyoma necrosis following Gelfoam (TM) embolization of uterine myomataMinimally Invasive Therapy & Allied Technologies
Archives of Gynecology and ObstetricsSuccessful use of uterine artery embolisation to treat placenta increta in the first trimesterArchives of Gynecology and Obstetrics
International Journal of Gynecological Cancer
Successful term pregnancy after selective embolization of a large postmolar uterine arteriovenous malformation
International Journal of Gynecological Cancer, 16():
Jama-Journal of the American Medical Association
A 41-Year-Old Woman With Menorrhagia, Anemia, and Fibroids Review of Treatment of Uterine Fibroids
Jama-Journal of the American Medical Association, 301(1):
Human ReproductionSuccessful spontaneous pregnancy following surgical removal of a post uterine artery embolized necrotic fibroid capsule: a case reportHuman Reproduction
Cardiovascular and Interventional RadiologyMidterm clinical and first reproductive results of a randomized controlled trial comparing uterine fibroid embolization and myomectomyCardiovascular and Interventional Radiology
Clinical Obstetrics and GynecologyEndovascular Treatment of Postpartum HemorrhageClinical Obstetrics and Gynecology
Clinical Obstetrics and GynecologyForewordClinical Obstetrics and Gynecology
Clinical Obstetrics and GynecologyUterine Artery Occlusion: What Is the Evidence?Clinical Obstetrics and Gynecology
Current Opinion in Obstetrics and GynecologyThe impact of uterine artery embolization on fertility and pregnancy outcomeCurrent Opinion in Obstetrics and Gynecology
Current Opinion in Obstetrics and GynecologyImpact of previous uterine artery embolization on fertilityCurrent Opinion in Obstetrics and Gynecology
Current Opinion in Obstetrics and GynecologyThe role of uterine artery embolization in the management of uterine fibroidsCurrent Opinion in Obstetrics and Gynecology
Current Opinion in Obstetrics and GynecologyMenorrhagia, mechanisms and targeted therapiesCurrent Opinion in Obstetrics and Gynecology
Current Opinion in Obstetrics and GynecologySurgical and radiological management of uterine fibroids in the UKCurrent Opinion in Obstetrics and Gynecology
Current Opinion in Obstetrics and GynecologyPregnancy outcomes following treatment for fibroids: uterine fibroid embolization versus laparoscopic myomectomyCurrent Opinion in Obstetrics and Gynecology
Current Opinion in Obstetrics and GynecologyRecent advances in uterine fibroid embolizationCurrent Opinion in Obstetrics and Gynecology
Obstetrics & GynecologyPregnancy After Uterine Artery Embolization for Leiomyomata: The Ontario Multicenter TrialObstetrics & Gynecology
Obstetrics & GynecologyPregnancy After Uterine Artery Embolization for Leiomyomata: The Ontario Multicenter TrialObstetrics & Gynecology
Obstetrics & GynecologyAssessment of New Technology in the Treatment of Idiopathic Menorrhagia and Uterine LeiomyomataObstetrics & Gynecology
© 2005 The American College of Obstetricians and Gynecologists