Journal of Minimally Invasive Gynecology (2006) 13, 398 – 402
Fertility after treatment of Asherman’s syndrome stage 3 and 4 Hervé Fernandez, MD, Fadheela Al-Najjar, MD, Aurélia Chauveaud-Lambling, MD, René Frydman, MD, and Amélie Gervaise, MD From the Department of Obstetrics and Gynecology, Hôpital Antoine Béclère, Assistance Publique-Hôpitaux de Paris,Clamart cedex, France (all authors).KEYWORDS: Abstract STUDY OBJECTIVE: To evaluate the efficacy of hysteroscopic adhesiolysis and subsequent fertility
in patients with adhesions stage 3 and 4. DESIGN: A retrospective cohort study (Canadian Task Force classification II-2). SETTING: A tertiary referral center for hysteroscopic surgery. PATIENTS: Seventy-one patients with intrauterine permanent adhesions. INTERVENTIONS: Hysteroscopic surgery with monopolar energy (n ϭ 31) or bipolar energy (n ϭ
40). Uterine cavity with at least one free ostial area was restored after one (n ϭ 31), two (n ϭ 20), three(n ϭ 15), or four or more (n ϭ 5) surgical procedures
RESULTS: Sixty-four patients were followed. Evaluation of the uterine cavity after surgery has been
performed by hysteroscopy for all the patients. All patients had resumption of menses, except for twopatients with a history of uterine artery embolization. Pregnancy index rate after the procedure was 28(43.8%) of 64, and the live birth rate was 21 (32.8%) of 64. In patients 35 years of age or younger, 20of 30 (66.6%) conceived compared with 8 of 34 (23.5%) in patients older than 35 years (p ϭ .01). Threepatients had either hysterectomy (n ϭ 2) or hypogastric arteries ligation for placenta accreta withuneventful postoperative course. CONCLUSIONS: Hysteroscopic adhesiolysis can be performed for severe adhesions stage 3 and 4
with safety and efficacy. Age is the main predictive factors of success: the pregnancies were at risk ofabnormal placentation. 2006 AAGL. All rights reserved.
Asherman’s syndrome is defined by the presence of
and 40% of uterine synechia are found after
intrauterine permanent adhesions, obliterating the uterine
repeated curettage for incomplete abortion or retained pla-
cavity partially or completely. The prevalence is 3.7% to
In addition, a prevalence of 2.7% has been report-
23.4% in women with a history of postpartum hemorrhag
ed in women undergoing hysterosalpingography for infer-
with curettage and 5% to 39% in women with recurrent
Women with Asherman’s syndrome may have menstrual
Corresponding author: Professeur Hervé Fernandez, MD, Service de
disturbance, while subfertility may be there main complaint.
Gynécologie-Obstétrique, Hôpital Antoine Béclère, Assistance Publique-
Hysteroscopic surgery currently is the optimal approach,
Hôpitaux de Paris (AP-HP), 157 rue de la Porte-de-Trivaux. 92141 Clamart
which has allowed rapid improvement in the diagnosis and
treatment of total or partial uterine adhesions. However, there
are very few studies concerning the treatment and fertility
Submitted November 17, 2005. Accepted for publication April 24,
prognosis of patients with severe adhesions.
1553-4650/$ -see front matter 2006 AAGL. All rights reserved. doi:10.1016/j.jmig.2006.04.013
Etiology of intrauterine adhesions and symptoms at initial consultation
D&C for missed or incomplete abortion
Subfertility and recurrent pregnancy loss
D&C ϭ dilatation and curettage.
We previously published a study of 31 patients with
Eight patients (11.3%) were referred to our tertiary care
reproductive center after first inefficient procedure. There
factors increased subsequent fertility: the role of age (Ͻ 35
was no case of tuberculosis endometritis in this series.
years) and the interest to repeat the procedures to restore a
Of the 71 patients, 31 patients (43.6%) reported amen-
normal cavity. Since this first short-term study, we intro-
orrhea, 19 (26.7%) profound hypomenorrhea, and 21
duced a new surgical technique with Versapoint electrode
(29.7%) normal cycles (exclusively in cases of stage 3).
Fifty patients experienced infertility (70.4%), and 21 pa-
Menlo Park, CA ) without cervical dilatation.
tients (29.6%) suffered recurrent pregnancy loss. Diagnosis
The aim of this study was to evaluate the safety and
was made by hysterosalpingography and confirmed by hys-
efficacy of this new hysteroscopic adhesiolysis surgical
technique in the treatment of 40 new patients and to eval-uate the results of 71 consecutive patients with severe Ash-
Surgical technique
erman’s syndrome by observing the complete elimination ofall synechia in the uterine cavity, postoperative resumptionof menses, and pregnancy rate in a retrospective case report
Hysteroscopy was performed under general or epidural
anesthesia in the early proliferative phase of the menstrualcycle in the patients who were menstruating.
For 31 patients (43%) operated on from 1990 through
1997, a 9-mm resectoscope equipped with hysteroscopic
Materials and methods
monopolar knife (Karl Storz GmbH, Tuttlingen, Germany)was introduced into the blind reduced cavity, obtained after
From January 1990 through December 2003, 302 pa-
prudent dilatation of the cervix by Hegar’s dilators. Glycine
tients underwent hysteroscopy treatment for intrauterine ad-
was used as distending medium. Starting in 1998, we used
hesions (IUA). We reviewed all operative reports and se-
Versapoint bipolar electrode exclusively with normal saline
lected all patients with severe adhesions, with partial
solution to distend the uterine cavity (n ϭ 40 [57%]). No
agglutination of uterine wall (stage 3) or total agglutination
cervical dilatation was needed with Versapoint 5F elec-
(stage 4) and both ostial area occluded (stage 3 and 4
trode. In both methods, fluid balance was recorded in all
according to the European Society of Sev-
enty-one patients (23%) were selected according to these
Treatment was performed by making several myometrial
incisions 4-mm deep: two or three lateral incisions from the
Median age was 36.1 years Ϯ 6.1 (range 26 – 47). Mean
fundus to the isthmus on both sides and two or three trans-
parity was 0.6 Ϯ 0.9 (range 0 –3). Risk factors for cavity
versal incisions of the fundus. Procedure was stopped at that
obliteration were the following: history of at least one di-
point, even if ostial areas were not visible. A simultaneous
latation and curettage (D&C) (range 1–5) for elective abor-
laparoscopy was performed only in three patients with a
tion in the first trimester (30 patients [42.3%]); at least one
history of pelvic inflammatory disease or ectopic preg-
D&C (range 1– 4) for missed abortion or incomplete abor-
nancy, to observe the distal tubal status. In our large expe-
tion in the first trimester (18 patients [25.4%]); and D&C for
rience, ultrasound and laparoscopic control are not used to
postpartum hemorrhage (5 patients [7%]). One patient
avoid uterine perforation with hysteroscopy, due to absence
(1.4%) had curettage for molar pregnancy. Fifteen patients
of usefulness in monitoring this surgery. Prophylactic anti-
(21.1%) had myomectomy involving hysterotomy, with six
biotics amoxicillin and clavulanic acid at the dose of 2 g
of them performed in another hospital, and two patients
(SmithKline Beecham, Nanterre, France) were given rou-
(2.8%) underwent uterine embolization for fibroid uterus in
tinely at the induction of anesthesia. No intrauterine con-
absence of rational indication . The interval be-
traceptive device was inserted, because no significant ad-
tween the causal procedure and hysteroscopy treatment of
vantages has been noted when compared with hormonal
IUA unfortunately was not available.
therapy Postoperative estrogen therapy (estradiol 4
Journal of Minimally Invasive Gynecology, Vol 13, No 5, September/October 2006
ing cervical dilatation (n ϭ 4) or during the procedure (n ϭ
3). No perforation occurred during the first surgery using
Versapoint electrode. If perforation occurred, the procedure
was terminated, and patients were operated on 2 months
later without any difficulty, and no difference in subsequent
A completed elimination of all synechia was obtained
after the initial procedure by outpatient control hysteros-
copy in 31 patients (43.6%), and these patients were al-
lowed to attempt pregnancy; nevertheless in 16 of these 31patients (51.6%), filmy adhesions easily ruptured duringpostoperative hysteroscopy. In the remaining 40 patients,postoperative hysteroscopy diagnosed the persistence of
mg daily; Laboratories Cassenne, Puteaux, France) was
moderate or severe IUA and justified a second operative
given to all patients for 2 months to plan postoperative
hysteroscopy with direct synechialysis. No difference was
observed between the two surgical techniques.
The anatomic result defined by complete elimination of
Finally reconstruction of normal uterine cavity was real-
synechia with restoration of normal size and shape of the
ized after one (n ϭ 31), two (n ϭ 20), three (n ϭ 15), or four
uterus was checked in all patients by an outpatient hyster-
or more (n ϭ 5) surgical procedures despite the heteroge-
oscopy without anesthesia. Hysteroscopy, even if it misses
neous quality of endometrium mucosa.
small areas of adhesions, conversely to hysterosalpingogra-
Menstruation was restored in all patients with history of
phy visualizes the restoration of endometrium—the cavity
amenorrhea and oligomenorrhea, with the exception of two
that appears to be the main prognostic factor—and can
patients who underwent uterine artery embolization for uter-
easily rupture filmy adhesion during this procedure. Subse-
quent fertility was studied by calling all patients by tele-
Seven patients were lost to follow-up after control hys-
phone. We considered only the first pregnancy after index
teroscopy. The median follow-up time was 41 months
(range 6 – 86) for the remaining 64 patients. The results in
We evaluated the results between the two surgical tech-
accordance with surgical techniques are presented in
niques. The 2, test modified by Yates correction when
appropriate, and Fisher’s exact test were used for statistical
Twenty-eight index pregnancies were obtained in 64
evaluation, and p Ͻ.05 was considered to be statistically
patients (43.8%) with no difference between surgical tech-
significant. Where appropriate, we used means, standard
niques, and the outcomes were as follows: 3 had first tri-
deviation, and CIs for normally distributed data; and for
mester missed abortions, 4 had second trimester fetal losses,
skewed data, we used medians and ranges.
and 21 (32.8%) had live births. Three out of four secondtrimester losses occurred after resectoscope technique. Allpatients conceived spontaneously with the exception of
three who underwent a first cycle of in vitro fertilization andembryo transfer .
Seventy-one patients underwent a total of 136 hystero-
Nine (42.9%) of 21 patients with a history of pregnancy
scopic procedures. The mean operating time for the proce-
loss and 12 (24%) of 50 patients with infertility had live
dure was 25.4 Ϯ 6.2 minutes (95% CI 24.35–26.45). All
births. In patients aged 35 years or younger, 20 out of 30
patients were discharged from the hospital on the day of
conceived (66.6%) compared with 8 out of 34 (23.5%) in
surgery. Complications were noted in seven patients (5.1%)
patients aged more than 35 years (p Ͻ.05) . In 21
of 136 hysteroscopies involving perforation occurring dur-
patients with live births, there were 12 vaginal deliveries at
Obstetrical history and pregnancy outcome after synechialysis with subsequent pregnancy and live birth rate
Obstetrical history and recent obstetric outcome after synechialysis
Current pregnancy fetal loss in second trimester
term and 9 cesarean sections (CS). Three CS were per-
ine myomas who continue to have amenorrhea. Coccia et al
formed for breech presentation with fetal distress, and an-
achieved a 33.3% pregnancy at term rate by using pressure
other three CS were performed for fetal distress with ce-
lavage under ultrasound guidance in adhesiolysis. The new
phalic presentation. Caesarean sections were performed in
Versapoint technique has been used in the last few years and
two patients with previous one and two CS, respectively, for
demonstrated its efficacy in treating intrauterine patholo-
placenta accreta. The last CS was performed for chorioam-
We observed only 1 out of 40 second trimester
fetal losses with Versapoint, whereas the rate was 3 out of
Severe complications occurred in 3 (14.3%) of 21 pa-
31 after resectoscope techniques. Versapoint could prevent
tients. Two patients had hysterectomy for placenta accreta
iatrogenic cervical incompetence due to cervical dilatation
(patients with previous one and two CS, respectively) with-
realized for resectoscope techniques. This difference can be
out postoperative complications. The third patient had CS
due to absence of cervical dilatation and/or less mucosa
for Candida albicans chorioamnionitis at 30 weeks’ gesta-
tion, after preterm rupture of membrane. Hemostasis was
From the above studies, the rate of pregnancy at term
obtained by hypogastric arteries ligation with an uneventful
after synechialysis was almost the same among the various
postoperative course. The newborn required respiratory
techniques of hysteroscopic surgery . All these
support initially. The pregnancy rate was 14 (48.4%) of 31,
series can be compared because, whatever the classification
10 (50%) of 20, and 4 (20%) of 20, respectively, after one,
used in each of these series, we always considered severe
two, and three or more surgical procedures.
However, the Versapoint technique has improved safety
by avoiding the complication of fluid overload and cervical
Discussion
laceration or uterine perforation due to cervical dilatation inpatients with stenosed cervix or nullipara and we
Management of uterine synechia improved progressively
observed no perforation with this technique. Moreover, the
during the last 10 years by the widespread use of hystero-
risk of excessive fluid absorbed is theoretically possible but
scopic surgery, which helps in diagnosis of uterine synechia
the short time of the procedure, always less than 30 minutes,
and restoration of normal size and shape to the uterus, which
decreases the risk of this complication.
is essential to carry a pregnancy to term. With this largest
There are probably few indications left for laparotomy,
series published of patients with severe adhesions, we con-
even in the treatment of severe IUA. Repeated hystero-
firmed the role of age and the interest to repeat the proce-
scopic procedures as and in our series al-
dures until restoration a normal cavity are predictive factors
lowed the re-establishment of a normal cavity in all patients,
of subsequent fertility. Moreover, in 90% of pregnancies in
and 20% fertility after three or more procedures in spite of
our series occurred by natural means.
a higher risk of uterine perforation, whichever surgical tech-
Various hysteroscopic adhesiolysis techniques were de-
nique was used during the repeat procedures.
scribed and published in the last decades, either division of
Many studies fail to present their results according to the
adhesion by hysteroscopic or by using the resecto-
severity of the adhesion. Therefore different techniques are
In our study, pregnancy to term was achieved in
difficult to compare. So in our study we treated severe
32.8% patients, and normal uterine cavity and menstruation
Asherman synechia stage 3 and 4, and we obtained a 32.8%
were achieved in all patients with the exception of two
live birth rate after adhesiolysis. The live birth rate observed
patients with history of uterine artery embolization for uter-
demonstrates the difficulty of having a normal endometrium
Delivery rate after adhesiolysis using various hysteroscopic methods
Valle and 47 Resectoscope with scissors 15 (31.9)Chen et 23 Resectoscope with Laminaria (MedGyne, Lombard, IL) 8 (34.9)Capella-Allouc et 28 Monopolar knife 9 (32.1)Coccia et 3 Pressure lavage under ultrasound guidance 1 (33.3)Our series (2004)
Journal of Minimally Invasive Gynecology, Vol 13, No 5, September/October 2006
suitable for nidation even after restoration of a normal
chance of parenthood in a substantial proportion of infertile
uterine cavity in patients with stage 4 adhesions, which
couples. However, these patients with IUA undergoing ad-
corresponds to what was reported by Valle and Scierr
hesiolysis should be appropriately informed about the oc-
where the severity of adhesions affected the chance of
currence of life-threatening complications if they became
pregnant and should be managed appropriately in a tertiary
When the patient’s age was considered, we found that 20
care center. Moreover, performance of repeat procedures is
(66.6%) of 30 patients aged 35 years or younger conceived,
not indicated in patients older than 35 years.
compared with 8 (23.5%) of 34 patients older than 35 years. These results confirm that it is worthwhile repeating hys-teroscopic treatments until a normal uterine cavity is re-
References
stored, especially for young women age 35 years or less. Forwomen older than 35 years, the principal aim of the treat-
1. Eriksen J, Kaestel C. The incidence of uterine atresia after post partum
ment should be resumption of normal menses, but obstetric
curettage: a follow-up examination of 141 patients. Danish Medical
2. Rabau E, David A. Intrauterine adhesions: etiology, prevention and
Complications are common in subsequent pregnancy af-
treatment. Obstet Gynecol. 1963;22:626 – 629.
ter adhesiolysis and have been described by many authors.
3. Westendrop IC, Ankum WM, Mol BW, Vonk J. Prevalence of Ash-
Placenta accreta is the most common complication reported
erman’s syndrome after secondary removal of placental remnants or a
after IUA with an incidence of about while in our
repeat curettage for incomplete abortion. Hum Reprod. 1998;12:3347–
study we had three patients (14.3%) with placenta accrete.
4. Sweeny WJ. Intrauterine synechia. Obstetrics and Gynecology. 1966;
Two of the three had a history of one and two CS, respec-
tively, which ended with hysterectomy, while the third pa-
5. Dmowski WP, Greenblatt RB. Asherman’s syndrome and risk of
tient underwent hypogastric arteries ligation. The high rate
placenta accreta. Obstet Gynecol. 1969;34:288 –299.
of placenta accreta in our series is explained by defective
6. Capella-Allouc S, Morsad F, Rongières-Bertrand C, Taylor S, Fernan-
lamina basalis after adhesiolysis especially in severe Ash-
dez H. Hysteroscopic treatment of severe Asherman’s syndrome andsubsequent fertility. Hum Reprod. 1999;14:1230 –1233.
erman’s syndrome, which allows abnormal placentation.
7. Wamsteker K, De Block S. Diagnostic hysteroscopy: technique and
Other complications have been described by many au-
documentation. In: Sutton C, Diamond M, eds. Endoscopic Surgery for
thors. Deaton et reported a spontaneous uterine rupture
Gynecologists. London, UK: Saunders; 1993:263–276.
during pregnancy after hysteroscopic treatment of severe
8. Sanfilippo JS, Fitzgerald MR, Badawy SZ, Nussbaum ML, Yussman
Asherman’s syndrome complicated by a fundal perforation.
MA. Asherman’s syndrome: a comparison of therapeutic methods. JReprod Med. 1982;27:328 –330.
Friedman et described three severe complications in a
9. Valle RF, Sciarra JJ. Intrauterine adhesions: hysteroscopic diagnosis,
series of 33 patients with mild to severe IUA: uterine sac-
classification, treatment and reproductive outcome. Am J Obstet Gy-
culation, uterine dehiscence, and placenta accreta. These
necol. 1988;158:1459 –1470.
complications could be due to resection of the myometrium
10. Chen FP, Soong YK, Hui YL. Successful treatment of severe uterine
synechiae with transcervical resectoscopy combined with laminariatent. Hum Reprod. 1997;12:943–947.
Our finding that the pregnancy rate was 14 (48.4%) of 31
11. Coccia ME, Becattini C, Bracco GL, et al. Pressure lavage under
with one surgical procedure, 10 (50%) of 20 after two
ultrasound guidance: a new approach for outpatient treatment of in-
surgical procedures, and 4 (20%) of 20 after three or more
trauterine adhesions. Fertil Steril. 2001;75:601– 606.
surgical procedures shows that it is worthwhile to repeat
12. Zikopoulos K, Kolibianakis EM, Tournaye H, et al. Hysteroscopic
lysis of IUA until a normal uterine cavity and shape are
septum resection using the Versapoint system in subfertile women. Reproductive Biomedicine Online. 2003;7:365–367.
restored. Second trimester fetal losses occurred in four pa-
13. Marwah V, Bhandari SK. Diagnostic and interventional microhyst-
tients: one patient had a one-step procedure, and three had
eroscopy with use of the coaxial bipolar electrode system. Fertil Steril.
undergone four surgical procedures. Two of the four pa-
tients became pregnant again and had uneventful pregnan-
14. Fernandez H, Gervaise A, de Tayrac R. Operative hysteroscopy for
cies after cervical cerclage at 12 weeks’ gestation. There-
infertility using normal saline solution and a coaxial bipolar electrode:a pilot study. Hum Reprod. 2000;15:1773–1775.
fore, we think that cervical cerclage should be discussed
15. Vilos GA. Intrauterine surgery using a new co-axial bipolar electrode
with patients with multiple-stage procedures. However, the
in normal saline solution (Versapoint): a pilot study. Fertil Steril.
Versapoint technique avoids cervical dilatation, and this can
explain the low incidence of cervical incompetence espe-
16. Chapman R, Chapman K. The value of two stage laser treatment for
cially since we started in 1998, with one second trimester
severs Asherman’s syndrome. Br J Obstet Gynaecol. 1996;103:1256 –1258.
loss with this surgical technique without dilatation.
17. Protopapas A, Shushan A, Magos A. Myometrial scoring: a new
technique for the management of severe Asherman’s syndrome. FertilSteril. 1998;69:860 – 864.
18. Deaton JL, Matier D, Andreoli J. Spontaneous uterine rupture during
pregnancy after treatment of Asherman’s syndrome. Am J ObstetConclusion Gynecol. 1980;160:1053–1054.
19. Friedman S, Defazio J, Decherney A. Severe obstetric complications
Hysteroscopic adhesiolysis can be performed for severe
after aggressive treatment of Asherman syndrome. Obstet Gynecol.
adhesions with safety and efficacy, which offers a real
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