ORIGINAL ARTICLES: FERTILITY PRESERVATION

Who will benet from

uterus-sparing surgery in
adenomyosis-associated subfertility?
Yohei Kishi, M.D., Maki Yabuta, M.D., and Fumiaki Taniguchi, M.D.
Department of Obstetrics and Gynecology, Takanohara Central Hospital, Nara, Japan

Objective: To analyze the determinants of successful pregnancy following laparoscopic adenomyomectomy.

Design: Retrospective cohort study.
Setting: A general hospital.
Patient(s): A total of 102 women who had a desire for pregnancy underwent laparoscopic adenomyomectomy from 2007 to 2012.
Intervention(s): Surgical excision of the uterine adenomyosis; statistical analysis for fertility outcomes.
Main Outcome Measure(s): Pregnancy rates and the results of univariable and multivariable analyses.
Result(s): When the women were divided into %39 years and R40 years age groups, clinical pregnancy rates were 41.3% and 3.7%,
respectively. Factors associated with clinical pregnancy were: history of IVF treatments, posterior wall involvements, and age, with odds
ratios of 6.22, 0.18, and 0.77, respectively. In the younger group, 60.8% of women with history of IVF failure showed successful
pregnancy after surgery. We experienced 2 cases of placenta accreta in far advanced cases.
Conclusion(s): This study demonstrated age as a determinant in fertility outcomes. Surgery could be a benecial treatment for women who
experienced IVF treatment failures, especially at ages of %39 years. We could not show a clear benet of the surgery on fertility outcomes of
the group aged R40 years. Extremely severe adenomyosis affecting a broad range of the uterine
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Key Words: Adenomyosis, surgery, subfertility, pregnancy, complication
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terine adenomyosis is dened

by the presence of endometrial
glands and stroma surrounded
by the hypertrophic and hyperplasic
myometrium (1), and its pathogenesis
is still not explained sufciently.
Generally, adenomyosis is accepted to
result from a direct invasion of the
endometrium into the myometrium,
and is thought to be found most likely
during the fourth and fth decades of
life and after childbearing activity.
However, with the trend of delayed
childbearing, adenomyosis has come
to be diagnosed more frequently in
fertility clinics (2, 3). This is also

thought to be caused by the recent

development of diagnostic tools such
as high-resolution transvaginal sonography and magnetic resonance imaging
(MRI). With the aid of these diagnostic
tools, uterine adenomyosis is becoming
a more common disease among women
with childbearing desire and showing
more diversity (49). Recently, the
correlation between adenomyosis and
endometriosis has gradually been
revealed (49). We often encounter
uterine
adenomyosis
without
junctional zone (JZ) changes. This
atypical adenomyosis often coexists
with severe endometriosis and is

Received February 21, 2014; revised and accepted May 16, 2014; published online June 19, 2014.
Y.K. has nothing to disclose. M.Y. has nothing to disclose. F.T. has nothing to disclose.
Reprint requests: Yohei Kishi, M.D., Department of Obstetrics and Gynecology, Takanohara Central
Hospital, U-Kyo 1-3-3, Nara 631-0805, Japan (E-mail: kishi@takanohara-ch.or.jp).
Fertility and Sterility Vol. 102, No. 3, September 2014 0015-0282/$36.00
Copyright 2014 American Society for Reproductive Medicine, Published by Elsevier Inc.
http://dx.doi.org/10.1016/j.fertnstert.2014.05.028
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localized at the outer myometrium

without
aberrations
of
the
subendometrial myometrium (5, 7, 9).
Major treatment options for
women wishing to preserve their
fertility are thought to be assisted
reproductive technologies (ART) and
surgical removal of the adenomyosis.
The impact of adenomyosis on in vitro
fertilization (IVF) treatment outcomes
is controversial (1014). Two studies
showed a positive effect of prolonged
down-regulation on IVF outcomes of
women with adenomyosis (10, 11),
whereas another study reported a
negative effect of adenomyosis on the
nal outcome of IVF treatment (12
14). Regarding surgical removal of
adenomyosis,
a
recent
review
concluded that uterus-sparing surgery
for adenomyosis appears to be feasible
and satisfactory although pointing out
the need of prospective well designed
VOL. 102 NO. 3 / SEPTEMBER 2014

Fertility and Sterility

studies (15). At this stage, the true impact of various treatments on fertility outcomes of adenomyosis-associated
subfertility has not been fully claried (16).
We have applied laparoscopic excision surgery of the
adenomyosis to symptomatic uterine adenomyosis, and
among these cases roughly 72% of the women desired postoperative pregnancy. In the present study, we aimed to compile
pregnancy outcomes following uterus-sparing surgery, and
analyzed the determining factors of successful pregnancy.
Furthermore, to the best of our knowledge, there is no study
that has analyzed postoperative pregnancy outcomes in terms
of the difference in localization of uterine adenomyosis. We
also tried to incorporate this factor into the analysis of fertility
outcomes.

MATERIALS AND METHODS

We retrospectively compiled the data of 141 women who underwent uterus-sparing surgery for uterine adenomyosis from
April 2007 to December 2012 at the Department of Obstetrics
and Gynecology, Takanohara Central Hospital, Nara, Japan.
Among them, 102 had the desire for pregnancy at the time
of surgery. Surgical and patient background data were
retrieved from our surgical and patient database. Pregnancy
outcomes were collected from questionnaires or interviews
of outpatients. The median follow-up period was 24 months
(range 960 months). We dened clinical pregnancy as the
presence of a fetal heart beat at 12 weeks of gestation. All
adenomyosis was diagnosed by preoperative MRI. The criteria
used for the denition of adenomyosis on MRI were: 1) a myometrial mass with indistinct margins of primarily low
intensity with all sequences; or 2) diffuse or local widening
of the junctional zone on T2-weighted images (>12 mm)
(1719). All the adenomyosis cases were conrmed
histologically. In the analysis of determining factors for
clinical pregnancy, we used a univariable analysis and a
multivariable regression analysis. In these analyses, we used
the following variables: age at surgery, coexisting
endometriosis, coexisting ovarian endometrioma, Revised
American Fertility Society (r-AFS) scores, anterior wall
involvements, posterior wall involvements, history of IVF
treatments, weight of adenomyotic nodule, presence of JZ
change in MR imaging. There was one missing piece of data.
We couldn't follow one patient who was categorized as
R40 years old, and the patient's pregnancy outcome was
treated as not pregnant. This study was approved by the
Institutional Ethical Committee, and informed consent was
obtained from each of the patients.

Statistical Analysis
The c2 test was used for the comparison of groups regarding
categoric variables; the Fisher exact test was used in the case
of small cell counts. Parametric and nonparametric continuous
variables were compared with the use of the Student t test, and
the Mann-Whitney U test was applied when the variables did
not pass the normality test. P values of < .05 were considered
to be statistically signicant. Stepwise logistic regression
analysis was used for the analysis of the factors related to clinical pregnancy (IBM statistics software, version 16; SPSS).
VOL. 102 NO. 3 / SEPTEMBER 2014

Surgical Procedures
The patient was placed in Trendelenburg position and triple
puncture laparoscopic surgery performed. We initiated
surgery by observation of the pelvic cavity to diagnose
associated disorders. In cases having severe rectovaginal
endometriosis, causing posterior cul-de-sac obliteration,
we initiated the procedure by excision of the rectal enodometriotic nodules from the anterior rectal wall, keeping the
rectal endometriotic nodules attached to the posterior wall
of the uterus; the excised nodules are removed en bloc
with the posterior wall adenomyosis foci. After these preparations, we conrmed the boundary between the adenomyosis foci and healthy uterine myometrium to determine the
extent of resection. An incision was made to the healthy
myometrium just adjacent to the adenomyosis foci with
the use of a potassium titanyl phosphate laser. The incision
was performed step by step by making traction between the
adenomyosis foci and the healthy muscles; the difference
between the adenomyotic nodule and healthy muscles could
be distinguished by the difference in extensibility. Adenomyosis tissues are less elastic than the normal uterine
muscles because of brotic changes. However, because the
border is unclear, we made incision to the healthy uterine
muscles just adjacent to the adenomyosis foci. In this way,
we remove the adenomyosis foci en bloc as completely as
possible. After removal of the adenomyosis foci, the defected
spaces were carefully repaired with continuous stitches of
2-0 synthetic absorbable sutures to close the residual
myometrium.

RESULTS
Patients' Backgrounds and Surgical Data
Background aspects of the 102 women who had a desire for
pregnancy are summarized in Table 1. When the women
were divided into %39 and R40 years age groups, signicant
differences were found in the number of years of infertile and
percentages of women who had coexisting endometriosis.
There was no signicant difference in stages of endometriosis
or r-AFS scores. The weight of adenomyotic nodules of the
older age group was relatively heavier than that of the
younger group (not signicantly); however, blood loss and
the open conversion rate of the older group were signicantly
higher.

Pregnancy Outcomes
Pregnancy outcomes are presented in Table 2. The clinical
pregnancy rate was totally 31.4% (32/102). When the women
were divided into %39 and R40 years, clinical pregnancy
rates were 41.3% and 3.7%, respectively. In the older group,
5/6 of the pregnancies ended in miscarriages. All of the
women who succeeded in clinical pregnancy were delivered
with the use of elective cesarean section. Next, we analyzed
fertility outcomes on women who had a history of IVF failures. In the younger group, 60.8% of the women succeeded
in postoperative clinical pregnancy. In contrast, the clinical
pregnancy rate of the older group was 7.1%. Most of the
women had successful pregnancies with the use of IVF
803

ORIGINAL ARTICLE: FERTILITY PRESERVATION

TABLE 1
Background aspects and surgical data of women who desired pregnancy.
39 y (n [ 75)
Age, median (range), y
Married women, n (%)
Parity, n (%)
Preoperative miscarriage, n/n (%)
Years infertile, mean
SD
History of IVF, n (%)
Coexisting endometriosis, n (%)
Stage 1, n (%)
Stage 2, n (%)
Stage 3, n (%)
Stage 4, n (%)
r-AFS score, median (range)
Clinical symptoms, n (%)
Menorrhagia
Dysmenorrhea
Dyschezia
Dyspareunia
Chronic pelvic pain
Operation time, median, range (min)
Blood loss, median, range (g)
Nodule weight, median, range (g)
Open conversion, n (%)
Transfusion, n (%)

36 (2639)
75 (100)
7 (9.3)
27 (36.0)
2.98
1.46
23 (30.6)
54 (72.0)
9/54 (16.7)
8/54 (14.8)
12/54 (22.2)
25/54 (46.2)
40 (2120)
65 (86.7)
71 (94.7)
43 (57.3)
42 (56.0)
35 (46.7)
149 (32406)
150 (101,400)
33 (3838)
4 (5.3)
1 (1.3)

40 y (n [ 27)

P value

42 (4051)
27 (100)
0 (0)
14 (51.9)
6.58
5.78
13 (48.1)
12 (44.4)
1/12 (8.3)
1/12 (8.3)
1/12 (8.3)
9/12 (75.0)
72 (498)

.099a
.149a
.011b,c
.103a
.010a,c
.479a
.553a
.273a
.071a
.119b

24 (88.9)
26 (96.3)
14 (51.9)
18 (63.0)
18 (63.0)
146 (89341)
279 (501,300)
92 (2362)
5 (18.5)
0 (0)

.766a
.736a
.622a
.334a
.074a
.718b
.0007b,d
.068b
.038a,c
.546a

Note: r-AFS Revised American Fertility Society.

a 2
c test.
b
Mann-Whitney U test.
c
P%.05.
d
P%.01.
Kishi. Adenomyomectomy for infertile women. Fertil Steril 2014.

treatment (13/15). The maximum age of the women succeeding in clinical pregnancy was 42 years.

Statistical Analysis
The results and variables of the univariable and the multivariable analyses for clinical pregnancy are presented in
Tables 3 and 4. The variables extracted in the multivariable
regression analysis were: history of IVF treatments,
posterior wall involvements, and age at surgery, with
odds ratios of 6.22 (95% CI 1.9020.33), 0.18 (95% CI

TABLE 2
Pregnancy outcomes.

Overall pregnancy, n (%)

Miscarriage, n
Ectopic pregnancy, n
Clinical pregnancy, n (%)
Spontaneous, n
IVF, n
History of IVF treatments, n
Overall pregnancy, n (%)
Miscarriage, n
Ectopic pregnancy, n
Clinical pregnancy, n (%)
Spontaneous, n
IVF, n

39 y (n [ 75)

40 y (n [ 27)

36 (48.0)
5
0
31 (41.3)
16
15
23
16/23 (69.5)
2
0
14/23 (60.8)
2
12

6 (22.2)
5
0
1 (3.7)
0
1
14
5/14 (35.7)
4
0
1/14 (7.1)
0
1

0.090.63), and 0.77 (95% CI 0.670.88), respectively.

We found signicant differences of these variables also
in the univariable analysis. With the use of univariable
analysis, there was a signicant difference in r-AFS scores
between the groups.

Perinatal Complications
Perinatal complications are shown in Supplemental Table 1
(available online at www.fertstert.org). Uterine rupture was
not found in this series. There were two cases of placenta accreta; they underwent postpartum hysterectomies, without
severe maternal or fetal complications. Two cases of threatened preterm birth were managed by tocolytic treatment
and underwent elective cesarean sections at 35 and 36 weeks
gestational age. There were no multiple pregnancies.

TABLE 3
Multivariable analysis for clinical pregnancy (stepwise logistic
regression analysis; n [ 101).
Variable
History of IVF treatments
Posterior wall involvements
Age at surgery

Odds ratio

95% CI

P value

6.22
0.18
0.77

1.9020.33
0.090.63
0.670.88

.002
.004
.002

Note: Median observation 24 months (range 960 months).

Note: Overall model t signicance level: P< .0001. Variables used: age at surgery, coexisting
endometriosis, coexisting endometrioma, anterior wall involvement, posterior wall involvement, history of IVF treatments, nodule weight, presence of junctional zone change, Revised
American Fertility Society score.

Kishi. Adenomyomectomy for infertile women. Fertil Steril 2014.

Kishi. Adenomyomectomy for infertile women. Fertil Steril 2014.

804

VOL. 102 NO. 3 / SEPTEMBER 2014

Fertility and Sterility

TABLE 4
Univariable analysis for clinical pregnancy.
Clinical
Clinical
pregnancy D pregnancy L
(n [ 32)
(n [ 69)
P value
Age, median (range), y
Coexisting endometriosis,
n (%)
Coexisting endometrioma,
n (%)
Anterior wall involvements,
n (%)
Posterior wall involvements,
n (%)
History of IVF treatments,
n (%)
Nodule weight, median
(range), g
Presence of JZ change, n (%)
r-AFS score, median (range)

33 (2542)
22 (66.7)

38 (2251)
36 (47.8)

.0006b,d
.117a

10 (31.2)

26 (37.6)

.530a

15 (46.8)

19 (23.2)

.055a

18 (56.2)

60 (86.9)

.0015a,d

15 (46.8)

18 (26.1)

.038a

22 (3316)

44 (2838)

.0891b

9 (28.1)
24 (2120)

29 (42.0)
64 (2106)

.179a
.022b,c

Note: Abbreviations as in Table 3.

a 2
c test.
b
Mann-Whitney U test.
c
P%.05.
d
P%.01.
Kishi. Adenomyomectomy for infertile women. Fertil Steril 2014.

DISCUSSION
In this study, we analyzed a variety of factors concerning the
fertility outcomes following uterus-sparing surgery to combat
uterine adenomyosis. The total clinical pregnancy rate in our
cases was 31.4% (32/102). Live birth rates following conservative surgery for uterine adenomyosis were reported to be
32%36% (16). Our results are thought to be consistent with
these fertility outcomes. Next, we analyzed pregnancy rates
dividing the cases into two groups by the age at surgery.
When the cases were grouped into %39 year and
R40 years age groups, the clinical pregnancy rates were
41.3% and 3.7%, respectively. The clinical pregnancy rate
of the R40 years group was signicantly lower, and 5/6 of
the pregnancies ended up with miscarriages. We also showed
an adverse impact of age on clinical pregnancy with the use of
multiple regression analysis (odds ratio 0.77). Our results may
indicate that an increased woman's age is a strong risk factor
for fertility outcomes, common to that of general populations.
Generally, fertility declines after 35 years of age, and the
chance of miscarriage increases (20). The inuence of female
age on fertility has been established by earlier studies that
have demonstrated a decline in pregnancy rates with
advancing maternal age (2124). The decrease in the
number and quality of oocytes is most commonly
considered to be the cause of age-related differences in
fertility outcomes.
We now further discuss the women who experienced preoperative IVF failures. History of preoperative IVF treatments
was extracted as a factor relating to clinical pregnancy in multivariable regression analysis. When we examine the details, in
the younger group (%39 years) a total of 60.8% of women
with a history of preoperative IVF failures showed successful
postoperative pregnancy. In contrast, the older age group
(R40 years) resulted in only a 7.1% clinical pregnancy rate
VOL. 102 NO. 3 / SEPTEMBER 2014

(1/14). In earlier reports, successful pregnancy rates following

IVF-ET of women with adenomyosis were reported to be
11%35% (1014). Our study included 37 women who were
recommended to have surgical intervention because of
repeated IVF failures. For these women we performed an
adenomyomectomy, and roughly 60% of those in the younger
group succeeded in postoperative IVF treatments. This result
suggests a possible benecial effect of adenomyomectomy on
patients who experience IVF failures, especially at ages %39
years. At the same time, it should be noted that we could not
show a clear benet of the surgery on fertility outcomes for
patients R40 years old. Also in an earlier study, the live birth
rates per cycle of IVF were shown to be drop from 31% at
35 years of age to <5% at 42 years of age (25). We should
recognize the fact that surgical and IVF treatments can not
completely compensate for an age-related decline in fertility.
To the best of our knowledge, there have been no studies
that evaluated the impact of the localization of uterine
adenomyosis on fertility outcomes. In this study, we tried to
categorize the localization of adenomyosis in a two-way categorization: functional aspect and simple topologic aspect.
In the functional aspect, uterine myometrium could be
divided into subendometrial myometrium (JZ) and outer myometrium, where the former is involved in preparation of the
endometrium for implantation and uterine peristalsis: sperm
transport and hemostasis during menstruation (2631).
Based on these ndings, we categorized the present cases
into two groups according to the functional aspect: the
presence or not of JZ changes. Moreover, we added a
topologic categorization: anterior and posterior wall
involvements. As a result, only the topologic factor of
posterior wall involvement of adenomyosis was extracted as
a negative factor relating to clinical pregnancy (odds ratio
0.18). How should we interpret this result? In our previous
study, we demonstrated that extrinsic adenomyosis has a
characteristic that it is found mostly on the posterior wall,
coexisting with pelvic endometriosis (9).
Again, with the use of univariable analysis, r-AFS scores
of the unsuccessful group were signicantly higher than
those of the successful group, which means that there was a
tendency of women in the unsuccessful group to have more
severe forms of endometriosis. On the other hand, we can
interpret this result from another viewpoint. In the unsuccessful group, 19/69 (27.5%) of the women had adenomyosis at
both anterior and posterior wall; in the successful group,
only one women was affected at both anterior and posterior
wall. From these details, the severity of endometriosis and
extent of adenomyosis could be considered to be negative
factors relating to clinical pregnancy.
In addition, we would like to consider another theory
relating to this result: Posterior wall involvements may
have negatively affected the process of embryo implantation.
Up to now, there have been no studies that evaluated the
difference between uterine anterior and posterior wall as a
dominant implantation site for human embryos. The only
ndings so far were concerned about sites of human embryo
implantation are that implantation occurs dominantly around
the fundus area (32, 33). On the other hand, in mice,
implantation of the embryo is known to always take place
805

ORIGINAL ARTICLE: FERTILITY PRESERVATION

on the ventral wall of the uterus (34, 35). Gravity might be
considered to be a reason of this ventral sidedominant
implantation. We consider it to be reasonable if there was a
difference between mice as quadrupeds and humans as
bipeds on the spacing of implantation sites under the
inuences of gravity. If so, there is no hard evidence to
make clear conclusions on this result. More research is
required on this subject.
Finally, we should discuss the perinatal complications of
the surgery. We experienced two cases of placenta accreta,
and both of them resulted from extremely severe adenomyosis affecting a broad range of the uterine subendometrial
myometrium. In such cases, it is quite difcult to balance
between complete removal and preservation of the endometrium. Accordingly in the majority of the far advanced cases,
we could not avoid small perforations of the endometrium,
which may become a crucial cause of invasion of the placenta
into the outer myometrium through the defected subendometrial myometrium. Another important subject that should be
taken account in this type of surgery is uterine rupture during
pregnancy or labor. In this study, we did not experience a
uterine rupture. However, recently we experienced a case of
uterine rupture after adenomyomectomy (this case was not
in the present study period), and that case also was far
advanced. We consider that the size of adenomyosis is the
most important factor linked to uterine ruptures. In the presence of uterine adenomyosis, myocytes are widely separated
by a loose connective tissue matrix lled with less elastic
collagen brils (30). This structural change may cause a
decline in elasticity of the tissues. When the adenomyotic tissues remained dense at the excised myometrium surface, the
repaired uterine wall could be lower in tensile strength, which
may increase the risk of uterine ruptures. Especially in far
advanced cases, it is quite difcult to balance between complete removal of adenomyosis and preservation of healthy
uterine muscles: Fibrotic adenomyotic tissue can remain
grossly at the excised myometrium surface. The more complete removal of the adenomyotic nodule may ensure stronger
wound healing on defected uterine myometrium, although
there must be a limit in size of adenomyosis regarding preservation of the uterine wall. From our experience, a nodule
weight of >100 g might be relatively risky as an indication
for uterus-sparing surgery for adenomyosis-associated infertility. On the other hand, it is thought to be relatively safe in
cases of small adenomyosis that localizes the intra or outer
myometrium and keeps the JZ intact. We do not consider
that all cases have the same risk of perinatal complications.
Precise diagnosis of the localization of each adenomyosis
would provide us with useful information regarding management of the surgery and assessment of the postoperative risk.
Deliberate consideration should be given in each facility of
indications for this type of surgery.

were able to determine their desire for pregnancy at the time

of surgery, particularly those who were unmarried. We categorized those subjects into the no desire for pregnancy category, and in this study none of them became pregnant after
the operation. Also, there is one set of incomplete data
because of lost follow-up. As we mentioned, this case was
treated as did not conceive. Thus, we think we prevented
our results from becoming overestimated.
Some factors related to infertility were difcult to be precisely evaluated. Not all of the women were fully assessed for
female and male factors, and their duration of infertility was
sometimes subjective. For this reason, we used variables that
could be assessed objectively. However, we consider that our
selection policy would not distort the results of the statistical
analyses for determinants. Preferably, a well conducted randomized study is required to evaluate and analyze the true
efcacy of adenomyosis on fertility outcomes and the determining factors.

CONCLUSION
This study demonstrated the advantage of fertility outcomes
in younger women after uterus-sparing surgery for the uterine adenomyosis. This type of surgery could be a benecial
treatment for women who have experienced IVF treatment
failures, especially at ages of %39 years. Unfortunately, we
could not show a clear benet of the surgery on fertility outcomes for patients R40 years old. We experienced two cases
of placenta accreta in far advanced cases. Extensive adenomyosis with subendometrium myometrium involvement
should be treated carefully during pregnancy or labor.

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807

Perinatal complications.
Patient Age, y
1
2
3

35
31
34

37

Complications

Type of adenomyosis

Nodule
weight, g

Placenta accreta
Placenta accreta
Threatened preterm
birth
Threatened preterm
birth

Anterior and posterior wall, with JZ change

Anterior and posterior wall, with JZ change
Posterior wall, without JZ change

273
126
30

Postpartum hysterectomy
35 wk elective C/S
Postpartum hysterectomy
36 wk elective C/S
Tocolytic treatment (27 wk) 36 wk elective C/S

2,095
2,635
2,286

26

Tocolytic treatment (26 wk) 36 wk elective C/S

2,364

Posterior wall, without JZ change

Note: C/S cesarean section; JZ junctional zone.

Kishi. Adenomyomectomy for infertile women. Fertil Steril 2014.

Treatments

Delivery data

Birth
weight, g

Other
Site of placenta: fundus posterior side
Site of placenta: posterior wall

ORIGINAL ARTICLE: FERTILITY PRESERVATION

807.e1

SUPPLEMENTAL TABLE 1

VOL. 102 NO. 3 / SEPTEMBER 2014