Uterus-sparing operative treatment for adenomyosis

Transcription

ORIGINAL ARTICLE: FERTILITY PRESERVATION
Uterus-sparing operative treatment
for adenomyosis
Grigoris F. Grimbizis, M.D., Ph.D., Themistoklis Mikos, M.D., M.Sc., Ph.D., and Basil Tarlatzis, M.D., Ph.D.
1st Department of Obstetrics and Gynecology, Aristotle University of Thessaloniki, Thessaloniki, Greece
Objective: To review systematically the literature on uterus-sparing surgical treatment options for adenomyosis.
Design: Systematic literature review.
Setting: Tertiary academic center.
Patient(s): Women with histologically proven adenomyosis treated with uterus-sparing surgical techniques.
Intervention(s): Conservative uterine-sparing surgery for adenomyosis classified as (1) complete excision of adenomyosis, (2)
cytoreductive surgery or incomplete removal of the lesion, or (3) nonexcisional techniques, with studies selected if women with
adenomyosis were treated surgically without performing hysterectomy.
Main Outcome Measure(s): The cure rate after interventional strategies, the rate of symptom (dysmenorrhea and menorrhagia) control, and pregnancy rate in each group of intervention.
Result(s): A quality assessment tool was used to assess the scientific value of each study. In total, 64 studies dealing with 1,049 patients
were identified. After complete excision, the dysmenorrhea reduction, menorrhagia control, and pregnancy rate were 82.0%, 68.8%,
and 60.5%, respectively. After partial excision, the dysmenorrhea reduction, menorrhagia control, and pregnancy rate were 81.8%,
50.0%, and 46.9%, respectively.
Conclusion(s): Uterine-sparing operative treatment of adenomyosis and its variants appear to be feasible and efficacious. Welldesigned, comparative studies are urgently needed to answer the multiple questions arising
from this intriguing intervention. (Fertil SterilÒ 2013;-:-–-. Ó2013 by American Society
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Key Words: Adenomyoma, adenomyosis, cytoreductive surgery, juvenile cystic adenomyoma,
and connect to the
uterus-sparing surgery
Discuss: You can discuss this article with its authors and with other ASRM members at http://
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I
n 1860, von Rokitansky was one of
the first to describe a condition
characterized by the heterotopic
occurrence of islands of endometrium
scattered throughout the myometrium
(1, 2), specified by Frankl in 1932 as
‘‘adenomyosis interna’’ (3). Quite a
few reports since the beginning of
the previous century have outlined
the feasibility of uterine-sparing surgery in women with postoperatively
proven adenomyosis causing subfertility (2). The term ‘‘hysteroplasty’’
has been proposed to describe the
conservative operation in which
childbearing function is preserved in
young women with extensive adenomyosis (4). During the last decades,
there is an increasing trend of getting
pregnant at a later age. Adenomyosis,
a disease mostly diagnosed between
30 and 45 years of age, increasingly
complicates the fertility potential of
women in this age group (5). Minimal
access surgery techniques and organpreserving surgery is a parallel trend
that characterizes modern gynecology
(6). Thus, the need for uterus-
Received May 27, 2013; revised and accepted October 15, 2013.
G.F.G. has nothing to disclose. T.M. has nothing to disclose. B.T. received unrestricted research grants,
travel grants, and honoraria from Merck Sharp and Dohme and Merck Serono, and travel grants
and honoraria from IBSA and Ferring.
Reprint requests: Grigoris F. Grimbizis, M.D., Ph.D., Assistant Professor in Obstetrics and Gynecology,
1st Department of Obstetrics and Gynecology, Aristotle University of Tsimiski 51 Str., Thessaloniki, Thessaloniki, Greece 54623 (E-mail: [email protected]).
Fertility and Sterility® Vol. -, No. -, - 2013 0015-0282/$36.00
Copyright ©2013 American Society for Reproductive Medicine, Published by Elsevier Inc.
http://dx.doi.org/10.1016/j.fertnstert.2013.10.025
VOL. - NO. - / - 2013
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preserving surgery in women with
symptomatic adenomyosis warrants a
conservative operative management
of the disease.
Adenomyosis is defined as the
presence of endometrial tissue (glands
and stroma) within the myometrium;
heterotopic endometrial tissue foci are
associated with a variable degree of
smooth muscle cell hyperplasia. Adenomyosis can either be diffuse or
localized (focal), depending on the
extend of myometrial invasion. Moreover, adenomyotic lesions may have a
histologic spectrum from mostly solid
to mostly cystic (7).
Adenomyosis is enigmatic in
terms of etiology, diagnosis, and clinical significance. Regarding the etiology of the disease, the current trend
in thought is that adenomyosis or adenomyoma results as a down-growth
and invagination of the endometrial
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basalis into the adjacent myometrium after disruption of the
normally intact boundary between them. The incidence of
adenomyosis is increased after uterine surgery (i.e., myomectomy), cesarean delivery, postpartum endometritis, pregnancy, uterine trauma, and endometrial interventions (i.e.,
endometrial ablation, dilation and curettage, or dilation
and evacuation of products of conception). Uterine manipulations appear to be a crucial factor predisposing the invasion of endometrial cells in the myometrium (8). A
dysfunction at the endometrial-myometrial junction is speculated that might be the causative factor of adenomyosis, a
condition that could theoretically link the disease to endometriosis as well (9).
There is no consensus on the appropriate management
of symptomatic adenomyosis in women seeking fertility.
This is because [1] the causative relationship between adenomyosis and subfertility has not been fully confirmed,
and [2] the incidence of subfertility in women with adenomyosis has not been defined (10). The concept of conservative, uterine-sparing surgery for adenomyosis is increasing
as fertility preservation and quality-of-life improvement
can be achieved in this group of patients (11). Nevertheless,
conservative surgery has not become the standard treatment
for adenomyosis. This is mainly because adenomyotic tissue
invades the uterine muscle layer in a way that make the borders of the lesion unclear, so complete excision of the
affected area remains inaccurate (11). Moreover, the excision of adenomyotic tissue is always accompanied by excision of myometrium, so it is partly destructive for the
uterine wall: the advantages of removing an affected area
must be balanced against the disadvantages of leaving a
possibly defective uterine wall. Hence, there is a recognized
difficulty in establishing the state-of-the-art conservative
surgical technique for uterine-sparing management of adenomyosis, and operative options include nonstandardized
cytoreductive approaches (12). Additionally, initial experience with simple excision of adenomyotic lesions and
covering or simply closing the myometrium was reported
to be disappointing because this group of patients had quick
recurrences and soon needed hysterectomy (13). Our study is
a systematic review of the literature about uterus-sparing
surgical treatment options for adenomyosis [1] aiming to review and categorize the available proposals of surgical
uterus-sparing techniques (open or laparoscopic) for the
treatment of symptomatic adenomyosis, and [2] to assess
the effect of each type of surgical treatment on symptoms
and future fertility, according to the best available data in
the literature.
could be classified into the following clinical/histologic
variants:
1. Diffuse adenomyosis. The extensive form of the disease,
characterized by foci of endometrial mucosa (glands
and stroma) scattered throughout the uterine musculature (14).
2. Focal adenomyosis. A restricted area of hypertrophic and
distorted endometrium and myometrium, usually
embedded within the myometrium (14, 15). The
histologic characteristics of focal adenomyosis may
differ from patient to patient, from almost solid to only
cystic (adenomyotic cysts); thus, this form could be
subdivided to:
a. Adenomyoma. Any disease that infiltrates a restricted
area of the myometrium with more or less clear borders
and with mainly solid characteristics. Practically, the
term adenomyoma seems to be used for grossly circumscribed adenomyotic masses (15, 16).
b. Cystic adenomyosis. An extreme form of adenomyosis
characterized mainly by the presence of a single adenomyotic cyst within myometrium (8).
I. In women younger than 30 years old, focal cystic
adenomyosis is described as juvenile cystic adenomyosis (JCA). For this variant, Takeuchi
et al. (17) proposed the following diagnostic
criteria: age less than 30 years, cystic lesion >1
cm clearly independent of the endometrium,
and severe dysmenorrhea.
3. Polypoid adenomyomas. Circumscribed endometrial
masses composed of predominantly endometrioid glands
and a stromal component predominantly of smooth
muscle (15).
a. Typical polypoid adenomyomas. Polypoid adenomyomas without architectural or cellular atypia (15).
b. Atypical polypoid adenomyomas. A rare variant of
polypoid adenomyomas characterized by atypical
endometrial glands, often squamous metaplasia, and
a cellular smooth muscle stroma (18).
4. Other forms.
a. Adenomyomas of the endocervical type. Rare forms of
adenomyomatous polyps in the uterine cervix that
contain epithelial component of endocervical type.
These lesions are important because they must be
differentiated from adenoma malignum (19).
b. Retroperitoneal adenomyomas. Adenomyotic nodules
that are thought to arise from metaplasia of m€
ullerian
remnants beneath the peritoneum and in the area of upper rectovaginal septum (7).
MATERIALS AND METHODS
Clinical/histologic classification of adenomyosis
Classification of Uterine-Sparing Techniques
Until now, a clear classification of adenomyosis has not
existed. This is further complicated by the histologic diversity, and the differences in the extent and location of
the disease. However, categorization of the patients is
necessary to evaluate the results of surgical treatment.
Thus, taking into account the histologic characteristics
and the extent of the myometrial invasion, adenomyosis
For most cases of adenomyosis, the lesion presents with a minor or major degree of myometrial infiltration. In these cases,
removal of healthy myometrium happens inevitably during
excision of the lesion. It seems sound to stipulate that any
classification of the currently available surgical techniques
regarding the excision of adenomyosis should be based on
the extent of removal of adjacent healthy myometrium and
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Fertility and Sterility®
the preservation of the integrity (and subsequently the functionality) of the uterine wall. Accordingly, one could classify
the currently available uterine preserving surgical options for
adenomyosis as following:
1. Complete excision of adenomyosis.
a. Adenomyomectomy. Preferably used in cases of localized adenomyosis (adenomyoma) but also in selected
cases of more diffuse adenomyosis with reconstruction
of the uterine wall. This includes the complete removal
of all clinically recognizable non-microscopic lesions.
The integrity of uterine wall is maintained (20).
b. Cystectomy. Used in cases of cystic focal adenomyosis,
including the entire removal of the adenomyotic cyst
(17, 21).
2. Cytoreductive surgery/partial adenomyomectomy. Used in
cases of diffuse adenomyosis, including the partial
removal of the clinically recognizable non-microscopic lesions because complete removal of the lesion would lead to
the concomitant excision of critical amount of healthy
myometrium, which could lead to ‘‘functional’’ hysterectomy (13, 22).
3. Nonexcisional techniques. Used in interventions where
removal of adenomyotic tissue is not included (22–24).
Selection Criteria
Studies were selected if women with adenomyosis were
treated surgically without performing a hysterectomy. For
the constellation of systematic review that examines the
outcome of conservative surgical methods of treatment of adenomyosis, we included randomized trials, cohort studies,
case-control studies, case series, and case reports. Both prospective and retrospective studies were included. Studies
were excluded if the outcome was not clearly stated. NonEnglish studies, duplicate publications, and studies published
only in abstract form were excluded.
Special issues of ambiguity were the mode of final diagnosis of adenomyosis before the intervention, the control of
the disease, and the reproductive outcome. Definitive diagnosis of adenomyosis is made with a biopsy (14). Preoperative
diagnosis of adenomyosis has been performed with ultrasound and/or magnetic resonance imaging (MRI); however,
MRI seems to exhibit higher sensitivity and specificity
compared with other diagnostic modalities (25, 26). In our
review, all articles where histology was not obtained were
excluded.
The control of the disease was evaluated by the reduction
of pain, menorrhagia, or symptoms. There was no restriction
on the modality of how the outcome was reported, whether it
was in a form of a questionnaire or was clinician of patient
reported. The reproductive outcome was measured by the
number and type of conceptions in patients who wished to
become pregnant, the pregnancy outcome, and the number
of babies taken home.
the titles and abstracts from the electronic searches were
examined by two reviewers (T.M. and G.G.), and full manuscripts of all articles that met the selection criteria were
retrieved. Second, full manuscripts were examined to make
final inclusion or exclusion decisions. Any disagreement in
the inclusion/exclusion stage was resolved by arbitration
from a third reviewer (B.C.T.).
All selected articles were assessed for the following: study
design, adequate description of patient characteristics,
completeness of information in the data sets, preoperative
or intraoperative diagnosis of adenomyosis, use of validated
assessment method of symptoms, pain, and bleeding, rates
and types of intraoperative complications, rates of recurrence
of adenomyosis and need for further interventions, and postinterventional rates of conception and full-term pregnancy.
Data Extraction
Two assessors (T.M. and G.G.) independently reviewed the titles and abstracts of all identified citations. From full text articles and using a standardized data collection form, the
reviewers independently extracted data regarding the study
design, the number of patients, the characteristics of the
participants, the modality of the initial diagnosis, the primary
intervention, the duration of follow-up observation, the postoperative outcomes in terms of symptom reduction, the pain
reduction, the uterine volume reduction, and the reproductive
outcome. The reproductive outcome after the primary intervention was recorded in terms of the number wishing to
conceive, the number of natural conceptions or conceptions
after assisted reproduction techniques (ART), and the number
of terminations of pregnancies (TOP), miscarriages, ongoing
pregnancies, preterm and full-term deliveries, including the
mode of delivery.
Quality Assessment of Studies
All of the studies were evaluated and consequently ranked to
ascertain the specific power of each, based on certain criteria.
This was performed solely to assist the reader in assessing
objectively the scientific value of each study. These criteria
are reported and explained in Supplemental Table 1 (available
online). The criteria were selected and modified from already
proposed quality assessment tools (Newcastle-Ottawa Quality
Assessment Scale) for clinical studies. Each criterion could be
graded either as 0 (study not meeting the criterion) or 1 (study
meeting the criterion). Each study was then graded with a
score ranging from 0 (poorest performance, minimum total
score) to 9 (best performance, maximum total score), depending on the fulfillment of the criteria. Studies that scored 5 or
more the trials with powerful evidence in their results; they
were selected for further analysis. Studied that scored less
than 4 were trials with poor evidence; they were not included
in subsequent analysis.
Statistical Analysis
Study Selection
Studies were included in the systematic review after a twostage process (Supplemental Fig. 1, available online). First,
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Statistical analyses were performed to establish the cure rate
after interventional strategies, the rate or recurrence of symptoms, the hysterectomy rate, and the pregnancy and the
3
delivery rate in each intervention group. For analysis, the log
rates were pooled, weighting each study by the inverse of its
variance, and the summary estimates were calculated. The
statistical analysis was performed using Microsoft Excel
and MedCalc 11.4.4 (MedCalc Software).
RESULTS
Currently Available Methods of Uterine-Sparing
Surgical Treatment
Adenomyomectomy for diffuse or focal adenomyosis, cytoreductive surgery (partial adenomyomectomy), or a variety of
nonexcisional techniques has been described thoroughly in
the literature for the uterine-sparing surgical treatment of
adenomyosis. The described proposals, classified according
to the radicality of the excision of the adenomyotic tissue
are shown in Table 1.
Complete Excision of Adenomyosis/
Adenomyomectomy
Classic technique. An adenomyomectomy (open or laparoscopic) includes the same steps as myomectomy (open or
laparoscopic). This technique involves [1] recognition of the
lesion's location and borders by inspection and/or palpation,
[2] longitudinal incision of the uterine wall along the adenomyoma (Fig. 1Aa), [3] sharp and blunt dissection of the lesion
with scissors, graspers, and/or diathermy in a fashion similar
to the removal of a fibroid (Fig. 1Ab), [4] suturing of the
uterine wall in a seromuscular layer (16, 27) or in two or
more layers (4, 10) (Fig. 1Ad), and suturing of the
endometrial cavity with absorbable suture when necessary.
In cases of laparoscopic adenomyomectomy (Fig. 1Ac), the
adenomyotic mass is removed with the use of a morcellator
(16). In cases where intraoperative recognition of the
adenomyotic lesion is arduous, the use of ultrasound
guidance has been proposed, either in the form of
hydroultrasonographic monitoring or in the form of
transtrocar ultrasonography (28, 29).
Modification in wall reconstruction: U-shaped suturing. In
this laparoscopic modification, after removal of adenomyomatous tissue, the wall's cavelike wound is approximated by Ushape sutures at the muscle layer; the seromuscular layer is
closed by figure-eight sutures (30).
Modification in wall reconstruction: overlapping flaps. In
this laparoscopic modification, a transverse incision is made
in the adenomyotic tissue, and the lesion is excised with a monopolar needle. The remaining seromuscular layers are overlapped and sutured to counteract the lost muscle layer of the
uterus (Fig. 1Ba–d) (31).
Triple-flap method. This laparotomy technique involves [1]
extraperitonealization of the uterus and rubber tourniquet
placement for hemostasis; [2] bisection of the uterus in the
midline and in the sagittal plane with a scalpel until the uterine cavity is reached (Fig. 1Ca); [3] opening of the endometrial
cavity to permit the introduction of the index finger to guide
during excision of adenomyotic tissues; [4] use of Martin
TABLE 1
Classification of uterine sparing surgical techniques and of their variants.
Surgical category
Complete excision
Techniques
Adenomyomectomy
Described variant
1. Classic technique (Hyams 1952; Grimbizis et al., 2008; Wang
et al. 2009)/plus intraoperative ultrasound guidance
(Nabeshima et al. 2003; Nabeshima et al. 2008)
Modifications:
U-shaped suturing (Sun et al. 2011)
Overlapping flaps (Tacheshi et al. 2006)
2. Triple flap method (Osada et al. 2011)
Cystectomy
Classic technique
Partial excision (cytoreductive surgery)
Partial adenomyomectomy
1. Classic technique (Fujishita et al. 2004)
2. Transverse H incision (Fujishita et al. 2004)
3. Wedge resection of the uterus (Sun et al. 2011)
4. Asymmetric dissection of the uterus (Nishida et al. 2010)
Nonexcisional techniques
Combined with excisional
Uterine artery ligation together with adenomyomectomy (Kang
et al. 2009)
1. Uterine artery ligation (Wang et al. 2002)
2. Electrocoagulation of myometrium (Wood, 1998; Philips,
1996)
1. Endometrial resection (Wood, 1998; Fernandez et al. 2007;
Kumar et al. 2007; Maia et al. 2007)
2. Endometrial ablation (Preuthhupan et al. 2010)
3. Hysteroscopic cystectomy
1. High-frequency ultrasound (HIFU) (Yang et al. 2009)
2. Alcohol instillation for cystic adenomyosis (Furman et al. 2007)
3. Endometrial nonhysteroscopic ablation
Radiofrequency (Ryo et al. 2006)
Microwave (Kanaoka et al. 2004)
Balloon (Chan et al. 2001)
Nonexcisional only
Hysteroscopic
Others
Grimbizis. Uterus sparing surgery for adenomyosis. Fertil Steril 2013.
4
VOL. - NO. - / - 2013
forceps to grasp adenomyotic tissues and to excise them from
surrounding myometrium, leaving a myometrial thickness of
1 cm from serosa above and endometrium below (Fig. 1Cb);
[5] closure of the endometrium with 3–0 Vicryl (Fig. 1Cc);
and [6] closure of the flaps of the uterine wall approximating
the myometrium and serosa of the one side of the bisected
uterus in the anteroposterior plane with interrupted 2–0 Vicryl
(Fig. 1Cd), while the contralateral side of the uterine wall is
brought over the reconstructed first side in such a way as to
cover it (Fig. 1Ce) (20).
Cytoreductive Surgery/Partial
Adenomyomectomy
Classic technique: excision of diffused adenomyosis. Cytoreductive surgery for adenomyosis includes the following
steps: [1] a vertical or transverse incision is applied in the
middle of the anterior or the posterior uterine wall; [2]
Ford T clamps (or an equivalent instrument) are applied to
the wound edges so as myometrium of the subserous layer,
which is rarely affected by adenomyosis (up to 10 mm),
can be preserved; [3] the uterine wall is inspected for clinically recognizable non-microscopic adenomyotic lesions
(coarse, white trabeculations), which are excised piece by
piece with as much of the adjacent normal myometrium as
possible being preserved; [4] if adenomyosis is extended to
the contralateral wall of the uterus as well, the incision is
extended over the top of the uterus and down toward the urinary bladder of the pouch of Douglas. Closure of myometrium is performed in one or more layers and closure of the
serosa in one layer with interrupted sutures. Attention is
taken to not leave any uterine defect that could increase
the risk of hematoma (12).
Transverse H incision technique. In this laparotomy modification, mainly described for anterior uterine wall adenomyosis, ligation of the uterine cervix throughout the broad
ligament and vasoconstricting agents are used to minimize
blood loss. A vertical incision is made in the uterine wall,
and two transverse incisions are applied perpendicularly to
the initial incision along the upper and lower edges of the
uterus (H incision). A 5-mm thickness of the uterine serosa
is resected from the uterine myometrium along the vertical
incision. This resection is extended, and the uterine serosa is
widely opened bilaterally at the area under the H incision.
Then, slices of adenomyotic tissue are removed, using manual
palpation to define the borders of healthy myometrium. Chromopertubation test using indigo-carmine allows assessment
of endometrial perforation. As above, closure of myometrium
is performed in one or more layers and closure of the serosa in
one layer with interrupted sutures (12).
Wedge resection of the uterine wall. In this technique (open
or laparoscopic), the part of the seromuscular layer where
adenomyosis is located is removed by wedge resection of
the uterine wall. The operation is completed with traditional
closure of the uterine wounds as described in the classic technique of partial adenomyomectomy (30).
Asymmetric dissection of uterus. In this laparotomy technique, the uterus is dissected longitudinally with a surgical
VOL. - NO. - / - 2013
electric knife in an asymmetrical fashion to divide the inside
from the outside, preserving both the uterine cavity and
bilateral uterine arteries. From this incision, the myometrium is dissected diagonally, as if hollowing out the uterine
cavity. With a transverse incision, the uterine cavity is then
opened; the index finger is inserted into the cavity, and adenomyotic lesions are excised using a loop electrode to a
thickness of 5 mm of the inner myometrium. The procedure
continues with excision of adenomyosis to a thickness of 5
mm of the serosal myometrium. Then the endometrial cavity
is closed, and the uterine flaps are rejoined in layers (muscle
and serosa) (13).
Laparoscopically assisted vaginal excision. In this technique, the surgeon initially confirms that the uterus is free
of any adhesions. A laparoscopic bilateral uterosacral ligament removal is performed, and a posterior colpotomy
follows. Through the vaginal incision, the uterus is extracted,
and under direct manipulation the surgeon removes
adenomyotic fragments verified by touch using monopolar
cautery. The residual myometrium is closed in two layers.
The advantages of this method are comparable to open adenomyomectomy because of excising adenomyotic tissue distinguished by touch and knotting manually with adequate
tension (32).
Nonexcisional Techniques
The following groups of nonexcisional techniques have been
described in the literature for the uterine-sparing management of adenomyosis.
1. Combination of excisional and nonexcisional techniques.
Kang et al. (33) described a technique of performing laparoscopic resection of diffuse adenomyosis after laparoscopic uterine artery occlusion.
2. Laparoscopic nonexcisional techniques. These techniques
include laparoscopic electrocoagulation of the myometrium (22, 23, 34) and laparoscopic uterine artery
ligation (24).
3. Hysteroscopic nonexcisional techniques. These techniques
include operative hysteroscopy (35), rollerball endometrial
ablation (36), transcervical resection of the endometrium
(37, 38), and endomyometrial resection (22).
4. Other techniques. These techniques include ablation of
focal adenomyosis with high frequency ultrasound
(HIFU) (39), alcohol instillation under ultrasound guidance
for the treatment of cystic adenomyosis (40), radiofrequency ablation of focal adenomyosis (41), microwave
endometrial ablation (42), and balloon thermoablation
(43) for diffuse adenomyosis.
Synopsis of the Literature that Deals with UterineSparing Treatment of Adenomyosis
In total, 64 studies dealing with 1,049 patients treated with
uterine-sparing surgical methods for adenomyosis were
analyzed. Complete excision of adenomyosis was described
in 20 studies (488 patients) (Supplemental Table 2); of these,
9 studies (469 patients) scored R5 during quality assessment (4, 10, 11, 16, 20, 30, 31, 44–56) (Table 2). Partial
5
FIGURE 1
excision of adenomyosis was described in 11 studies (128
patients) (Supplemental Table 3); of these, 3 studies (83
patients) scored R5 during quality assessment (10, 12, 13,
22, 30, 32, 57–61). Complete excision of cystic
adenomyomas was described in 22 studies (38 patients)
(see Supplemental Table 4); of these, 2 studies (13
6
patients) scored R5 during quality assessment (8, 17, 21,
28, 29, 62–77)(Table 2). Nonexcisional methods for
adenomyosis were applied in 15 studies (395 patients) (see
Supplemental Table 5); of these, 4 studies (342 patients)
scored R5 during quality assessment (22–24, 33, 35–43,
78)(Table 2).
VOL. - NO. - / - 2013
FIGURE 1 Continued
(A) Complete adenomyomectomy classic technique: (a) Longitudinal incision along the adenomyoma. (b) Sharp and blunt dissection with scissors,
graspers and/or diathermy. (c) Suturing of the endometrial cavity. (d) Suturing of the uterine wall. (B) Complete adenomyomectomy classic
technique with overlapping flaps: (a) Transverse incision. (b) The lesion is excised with monopolar needle. (c, d) The remaining seromuscular
layers are overlapped and sutured to counteract the lost muscle layer of the uterus. (C) Complete adenomyomectomy with triple flap
technique: (a) Bisection of the uterus in the midline and in the sagittal plane. (b) Opening of the endometrial cavity and excision of
adenomyotic tissues leaving a myometrial thickness of 1 cm. (c) Closure of the endometrium. (d) Closure of the flaps approximating the
myometrium and serosa of the one side of the bisected uterus in the anteroposterior plane. (e) The contralateral side of the uterine wall is
brought over the reconstructed first side in such a way as to cover it.
Results after complete excision of adenomyosis/adenomyomectomy. In 9 studies, 469 patients were treated with
complete excision of adenomyosis/adenomyomectomy
(Supplemental Table 2, available online). Overall, the mean
patient age was 37.5 years old (1.5 years), and the mean
VOL. - NO. - / - 2013
follow-up period was 25.1 months (7.0 months). The mean
reduction of pain was 82.0% (5.4%), and the mean reduction of bleeding was 68.8% (14.8%) (see Table 3). After
excluding the studies where fertility preservation was not
the primary outcome, 147 out of 341 patients wishing to
7
Uterus sparing surgical treatment of adenomyosis: quality assessment of the relevant studies.
Author, year
Complete
adenomyomectomy
Dai et al. 2012
Study
design
No. of
patients
Modality of initial
diagnosis/definition of extent of
the disease
Pro
1
38
1
U/S
Osada et al. 2011
Pro
1
104
1
U/S, MRI
Wang et al. 2009
Pro
1
165
1
U/S
Takeuchi et al. 2006
Pro
1
14
0
MRI
Al Jama et al. 2011
Retro
0
18
0
U/S, MRI
Focal
adenomyosis
(adenomyoma)
Diffuse/focal
adenomyosis
Representativeness
of the cases
Ascertainment of exposure/detailed
surgical technique
1
Consecutive
1
Surgical
records
1
Consecutive
1
Surgical
records
1
Consecutive
1
Surgical
records
1
Consecutive
1
Surgical
records
Focal adenomyosis
(adenomyoma)
1
Consecutive
1
Surgical
records
Focal
adenomyosis
(adenomyoma)
Focal
adenomyosis
(adenomyoma)
Koo et al. 2011
Retro
0
18
0
U/S
Focal adenomyosis
(adenomyoma)
1
Consecutive
1
Surgical
records
Sun et al. 2011
Retro
0
40
0
NA
Focal adenomyosis
(adenomyoma)
0
Consecutive
1
Surgical
records
Grimbizis et al. 2008
Retro
0
6
0
U/S
Focal adenomyosis
(adenomyoma)
1
Consecutive
1
Surgical
records
Fedele et al. 1993
Retro
0
18
1
Histology
Focal
adenomyosis
(adenomyoma)
0
Consecutive
1
Surgical
records
Focal
adenomyosis
(adenomyoma)
Diffuse adenomyosis
0
1
Consecutive
1
Surgical
records
Partial excision of
adenomyosis/partial
adenomyomectomy
Sun et al. 2011
Retro
0
13
0
NA
Consecutive
1
Surgical
records
VOL. - NO. - / - 2013
Nishida et al. 2010
Retro
0
44
1
MRI
Wang et al. 2009
Retro
0
28
1
U/S
Diffuse
adenomyosis
1
Consecutive
1
Surgical
records
Fujishita et al. 2004
Retro
0
11
0
U/S, MRI
Diffuse
adenomyosis
1
Consecutive
1
Surgical
records
Diffuse/focal
adenomyosis
0
Wood, 1998
Retro
0
25
1
NA
NA
0
Surgical
records
Open
excision/classic
technique
Open
excision/triple
flap technique
Open or lap
excision/classic
technique
Lap
excision/uterine
wall reconstruction
with overlapping
flaps
Open or lap
excision/classic
technique
Open or lap
excision/classic
technique
Open or lap
complete
excision/classic
technique with
additional U-shape
suturing
Lap
excision/classic
technique
Open
excision/classic
technique
Lap partial
excision/classic
reconstruction
Open
excisiona/asymmetric
dissection of uterus
Open
excisiona/classic
technique
Open partial
excision/modified
H incision
Lap
excisiona/classic
technique
Follow
up/adequate
length
Outcome
evaluation
Adequacy
of follow-up
of cohorts
Statistical
analysis
Total
grade
1
Structured
questionnaire
1
24/12
1
Yes
1
Yes
1
9
1
Structured
questionnaire
1
24/12
1
Yes
1
Yes
1
9
1
Structured
questionnaire
1
24/12
1
Yes
1
Yes
1
9
1
Structured
questionnaire
1
NA
0
No
0
Yes
1
6
1
Self
0
36/12
1
Yes
1
Yes
1
6
report
1
Structured
questionnaire
1
9/12
0
Yes
1
Yes
1
6
1
Self
0
27/12
1
Yes
1
Yes
1
5
report
1
Structured
questionnaire
1
13/12
0
Yes
1
No
0
5
1
Self
0
53/12
1
Yes
1
No
0
4
0
20/12
0
Yes
1
Yes
1
4
report
1
Self
report
1
Structured
questionnaire
1
12/12
0
Yes
1
No
0
6
1
Structured
questionnaire
1
36/12
1
Yes
1
Yes
1
8
1
Self
0
36/12
1
Yes
1
Yes
1
6
0
24/12
1
Yes
1
No
0
4
report
1
Self
report
8
TABLE 2
VOL. - NO. - / - 2013
TABLE 2
Continued.
Author, year
Study
design
No. of
patients
Modality of initial
diagnosis/definition of extent of
the disease
Representativeness
of the cases
surgical technique
Follow
up/adequate
length
Outcome
evaluation
Adequacy
of follow-up
of cohorts
Statistical
analysis
Total
grade
Cystic
adenomyomas and
juvenile cystic
adenomyomas
Takeuchi
et al. 2010
Kriplani
et al. 2011
Nonexcisional
techniques
Kang et al. 2009
Retro
Retro
1
0
9
4
0
0
U/S, MRI
U/S, MRI
JCA
JCA
1
1
Consecutive
Consecutive
1
1
Surgical
records
Lap
Surgical
records
Lap
Laparoscopic
partial resection
of adenomyosis
þ UAO
Laparoscopic
uterine artery
ligation
Myometrial
electrocoagulation
Laparoscopic
bipolar
coagulation
Rollerball
endometrial
ablation
TCRE Mirena
Retro
0
37
1
U/S
Diffuse/focal
adenomyosis
1
Consecutive
1
Surgical
records
Wang et al. 2002
Pro
1
20
0
U/S, MRI
0
Consecutive
1
Surgical
records
Wood, 1998
Retro
0
11
0
NA
0
NA
0
Philips et al. 1996
Pro
1
10
0
MRI
0
NA
0
Surgical
records
Surgical
records
Preutthupan
et al. 2010
Retro
0
190
1
U/S
Unclear
description
of lesion
Diffuse/focal
adenomyosis
Unclear
description
of lesion
Diffuse/focal
adenomyosis
1
Consecutive
1
Surgical
records
Maia et al. 2003
Retro
0
95
1
U/S
0
Consecutive
1
Surgical
records
Wood, 1998
Retro
0
18
0
NA
0
NA
0
Surgical
records
Unclear
description
of lesion
Diffuse/focal
adenomyosis
1
Structured
questionnaire
1
35/12
1
Yes
1
Yes
1
8
1
Structured
questionnaire
1
18/12
0
Yes
1
No
0
5
1
Structured
questionnaire
1
12/12
0
Yes
1
Yes
1
7
1
Structured
questionnaire
1
8/12
0
Yes
1
Yes
1
6
1
Self report
0
24/12
1
Yes
1
No
0
3
1
Self report
0
25/12
1
Yes
1
No
0
4
1
Self report
0
60/12
1
Yes
1
Yes
1
7
1
Self report
0
12/12
0
Yes
1
Yes
1
5
1
Self report
0
24/12
1
Yes
1
No
0
3
excision/classic
technique
excision/classic
technique
Endomyometrial
resection
Note: HIFU ¼ high-intensity focal ultrasound; HSG ¼ hysterosalpingogram; Lap ¼ Laparoscopic; MEA ¼ microwave endometrial ablation; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective, Retro ¼ retrospective; TCRE ¼ transcervical endometrial resection, UAO ¼ uterine artery occlusion; U/S ¼ ultrasound.
a
Unclear description of the radicality of adenomyotic tissue excision.
9
Postoperative results, pregnancy rates, and pregnancy outcomes after uterus-sparing surgery for adenomyosis.
Author, year
Reduction
No. of of symptoms
patients
(%)
Complete adenomyomectomy
Dai et al. 2012
38
Osada et al. 2011
104
Wang PH
et al. 2009
Surgical group
Reduction
of pain (%)
Reduction of
bleeding (%)
Patients wishing
to conceive
(n, %)
Natural
Conceptions
(n, %)
Conceptions
after ART
(n, %)
Total
Conceptions
(n, %)
Miscarriages
(n, %)
Ongoing
pregnancy
(n, %)
Preterm
(n, %)
Full-term
(n, %)
Total
deliveries
(n, %)
NA
NA
>80%
VAS: 10–1.6
>80%
VAS: 10–2.8
—
26
—
4
—
12
—
16
—
2
—
—
—
—
—
14
—
14
Recurrence 7
No uterine
rupture
VNRS-6:
3.8–1.1
VNRS: 6:
3.9–0.7
NA
Adenomyoma
relapse 49.0%
Adenomyoma
relapse 28.1%
VD 1
51
NA
Surgicalmedical
Takeuchi et al.
2006
Al Jama et al.
2011
Koo et al. 2011
114
NA
14
NA
18
NA
18
NA
Sun et al. 2011
40
NA
Grimbizis et al.
6
2008
Subtotal
(Symptoms)
Subtotal
341
(Fertility
outcome)
Partial adenomyomectomy
Nishida
44
et al. 2010
Cure
—
Scale: 3.08–1.2
27
20 (74.1%)
—
20
3 (11.1%)
—
2 (7.4%)
15 (55.6%)
17
Scale: 3.68–0.9
44
35 (79.5%)
—
35
3 (6.8%)
—
5 (11.4%)
27 (61.4%)
32
VAS: 10–2.5
8
2
—
2
—
1
—
1
2
NA
NA
18
8
—
8
2
—
—
6
6
NRS: 8.1–1.3
MVJ: 4.3–3.2
—
—
—
—
—
—
—
—
—
40%
24
8
5
—
—
3
3
Cure
—
—
—
—
—
—
—
91.2%
Cure
82.00
VAS: 9.4–0.8
NA
VNRS-6:
4.9–1.8
NA
Wang PH
et al. 2009
Fujishita
et al. 2004
(modified)
28
6
55%
Fujishita
et al. 2004
(classic)
5
18%
VOL. - NO. - / - 2013
Subtotal
56.11
(symptoms)
Subtotal
34
(fertility
outcome)
Complete adenomyomectomy (JCA)
Takeuchi
9
NA
et al. 2010
Kriplani
4
Cure
et al. 2011
NA
81.78
Improve
—
NA
28
NA
4
NA
—
—
72/147
(48.98)
—
17/147
(11.56)
89/147
(60.54)
—
—
—
13
2
—
2
—
—
—
13 (46.4%)
15/89
(16.85)
—
1/89
(1.13)
7/89
(7.87)
66/89
(74.16)
—
—
—
—
—
1
—
1
2
—
—
—
—
—
4 (14.3%)
—
74/89
(83.15)
9 (32.1%)
—
9
Report of 2
incidental
pregnancies;
recurrence 3
GnRH-a 6/12
C/S 1,
Recurrence 1;
endometrium
perforation 1
Recurrence 4;
endometrium
perforation 2
50.00
32/34
(94.12)
Pain score:
10–2
Pain score:
9.75–0.25
—
5/11 (45.5%)
C/S 6/18;
TAH 3
GnRH therapy;
uterine scar
dehiscence
U/S relapse
rate 15.0%
None
68.79
147/341
(43.11)
NA
3/13 (23.1%)
Comment
15/32
(46.88)
0/32
(0.00)
15/32
(46.88)
4/15
(26.67)
1/15
(6.67)
0/15
(0.00)
10/15
(66.67)
11/15
(73.33)
NA
3
3
—
3
—
—
—
3
3
NA
—
—
—
—
—
—
—
—
—
V/D 2; C/S 1
None
10
TABLE 3
VOL. - NO. - / - 2013
TABLE 3
Continued.
Author, year
Reduction
No. of of symptoms
patients
(%)
Subtotal
(symptoms)
Nonexcisional techniques
Kang
37
et al. 2009
86.13
Reduction
of pain (%)
84.62
NA
Median
Pain score
8/11–4/11
Pain score
2.4–1.1
(53% red)
Patients wishing
to conceive
(n, %)
Natural
Conceptions
(n, %)
Conceptions
after ART
(n, %)
Total
Conceptions
(n, %)
Miscarriages
(n, %)
Ongoing
pregnancy
(n, %)
Preterm
(n, %)
Full-term
(n, %)
Total
deliveries
(n, %)
Median
PBAC:
158–59
—
—
—
—
—
—
—
—
—
PBAC:
516–263
(49% red)
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
Reduction of
bleeding (%)
—
Wang
et al. 2002
20
NA
Preutthupan
et al. 2010
190
NA
NA
Maia
et al. 2003
(Mirena)
53
NA
NA
20%
—
—
—
—
—
—
—
—
—
Maia, 2003
(no Mirena)
Subtotal
(symptoms)
Total (fertility
outcome)
42
NA
NA
90%
—
—
—
—
—
—
—
—
—
—
54.62
384
Comment
Reduced/healed:
165 (86.8%)
Hysterectomy 2;
reduction of
volume (%):
224.6–91.6
(59.2)
Hysterectomy 3;
45%
dissatisfied;
reduction of
volume (%):
268–217
(12%)
Hysterectomy 3;
GnRH
pretreatment
Repeat
TCRE 4;
hysterectomy
4
None
73.68
182/384
(47.39)
90/182
(49.45)
17/182
(9.34)
107/182
19/107
(58.79)
(17.76)
2/107
(1.87)
7/107
(6.54)
79/107
(73.83)
88/107
(82.24)
Note: C/S ¼ cesarean section; MVJ ¼ Mansfield-Voda-Jorgensen menstrual bleeding scale; NA ¼ not applicable; NRS ¼ numerical rating scale; PBAC ¼ pictorial blood loss assessment chart; TAH ¼ total abdominal hysterectomy; TCRE ¼ transcervical endometrial resection;
U/S¼ ultrasound; VAS ¼ Visual Analogue Score; VD ¼ vaginal delivery; VNRS ¼ verbal numeric rating scale.
11
conceive (43.1%) were found; these patients achieved 89 conceptions (pregnancy rate: 60.5%) and delivered 74 babies
(delivery rate: 83.1%) (see Table 3).
Results after partial excision of adenomyosis/cytoreductive
surgery. In 3 studies, 83 patients underwent open or laparoscopic partial excision of adenomyosis/adenomyomas
(Supplemental Table 3, available online). All were retrospective cohort studies; the mean age of patients was 35.4 years
(1.9 years), and the mean follow-up period was 24.1 months
(13.3 months). In this group of patients, the mean reduction
of pain was 81.8% (0.0), and the mean reduction of bleeding
was 50.0% (0.0) (see Table 3). After excluding the studies
where fertility preservation was not the primary outcome,
there were 32 out of 34 patients wishing to conceive
(94.1%), who achieved 15 conceptions (46.9%) and gave birth
to 11 babies (73.3%) (see Table 3).
Results after complete excision of cystic adenomyomas
(including juvenile cystic adenomyomas). In 2 studies [13
patients, mean age 23.1 (3.2) years, follow-up period 29.8
(8.2) months], there was a reported 86.1% (9.6%) reduction of symptoms and 84.6% (7.2%) reduction of pain after
excision of cystic adenomyomas (see Table 3; Supplemental
Table 4, available online). Out of three patients wishing to
conceive, there were three conceptions and three deliveries
(see Table 3).
Results after nonexcisional techniques. In 4 studies [342
patients, mean age 42.03 (1.65) years, follow-up period
38.43 (24.17) months], there was a reported 54.6%
(1.2%) reduction of pain and 73.7% (23.6%) reduction of
bleeding (see Table 3; Supplemental Table 5, available online).
Out of 9 patients wishing to conceive, there were 5 (55.6%)
conceptions and 1 delivery (50.0%).
DISCUSSION
Uterine-sparing treatment of adenomyosis appears to be
feasible and efficacious. The reduction of dysmenorrhea after
conservative surgery ranges from 54.6% (nonexcisional
techniques) to 84.6% (complete adenomyomectomy). The
reduction of menorrhagia ranges from 50.00% (partial adenomyomectomy) to 68.8% or even 73.68% (nonexcisional techniques). The pregnancy rate ranges from 46.9% (partial
adenomyomectomy) to 60.5% (complete adenomyomectomy).
Comments on Quality of Data
The main problem of an attempt to systematically review
these procedures is that there are few good quality studies.
In an effort to qualify the data of each study, a 9-item quality
assessment tool was created. This tool was based on the
Newcastle-Ottawa Quality Assessment scale. Based on this
tool, data from only 17 out of the 64 studies were used to
calculate the results after uterus-sparing surgery for adenomyosis, in terms of dysmenorrhea reduction, menorrhagia
reduction, and pregnancy outcome. In fact, a small number
of prospective studies deal with the conservative surgical
treatment of adenomyosis, and there has been no uniform
design and/or outcome, so the feasibility of pooling the results
may be suboptimal. Overall, the quality of the results may be
12
inferior, especially regarding therapies such as partial excision of adenomyosis (no prospective studies identified, small
number of patients), the complete excision of cystic adenomyomas (one prospective study, but the total number of
patients was very small for eliciting secure results), and the
nonexcisional techniques (three prospective studies, but the
treatments were totally different, so the results cannot be
combined).
On the other hand, for the treatment of adenomyosis
with complete excision of the lesion, we found four prospective studies and a total of 8 studies scoring R5 after
applying the assessment tool. In this subgroup, the investigators reported the use of surgical techniques based on the
same operative principles, so a total of 469 treated patients
accumulated, which offered good quality data for further
analysis. In this subgroup of patients, both treatment and
fertility rates appear to be increased (dysmenorrhea control:
82.0%; menorrhagia control: 68.8%; pregnancy rate:
60.5%).
Comments on the Control of Symptoms
In terms of dysmenorrhoea control, the main contemporary
techniques applied for the uterine-sparing techniques for the
treatment of adenomyosis appear to yield comparable clinical results. After complete excision of adenomyosis, partial
excision of adenomyosis, and complete excision of cystic
adenomyomas, the reduction of dysmenorrhoea was found
to be 82.0%, 81.8%, and 84.6%, respectively (P ¼ not statistically significant). It seems that the excision of the bulk of
adenomyosis controls the pain even if some amount of residual lesion has been left, as happens in cases of cytoreductive
surgery. However, all the series included are studies where
specially designed cytoreductive techniques were applied,
such as the triple flap Osada technique (20), and these results
could not be generalized across all the techniques used for
the conservative surgery (such as the ‘‘wedge’’ resection
technique, represented in this review by only a few case
reports).
In terms of menorrhagia control, the results differed after
partial excision of adenomyosis (50.00% reduction) and complete excision of adenomyosis (68.79% reduction). With nonexcisional techniques, the control of menorrhagia appears to
be better compared with the partial excision techniques, and
to be comparable to that of the complete excision techniques
(73.7%). Nonexcisional techniques is an heterogeneous group
of operations including many cases of hysteroscopic ablation.
In these cases, the control of bleeding is achieved through the
destruction/excision of endometrium, resulting in loss of the
fertility of the patient; in addition, in the group of nonexcisional techniques, control of symptoms is achieved indirectly
and without treatment of the primary disease. Furthermore, it
seems that, especially after partial excision of adenomyosis,
the residual lesion adjacent to the endometrium continues
to cause bleeding symptoms. This is an implication for clinical
practice: in cases of diffuse adenomyosis with menorrhagia,
cytoreductive partial excision of the lesion is less effective
compared with complete excision techniques or nonexcisional techniques where fertility may be lost.
VOL. - NO. - / - 2013
Comments on Fertility after Treatment
Complications
Overall, there was a restriction in the design of the studies
included in this review regarding the fertility potential after
uterine-sparing surgery for adenomyosis. Most of the studies
were not primarily designed to address this issue, as the study
populations were mainly women with adenomyosis but not
necessarily and subfertility. On the other hand, uterussparing surgery for adenomyosis involves techniques that
modify the anatomy of the uterus (i.e., pelvic adhesions, uterine deformities, intrauterine adhesions, or reduced uterine
capacity). These deformities may contribute to a declined
postoperative pregnancy rate (13). Nevertheless, not only
was fertility finally preserved, but any subfertility related to
adenomyosis appears largely to be treated after cytoreductive
surgery, considering that the crude delivery rate appears to be
higher than 70%. In view of the fact that pregnancy rates after
surgical treatment of fibroids appear to be 50%, the postoperative fertility outcome after excision of adenomyosis should
be considered satisfactory (79). Nevertheless, although the
existing evidence for the burden on clinical pregnancy and
delivery rate caused by intramural fibroids is based on
comparative studies (the common odds ratio [95% confidence
interval] is 0.8 [0.6–0.9] and 0.7 [0.5–0.8], respectively),
research of similar design (prospective, controlled) for the
burden on fertility caused by adenomyosis is lacking (79).
According to the findings of this review, the conception
rates do not appear to be statistically significantly different
between partial excision of adenomyosis (46.8%) and complete excision of adenomyosis (60.5%) (P¼ .22). These results
are in agreement with analogous research published in the
literature about the role of treatment of adenomyosis in subfertility (80). Similar results have been accumulated about the
delivery rate after partial (73.3%) and complete (83.1%) excision of adenomyosis (P¼ .58), and the miscarriage rate after
partial (26.7%) and complete (16.9%) excision of adenomyosis (P¼ .58). No comment upon the achievement of pregnancy
after nonexcisional techniques can be made because of the
lack of reliable data. It appears that there is a trend for
increased fertility after surgery for adenomyosis in the complete excision group, but more data are needed to elicit safe
results for clinical practice.
Adenomyosis and uterine rupture. A spontaneous uterine
rupture during pregnancy in gravid uteri complicated by
adenomyosis has been recorded in isolated case reports,
even with no prior cytoreductive surgery (2). Furthermore,
there is a recognized risk of uterine rupture during pregnancy
or labor after conservative surgery for adenomyosis (32).
However, the risk of rupture accompanies all types of uterine
surgery: the incidence of symptomatic uterine rupture during
vaginal birth after cesarean delivery (VBAC) or laparoscopic
myomectomy is reported to be 0.27% and 1.0%, respectively
(27, 81). After adenomyomectomy, it is speculated that
subsequent uterine scars may conceal dense residual
adenomyotic foci, and as a consequence the tensile strength
of the uterus may decline leading to possible rupture of
pregnant uterus (82). Wang et al. (48) described this risk as
being as high as one out of eight women experiencing
uterine rupture in pregnancy/labor after cytoreductive
surgery for adenomyosis. Moreover, there are some studies
where alternative operative procedures are proposed for the
adequate healing of uterine wound after this type of
intervention to prevent major complications such as uterine
rupture during labor (11).
Pregnancy Issues
Intervention to conception time. In most of the studies that
dealt with pregnancy after surgery for adenomyosis, attempts
for conception were permitted at least 3 months after the
intervention (13, 62).
Implication to ART methods. It has been reported that ART
methods show increased pregnancy rates compared with natural cycles after an operative intervention for adenomyosis
(30). Moreover, a single-embryo transfer policy ensures less
risk of uterine rupture, because a twin pregnancy generates
uterine activity at an earlier gestational age, which may
lead to this devastating event (32). Although the data dealing
with this issue are still scarce, our results do not support the
use of a particular technique to increase the conception rates
after ART methods in women with adenomyosis.
VOL. - NO. - / - 2013
Adenomyosis and delivery. Although most of the reported
deliveries have been completed by cesarean delivery, there
have been a few reports vaginal deliveries being allowed. Sporadic reports have outlined the risk of severe atonic postpartum hemorrhage in women with known adenomyosis,
which can necessitate a peripartum hysterectomy (2). Because
of the absence of data and experience, an elective caesarian
delivery after adenomyomectomy seem preferable for patient
safety, especially in nonorganized centers.
General Comments
Conservative surgical intervention: first-line approach for
adenomyosis. This study shows that conservative surgical
intervention is quite likely to improve symptoms from diffuse
adenomyosis, and in cases of focal adenomyosis there is a
good possibility of permanent treatment. So it is sound to
select the appropriate treatment for the right patient: in cases
of focal adenomyosis, laparoscopic excision appears to be the
first-line approach; in women with diffuse adenomyosis who
are interested in a future pregnancy, aggressive excision of
the lesion with secure restoration of the uterine wall thickness
might offer the best results.
It is of outmost important to preoperatively [1] ensure the
definite diagnosis of adenomyosis, and [2] assess the location
and the size of each adenomyotic focus. Magnetic resonance
imaging assists in the achievement of both of these preoperative goals and helps the surgeon to remove completely each
focus of adenomyosis (26, 51).
Preoperative and postoperative use of GnRH agonist therapy. The role of combination approach to adenomyosis with
cytoreductive surgery and administering a gonadotropinreleasing hormone (GnRH) agonist in the management of
patients wishing to preserve their uterus is not clear. It is
hypothesized have a synergistic effect because during
13
cytoreductive surgery the affected tissues with relatively poor
blood supply are removed and the response of the remaining
adenomyosis to hormone treatment is therefore enhanced
(83). The advantages of preoperative use of GnRH-agonist
therapy include the reduction of uterine vascularity, the
correction of anemia, and the reduction of operative bleeding
(facilitates laparoscopy rather than laparotomy) (12).
The disadvantages of preoperative use of GnRH-agonist
therapy are that normal size uteri recognizing adenomyotic tissues after GnRH treatment is difficult, assessing the demarcation between adenomyosis and normal myometrium is
difficult, the risk of endometrial perforation is increased, and
removing a large amount of adenomyotic lesions becomes
difficult (an adverse effect of GnRH-agonist therapy) (12).
Laparotomy or Laparoscopy
4.
5.
6.
7.
8.
9.
10.
11.
12.
Traditionally, laparotomy has been used for the surgical treatment of adenomyosis because of the extension of the disease
within the myometrium and the difficulty in suturing the
remaining uterine wedges after the excision. The main advantage of laparotomy remains the ability of the surgeon to
palpate and recognize the adenomyotic lesions intraoperatively. However, when the adenomyotic lesion can be clearly
outlined via MRI, laparoscopy is feasible either for ablation of
the adenomyotic foci or for excision of adenomyomas,
whereas laparoscopic suturing presents no more difficulty
compared with suturing after myomectomy (16, 51).
16.
Which Technique is Better?
17.
There is no strong evidence to indicate a technique that
secures the best clinical and reproductive performance. Each
investigator describes the theoretical advantages of his or
her technique, but in practice the results show no statistically
significant clinical differences. Mainly, most of the modifications aim [1] to maximize the amount of adenomyosis excised
during surgery by offering an increased area where surgical
manipulations can be performed, and [2] to empower the uterine wall integrity so that a future pregnancy can be sustained
without uterine rupture.
CONCLUSION
Uterine-sparing operative treatment of adenomyosis and its
variants appears to be feasible and efficacious. Control of
symptoms is achieved in more than 81% (dysmenorrhea control) and 50% (menorrhagia control) of the patients, and the
pregnancy rates appear to be higher than 46%. Nevertheless,
data supporting this type of intervention are still suboptimal,
and prospective, well-designed, comparative studies are
urgently needed to answer multiple questions arising from
this intriguing intervention.
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VOL. - NO. - / - 2013
SUPPLEMENTAL FIGURE 1
Flow diagram of search strategy.
VOL. - NO. - / - 2013
16.e1
SUPPLEMENTAL TABLE 1
Criteria for evaluation of the studies included in the review.
Selection
1. Type of study design
2. No. of patients
3. Is the definition of the extent of the adenomyosis
adequate?
Is the definition of the type of adenomyosis
adequate?
4. Representativeness of the cases
Exposure
5. Ascertainment of surgical technique
Is there a detailed description of the surgical
technique?
Outcome
6. Outcome evaluation
7. Was follow-up long enough for outcomes to
occur?
8. Adequacy of follow-up of cohorts
9. Statistical analysis
Maximum grading
Criteria for study evaluation
Grading
Prospective
Retrospective
>25
<25
Clinical/not reported
MRI or U/S and clinical
Yes
No
Consecutive or obviously representative series of cases
Potential for selection biases or not stated
1
0
1
0
1
0
1
0
1
0
Secure record (e.g., surgical records)
Written self report of medical record only
No description
Yes
No
1
0
0
1
0
Structured questionnaire
1
Self report/No description
>24 months
<24 months
Complete follow-up/all subjects accounted for
Subjects lost to follow-up unlikely to introduce bias,
small number lost
Inadequate follow-up rate
No statement
Existence of statistical analysis
Absence of statistical analysis
0
1
0
1
1
0
0
1
0
9/9
Note: Studies accumulating a score R5 were considered as trials with powerful evidence of their results, but those with a score <5 were considered as poor. MRI ¼ magnetic resonance imaging; U/S
¼ ultrasound.
16.e2
VOL. - NO. - / - 2013
VOL. - NO. - / - 2013
Complete adenomyomectomy: quality assessment of the relevant studies.
Author, year
Study No. of
design patients
Prospective
studies
Dai
Pro
2012/EJOGRB
1
Focal
1 Consecutive
adenomyosis
(adenomyoma)
1 104 1 U/S, MRI Diffuse/focal
1 Consecutive
adenomyosis
Pro
Wang PH
2009/FS
Pro
1 165 1 U/S
Takeuchi
2006/JMIG
Pro
1
Retrospective studies
Al Jama
Retro 0
2011/Oman
Koo
Retro 0
2011/Pak JMS
Sun
Retro 0
2011/Chin MJ
Grimbizis
2008/FS
Retro 0
Fedele
1993/HR
Retro 0
14 0 MRI
Focal
1 Consecutive
adenomyosis
(adenomyoma)
Focal
1 Consecutive
adenomyosis
(adenomyoma)
18 0 U/S, MRI Focal
1 Consecutive
adenomyosis
(adenomyoma)
18 0 U/S
Focal
1 Consecutive
adenomyosis
(adenomyoma)
40 0 NA
Focal
0 Consecutive
adenomyosis
(adenomyoma)
6 0 U/S
Focal
1 Consecutive
adenomyosis
(adenomyoma)
18 1 Histology Focal
0 Consecutive
adenomyosis
(adenomyoma)
Retro 0
2 0 U/S
Retro 0
1 0 U/S
Focal
1 NA
adenomyosis
(adenomyoma)
Focal
1 NA
adenomyosis
(adenomyoma)
Outcome
evaluation
Follow
Adequacy of
up/adequate follow-up Statistical Total
length
of cohorts
analysis grade
1 Surgical
Open
records
excision/classic
technique
1 Surgical
Open
records
excision/triple
flap technique
1 Surgical
Open or lap
records
excision/classic
technique
1 Surgical
Lap excision/
records
uterine wall
reconstruction
with overlapping
flaps
1 Structured
1 24/12
questionnaire
1 Yes
1
Yes
1
9
1 Structured
1 24/12
questionnaire
1 Yes
1
Yes
1
9
1 Structured
1 24/12
questionnaire
1 Yes
1
Yes
1
9
1 Structured
1 NA
questionnaire
0 No
0
Yes
1
6
1 Surgical
Open or Lap
records
excision/classic
technique
1 Surgical
Open or Lap
records
excision/classic
technique
1 Surgical
Open or Lap
records
complete
excision/classic
technique with
additional Ushape suturing
1 Surgical
Lap
records
excision/classic
technique
1 Surgical
Open
records
excision/classic
technique
1 Self-report
1 Yes
1
Yes
1
6
1 9/12
1 Structured
questionnaire
0 Yes
1
Yes
1
6
1 Self-report
0 27/12
1 Yes
1
Yes
1
5
1 Structured
1 13/12
questionnaire
0 Yes
1
No
0
5
1 Self-report
0 53/12
1 Yes
1
No
0
5
1 Self-report
0 25/12
1 NA
0
No
0
3
1 Self-report
0 NA
0 NA
0
No
0
2
0 Surgical
Lap
records
excision/classic
technique
0 Surgical
Open
records
excisiona/classic
technique
0 36/12
16.e3
Ferrero
2005, AOG
Representativeness
Ascertainment of
of the cases
exposure/detailed surgical technique
38 1 U/S
Osada
2011/RBM
Case reports
Wang
CJ 2006/FS
Modality of initial
diagnosis/definition
of extent of
the disease
Continued.
Author, year
Study No. of
design patients
Modality of initial
of extent of
the disease
La Fianza
2004/JCU
Retro 0
1 0 U/S
Morita
2004/JAAGL
Retro 0
3 0 MRI
Wei 2004,
Gyn Oncol
Retro 0
1 0 Clinical
Ozaki
1999/IJFWM
Retro 0
1 0 MRI
Kataoka
1998, JCAT
Retro 0
3 0 MRI
Hoffman
1989/O&G
Retro 0
1 0 HSG
Honore
1988/JRM
Retro 0
3 0 U/S
Hyams 1952
Retro 0
2 0 Clinical
Coghlin
1947/CMJ
Retro 0
1 0 Clinical
Focal
adenomyosis
(adenomyoma)
Focal
adenomyosis
(adenomyoma)
Focal
adenomyosis
(adenomyoma)
Focal
adenomyosis
(adenomyoma)
Focal
adenomyosis
(adenomyoma)
Focal
adenomyosis
(adenomyoma)
Focal
adenomyosis
(adenomyoma)
Diffuse
adenomyosis
Representativeness
Ascertainment of
of the cases
exposure/detailed surgical technique
1 NA
0 Medical
record
1 NA
0 Surgical
records
0 NA
0 Surgical
records
1 NA
0 Surgical
records
1 NA
0 Surgical
records
0 NA
0 Surgical
records
1 NA
0 Surgical
records
0 NA
0 Surgical
records
Focal
0 NA
adenomyosis
(adenomyoma)
0 Surgical
records
Open
excisiona/classic
technique
Lap
excision/classic
technique
Open
excisiona/classic
technique
Open
excisiona/classic
technique
Open
excision/classic
technique
Open
excision/classic
technique
Open
excision/classic
technique
Open
excision/classic
technique
(hysteroplasty)
Open
excision/classic
technique
Follow
Adequacy of
length
of cohorts
analysis grade
0 Self-report
0 NA
0 NA
0
No
0
1
1 Self-report
0 36/12
1 NA
0
No
0
3
1 Self-report
0 6/12
0 NA
0
No
0
1
1 Self-report
0 5/12
0 NA
0
No
0
2
1 Self-report
0 NA
0 NA
0
No
0
2
1 Self-report
0 NA
0 NA
0
No
0
1
1 Self-report
0 36/12
1 NA
0
No
0
3
1 Self-report
0 36/12
1 NA
0
No
0
2
1 Self-report
0 NA
0 NA
0
No
0
1
Note: HSG ¼ hysterosalpingogram; Lap ¼ laparoscopic; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective; Retro ¼ retrospective; U/S ¼ ultrasound.
a
Outcome
evaluation
16.e4
VOL. - NO. - / - 2013
VOL. - NO. - / - 2013
Partial excision of adenomyosis/partial adenomyomectomy: quality assessment of the relevant studies.
Author, year
Study No. of
design patients
Retrospective
studies
Sun
Retro 0 13
2011/Chin MJ
Modality of initial
of extent of the disease
Representativeness
of the cases
0 NA
Focal
0 Consecutive
adenomyosis
(adenomyoma)
Ascertainment of
exposure/detailed
surgical technique
1 Surgical
Lap
records
partial
excision/classic
reconstruction
1 Surgical
Open
records
excisiona/Asymmetric
dissection of uterus
1 Surgical
Open
records
excisiona/classic
technique
1 Surgical
Open
records
partial
excision/modified
H incision
0 Surgical
Lap
records
excisiona/classic
technique
Outcome
evaluation
0 Yes
1
Yes
1
4
1 Structured
1 12/12
questionnaire
0 Yes
1
No
0
6
1 Structured
1 36/12
questionnaire
1 Yes
1
Yes
1
8
1 Self-report
0 36/12
1 Yes
1
Yes
1
6
1 Self-report
0 24/12
1 Yes
1
No
0
4
0 Surgical
Lap assisted vaginal
records
excisiona/classic
technique
0 Surgical
Lap excision/classic
records
technique
1 Self-report
0 12/12
0 NA
0
No
0
1
1 Self-report
0 3/12
0 NA
0
No
0
1
0 NA
0 Surgical
Open excisiona/classic
technique
records
1 Self-report
0 12/12
0 NA
0
No
0
1
0 NA
0 Surgical
Open excisiona/classic
technique
records
1 Self-report
0 1/12
0 NA
0
No
0
1
0 NA
0 Surgical
Open excision/classic
records
technique
0 Surgical
Open
records
excision/wedge
resection
1 Self-report
0 12/12
0 NA
0
No
0
1
1 Self-report
0 <24/12
0 NA
0
No
0
1
Retro 0 44
1 MRI
Diffuse
adenomyosis
1 Consecutive
Wang PH
2009/JOGR
Retro 0 28
1 U/S
Diffuse
adenomyosis
1 Consecutive
Fujishita
2004/GOI
Retro 0 11
0 U/S, MRI Diffuse
adenomyosis
1 Consecutive
Wood
1998/HRU
Retro 0 25
1 NA
Diffuse/focal
adenomyosis
0 NA
Case reports
Wada
2006/JMIG
Retro 0
1
0 MRI
0 NA
Lin 2000/CMJa
Retro 0
2
Huang 1998, CMJ Retro 0
1
Kammerer-Doak
1996/JRM
Retro 0
1
Van Praagh
CJMA, 1965
Naidu 1958
Retro 0
1
Retro 0
1
Unclear
description
of lesion
0 U/S
Unclear
description
of lesion
0 NA
Unclear
description
of lesion
0 CT
Unclear
description
of lesion
0 Clinical Diffuse
adenomyosis
0 Clinical Diffuse
adenomyosis
0 NA
0 NA
Note: HSG ¼ hysterosalpingogram; Lap ¼ laparoscopic; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective; Retro ¼ retrospective; U/S ¼ ultrasound.
a
16.e5
0 20/12
Nishida 2010/FS
1 Self-report
Follow
Adequacy of
length
of cohorts
analysis grade
Cystic adenomyomas and juvenile cystic adenomyomas: quality assessment of the relevant studies.
Author, year
Retrospective
studies
Takeuchi
2010/FS
Kriplani
2011/JMIG
Cases: Juvenile
Acien 2012/HR
Study
design
No. of
patients
Retro 1
9
Retro 0
4
Retro 0
3
Chun
2011/JLAST
Retro 0
<5
Acien
2010/O&G
Akar
2010/F&S
Retro 0 <25
Modality of initial
of extent of the
disease
0 U/S, MRI JCA
0 U/S, MRI JCA
0 U/S, MRI JCA (reported
as ACUM)
1 MRI
JCA
Representativeness
of the cases
1 Consecutive
1 Consecutive
1
1
1 NA
0
1 NA
0
1 NA
0
Retro 0 <25
2 U/S, MRI JCA (reported
as ACUM)
1 U/S
JCA
1 NA
0
Liang
2010/F&S
Ball
2009/
GynSurg
Ho
2009/JPAG
Dogan
2008/AOG
Retro 0 <25
1 U/S
1 NA
0
Retro 0 <25
1 U/S
1 NA
0
JCA (reported
as ACUM)
JCA
surgical technique
VOL. - NO. - / - 2013
0
Retro 0
1
0 MRI
JCA
1 NA
0
Nabeshima
2008/JMIG
Retro 0
1
0 MRI
JCA
1 NA
0
Surgical
records
Kamio
2007/JOGR
Takeda
2007/JMIG
Retro 0
1
0 MRI
JCA
1 NA
0
Retro 0
1
0 MRI
JCA
1 NA
0
Surgical
records
Surgical
records
Nabeshima
Retro 0
2003/JAAGL
1
0 MRI
JCA
1 NA
0
Surgical
records
Potter 1998/F&S Retro 0
1
0 U/S
1 NA
0
Surgical
records
Surgical
records
Tamura
1996/TJEM
Cases: adults
Retro 0
1
1 NA
0
Yes
1
8
1 Structured
1 18/12
questionnaire
0
Yes
1
No
0
5
Open excisiona
1 Self-report
0 2/12
0
NA
0
No
0
2
Lap
1 Self-report
0 12/12
0
NA
0
No
0
2
excision/classic
technique
Open excisiona
1 Self-report
0 18/12
0
NA
0
No
0
2
Robotic
excision/classic
technique
Open excisiona
1 Self-report
0 NA
0
NA
0
No
0
2
1 Self-report
0 18/12
0
NA
0
No
0
2
Lap
1 Self-report
0 18/12
0
NA
0
No
0
2
excision/classic
technique
Open excisiona
1 Self-report
0 NA
0
NA
0
No
0
2
1 Self-report
0 NA
0
NA
0
No
0
2
1 Self-report
0 12/12
0
NA
0
No
0
2
1 Self-report
0 NA
0
NA
0
No
0
2
1 Self-report
0 3/12
0
NA
0
No
0
2
1 Self-report
0 3/12
0
NA
0
No
0
2
1 Self-report
0 12/12
0
NA
0
No
0
2
1 Self-report
0 NA
0
NA
0
No
0
2
Surgical
records
Surgical
records
1 NA
JCA (reported
as ACUM)
0 U/S, MRI JCA
1
Lap
1 U/S, MRI JCA
Surgical
records
Surgical
records
Statistical Total
analysis grade
Yes
Surgical
records
Retro 0 <25
Adequacy of
follow-up
of cohorts
1
Lap
Surgical
records
Surgical
records
Follow
up/adequate
length
1 Structured
1 35/12
questionnaire
Surgical
records
Surgical
records
Surgical
records
Outcome
evaluation
excision/classic
technique
excision/classic
technique
Open
excision/classic
technique
Lap
excision/classic
technique
Open
excisiona
Lap
excision/classic
technique
Lap
excision/classic
technique
Open excisiona
Open excision
a
16.e6
VOL. - NO. - / - 2013
Continued.
Study
design
No. of
patients
Retro 0
1
Ors 2009/Anatol Retro 0
1
Protopapas
2008
Retro 0
3
Wang JH
2007/FS
Retro 0
1
Iribarne
1994, JCUS
Retro 0
1
Parulekar
1990/JPGM
Retro 0
1
Author, year
Acien
2010/O&G
Modality of initial
of extent of the
disease
0 U/S, MRI Cystic
adenomyoma
(reported as
ACUM)
0 U/S, MRI Cystic
adenomyoma
(Focal
adenomyosis)
0 U/S
Cystic
adenomyoma
(Focal
adenomyosis)
0 U/S
Cystic
adenomyoma
(Focal
adenomyosis)
0 U/S
Cystic
adenomyoma
(Focal
adenomyosis)
0 U/S
Cystic
adenomyoma
(Focal
adenomyosis)
Representativeness
of the cases
surgical technique
Outcome
evaluation
Follow
up/adequate
length
Adequacy of
follow-up
of cohorts
Statistical Total
analysis grade
1 NA
0
Surgical
records
Open excisiona
1
Self-report
0 NA
0
NA
0
No
0
2
1 NA
0
Surgical
records
Open
excision/classic
technique
1
Self-report
0 NA
0
NA
0
No
0
2
1 NA
0
Surgical
records
Open excisiona
1
Self-report
0 NA
0
NA
0
No
0
2
1 NA
0
Surgical
records
Open
excision/classic
technique
1
Self-report
0 10/12
0
NA
0
No
0
2
1 NA
0
Surgical
records
Open
excision/classic
technique
1
Self-report
0 NA
0
NA
0
No
0
2
1 NA
0
Surgical
records
Open
excision/classic
technique
1
Self-report
0 NA
0
NA
0
No
0
2
Note: HSG ¼ hysterosalpingogram; JCA ¼ juvenile cystic adenomyoma; Lap ¼ laparoscopic; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective; Retro ¼ retrospective; U/S ¼ ultrasound.
a
16.e7
Nonexcisional techniques of surgical treatment of adenomyosis: quality assessment of the relevant studies.
Author, year
Kang
2009/JMIG
Study
design
Retro 0
No. of
Patients
Modality of initial
of extent of the disease
37
1 U/S
1 Consecutive
1
1
20
0 U/S, MRI Unclear
0 Consecutive
description of lesion
1
Retro 0
11
0 NA
Pro
10
0 MRI
Retro 0 190
1 U/S
Retro 0
1
0 U/S
Retro 0
1
0 Clinical
Retro 0
1
0 U/S
Maia
Retro 0
2003/JAAGL
Wood
Retro 0
1998/HRU
Yang 2009/FS
Pro 1
95
1 U/S
18
0 NA
7
0 U/S
Retro 0
1
0 U/S
Retro 0
1
0 U/S
Kanaoka
Retro 0
2004/Osaka
Retro 0
Chan
2001/Med J
Malaysia
1
1
Wang
Pro
2002/JAAGL
Wood
1998/HRU
Philips
1996/JAAGL
Preutthupan,
2010/JOGR
Fernadez
2007/JMIG
Kumar
2007/JMIG
Giana
2005/EJGO
Furman
2007/UOG
Ryo 2006/JRM
1
Diffuse/focal
adenomyosis
Representativeness
of the cases
Diffuse/focal
adenomyosis
Unclear description
of lesion
Diffuse/focal
adenomyosis
Diffuse adenomyosis
0 NA
0
0 NA
0
1 Consecutive
1
1 NA
0
Unclear description
of lesion
Focal
adenomyosis (cystic
adenomyoma)
Unclear description
of lesion
Diffuse/focal
adenomyosis
Focal adenomyosis
0 NA
0
1 NA
0
0 Consecutive
1
0 NA
0
1 Consecutive
1
0
0 MRI
Focal Adenomyosis
1 NA
(cystic adenomyoma)
Focal Adenomyosis
1 NA
(cystic adenomyoma)
Diffuse adenomyosis
1 NA
0 U/S
Diffuse adenomyosis
0
1 NA
0
0
Ascertainment of
exposure/detailed
surgical technique
Follow
up/adequate
length
Adequacy of
follow-up
of cohorts
Statistical Total
analysis grade
1 Structured
1 12/12
questionnaire
0
Yes
1
Yes
1
7
1 Structured
1 8/12
questionnaire
0
Yes
1
Yes
1
6
1 Self-report
0 24/12
1
Yes
1
No
0
3
1 Self-report
0 25/12
1
Yes
1
No
0
4
1 Self-report
0 60/12
1
Yes
1
Yes
1
7
1 Self-report
0 NA
0
NA
0
No
0
2
1 Self-report
0 18/12
0
NA
0
No
0
1
1 Self-report
0 6/12
0
NA
0
No
0
2
TCRE Mirena
1 Self-report
0 12/12
0
Yes
1
Yes
1
5
Endomyometrial
resection
Open HIFU
1 Self-report
0 24/12
1
Yes
1
No
0
3
1 NA
0 NA
0
NA
0
Yes
1
4
0 36/12
1
NA
0
No
0
3
0 NA
0
NA
0
No
0
2
0 12/12
0
NA
0
No
0
2
1 Structured
1 36/12
questionnaire
1
NA
0
No
0
4
Surgical
Laparoscopic
records
partial resection
of adenomyosis
þ UAO
Surgical
Laparoscopic
records
uterine artery
ligation
Surgical
Myometrial
records
electrocoagulation
Surgical
Laparoscopic bipolar
records
coagulation
Surgical
Rollerball endometrial
records
ablation
Surgical
Operative
records
hysteroscopy
Surgical
TCRE
records
Surgical
Resectoscope
records
Surgical
records
Surgical
records
Surgical
records
Surgical
records
Surgical
records
Surgical
records
Surgical
records
Outcome
evaluation
U/S aspiration,
1 Self-report
alcohol instillation
Radiofrequency
1 Self-report
ablation
MEA
1 Self-report
Balloon
thermoablation
VOL. - NO. - / - 2013
Note: HIFU ¼ high-intensity focal ultrasound; HSG ¼ hysterosalpingogram; JCA ¼ juvenile cystic adenomyoma; Lap ¼ laparoscopic; MEA ¼ microwave endometrial ablation; MRI ¼ magnetic resonance imaging; NA ¼ not applicable; Pro ¼ prospective; Retro ¼ retrospective; TCRE ¼ transcervical endometrial resection; UAO ¼ uterine artery occlusion; U/S ¼ ultrasound.
16.e8

Uterus-sparing operative treatment for adenomyosis

Transcription

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