Key words adenomyomectomy - bilateral uterine artery - utero-ovarian vessels - double/multiple
flap - temporary occlusion
Schlüsselwörter Adenomyomektomie - bilaterale Arteria uterina - uteroovarielle Gefäße - Doppel-/Mehrfach-Lappen
- vorübergehende Okklusion
Introduction
Adenomyosis is a common gynecological tumor that is characterized by endometrial tissue
and stroma invading the myometrium. Depending on the extent of the lesion, the disease
is categorized either as localized or diffuse adenomyosis. The major clinical manifestations
include severe dysmenorrhea, hypermenorrhea, chronic pelvic pain, and infertility
[1 ]. This condition is usually complicated by endometrial cysts of the ovary, pelvic
endometriosis, hysteromyoma, or other estrogen-dependent diseases. There is no consensus
about the most appropriate method to treat symptomatic uterine adenomyosis in patients
who desire to preserve their fertility. Medical treatment is often the first choice
for adenomyosis and includes the administration of gonadotropin-releasing hormone
(GnRH) agonists, oral contraceptives, progestins, aromatase inhibitors, and danazol
[2 ]. However, the effect of these treatments is transient;
following withdrawal of the medication, the lesions undergo rapid regrowth and
there is a relapse in symptoms, particularly pain [3 ]. When medical treatment fails, complete hysterectomy is a definitive approach that
can be used to treat symptomatic adenomyosis. However, total hysterectomy is inappropriate
for women who wish to preserve their fertility and uterus. Many conservative surgical
options have been developed to treat adenomyosis; adenomyomectomy is the most conservative
surgical method that can be used to preserve fertility [4 ], [5 ]. Excisional surgical techniques for adenomyosis include the transverse H-incision
technique and wedge-shaped excision of the uterine wall; however, these methods are
frequently associated with spontaneous uterine rupture during a subsequent pregnancy,
as well as the recurrence of adenomyosis [5 ]. In a previous
study, Hisao et al. [1 ] reported a novel laparoscopic protocol for adenomyomectomy which incorporated a
triple-flap method; this method was shown to achieve good results. Subsequently, Grimbizis
et al. [6 ] showed that the therapeutic effect of a double-flap method was significantly better
than conventional surgery, and that the clinical effect was the same as that of the
triple-flap method. However, the triple-flap method for laparoscopic adenomyomectomy
is limited by heavy bleeding. For this form of surgery to be carried out safely, it
is important that the operative field is clean and stable. Kwon et al. [7 ] introduced a laparoscopic technique for adenomyomectomy that was carried out under
transient occlusion of the uterine arteries (TOUA). In the current study, we report
on an operative procedure, based on the pioneering work of Kwon et al., consisting
of a laparoscopic-assisted
adenomyomectomy using the double/multiple-flap method combined with temporary
occlusion of the bilateral uterine artery and utero-ovarian vessels to treat uterine
adenomyosis.
Material and Methods
Patient selection
This single-center study involved a retrospective analysis of symptomatic patients
with adenomyosis who were treated at the Jinhua Municipal Central Hospital from May
2014 to January 2017. Group A consisted of 76 patients and Group B consisted of 79
patients ([Fig. 1 ]). All patients provided written informed consent before recruitment. All eligible
women were informed of the potential complications, benefits, and alternatives of
each approach before they were assigned into one of the two groups. This research
was approved by the Ethics Committee of Jinhua Municipal Central Hospital. Adenomyosis
can be classified into four subtypes based on magnetic resonance imaging (MRI) geography
[8 ]. Subtype I (intrinsic) adenomyosis resides in the inner layer of the uterus without
disrupting the other components. Subtype II (extrinsic) adenomyosis occurs in the
outer layer of the uterus without affecting the inner
structures. Subtype III (intramural) adenomyosis occurs only in the myometrium.
Adenomyosis that does not satisfy the above criteria is known as subtype IV; this
subtype does not have a specific definition and represents a mixture of advanced cases
from subtypes I – III. All patients were required to undergo a preoperative diagnostic
examination to rule out other comorbidities.
Fig. 1 CONSORT flow diagram.
The inclusion criteria were as follows:
women with subtype II, III and IV adenomyosis;
women experiencing severe dysmenorrhea (VAS ≥ 7) with or without hypermenorrhea, and
in whom drug treatment had failed, including oral contraceptives, GnRHa, progestins,
and aromatase inhibitors;
women who wished to preserve their uterus, although their fertility was not an essential
requirement;
women in whom adenomyosis had been verified preoperatively by ultrasound (which helped
to eliminate other conditions with similar symptoms) and pelvic magnetic resonance
imaging (MRI) had been carried out to identify the exact location and size of the
lesion and its relationship with the uterine cavity according to specific diagnostic
criteria; and
women with symptomatic adenomyosis measuring 30 mm or greater in focal adenomyosis
and affecting more than 70% of the anterior and/or posterior myometrium with an enlargement
of more than 5 cm in thickness in diffuse adenomyosis.
The MRI films of 8 of the 146 patients (3 patients in group A and 5 patients in group
B) were not available in our hospital because imaging had been performed in other
institutions.
The exclusion criteria included the coexistence of pelvic disease, such as extensive
endometriosis, pelvic inflammatory disease, or genital malignant tumor. We also excluded
patients whose postoperative pathological findings for adenomyoma were negative.
All patients were informed about the potential risks of hysterectomy or laparotomy.
The operating time was measured from the first skin incision to closure. The size
of the adenomyosis was defined as the maximum diameter of the adenomyosis, as determined
by MRI. Operative blood loss was estimated by gathering the blood volume in suction
bottles during surgery.
Surgical technique
All of the cases recruited in this study were operated on by five experienced gynecologists
(“Associate Senior” or above). The patients were placed in the Trendelenburg position
at 30 degrees. After general anesthesia, we performed the laparoscopic procedure with
4 trocars. In all cases, diluted vasopressin was injected into the myometrium at the
beginning of surgery.
In group A, the uterine serosa covering the adenomyotic tissue was incised using a
monopolar cutting electrode until the endometrium or the interior of the uterine cavity
was visually exposed. Because we needed a sufficient depth of incision, the adenomyotic
tissue was split into two or more parts ([Fig. 2 a ]). The adenomyotic tissue was then excised with endoscopic scissors ([Fig. 2 b ] and [c ]). The surgeon differentiated adenomyotic tissue from normal muscle layer based on
tactile and visual sensation for complete cytoreductive excision in cases with diffuse
adenomyosis. In cases with localized adenomyosis, the focal lesions were completely
removed. The involved endometrium was spared as much as possible, and the serosa covering
the adenomyoma was retained at a depth of 5 mm to help with subsequent triple or double/multiple-flap
reconstruction of excisional defects.
Fig. 2 a The adenomyotic tissue is split into two or more parts. b and c The adenomyotic tissue is excised with endoscopic scissors. d The reconstruction process between the flaps. e A titanium clip on the left side of uterine artery. f Transient occlusion of utero-ovarian vessels with a vascular bulldog clamp.
The defect area was closed using a specific suturing pattern. First, we sutured the
endometrium; then we sutured one side of the multi-sectioned myometrium and the serosal
flap to the endometrial side of the uterus with many deep and single interrupted sutures.
During the reconstruction process, sutures were placed meticulously in order to avoid
the development of hematoma between the flaps. Next, the serosal surface of the previously
covered flap was removed to ensure that the tissue between the flaps was strongly
attached. Finally, the other side of the flap was used to cover and suture the previous
flap ([Fig. 2 d ]). The reconstruction process should be carried out in such a way that all sides
of the uterus are evenly reconstructed without weak or thin areas. The external serous
flap was sutured using the “baseball” method, so that the cutting edges could be inverted
inside to reduce adhesion of the incision to the intestines, omentum,
and peritoneum.
In group B, the anterior leaf of the broad ligament was separated by blunt and sharp
dissection. We located the uterine artery via the posterior leaf of the broad ligament
between the mesosalpinx and the round ligament. Application and removal of the titanium
clip and clamp was performed according to the approach described in our previous paper
([Fig. 2 e ] and [f ]) [9 ]. Compared with other instruments, the clamp and titanium clip are easy to apply
and remove and seem to cause less damage to the vessels involved. The remainder of
the procedure was then carried out as described for group A. Finally, the titanium
clips and the clamps were safely removed to allow the vessels to re-perfuse, and the
peritoneum was closed with absorbable sutures. All specimens were confirmed by histopathological
examination and malignancy was excluded postoperatively.
Post-surgical follow-up and treatment
After obtaining a pathological diagnosis, we treated all patients with six postoperative
cycles of GnRH agonists (Ipsen Pharma Biotech, France). The first dose was given to
all patients at the beginning of the first menstrual cycle after surgery, and use
of the levonorgestrel-releasing intrauterine system (LNG-IUS, Mirena, Bayer, Germany)
was suggested after the completion of GnRHa treatment.
For a total of 2 years after surgery, we assessed improvements in symptoms, carried
out ultrasound examinations and monitored anti-Mullerian hormone (AMH) levels as an
indicator of fertility. The severity of pelvic pain was recorded using a standardized
questionnaire with a visual analog scale (VAS) score ranging from 0 (no pain) to 10
(excruciating pain) [7 ]. All patients were asked to judge the amount of postoperative menstrual fluid discharge
against the pre-surgery amount (classified as a 10) [10 ]; this was a relatively accurate method to compare postoperative with preoperative
levels. changes in symptoms before and after surgery were compared.
Uterine volume was measured by ultrasonography (Volume = A × B × C × 0.5233 [in which
A, B, and C are the longitudinal dimension, anteroposterior dimension, and transverse
dimension of the uterus, respectively]). Ultrasonography was performed by the same
physician, who was not involved in this investigation and was also blinded to the
ultrasonography findings before and after surgery. The maximum diameter of the lesion
was used for analysis. MRI was not routinely evaluated after surgery due to excessive
costs.
Evaluation of therapeutic efficacy
Therapeutic efficacy was graded according to the following criteria:
complete remission, in which dysmenorrhea completely disappeared after surgery;
significant remission, in which dysmenorrhea did not disappear completely and the
VAS score was reduced by more than 3 grades;
partial remission, in which the VAS score was reduced by less than 2 grades, and dysmenorrhea
did not disappear;
no remission, in which the VAS score did not change compared with preoperative levels;
and
recurrence, in which complete or significant remission was achieved, but dysmenorrhea
recurred and progressively increased 1 year after surgery, and the appearance of adenomyotic
lesions was confirmed by ultrasound or MRI.
Complete remission and significant remission were defined as clinically effective
treatment.
Statistical Analysis
SPSS version 17.0 (SPSS, Inc., IBM, Chicago, IL) was used to perform all statistical
analyses. Data are presented as mean ± standard deviation (SD), median (range), or
absolute numbers (%). The difference in means between the two groups was tested by
analysis of variance (ANOVA). All p-values were two-tailed, and a p-value < 0.05 was
considered statistically significant.
Results
Patient characteristics
None of the patients required conversion to laparotomy, and none suffered from major
intraoperative or postoperative complications. Six patients (three in group A and
three in group B) refused to take GnRHa or LNG-IUS treatment because they experienced
complete remission of dysmenorrhea. One patient in group A was lost to follow-up and
2 patients in group B were given LNG-IUS 4 months after implantation. After surgery,
42 patients (19 patients in group A and 23 patients in group B) had ovarian endometriosis
confirmed by laparoscopy and postoperative pathology. Of the 42 patients, deep infiltrating
endometriosis (DIE) was found during surgery in 19 women (9 patients in group A and
10 patients in group B) ([Table 1 ]). The extent of DIE was determined intraoperatively using the revised ENZIAN and
AFS score [11 ] ([Tables 1 ] and [2 ]) The remaining
patients (72 in group A and 74 in group B) were all treated with GnRHa and LNG-IUS
during the follow-up period. There were no statistical differences in terms of body
mass index (BMI), age, uterine volume, VAS score and menorrhagia, when the two groups
were compared preoperatively (p > 0.05) ([Table 1 ]).
Table 1 Patient characteristics. The distribution of the enrolled patientsʼ age, body mass
index, operative time, and mean blood loss, and the subtypes and weight of the adenomyosis
are described in detail. There was no difference in age, body mass index, operating
time, weight of adenomyotic tissue and patientsʼ adenomyosis subtypes between groups.
The mean blood loss in group B was significantly lower than in group A (p < 0.001).
Characteristics
Group A (n = 72)
Group B (n = 74)
p value
Values are given as mean ± standard deviation, absolute number (%), or median (range).
Age (year)
35.15 ± 6.41
34.05 ± 5.73
0.277
Body mass index (kg/m2 )
20.06 ± 1.42
20.47 ± 2.32
0.190
Operating time (minutes)
153.35 ± 34.27
161.69 ± 42.99
0.198
Blood loss (ml)
344.26 ± 95.52
112.38 ± 42.25
< 0.001
Weight of adenomyotic tissue (g)
77.54 ± 73.72
86.55 ± 46.38
0.229
Adenomyosis subtypes
36
39
0.890
17
18
19
17
AFS stage
0
0
0.939
6
7
9
12
4
4
Coexisting endometriosis
Ovarian endometriosis
19
23
0.531
Deep infiltrating endometriosis
9
10
0.856
Table 2 Histopathological ENZIAN staging for all observed DIE lesions.
Lesions
Group A (n = 76)
Group B (n = 79)
A = vaginal/rectovaginal endometriosis
B = endometriosis of the uterosacral ligaments
C = rectosigmoid endometriosis
FA = adenomyosis
FB = bladder endometriosis
FU = ureteral endometriosis
FI = endometriosis of the sigma, cecum and ileum
FO = other types of endometriosis (such as diaphragm, liver, abdominal wall, etc.)
1A
3
2
2A
2
1
3A
1
1
1B
4
5
2B
1
2
3B
0
1
1C
1
2
2C
2
1
3C
1
0
FA
76
79
FB
1
0
FU
0
2
FI
0
0
FO
0
0
Comparison of mean blood loss, operating time and the weight of excised tissue between
the two groups
In group B, the mean blood loss was 112.38 ± 42.25 ml; this was significantly lower
than that in group A (344.26 ± 95.52 ml; p < 0.001). When the two groups were compared,
there were no statistical differences in terms of adenomyosis subtypes, operating
times, or the weight of the excised tissues (p > 0.05) ([Table 1 ]).
Comparison of VAS scores between the two groups
At the 24-month follow-up point, the VAS scores in both groups were significantly
lower than their preoperative scores (p < 0.001). Compared with the preoperative status,
the VAS score at the first menstrual cycle after surgery was statistically lower in
both groups (p < 0.001). At the first follow-up after the first postoperative menstruation,
it was evident that in both groups, VAS scores had improved significantly after medical
treatment (p < 0.001). The VAS scores were similar in both groups when compared at
6 and 12 months after surgery and at 12 and 24 months after surgery (p > 0.05) and
there were no significant differences between the two groups in the following period
(p > 0.05); the scores for each group were significantly lower than those recorded
before surgery (p < 0.001) ([Table 3 ]). The effective rate of dysmenorrhea remission decreased gradually over time in
the 6 months after surgery, and the differences
with respect to the effective rate between the two groups at each time-point
after surgery did not reach statistical significance (p > 0.05) ([Table 4 ]). However, 24 months after surgery, one patient (1/72, 1.35%) in group A showed
dysmenorrhea; the VAS score of this patient was 6.5.
Table 3 Therapeutic outcomes during follow-up. In the period after surgery, VAS scores, menstrual
blood flow, menstrual volume, the uterine size and serum AMH levels were recorded.
The VAS scores in both groups decreased significantly compared with those before surgery
(p < 0.001); the VAS scores were similar at 6 and 12 months after surgery and at 12
and 24 months after surgery in both groups (p > 0.05) and there were no significant
differences between the two groups (p > 0.05). Menstrual blood flow was not significantly
different between the two groups during menstruation at 12 and 24 months after surgery
(p > 0.05), and menstrual volume in each group was significantly lower compared to
the volumes prior to surgery (p < 0.001). Uterine size and serum AMH levels did not
differ significantly between the two groups (p > 0.05), and both parameters in each
group had decreased significantly compared with those obtained prior to surgery
(p < 0.001).
VAS
Menorrhagia
Estimated uterine volume, cm3
AMH, ng/ml
Data are presented as mean ± SD.
Baseline
8.22 ± 0.81
10
228.33 ± 36.63
4.47 ± 2.26
8.35 ± 0.82
10
218.70 ± 38.59
5.08 ± 1.40
0.355
–
0.124
0.057
At the first postoperative menstruation
2.48 ± 1.49
4.23 ± 1.84
–
3.64 ± 1.92
2.91 ± 1.54
3.87 ± 2.13
–
3.81 ± 1.89
0.085
0.272
–
0.594
3 months
–
–
72.76 ± 10.98
–
–
–
69.85 ± 10.02
–
–
–
0.096
–
6 months
0.29 ± 0.71
–
69.92 ± 12.09
–
0.31 ± 084
–
67.95 ± 13.01
–
0.891
–
0.345
–
12 months
0.39 ± 0.93
1.24 ± 0.64
70.07 ± 11.12
4.28 ± 2.02
0.36 ± 0.81
1.32 ± 0.76
66.55 ± 11.19
4.77 ± 1.80
0.831
0.487
0.059
0.122
24 months
0.40 ± 1.04
1.37 ± 0.68
72.56 ± 13.37
4.03 ± 2.04
0.31 ± 0.70
1.41 ± 0.81
70.30 ± 10.03
4.61 ± 2.07
0.530
0.723
0.249
0.091
Table 4 Dysmenorrhea relief and adenomyosis recurrence after adenomyomectomy. Rates of dysmenorrhea
remission were recorded in the period after surgery. The effective rate of dysmenorrhea
remission decreased over time 6 months after surgery, and the differences in the effective
rate between the two groups at each time-point after surgery did not reach statistical
significance (p > 0.05).
Dysmenorrhea remission (%)
Effective
Complete remission
Significant remission
Partial remission
No remission
Notes: months after surgery (% [Effective cases/Total cases])
Group A
At the first postoperative menstruation
48.61 (35/72)
13.89 (10/72)
30.56 (22/72)
6.94 (5/72)
62.5 (45/72)
6 months
93.06 (67/72)
6.97 (5/72)
0
0
100 (72/72)
12 months
84.72 (61/72)
12.5 (9/72)
2.78 (2/72)
0
97.22 (70/72)
24 months
80.55 (58/72)
15.28 (11/72)
2.78 (2/72)
1.39 (1/72)
95.83 (69/72)
Group B
At the first postoperative menstruation
50 (36/74)
13.51 (10/74)
32.43 (24/74)
5.41 (4/74)
62.16 (46/74)
6 months
91.89 (68/74)
8.11 (6/74)
0
0
100 (74/74)
12 months
85.14 (63/74)
13.51 (10/74)
1.35 (1/74)
0
96.65 (73/74)
24 months
78.38 (58/74)
18.92 (14/74)
2.70 (2/74)
0
97.30 (72/74)
Comparison of uterine size, AMH, and menstrual blood flow between the two groups
After surgery, uterine sizes did not differ significantly between the two groups (p > 0.05),
and mean size (in both groups) was significantly lower than preoperative values (p < 0.001)
([Table 3 ]). AMH levels did not differ significantly between the two groups at first menstruation,
12 months, and 24 months postoperatively. The AMH levels in both groups showed a small
but significant decrease at the time of the first postoperative menstruation (p < 0.05)
([Table 3 ]).
There was no significant difference in menstrual blood flow between the two groups
during the first menstrual cycle after surgery, or at 12 and 24 months after surgery
(p > 0.05). The menstrual volume in each group was significantly lower compared to
preoperative volumes (p < 0.001) ([Table 3 ]). In group A, all cases experienced normal menstruation after surgery. However,
one patient in group B suffered from menorrhagia at 24 months after surgery; the menstrual
volume was 5.5. In both groups, menstrual flow at 24 months after surgery did not
differ significantly compared with that at 12 months after surgery (p > 0.05).
Two cases experienced menorrhagia and dysmenorrhea after surgery. One patient in group
A suffered from dysmenorrhea (VAS = 6.5) and required a second round of surgery. In
the process of carrying out hysteroscopic endometriosis surgery as a definitive treatment
28 months after surgery, we found multiple cystic adenomyoma lesions in the myometrium.
The other patient who suffered from dysmenorrhea is still being followed up.
Discussion
Adenomyosis is the most frequently identified gynecological tumor in women in their
late reproductive years [12 ]. In severe cases, this condition not only influences physical health, it can also
affect mental health and have a negative impact on quality of life. Generally, women
wish to preserve their uterus, particularly in the Chinese population. This is for
cultural and emotional reasons and because they may wish to become pregnant in the
future. In patients with diffuse adenomyosis, laparotomic adenomyomectomy has recently
been considered to be the ideal choice for the radical resection of adenomyotic tissue
to relieve adenomyoma-related symptoms and preserve fertility [5 ]. As our clinical experience has grown and minimally invasive techniques have become
increasingly popular, we have been able to address the difficulties associated with
laparoscopic adenomyomectomy, at least to a certain extent. We suggest
that a laparoscopic approach is an appropriate treatment to treat uterine adenomyosis.
Conventional partial adenomyomectomy procedures such as the transverse H incision
technique and wedge-shaped excision of the uterine wall have also been reported [5 ]. Excision results in the incomplete removal of adenomyotic tissue and may create
difficulties when attempting functional reconstruction of the remaining myometrium;
this is due to the extensive loss of the muscle layer [5 ]. In adenomyosis, the endometrial tissue penetrates the myometrium; the boundary
between the adjacent normal layer and the adenomyotic tissue thus becomes unclear.
This causes difficulties during dissection and can result in heavy intraoperative
bleeding. The operating time is usually longer for laparoscopic excision of adenomyosis
than for laparoscopic myomectomy, and operating times depend very much on difficulties
encountered during the
suturing process and levels of intraoperative bleeding. Therefore, controlling
bleeding is an important factor. Efforts to control intraoperative bleeding have were
introduced by Morita et al. [13 ] who administrated local vasopressin, Osada et al. [10 ] who reported the use of a supracervical tourniquet, and Kwon et al. [7 ] who used a clip to transiently occlude the uterine arteries during laparotomy. Maintaining
a stable condition and limiting the amount of bleeding is very important if we are
to complete laparoscopic adenomyomectomy procedures safely and relatively simply.
In the present investigation, we based our concept on pioneering work and carried
out laparoscopic adenomyomectomy using the double/multiple-flap method combined with
temporary occlusion of the bilateral uterine artery and utero-ovarian vessels to excise
the adenomyotic tissue.
Our results show that all of our cases experienced significant remission in terms
of uterine size, menorrhagia and pain symptoms after surgery. None of the patients
developed endometriotic lesions in other areas during the follow-up period. Menorrhagia
and dysmenorrhea are the characteristic symptoms of adenomyosis and are directly related
to the therapeutic efficacy of adenomyomectomy [14 ], [15 ], [16 ]. An enlarged uterus is also a primary symptom of adenomyosis, and the reduction
of uterine size is also correlated with surgical efficacy [17 ], [18 ]. Long-term follow-up suggested that, compared to the preoperative state, both group
A and group B achieved a reduction in uterine volumes (p < 0.001). It is clear that
laparoscopic adenomyomectomy can be used to treat uterine adenomyosis effectively
[5 ]. However, the efficacy of wedge resection for adenomyosis has been reported to be
less than 65% [19 ]; furthermore, when postoperative follow-up was prolonged, menorrhagia and uterine
size relapsed. We identified statistical differences in VAS scores and menstrual volume
compared to preoperative parameters and at the first menstrual cycle after surgery
(p < 0.001). At the first follow-up after the first postoperative menstruation, we
found that VAS scores had significantly improved following medical treatment (p < 0.001).
In a previous study, Wang et al. [20 ] reported that a combination of surgical and medical (GnRHa) treatment provided more
effective symptom control than surgery alone during the first two years after treatment.
The effect of GnRH agonists is known to be transient [3 ]. In the present study, we introduced the use of LNG-IUS
following the completion of GnRHa treatment. The LNG-IUD releases 20 mg of levonorgestrel
each day and represents an effective treatment for adenomyosis [21 ]. Zhu et al. [22 ] further reported that the recurrence rate was significantly higher in patients who
were only treated with GnRHa after surgery than in patients who were treated with
GnRHa plus LNG-IUS after surgery (51.6 vs. 8.3%; p < 0.05). In our study, patients
in both groups showed a lower rate of relapse (n = 1, 1.39% vs. n = 1, 1.35%) than
previously reported (n = 32, 28.1%) [20 ] at the end of the 2-year follow-up period. These results are consistent with those
reported previously by Zhu et al. [22 ]. In our study, we found that the double/multiple-flap method could remove adenomyomatic
lesions more radically and could reduce the risk of recurrence over time, at least
theoretically.
Another study has demonstrated that LNG-IUS may have a direct influence on the
eutopic endometrium as the origin of the disease [23 ] and indicated that LNG-IUS can control symptoms and prevent recurrence after surgery.
These previous findings are consistent with our present results in that we demonstrated
a low rate of relapse for related symptoms and none of the patients developed adenomyotic
lesions or ovarian endometriosis in the uterus or ovaries, as confirmed by ultrasound
or MRI during follow-up.
The therapeutic efficacy of adenomyomectomy is mainly dependent on the extent and
type of adenomyosis as well as the surgical technique used [5 ]. It is necessary to select the optimal treatment for the right patient. In cases
involving focal adenomyosis (subtype III), the first-line approach is laparoscopic
total lesion excision. In women with diffuse and mixed adenomyosis (subtypes II and
IV), aggressive excision of the adenomyotic lesion may be the best course of treatment.
The surgical techniques used for adenomyomectomy can be divided into two types, according
to how much of the adjacent normal layer is removed and the extent to which the integrity
and function of the uterus is preserved. Type I involves the total and complete eradication
of adenomyosis while type II is a cytoreductive procedure [24 ]. In the present study, the method we adopted for subtype III was classified as type
I while subtypes II and
IV were classified as type II. We attempted to perform laparoscopic adenomyomectomy
based on the technique described by Osada et al. [10 ] and Kim et al. [25 ]. During surgery, the bilateral uterine artery and utero-ovarian vessels were occluded
to avoid excessive bleeding. In addition, the uterine cavity was opened entirely so
that the full extent of the adenomyosis was visible, including the crucial landmarks
of the endometrium and the serosal surface. This facilitated the excision of affected
tissues more thoroughly than conventional surgery.
As follow-up time increased, almost all of the cases experienced normal menstruation.
VAS scores and uterine volumes were similar during follow-up. These results indicate
that laparoscopic adenomyomectomy using the double/multiple-flap method was more effective
at treating uterine adenomyosis than conventional surgery; these findings concur with
other previously reported findings [5 ], [24 ]. However, two of our patients still experienced menorrhagia and dysmenorrhea after
surgery. MRI revealed that one of these patients suffered from dysmenorrhea; this
manifested in the form of multiple cystic adenomyoma lesions (1 – 10 mm in diameter)
in the myometrium. Dysmenorrhea and other symptoms, including hypogastric pain and
lumbago, can develop over time in cases with cystic adenomyoma [26 ].
Estimated blood loss was 112.38 ± 42.25 ml in group B; this was significantly lower
than that in the double/multiple-flap only group (344.26 ± 95.52 ml; p < 0.001). These
findings concur with a previous report [1 ]. Morita et al. [13 ] administered vasopressin locally to control bleeding; however, the half-life of
vasopressin is only 24.1 minutes [27 ] and the time taken to suppress bleeding from the incision was short compared with
the duration of the procedure; furthermore, repeated doses of vasopressin can have
an adverse effect on systemic circulation [28 ]. In our study, approximately 5 min was spent separating the uterine artery and occluding
the transient uterine artery and utero-ovarian vessels in group B. This allowed us
to successfully control intraoperative bleeding and did not lead to a significant
increase in operating times (p = 0.198).
It is important to note that the clips applied to the uterine artery do not affect
ovarian blood supply or function [9 ] and that the vascular clamps have a gap at the most proximal section of the device
where there are no serrations. When applied to this area, the clamp does not damage
the fallopian tubes or vessels [9 ]. In a previous study, Seifer et al. [29 ], [30 ] showed that serum AMH levels may be the most reliable and easily measurable marker
for ovarian reserve. According to the results of the present study, AMH levels showed
a small but significant trend towards reduction (in both group A and B) at the time
of the first menstruation after surgery (p < 0.05); however, there was no significant
difference between the two groups with regard to AMH levels thereafter (p > 0.05).
There are some limitations associated with our current research that should be taken
into consideration. The follow-up period was short and the pregnancy rate was not
considered because most patients in our study had completed childbearing and their
fertility was not an essential requirement. The pregnancy rate needs to be investigated
further in a randomized controlled study involving a larger number of cases.
Laparoscopic adenomyomectomy with temporary occlusion of the bilateral uterine artery
and utero-ovarian vessels combined with the double/multiple-flap method is associated
with significant advantages over the traditional form of double/multiple-flap surgery,
including reduced blood loss and no increase in operating times.
Disclosure Statement
The authors report no conflicts of relevant financial, personal, political, intellectual
or religious interests. The study was approved by the Ethics Committee of Jinhua Municipal
Central Hospital (ethics approval number: 2017-52).
Funding/Support Statement
Funding/Support Statement
This research received no specific grant from any funding agency in the public, commercial,
or not-for-profit sectors.
Author Contributions
MH conceived and designed this research study. DC, SZ, and MS acquired data. LJi,
LJin and MS analyzed and interpreted the data. LJi drafted the manuscript and MH revised
the manuscript.
