Conservative surgery of diffuse adenomyosis with TOUA: Single surgeon experience of one hundred sixteen cases and report of fertility outcomes

Abstract

The aim of this study is to evaluate the clinical outcomes of conservative adenomyomectomy with TOUA for diffuse uterine adenomyosis and to determine the feasibility and safety. One hundred and sixteen patients with symptomatic diffuse uterine adenomyosis underwent adenomyomectomy with TOUA by a single surgeon at Ulsan University Hospital between May 2011 and March 2016. Surgical outcomes included operative time, intraoperative injury and operative blood loss. We assessed the degree of improvement in dysmenorrhea and menorrhagia at the 7‐month follow‐up visit after the operation. The mean age of patients was 37.49 years (range: 26–49). The mean total surgical time was 116.12 min (range: 60–300, SD: 37.27). The mean estimated blood loss was 207.22 mL (range: 30–1200, SD: 161.08) and there were no cases of injury to the uterine arteries or pelvic nerves. The mean duration of hospital stay was 5.05 days (range: 4–7, SD: 0.68) and the mean follow‐up period of 16.67 months (range: 6–49, SD: 12.77). At the 7‐month follow‐up after adenomyomectomy with TOUA, dysmenorrhea and menorrhagia were improved in 100% and 89% of the patients, respectively. In patients with diffuse uterine adenomyosis, even when the whole uterus is involved, for relief of severe adenomyosis‐related symptoms, adenomyomectomy with TOUA could be a safe and effective surgical treatment option for those who want to preserve their fertility.

Introduction

Adenomyosis is defined as the presence of endometrial tissue within the myometrium. According to the extent of adenomyosis, it can be classified into the “focal type” or the “diffuse type”. Diffuse type is defined as uterine adenomyosis involving the whole uterine myometrium or more than half of the total uterine myometrium. Unlike focal localized adenomyosis (adenomyoma), diffuse uterine adenomyosis causes more severe menstrual symptoms and there are several limitations in the surgical or medical treatment of this disease entity.

Recent concerns have been raised over conservative surgical treatment by the patients with adenomyosis who want to preserve fertility and the surgeons who are trying to find a way to preserve the uterus during the treatment of benign uterine diseases. This trend of conservative surgery for the treatment of adenomyosis has been gradually increasing [[1], [2], [3], [4]]. However, there are only a few reports on conservative surgical treatment of focal localized adenomyosis, adenomyoma, and they are especially rare in the group of patients with pure diffuse adenomyosis [2].

There are several limitations and problems in the medical treatment of diffuse uterine adenomyosis because some cases are refractory to medical treatment: hormonal pills or intrauterine device and symptomatic relief medication, NSAIDs. However, in order to preserve fertility, it is difficult to perform conservative surgical treatment without any intra‐operative or postoperative complications because unlike uterine leiomyoma, adenomyosis does not have an obscure boundary with normal myometrium and there are many small vessels within the adenomyotic lesion which can cause profuse bleeding. Also, there may be a high rate of transfusion during the intra‐operative or post‐operative period and conversion to hysterectomy during conservative surgery. Moreover, depending on the extent of the excised lesion and completion of uteroplasty, there may be a possibility of uterine rupture during pregnancy.

In this work, to determine the safety and efficacy of conservative surgical treatment in patients with diffuse uterine adenomyosis we present one hundred and sixteen patients who underwent diffuse adenomyomectomy with TOUA by a single surgeon at Ulsan University Hospital in Ulsan, South Korea.

Methods

From May 2011 to March 2016, 116 patients undergoing laparotomic diffuse adenomyomectomy with, transient occlusion of uterine arteries (TOUA) were enrolled in this study. The patients were selected consecutively. The inclusion criteria for extensive adenomyomectomy with TOUA included patients who had symptomatic diffuse uterine adenomyosis (ranging from a maximal diameter ≥5.0 cm or involvement of more than half of the uterine body to involvement of the whole uterine myometrium in a longitudinal view of uterus by ultrasonography) diagnosed by ultrasonographic examination or pelvic magnetic resonance imaging (MRI), adenomyosis refractory to conservative medical treatment, and patients who had a strong desire for preservation of the uterus. Patients with focally localized adenomyosis or uterine adenomyoma were excluded from this study. Patients in whom the postoperative pathology report did not confirm adenomyosis were also excluded.

The operating time was defined as the period from skin incision to closure; the size of adenomyosis was defined as the maximal diameter of adenomyosis on ultrasonography or MRI; the weight of adenomyosis lesion was defined as the total weight of the excised lesion (only in the latest cases); the operative blood loss was estimated by subtracting the rinse volume from the blood volume that was collected in the suction apparatus. Three cycles of adjuvant gonadotropin‐releasing hormone agonist (GnRHa) were injected subcutaneously at a monthly interval after the operation. In all cases of the current study, adenomyomectomy with TOUA was performed by a single surgeon, Y. S. Kwon. This study was approved by the Institutional Review Board of the Ulsan University Hospital.

Surgical technique

Detailed description of the surgical technique of extensive adenomyomectomy with TOUA has been mentioned in the previously published report “Conservative adenomyomectomy with transient occlusion of uterine arteries for diffuse uterine adenomyosis” by Yong‐Soon Kwon et al. [2]. In all cases, we applied TOUA, transient occlusion of uterine arteries for achieving bleeding control during the surgery with TOUA using vascular clips. The uterus with diffuse adenomyosis was bisected perpendicular to the axis with a scalpel and opened the endometrial cavity. With preservation of a minimal 5‐mm depth of outer and inner surface of adenomyotic myometrium and endometrium the endometrial lining was approximated with interrupted sutures. Defect of myometrium was sutured with out‐in‐out fashion and serosa surface is approximated with interrupted sutures.

At the 7‐month follow‐up, we assessed the improvement in symptoms, including dysmenorrhea and menorrhagia, by administering standardized questionnaires and we performed transvaginal ultrasonography to monitor recurrence in the imaging study. The questionnaire with a focus on specific pelvic symptoms included items to evaluate the severity of dysmenorrhea and menorrhagia. The questionnaire was completed during a simple, clinical interview. A visual analog scale was used ranging from no pain (0 cm) to the worst possible pain (10 cm) to evaluate the intensity of pain during menstruation. The Mansfield–Voda–Jorgensen menstrual bleeding scale (MVJ) was used to evaluate menorrhagia. This is a subjective Likert‐type scale from 1 (spotting) to 6 (very heavy bleeding or gushing). Complete remission (CR) of dysmenorrhea was defined as 0 on the VAS scale and CR of menorrhagia was defined as 2–3 on the MVJ scale at 7 months after adenomyomectomy with TOUA. Partial remission (PR) was defined as >50% improvement in symptoms at 7 months after adenomyomectomy with TOUA.

Transvaginal sonography was performed by the same physician, who was not involved in this study, before and after surgery, and the sonographer was blinded to preoperative ultrasonographic findings. The maximum diameter of the adenomyotic lesion was used for analysis. The criteria for assessing recurrence were increment in the size of the residual lesion or development of new lesions as detected by ultrasonography during the follow‐up period. SPSS was used for the statistical analysis. Data are expressed as mean ± standard deviation (SD) or absolute number (%).

Results

From May 2011 to March 2016, 116 patients with symptomatic diffuse uterine adenomyosis, who were refractory to medical treatments and who had a strong desire for preservation of the uterus, were enrolled. All patients underwent laparotomic adenomyomectomy with TOUA by a single surgeon (Y. S. K.). The mean age was 37.49 years (range, 26–49 years). The major site of adenomyosis was the posterior uterine body (44.0%), and the most common symptom associated with uterine adenomyosis was dysmenorrhea combined with menorrhagia (59.5%) (Table 1). The mean maximal diameter of uterine adenomyosis was 6.48 cm (range = 5–15 cm, SD = 2.15) and the mean weight of the excised adenomyotic lesion was 108.29 g (range, 10–610 g, SD = 107.12). In all of the cases, the pathology reports confirmed adenomyosis. The mean total surgical time was 116.12 min (range = 60–300 min, SD = 37.27). The mean estimated blood loss was 207.22 mL (range = 30–1200 mL, SD = 161.08), and there were no cases of injury to the uterine arteries or pelvic nerves. The mean time of TOUA was 5.73 min (range = 3–10 min, SD = 1.29). The mean duration of hospital stay was 5.05 days (range, 4–7 days; SD, 0.68) (Table 2). There were no major complications requiring reoperation or readmission during the mean follow‐up period of 16.67 months (range = 6–49 months, SD = 12.77).

Table 1.

Clinical characteristics of the patients (n = 116).

Age (years)	37.49 ± 4.73 (26–49)
Main site of adenomyosis
Anterior body of uterus	19 (16.4%)
Posterior body of uterus	51 (44.0%)
Fundal portion of uterus	8 (6.9%)
Whole uterus	38 (32.8%)
Main symptom
Dysmenorrhea	36 (31.0%)
Menorrhagia	10 (8.6%)
Combined	69 (59.5%)
Others	1 (0.9%)

Data are mean ± standard deviation (range) or absolute number (%). Combined, mixed symptoms of menorrhagia and dysmenorrhea.

Table 2.

Surgical outcomes of adenomyomectomy with transient occlusion of uterine arteries.

N = 116	Mean	Range	Standard deviation
Maximal diameter (cm)	6.48	5–15	2.15
Weight (gram) (n = 38)	108.29	10–610	107.12
Operation time (min)	116.12	60–300	37.27
Estimated blood loss (mL)	207.22	30–1200	161.08
Preoperative Hb (g/dL)	11.42	7.8–15.0	1.52
Postoperative 1 day Hb	9.54	6.1–13.7	1.45
Transfusion with Pack RBC (pints) (n = 52/116, 44.8%)	1.41	1–16	2.02
TOUA time (min)	5.73	3–10	1.29
Hospital staying (days)	5.05	4–7	0.68

EBL, estimated blood loss; Hb, hemoglobin; Maximal diameter, maximal diameter of uterine adenomyoma; Time of TOUA, from the time of incision of serosa of right adnexa to the time of occlusion of left uterine artery; TOUA, transient occlusion of uterine arteries.

At the 7‐month follow‐up after adenomyomectomy with TOUA, the main symptoms, dysmenorrhea and menorrhagia, were improved. Total response rate of dysmenorrhea was 100%, complete remission rate of dysmenorrhea was 98% and partial remission rate was 15.5%, respectively. The response rate of menorrhagia was 89%, respectively. Six of the 116 patients showed a remnant or recurrent adenomyotic lesion which was more than 1.0 cm in the maximum diameter by ultrasonography without aggravation of symptoms and two of the 116 patients complained of aggravation of symptoms although they did not have a definite lesion on ultrasonography. Two of the 116 patients had both recurrent lesion and aggravation of symptoms. Total recurrence rate was 8.6% (10 of 116 patients). One of the ten patients with recurrence received hysterectomy because of recurrence, and in the other patients, medical treatment was restarted to control their symptoms (Table 3).

Table 3.

Symptom follow‐up 7 months after adenomyomectomy with transient occlusion of uterine arteries (TOUA).

N = 116	Laparotomic adenomyomectomy with TOUA
Follow‐up period (month)	16.67 (6–49, SD = 12.77)
Symptom improvement a	CR	PR	SD
Dysmenorrhea (%)	98 (84.5%)	18 (15.5%)	0 (0)
Menorrhagia (%)	52 (44.83%)	53 (45.69%)	11 (9.48)
Relapse rate	10/116 (8.62%)
Period until relapse (month)	17.4 ± 9.57
Only symptomatic	2
Only sonographic	6
Symptomatic and sonographic	2
Eventual Hysterectomy	1 b
Complication	1 c

Data are expressed as mean ± standard deviation or absolute numbers (%).

^aComplete remission (CR) of dysmenorrhea was defined as 0 on the NRS scale and CR of menorrhagia was defined as 2–3 on the MVJ scale at 7 months after the adenomyomectomy with TOUA. Partial remission (PR) was defined as >50% improvement in symptoms at 7 months after the adenomyomectomy with TOUA. Dysmenorrhea was checked by a visual analog scale was used ranging from no pain (0 cm) to the worst possible pain (10 cm).

^bThe patient received laparotomy hysterectomy 31 month later after adenomyomectomy because of recurrence.

^cSmall bowel perforation.

Eleven out of the 116 patients had tried assisted reproductive technique, such as intrauterine insemination or in vitro fertilization, and among these 11 patients, five were successful in becoming pregnant. Number of cases of natural conception was five and total ten patients conceived. Three patients were diagnosed with missed abortion in the early gestational age. Seven of the ten patients who had become pregnant delivered at a mean 36 + 0 weeks gestational age via the cesarean delivery mode without any uterine rupture during pregnancy and one of them had a twin delivery (Table 4).

Table 4.

Pregnancy and complications after adenomyomectomy of diffuse adenomyosis.

Conception	10
Conception by natural	5/116
Conception by ART	5/11
Number of patients with trying of ART	11/116
Mean number of ART	1.9 (1–3)
Missed abortion	3
Delivery (Cesarean delivery in all cases)	7
Mean gestational age	36 + 0 wks
Number of uterine rupture during pregnancy	0

Abbreviation: ART, Artificial reproductive technology.

One patient on pregnancy; no data of delivery.

One of the six patient with delivery; twin pregnancy.

Discussion

Recently, conservative adenomyomectomy in patients with symptomatic uterine adenomyosis has become a topic of interest with respect to preservation of fertility to maintain fecundity and the patient's cultural desire. The aims of conservative surgical treatment of diffuse adenomyosis are fertility preservation, relief of severe menstrual symptoms during the patient's life without medication, and improvement in the stability of the patient's mind such that she preserves not only her uterus but also her femininity, especially Asian women.

However, there are few reports supporting the use of conservative surgical adenomyomectomy and the number of cases that underwent adenomyomectomy was insufficient for clinical analysis of efficacy, safety, clinical outcomes, and pregnancy‐related outcomes of adenomyomectomy via laparoscopy or laparotomy [[1], [2], [3], [4], [5], [6], [7], [8], [9]]. Especially, there are extremely rare reports supporting conservative surgical adenomyomectomy in patients with diffuse uterine adenomyosis that invades more than half of the total uterine myometrium or involves the whole uterus [2].

The strength of this study is that all operations were performed by a single surgeon, Y.S. Kwon, with use of a uniform surgical technique; hence, we can analyze the surgical outcomes related to pregnancy. As mentioned above, although there were a small number of patients who tried ART, six cesarean deliveries were achieved at a mean 36 weeks gestational age without uterine rupture, uterine atony complications after expulsion of placenta, and placental complications such as placenta accreta.

Although we achieved good outcomes, more cases of pregnancies and deliveries in patients who undergo extensive adenomyomectomy with TOUA are required to determine the safety and to identify the risk factors related to complicated pregnancy in patients who receive adenomyomectomy for diffuse type adenomyosis.

In extensive adenomyomectomy, an expert surgeon who has sufficient skillful experience is needed to avoid major intra‐operative complications and to guarantee good progress in recovery after the operation. Prognosis would be related to pregnancy outcomes, which are evaluated as fecundity, uterine rupture during pregnancy, term of delivery and other obstetric complications. Also, a surgeon needs to have practice to achieve shortened operation time without any major intra‐operative complication or heavy bleeding. In the current study, repeated learning regarding the adenomyomectomy operation helped the single surgeon, to improve himself in terms of surgical skill to shorten the operation time and completeness of uteroplasty after excision of the adenomyotic lesion in patients with uterine adenomyosis in diverse sizes (range = 5–15 cm, maximal diameter of the lesion). In the previously published reports [[1], [2], [10], [11]], we introduced that TOUA is a good technical method to reduce intra‐operative bleeding and to maintain a clean operation field until completion of the uterine operation. In conservative surgical adenomyomectomy for diffuse adenomyosis and an enlarged uterus, an intra‐operative bleeding control technique like TOUA is very important to increase the efficiency of the operation. In the study, patients who underwent adenomyomectomy with TOUA showed much less blood loss during the operation, mean EBL = 207.22 mL, when compared with that in previously reported studies [[2], [3], [12]].

Compared with the previously published report, after we collected more cases, several differences were observed in surgical outcomes and clinical outcomes. First, the operation time was shortened because the surgeon had learned the surgical technique and performance of the operation during a period of approximately five years. Also, a more safe operation with uniform uteroplasty after the excisional procedure gradually resulted in less intra‐operative bleeding. In terms of clinical outcomes, the recurrence rate was reduced from 11.5% in the previous report to 8.62% [2].

To detect recurrence of uterine adenomyosis after conservative surgical treatment, attention should be focused on a newly developed mass and the increase in size of the existing lesion in the uterus. Also, relapse of symptoms is important to determine the clinical significance of recurrence after conservative surgical treatment. Six patients had a suspicious recurrent lesion that was increased in size but they did not have relapse of symptoms. All these patients are now undergoing their follow‐up without medication for adenomyosis. We suggest that the definition and diagnostic criteria for recurrence after adenomyomectomy must be considered not only for a visible lesion but also for the patient's symptom during a long‐term outpatient follow‐up.

In this study, eleven of the total 116 patients after extensive adenomyomectomy had tried ART (assisted reproductive technology) and the mean number of ART was 1.9 attempts. The percentage of patients who tried ART was only 9.48%. The percentage of patients who tried ART was relatively low and this can be explained by several reasons; unmarried women have a large proportion of diffuse uterine adenomyosis compared to focal uterine adenomyoma. In Asian countries, especially, Korea, there is a trend of low birth rate owing to lack of social and economic support for women. However, most patients who did not try to become pregnant were satisfied with relief of menstrual symptoms, which had disrupted their quality of life.

Ovarian function could be strongly related to the postoperative status after adenomyomectomy. Uterine arterial flow passing through the myometrium supplies the ovary, and it accounts for approximately 95% of the ovarian blood flow. To avoid premature ovarian failure after uterine surgery, it is very important to maintain the uterine artery blood flow to the ovary after the uterine operation [[13], [14]]. In our experience, there were extremely rare cases of premature ovarian failure because of restoration of uterine blood flow to the ovary through the TOUA technique [11]. A surgeon should avoid causing injury to the ascending uterine artery when excision of the adenomyotic lesion is performed at the lateral border of the uterine body.

In the future, to achieve safer pregnancy‐related outcomes and low recurrence rate, an accurate and detailed analysis of diverse factors that affect the surgical technique is needed, with more cases of extensive adenomyomectomy performed by different surgeons using diverse surgical techniques.

In conclusion, conservative adenomyomectomy with TOUA is a safe and effective therapeutic method for conservative treatment of patients with diffuse uterine adenomyosis who want to preserve their fertility along with obtaining relief of menstrual symptoms. To determine the safety and clinical outcomes of pregnancy and delivery in patients who received extensive adenomyomectomy with TOUA, an additional analysis is required.

Supporting information

Supplementary data

Supplementary data

Supplementary data related to this article can be found at https://doi.org/10.1016/j.kjms.2017.12.008.