RETRACTED ARTICLE: Conservative laparoscopic electrocoagulation adenomyolysis for the management of symptomatic adenomyosis

The objective of the study was to assess the safety and efficacy of conservative laparoscopic electrocoagulation adenomyolysis (CLEA) in the management of women with symptomatic adenomyosis. The study design is prospective observational study. The setting was Department of Obstetrics and Gynecology, Mansoura University Hospital. Thirty-nine premenopausal women, complaining of chronic pelvic pain and/or menorrhagia, were diagnosed to have adenomyosis by transvaginal ultrasonography (TVS) and/or magnetic reso- nance imaging (MRI), between June 2008 and June 2011. They were subjected to laparoscopic multiple uterine unipolar electrocoagulation diathermy punctures aiming at adenomyolysis. Women were evaluated before and at 3, 6, and 12 months after the procedure. Main outcome is the mag- nitude of pain by using the visual analog scale (V AS) and the overall patient self satisfaction as assessed by short form 36 (SF-36) questionnaires; secondary outcome is the uterine vol- ume as measured by TVS. At 3-, 6-, and 12-month follow-up visits, there was a gradual, yet a significant, reduction in the median V AS scoring system of pain ( p<0.01), a significant improvement in every scale of the SF-36 (p<0.01), and also a significant reduction (p<0.01) in the median uterine volume as assessed by TVS. Conservative laparoscopic electrocoagulation adenomyolysis may be an effective and safer minimal invasive procedure for the management of symptomatic adenomyosis in premenopausal women.

Adenomyosis . Pain . Laparascopy . Adenomyolysis

Adenomyosis is a benign gynecological disease in which the endometrial stroma invades the uterine myometrium. Adenomyosis is divided into diffuse and localized forms ac- cording to the extent of the lesion. Localized adenomyosis is also known as adenomyoma [1]. The incidence of the disease varies between 5 and 70 %. Generally, it occurs in women aged between 40 and 50 years, with a prevalence rate of 70 –80 %. Adenomyosis was found in 23 % of uteri that were removed due to fibroids [ 2]. The etiology of this disease has not been clearly elucidated. However, several pathophysiological mechanisms have been proposed, such as damage of endometrial-myometrial border due to trauma and high estrogen biosynthesis associated with increased activities of aromatase enzyme [ 3]. The clinical manifestations include dysmenorrhea, chronic pelvic pain, and menorrhagia. It is usually combined with pelvic endome- triosis, endometrial cysts of the ovary, uterine fibroids, or oth- er estrogen-dependent diseases [4]. The diagnosis of adenomyosis was based on clinical symp- toms. In recent years, the development of imaging techniques has made diagnosis more accurate. It has been reported that the sensitivity of diagnosis by vaginal ultrasound was 80 – 86 % and the specificity was 74 –86 %. The sensitivity of magnetic resonance imaging (MRI) was 80 –86 % and the specificity was 74–86 % [ 5]. The myometrium has three distinct sonographic layers: the outer, middle, and inner layers. The middle layer is the most echogenic and is separated from the outer layer by the arcuate venous and arterial plexus. The inner layer (the * Adel Saad Helal [email protected] 1 Department of Obstetrics and Gynecology, Mansoura University, Mansoura, Egypt 2 Department of Diagnostic Radiology, Mansoura University, Mansoura, Egypt Gynecol Surg (2015) 12:139–147 DOI 10.1007/s10397-015-0890-8 RETRACTED ARTICLE subendometrial halo) is composed of longitudinal and circular closely packed smooth muscle fibers. The inner layer (archimyometrium or stratum subvasculare, e.g., the subendometrial halo) is hypoechogenic at transvaginal ultra- sonography (TVS) but at MRI, it is readily and more distinctly seen as a low-signal intensity (SI) band referred to as the JZ [6]. The sonographic findings of adenomyosis, best obtained by transvaginal sonography, include the following [7]: 1. Uterine enlargement—globular uterine enlargement that is generally up to 12 cm in uterine length and that is not explained by the presence of leiomyomata is a character- istic finding (Fig. 1). 2. Cystic anechoic spaces or lakes in the myometrium —the cystic anechoic spaces within the myometrium are vari- able in size and can occur throughout the myometrium. The cystic changes in the outer myometrium may on oc- casion represent small arcuate veins rather than adenomyomas. The application of color Doppler imaging at low velocity scales may help in this differentiation (Fig. 2). 3. Uterine wall thickening—the uterine wall thickening can show antero-posterior asymmetry, especially when the disease is focal (Fig. 3). 4. Subendometrial echogenic linear striations —invasion of the endometrial glands into the subendometrial tissue in- duces a hyperplastic reaction, which appears as echogenic linear striations fanning out from three endometrial layer (Fig. 4). 5. Heterogeneous echo texture—there is a lack of homoge- neity within the myometrium with evidence of architec- tural disturbance (Fig. 5). This finding has been shown to be the most predictive of adenomyosis. 6. Obscure endometrial/myometrial border—invasion of the myometrium by the glands also obscures the normally distinct endometrial/myometrial border (Fig. 6). 7. Thickening of the transition zone—this zone is a layer that appears as a hypoechoic halo surrounding the endometrial layer. A thickness of 12 mm or greater has been shown to be associated with adenomyosis. Doppler sonography may fac ilitate the differentiation between myomas and adenomyosis (Fig. 7). V essels around myomas produce a well-defined rim with a few vessels entering the body of the mass. In contrast, in adenomyosis, vessels follow their normal perpendicular course in myometrial areas [ 8]. Adenomyosis typically presents as either diffuse or focal thickening of the inner myometrium or an ill-defined myometrial nodule of low SI on MRI T2-WIs (Figs. 8, 9, and 10). In healthy women of reproductive age, the inner myometrium, which is also called the JZ, appears as the band of low SI between the endometrium of high SI and the outer myometrium of intermediate SI. Although adenomyosis can be readily suspected when it present as focal thickening of the JZ, diffuse thickening of the JZ should be carefully distin- guished from physiological change since the thickness of the JZ varies considerably during the menstrual cycle [ 9]. The JZ is generally widest and most clearly visible in the late secretory phase. Generally, a maximal thickness of the JZ (>12 mm) is highly predictive of the presence of adenomyosis, while a uterus with the JZ (12 mm during menstruation, especially on cycle days 1 and 2 in our experience (Fig. 11), MR examination during the men- strual phase should be avoided for evaluating adenomyosis [10]. The decreased SI on T2-WIs represents smooth muscle hyperplasia associated with ectopic endometrium. Occasion- ally, the islands of ectopic endometrial tissue can be demon- strated as punctate foci of high SI on T2-WIs (Fig.12a). When menstrual hemorrhage occurs within these ectopic endometri- al glands, cystically dilated glands are presented as foci of high SI on T1-WIs (Fig. 12b). Less commonly, benign inva- sion of the basal endometrium into the myometrium can man- ifest as Blinear striations^ of high SI radiating out from the Fig. 1 Globular uterine enlargement with an obscure endometrialmyometrial border (arrow) Fig. 2 The application of color Doppler imaging at low velocity scales 140 Gynecol Surg (2015) 12:139–147 RETRACTED ARTICLE endometrium on T2-WIs, resulting in Bpseudowidening^ of the endometrium (Fig. 13)[ 11]. V a r i a t i o ni nM Rf e a t u r e so fa d e n o m y o s i s Adenomyoma Adenomyoma is a localized and well-circumscribed form of adenomyosis. Recognition of this entity is of clinical impor- tance because adenomyomas are frequently confused with leiomyomas, not only on MRI but also at pathological exam- ination. On MRI, myometrial adenomyomas typically exhibit low SI on T2-WIs, which may closely simulate leiomyoma. When the lesion is accompanied by hyperintense foci representing ectopic endometrium on T2-WIs, MRI can allow correct diagnosis of this entity (Fig. 14). Unlike the ordinary form of adenomyosis, myometrial adenomyoma can be treat- ed surgically with myomectomy [12]. Adenomyomatous polyp (polypoid adenomyoma) Adenomyomatous polyp (polypoid adenomyoma) presents as a pedunculated or sessile polypoid mass in the lower uterine endometrium or endocervix, and accounts for about (2 %) of all endometrial polyps. It typically affects premenopausal women, presenting as abnormal genital bleeding. On MRI, the lesion typically presents as a hypointense polypoid mass representing myometrial tissue, associated with hyperintense foci on T2-WIs. The recognition of the attachment site of the polypoid lesion and the typical signal pattern on MRI may allow preoperative diagnosis of polypoid adenomyoma. Atyp- ical polypoid adenomyoma is a rare variant of a polypoid adenomyoma, microscopically characterized by architectural and cytologic atypia. MR findings are similar to those an ordinary polypoid adenomyoma and may reveal a hemorrhag- ic cyst within the lesion (Fig. 15)[ 10]. Adenomyotic cyst (cystic adenomyosis) Adenomyotic cyst is a rare variant of adenomyosis character- ized by the presence of a large hemorrhagic cyst resulting from extensive menstrual bleeding in the ectopic endometrial gland. The lesion can be entirely within the myometrial, sub- mucosal, or subserosal tissue. On MRI, fluid content exhibits high SI on T1-WIs, and the surrounding solid wall exhibits a distinct low SI on T2-WIs (Fig. 16). Occasionally, the solid wall may consist of an inner zone of low SI that resembles a JZ and an outer zone of a relatively increased intensity; an adenomyoma with this finding can be called a Bminiature uterus^ [10]. Different strategies for the management of adenomyosis have been tried [ 13]; for patients who prefer conservative measures, medical therapy may be the least invasive and most acceptable strategy and includes the use of prostaglandin in- hibitors, oral contraceptive pills, progestogens, danazol, Fig. 3 Uterine wall thickening which shows antero-posterior asymmetry Fig. 4 Subendometrial echogenic linear striations Fig. 5 Heterogeneous echo texture Fig. 6 Obscure endometrial/myometrial border Gynecol Surg (2015) 12:139–147 141 RETRACTED ARTICLE gestrinone, and gonadotropin-releasing hormone (GnRH) ag- onists. Unfortunately, the effect of these medical treatments is often transient, and the symptoms (especially pain) usually reappear after discontinuing medication [14]. The surgical approach for preserving the uterus can be con- sidered when dysmenorrhea does not respond to drug treat- ment; these include excision of the myometrial adenomyoma through a laparotomy. Less invasive conservative surgical ap- proaches, including endomyometrial ablation, laparoscopic myometrial electrocoagulation, and laparoscopic surgery, have been attempted [15]. All conservative surgical treatments Fig. 7 a , b Doppler sonography may facilitate the differentiation between myomas and adenomyosis Fig. 8 Adenomyosis presenting as diffuse thickening of the JZ. MRI Sagittal T2-WI shows an enlarged uterus with diffusely thickened JZ which measures >12 mm in thickness Fig. 9 Adenomyosis presenting as focal thickening of the JZ. MRI Sagittal T2-WI shows focal thickening of the JZ in the posterior wall of the uterus (arrows) 142 Gynecol Surg (2015) 12:139–147 RETRACTED ARTICLE have proven effective in up to 50 % of patients; however, the follow-up assessment periods have been of short duration [16]. The conventional and definitive management of symptom- atic adenomyosis is hysterectomy [ 17]. Phillips et al. [ 18] studied laparoscopic bipolar coagulation for conservative treatment of adenomyomata with preoperative GnRH analog and concluded that further evaluation of this technique is nec- essary to determine its definitive role. Wood’ss t u d y[ 16] showed that endometrial ablation, myometrial electrocoagulation, or laparoscopic excision were effective in >50 % of patients. Laparoscopic resection versus myolysis in the management of symptomatic uterine adenomyosis was also studied before [ 2]; no significant dif- ferences were found in the median reduction of menorrhagia and dysmenorrhea scores between the resection and the myolysis groups. Patients and methods This study included 39 women admitted to the Department of Obstetrics and Gynecology, Mansoura University Hospital, between June 2008 and June 2011. They complained of chronic pelvic pain and/or menorrhagia with a provisional diagnosis of adenomyosis. The inclusion criteria included pre- menopausal women (40–50 years), who had completed their families and were not willing to undergo hysterectomy; other pelvic pathology was excluded. Diagnosis of adenomyosis was established by TVS, color Doppler, and MRI. Laparosco- py was decided, and the intended procedure was explained; a written consent was signed by the patient and her husband. Also, the procedure was approved by Mansoura Medical Eth- ical Committee. Usual preoperative investigations and prepa- rations including 400μg prostaglandin E1 analog, misoprostol (Misotac Sigma) per rectum were immediately placed before laparoscopy. Laparoscopy was performed under general anes- thesia in the neutral-lithotomy position. Patients were cathe- terized and vaginally prepared, and uterine manipulator was inserted. Pneumo-peritoneum was done with V eress needle through the umblicus. For the primary puncture, 10-mm port was inserted through the umblical incision with a video lapa- roscope introduced. For the second puncture, 5-mm port was placed laterally on Pfannenstiel line for uterine manipulation. For the third puncture, 5-mm port was inserted in the middle of Pfannenstiel line for adenomyolysis diathermy needle. A unipolar diathermy needle was introduced for puncture and cauterization of the anterior and posterior uterine wall, as well as the fundus. An average of 6 –10 punctures was placed through the anterior uterine wall and 4 –6 punctures for the fundus; the latter was brought perpendicular to the needle axis by extreme anteflexion by an instrument through second port. The posterior wall was approached perpendicularly by the diathermy needle introduced in a 5-mm reducer through the primary port, and the procedure was monitored by 5-mm scope through the suprapubic incision (changing entry) and 6–10 punctures were done in posterior wall. The needle punc- tures were 1 –2 cm using 100-W current; the depth of punc- tures was about 10 –15 mm; saline wash was done. Finally, intaperitoneal drain was left in place for 24 h. Women were advised to use condoms for contraception, to avoid the effects of hormonal therapy and the intra uterine device. Patients were followed up at 3, 6, and 12 months. At each visit, patients were evaluated as regards (a) chronic pelvic pain, which was assessed by the visual analog score (V AS), (b) quality of life scales which was assessed by the short form 36 (SF-36), and (c) the uterine volume which was evaluated by TVS. Fig. 10 Diffuse adenomyosis presenting as an ill-defined myometrial mass. MRI Sagittal T2-WI shows a diffusely enlarged uterus with indis- tinct zonal anatomy. There is an ill-defined mass of decreased SI in the myometrium of the anterior wall and the fundus Fig. 11 JZ can frequently show thickness of >12 mm during Gynecol Surg (2015) 12:139–147 143 RETRACTED ARTICLE Statistical analysis used SPSS (version 11) with median values and SD, and Student ’s t test was used to compare be- tween preoperative and follow-up visits. The difference was considered significant when p value was less than 0.05.

The magnitude of pelvic pain was significantly improved (p<0.01), following the procedure and at 3, 6, and 12 months as assessed by the visual analog score as given in Table1.T h e quality of life scores showed significant improvement as assessed by the SF-36 scores. By 12 months following the procedure, a significant improvement was observed in each item of the SF-36 scores ( p<0.01) as given in Table 2. The uterine volume as assessed by transvaginal ultrasound showed a gradual, yet a significant, reduction in the mean Fig. 12 a The islands of ectopic endometrial tissue can be demonstrated as punctate foci of high SI and b when menstrual haemorrhage occurs within ectopic endometrial glands, cystically dilated glands are presented as foci of high SI on T1- WIs Fig. 13 a , b Benign invasion of the basal endometrium into the myometrium can manifest as Blinear striations^ of high SI radiating out from the endometrium on T2-WIs, resulting in Bpseudowidening^ of the endometrium Fig. 14 When the lesion is accompanied by hyperintense foci representing ectopic endometrium on T2-WIs, MRI can allow correct diagnosis of this entity 144 Gynecol Surg (2015) 12:139–147 RETRACTED ARTICLE uterine volume with an average reduction of volume by 43 % at 12 months following the procedure ( p<0.01) as given in Table 3. The procedure was not associated with significant complication apart from any routine laparoscopic procedure. Patients’ requirements for analgesics were comparable to any routine laparoscopic procedure.

This study includes 39 women with symptomatic adenomyosis aged between 40 and 50 years who were sub- jected to conservative laparoscopic adenomyolysis from the period of June 2008 to June 2011, as shown in Fig. 1.A n d they were followed up for 12 months. Many patients in such an age group especially in early 1940s may prefer a rather minimally invasive technique to improve their symptoms. Hysterectomy, as a standard surgical procedure for the management of symptomatic adenomyosis, may not be an accepted modality option by many premenopausal women. Simple random unipolar electrocauterization of adenomyotic uteri was tried in this study, assuming that necrosis of adenomyotic implants will improve the symptoms. Main findings A recoded significant improvement at 3-, 6-, and 12-month follow-up include the severity of pain as assessed by the V AS as well as the quality of life as assessed by SF-36 scores following conservative laparoscopic electrocoagulation adenomyolysis (CLEA) procedure as given in Tables 1 and 2. Also, the assessment of the uterine volume by TVS revealed a significant reduction, average 43 %, by the end of 1 year as given in Table 3 as a secondary outcome. There were no re- corded significant complications following the procedure. Fig. 15 a , b Haemorrhagic cyst within the lesion Fig. 16 a , b On MRI, fluid content exhibits high SI on T1- WIs and the surrounding solid wall exhibits a distinct low SI on T2-WIs Gynecol Surg (2015) 12:139–147 145 RETRACTED ARTICLE Strength and limitations Small sample size represents the main limitation in this study as the use of unipolar diathermy was the first trial and also no preceding adjuvant medical treatment. Interpretation The use of unipolar diathermy needle in our study was intended to ensure better speed of current through the tissues, rather than the use of bipolar needle. The latter was tried by others [ 2, 18], on a smaller number of cases. In these studies, either pre- or postoperative ad- juvant GnRH therapy was us ed. In this study, CLEA was attempted only with no added adjuvant medical treatment. Two unplanned pregnancies occurred in this series within the follow-up period. One pregnancy end- ed in a spontaneous miscarriage at 8 weeks, and the other pregnancy continued with no adverse effects up to 38 weeks and the baby was born by an elective cesarean section; a healthy baby weighing 3 kg was born (data not shown).

Laparoscopic electrocoagulation adenomyolysis is recom- mended as an effective and safer minimal invasive procedure for the management of symptomatic adenomyosis. Y et, more studies and larger number of patients are recom- mended to assess the effectiveness and side effects of this procedure. Acknowledgments The authors thank all the staff members in the De- partment of Obstetrics and Gynecology, the operating room staff mem- bers, and all the patients who shared information and experiences in this research. This research is approved by local ethical research committee of Mansoura University, Faculty of Medicine on May 2008. Conflict of interest There is no conflict of interest in this work. Funding None. Authors’ contributions Hossam abd elfatah, Nasser Allakany, and Adel Saad Helal made the design and did the operations. Alaa mesbah performed the preoperative and postoperative TVS evaluation of all pa- tients. Mahmoud abd elshahied did the preoperative and postoperative Doppler study of all patients. Elsaid M. Abd elhady wrote the paper and helped in statistical analysis.

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