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* Diagnosis, laparoscopic management, and histopathologic findings of juvenile cystic adenomyoma: a review of nine cases Hiroyuki Takeuchi, M.D.[image: Corresponding Author Information][image: email address] , Mari Kitade, M.D., Iwaho Kikuchi, M.D., Jun Kumakiri, M.D., Keiji Kuroda, M.D.,Makoto Jinushi, M.D. Received 1 May 2008; received in revised form 27 April 2009; accepted 7 May 2009. published online 19 June 2009. Objective To define diagnostic criteria for juvenile cystic adenomyoma (JCA), describe the histologic features of the condition and evaluate laparoscopic excision for treating associated dysmenorrhea and pelvic pain. Design Prospective long-term follow-up study. Setting University-affiliated hospital. Patient(s) Nine consecutive patients with JCA. Intervention(s) Patients meeting the diagnostic criteria for JCA underwent laparoscopic enucleation of the lesion. The severity of dysmenorrhea was evaluated before surgery and every 6 months after surgery. Five patients underwent second-look laparoscopy (SLL) 6 months after surgery. Main Outcome Measure(s) Relief of dysmenorrhea as measured by a visual analog scale, postoperative healing at SLL, and subsequent pregnancy when desired by the patient. Result(s) Laparoscopic enucleation of the cystic adenomyoma resulted in a statistically and clinically significant reduction in dysmenorrhea and improved chronic pelvic pain. Neither cystic adenomyoma nor severe dysmenorrhea recurred during the follow-up period. Adhesions were minimal at SLL. Two of the three patients who desired pregnancy conceived after surgery. The histologic findings of the JCA lesion and adenomyosis were similar, and the endometrial glands and stroma infiltrating the surrounding myometrium in all patients were consistent with the appearance of adenomyosis. Conclusion(s) We defined the diagnostic criteria for JCA, and demonstrated significant improvement of dysmenorrhea after laparoscopic excision of the lesion. Key Words: Cystic adenomyoma , laparoscopy , cystic lesion , uterus , cystic adenomyosis , Medline search , adolescent ,congenital Article Outline • Abstract • Materials and methods • Laparoscopic Procedure • Statistical Analysis • Results • Symptoms () • Diagnostic Studies for JCA • Surgical Results • Pathologic Findings • Postoperative Course • Discussion • Diagnostic Criteria for JCA • Diagnosis of JCA • Therapeutic Options for JCA • Laparoscopic Surgery • Clinical Misnomenclature Without Reference to Pathological Terminology • Problems With Current Medline Search for JCA • Pathogenesis • Conclusion • Acknowledgment • References • Copyright Most uterine tumors are solid, and large cystic lesions are quite rare. The introduction of novel magnetic resonance imaging (MRI) devices that can clearly resolve soft tissue lesions has allowed visualization of even small cystic lesions of the uterus 1 , 2 , 3 . Most uterine cysts visualized by MRI are considered to represent small bleeds into the myometrium because of uterine adenomyosis, and they are usually ≤5 mm in diameter(1) . In 1996, Tamura et al. (4) described juvenile adenomyotic cyst of the corpus uteri in a 16-year-old girl manifesting as a cystic lesion measuring 15 mm in diameter and independent of the normal uterine lumen. The girl complained of severe dysmenorrhea that had started 3 years after menarche. Since then, 30 patients, including those that we described, have been reported, and they can be found by a Medline search of Japanese-language publications (Ichushi) using the term “cystic adenomyoma.” Cases are also often presented at Japanese academic meetings. Thus, the pathologic features of this type of cystic lesion have become widely recognized in Japan as cystic adenomyoma. After reviewing the information available from patients described in Japan, we established a diagnosis of juvenile cystic adenomyoma (JCA) in the nine patients described here, based on the following diagnostic criteria: 1) age ≤30 years; 2) cystic lesion of ≥1 cm in diameter independent of the uterine lumen and covered by hypertrophic myometrium on diagnostic images; and 3) associated with severe dysmenorrhea. The most important differential diagnosis for JCA is an obstructive uterine anomaly associated with severe dysmenorrhea. The most important differentiating characteristic between the two conditions is that JCA is a cystic lesion that is independent of the normal uterine lumen, whereas in obstructive uterine anomaly, such as double uterus with a noncommunicating horn and various other lower genitourinary tract obstructions, there is liquefied blood present within the uterine lumen or upper vagina. Because JCA has not been clearly defined, it has been referred to as adenomyotic cyst 4 , 5 and as cystic adenomyoma 6 , 7 , 8 . The pathogenesis of the disease also remains unclear. The key words “cystic adenomyoma and uterus” and “adenomyotic cyst and uterus” have been cited in fifteen and two English publications, respectively, in Medline. Seven articles that apparently described polypoid adenomyoma of the uterus and three explaining the imaging findings were excluded. An investigative review revealed that the described pathology was consistent with JCA in five articles published in Japan 4 , 5 , 6 , 7 , 9 , one in China (8), and one in the United States (10). A review of the back issues ofFertility and Sterility from 1998 through 2007 uncovered three articles on JCA 8 , 11 , 12 . Only one of these, which discussed cornual pregnancy(8), was included among the articles uncovered by a Medline search, and the other two 11 , 12 , both from the U.S., could not be found in Medline. Thus, JCA remains a rather confusing disease or syndrome. Enucleation similar to laparoscopic myomectomy was performed in nine patients treated at our department between 2000 and 2007, and tissue samples collected at surgery were histopathologically examined. The primary objectives of the present study were to examine the relevance of laparoscopic enucleation of JCA based on data from second-look laparoscopy (SLL) and long-term follow-up. The secondary objectives were to clarify the disease concept of JCA, examine the problems associated with the diagnosis/treatment of this disease, and discuss its pathogenesis. Materials and methods [image: return to Article Outline] We enrolled nine consecutive patients with cystic adenomyoma, diagnosed with JCA according to our proposed criteria, at our hospital between 2000 and 2007. Each of them provided written informed consent to undergo laparoscopic tumor enucleation at our department (Table 1), and the Ethics Committee of Juntendo University approved the study protocol. Cystic adenomyoma was diagnosed by transvaginal ultrasonography (TVUS) and MRI (Fig. 1). Associated urogenital anomalies were checked using intravenous pyelography (IP). Four of the patients with steady partners underwent hysterosalpingography (HSG). Table 1. Patients' characteristics. Case no. Age (y) G P PP DP SOM (y) ICS (mm) OCS (mm) CA-125 (U/mL) OC GnRHa 1 30 0 0Y 0 7 23 35 43 2 29 0 0Y Y 9 15 30 141 3 27 2 2N Y 13 19 42 36 42000 Y 0 4 15 28 551Y 5 30 2 2N N 4 15 30 34 6 28 0 0N Y 13 19 25 12Y Y 7 23 00 Y 0 3 18 28 157Y 8 20 0 0Y 0 1 10.5 34 34 Y 9 20 0 0Y 0 5 16 34 14 Y Mean25.2 6.616.731.8113.6 SD 4.4 4.3 3.5 5.1 172.4 Note: DP = dyspareunia (0 = no experience of intercourse); G = gravidity; GnRHa = GnRH agonist; ICS = inner cyst size; P = parity; PP = pelvic pain; OC = oral contraceptive; OCS = outer capsule size; SOM = symptom onset from menarche. [image: View full-size image.] View Large Image Download to PowerPoint Figure 1. Imaging findings. (A) Transvaginal ultrasound of uterus in axial view. Arrows show lesion. (B) Axial T1-weighted magnetic resonance image of cystic adenomyoma (arrow). T1-weighted image shows cyst as area of high intensity. (C) Axial T2-weighted magnetic resonance image of cystic adenomyoma (arrow). T2-weighted image shows cyst as area of high intensity. Normal uterine cavity is visualized as triangular area near cyst. A thorough clinical history was obtained from the patients before undergoing surgery to determine the time of onset and severity of dysmenorrhea. The size of the cystic lesion, comprising the inner cyst and outer capsule, was evaluated by TVUS, and the precise location was defined by MRI and intraoperative findings. Before and after the procedure, all patients recorded the severity of dysmenorrhea on a visual analog scale (VAS) ranging from 0 (no pain) to 10 (extremely severe pain). The pre- and postoperative presence or absence of chronic pelvic pain and dyspareuria in each patient was also documented. Laparoscopic Procedure Laparoscopic surgery was performed in the lithotomy position (∼15°-Trendelenburg position) under endotracheal general anesthesia (Fig. 2). The laparoscope was inserted through an 11-mm trocar (Versastep; Tyco Healthcare, Tokyo, Japan) into the abdominal cavity via the umbilicus using the closed technique. Two 5-mm trocars were bilaterally inserted into the lower abdomen, and a 12-mm trocar was inserted into the left upper abdomen on the anterior axillary line on the surgeon's side. A Uterine Manipulator (Ethicon, Tokyo, Japan) was inserted into the uterine cavity for chromotubation using indigo carmine during surgery. [image: View full-size image.] View Large Image Download to PowerPoint Figure 2. Surgical procedure. (A) Cystic adenomyoma located on right side of uterine fundus. (B) Diluted vasopressin injected around cystic adenomyoma. ( C) Transverse incision of tumor and suture pulled from tumor using forceps to create lysis border. (D) Uterine myometrium closed laparoscopically in two layers by continuous suture. (E) Trocar (11 mm) inserted via posterior fornix and Endocatch inserted. (F) Tumor entrapped by Endocatch removed transvaginally. The presence or absence of endometriosis was checked in the peritoneum according to the revised American Society for Reproductive Medicine classification (Re-ASRM). Four to eight units of vasopressin (1 mL of 20 U Pitressin diluted with 100 mL physiologic saline) was locally injected into the myometrium around the tumor. The serosa over the tumor was incised horizontally using a monopolar needle (Probe Plus II; Ethicon) to separate the tumor from the serosa. The preoperative localization of the tumor by MRI was confirmed intraoperatively. A Z-suture was made in the parenchyma using 0-Polysorb (Tyco Healthcare) to extract the tumor, which was finally enucleated with part of the normal myometrium. Thereafter, the normal myometrium was closed with a continuous suture using 0-Polysorb in two or three layers, depending on the depth of the myometrial defect. The serosa was also closed by a continuous mattress or baseball suture using 0-Polysorb. An 11-mm trocar (Versaport; Tyco Health Care Japan, Tokyo, Japan) was inserted via the posterior vaginal fornix into the pouch of Douglas, and an Endocatch (Tyco Health Care Japan) was introduced through the trocar into the abdominal cavity to collect tissue samples. After the trocar was withdrawn, the insertion site on the vaginal wall was closed laparoscopically with a continuous suture using 2/0-Polysorb. The abdominal cavity was thoroughly irrigated with physiologic saline, and the uterine wound was covered with InterCeed (Ethicon) or Seprafilm (Kaken, Tokyo, Japan). Patients with endometriotic lesions underwent additional procedures. The peritoneal lesions were cauterized with a monopolar needle. Endometriomas were lysed from the posterior broad ligament, and the cyst walls were stripped from the ovarian cortex, which was reapproximated with a tobacco suture using 2/0 Polysorb. The enucleated specimen was fixed with 10% formalin and embedded in paraffin. Sections (4 μm thick) were histologically stained with hematoxylin-eosin and azan, and we performed immunohistochemical staining for CD10, estrogen receptor (ER), and progesterone receptor (PR). All patients were followed-up on an outpatient basis every 6 months after surgery to monitor the appearance of symptoms and/or JCA recurrence based on clinical history, pelvic examination, and TVUS. Five of the patients, who provided further written informed consent, underwent SLL 6 months after the initial surgery to evaluate the uterine wound and to check for postoperative adnexal de novo adhesions. Statistical Analysis Data were statistically analyzed using Wilcoxon rank test. Differences with a probability value of <.05 were regarded to be statistically significant. Results [image: return to Article Outline] Symptoms (Table 1 ) The age at onset of dysmenorrhea in the patients with JCA was 19.3 ± 4.2 years (mean ± SD). In general, JCA develops within 15 years of menarche. The condition was diagnosed in our patients at a mean ± SD of 6.6 ± 4.3 years after menarche, and most of them described the severity of dysmenorrhea as being 8–10 on the VAS. Reports indicate that symptoms other than dysmenorrhea can develop over time, such as hypogastric pain and lumbago during menstruation. Indeed, all of our patients had these symptoms in addition to dysmenorrhea, and six of them complained of chronic pelvic pain and dyspareunia. Some patients with JCA have become pregnant even after the onset of dysmenorrhea: two (cases 3 and 5) of the three married patients presented delivered children before treatment. The preoperative serum level of CA125, a marker of endometriosis, varied considerably among the patients from within the normal range to >500 U/mL. Diagnostic Studies for JCA The JCAs were visualized (Fig. 2) by TVUS as an inner cyst cavity measuring 16.6 ± 3.5 mm in diameter that was surrounded by another capsule, with a total diameter of 31.8 ± 5.1 mm. Cysts were visualized as ground-glass isoechoic lesions that were similar in appearance to endometrioma. The size of the cyst varied with the phase of the menstrual cycle, and peaked immediately after menstruation. No cyst completely vanished at any time during preoperative menstrual cycles. The cyst did not communicate with the uterine cavity in any of the patients. Tumors were visualized on MRI as high-intensity areas on T1-weighted images and as hypo- to high-intensity areas on T2-weighted images. These features were similar to those of endometrioma. Fat suppression was negative. The capsule around cysts was visualized as a hypointensity region relative to normal myometrial intensity on T2-weighted images. None of the patients had any associated urologic abnormalities as assessed by IP. The uterine cavity was normal, and fallopian tubes were patent in all four patients who underwent HSG. Surgical Results The tumor was located on the left side in three patients and on the right side in six (Table 2). Only one patient (case 2) was complicated with an endometrioma of the right ovary (Re-ASRM score 36). Five patients had peritoneal endometriosis lesions with a Re-ASRM score of 1–2. The remaining three patients did not have endometriotic lesions. The surgical duration was 78.0 ± 19.8 minutes, and blood loss during surgery was 33.6 ± 32.1 mL. Table 2. Intra- and postoperative findings. Laparoscopy DM VAS Case no. Re-ASRM OD (min) BL (mL) MW (g) SLL Preopa Postopa POP (y) MD 1 1 70 20 10 8 27 CS 2 36 120 100 10Y 10 32 ND×2 3 0 70 50 10 10 2 4 2 96 52 11Y 8 2 5 1 76 5 7 10 1 6 1 70 10 7Y 10 2 7 0 75 50 3.5Y 10 3 8 1 76 50 11.5Y 10 2 9 0 49 10 4.1 9 1 Mean 78 33.6 8.2 SD 19.8 32.1 3.1 Note: BL = blood loss; CS = cesarean section; DM VAS = visual analog scale of dysmenorrhea (0–10); MD = method of delivery; MW = material weight; ND = normal delivery; OD = operation duration; POP = postoperative pregnancy; Re-ASRM = revised American Society for Reproductive Medicine criteria points; SLL = second-look laparoscopy. a P<.05. Pathologic Findings Figure 3 shows the pathologic findings. The mean ± SD material weight was 8.2 ± 3.1 g. Macroscopically, the cystic tumors contained a chocolate-colored fluid. Despite a hypertrophic myometrium surrounding the cavity, smooth muscle proliferation was not evident. The histologic findings revealed glands and stroma similar to the endometrial tissue that lined the inner surface of the tumor cavity. The interstitial tissue showed edema, bleeding, and exfoliation. The endometrium-like tissue lining the inner surface of the tumor had no clear basal layer, and infiltration of the endometrial glands with stromal tissue into parts of the myometrium (a feature of uterine adenomyosis) was evident in all of the patients. The endometrium-like tissues of all patients was positively stained for CD10, ER, and PR, which are markers of normal endometrium. [image: View full-size image.] View Large Image Download to PowerPoint Figure 3. Histologic findings of resected tumor. (A) Macroscopic finding. (B) Cyst is lined with eutopic endometrium-like tissue. Adenomyosis lesion has infiltrated below cyst wall (arrows). (C) Basal layer of endometrium not evident in cystic adenomyoma. (D) Endometrium-like tissue lining cyst is stained positively for CD10, ER, and PR. Postoperative Course The mean ± SD duration of follow-up was 35.9 ± 21.4 months. The dysmenorrhea remarkably improved in all of the patients who underwent laparoscopic enucleation of a cystic uterine adenomyoma (Table 2). The median severity of the dysmenorrhea, preoperatively scored as 10 (range 8–10) on the VAS, had significantly decreased (P5 on the VAS. Three pregnancies were confirmed in two of the three patients who wished to become pregnant. Case 2 became pregnant twice within 2 years of the surgery and had normal transvaginal deliveries in the 37th and 38th weeks of pregnancy. Case 1 became pregnant 7 years after surgery and delivered by elective cesarean section in the 38th week of pregnancy (Table 2 ). Five patients underwent SLL 6 months after initial surgery (Table 2). Chromotubation with indigo carmine during the SLL confirmed patent fallopian tubes bilaterally in all patients. The uterine wound healed well, and wound dehiscence did not occur in any of the patients. No de novo adhesions developed around the fallopian tubes of any of the patients. Discussion [image: return to Article Outline] Diagnostic Criteria for JCA The mean ± SD age of our nine patients was 25.2 ± 4.4 years (range 20 to 30 years). Although most patients described in earlier studies were ≤20 years of age, our experience indicated that the diagnostic criteria for JCA should include women ranging from adolescence to 30 years of age. Furthermore, the cystic lesions of JCA have similar characteristics on TVUS and MRI in appearance and location regardless of age. The interval from menarche to the appearance of JCA symptoms tended to be longer in our patients than in other reports, although this might be because we considered severe dysmenorrhea as a characteristic symptom. Some uterine cystic lesions can be acquired (13), and develop when the endometrium is sutured into the myometrium during surgery (14). Such cystic lesions should be excluded from JCA, because their clinical background is different; i.e., they appear after delivery, uterine myomectomy (14), or dilatation and curettage (8) . Diagnosis of JCA Juvenile cystic adenomyoma should be differentiated from adenomyosis with internal bleeding, an obstructive uterine anomaly such as double uterus with a noncommunicating horn, and various other lower genitourinary tract obstructions. Hysterosalpingography is useful for a differential diagnosis, because it can visualize the bilateral fallopian tubes in patients with JCA but not müllerian uterine anomalies such as a noncommunicating rudimentary horn with the uterine unicornis. Moreover, because urinary tract anomalies are often associated with uterine malformation, the probability of a differential diagnosis is increased by performing IP (7). However, experienced gynecologists with a good understanding can diagnose this disease correctly based on TVUS findings alone. They can also diagnose the presence or absence of a unilateral kidney by TVUS alone with some degree of accuracy. On the other hand, MRI is very useful as a guide to locate tumors during laparoscopic surgery. Therapeutic Options for JCA Nonsteroidal antiinflammatory drugs were ineffective for all of our patients. Hormone therapy with GnRH agonists or oral contraceptives was somewhat effective, but the symptoms rapidly recurred after the therapy was stopped. Laparoscopic Surgery The salient points of our surgical procedure are as follows. Cystic adenomyomas are mostly located in the lateral wall near the uterine round ligament attachment site. Therefore, we usually select the anterior wall approach, because the posterior approach carries a risk of damage to the ascending branch of the uterine artery. Cystic adenomyomas are more clearly delineated from the normal myometrium than uterine adenomyosis, but less so than uterine myomas. The myometrium and serosa were closed with continuous suture after enucleation, similar to the procedure adopted after laparoscopic myomectomy (15) . The mean ± SD duration of follow-up of our patients was 35.9 ± 21.4 months. All those who underwent laparoscopic enucleation of the cystic uterine adenomyoma described a remarkable improvement of the dysmenorrhea as well as of chronic pelvic pain. None of the five patients who underwent SLL showed dimpling or thinning at the uterine wound or adnexal de novo adhesions, and all of these five patients demonstrated bilateral fallopian tube patency. None of the patients developed uterine JCA and adenomyosis during the follow-up period. Clinical Misnomenclature Without Reference to Pathological Terminology Adenomyosis and adenomyoma are defined in textbooks of pathology (16) as follows: “Adenomyosis is a common condition detected in 15%–30% of cases undergoing hysterectomy (17). It is a nonneoplastic condition characterized by the presence of endometrial glands and stroma within the myometrium. Small blood-filled cysts may be noted. On the other hand, adenomyoma is a neoplastic tumor classified as a benign mixed epithelial-nonepithelial tumor. The designation of adenomyoma should be reserved for polypoid lesions in which the stromal component is almost exclusively composed of smooth muscle. The term adenomyoma is not recommended for defining a solitary myometrial nodule of adenomyosis” (16). According to these definitions, JCA should be considered as adenomyosis rather than adenomyoma, because the histopathologic findings include the absence of proliferative growth of the surrounding myometrium. That is, JCA should be regarded from a histologic perspective as “cystic adenomyosis” or a “cystic variation of adenomyosis.” To propose a new disease concept, the name of the new entity should be consistent with related pathologic definitions. Problems With Current Medline Search for JCA Potter and Schenken (11) reported that JCA represents a noncommunicating accessory uterine cavity, suggesting that it is a new type of uterine malformation. This valuable article, which was published in 1996 after the first description of JCA by Tamura et al. (4) , included the key words müllerian, congenital anomaly, uterus, and dysmenorrhea. Fisseha et al. (12) described a cystic myometrial lesion of a young adolescent girl as most likely cystic adenomyosis, a very rare form of adenomyosis of the uterus, despite similarities to earlier reports. These articles received no attention, probably because they were in a different field of search in Medline. A simultaneous search for a disease registered under various names in different fields of search in Medline is difficult, and thus one factor that makes determining the etiology of JCA so complex. When the three additional cases 4 , 11 , 12 are included, six 4 , 5 , 6 , 7 , 9 and three 10 , 11 , 12 instances of JCA have been described in Japan and in the U.S., respectively. Therefore, the notion that JCA occurs more commonly in Japan is no longer substantiated. Although JCA might be a pathologically questionable name, the disease concept of JCA was established earlier in Japan. This may be the only reason why more Japanese patients with JCA have been described in the literature. Pathogenesis Some reports suggest that JCA is a congenital disease, because it presents immediately after menarche as a symptomatic intrauterine cystic lesion with a mean central cyst size of 20.8 ± 8.9 mm, which is significantly larger than that of adenomyosis 1 , 4 , 6 , 7. Because the most common intrauterine cystic lesion is intracystic bleeding associated with adenomyosis, it is important to differentiate JCA from adenomyosis. Histopathologically, all nine patients described here had confirmed adenomyosis in the smooth muscle layer. Furthermore, to exclude adenomyosis from JCA by findings such as the absence of the basal layer of the endometrium-like tissue covering the cystic lumen is difficult. The present findings indicate that JCA is probably a cystic variant of adenomyosis rather than a congenital abnormality. Further studies are required to understand the precise pathogenetic mechanisms of JCA. Conclusion [image: return to Article Outline] Juvenile cystic adenomyoma is defined as a solitary myometrial cyst measuring ≥1 cm that is surrounded by hypertrophic endometrium, independent of the uterine lumen, and presents in women ≤30 years of age in association with severe dysmenorrhea. Laparoscopic excision can significantly improve the associated dysmenorrhea and increase the likelihood of successful pregnancy. The condition might represent a larger more discrete variant of adenomyosis among young women. Similar disease entities have been reported using different nomenclature, thus yielding inconsistent associations between studies in a Medline search of the literature. * 博元婦產科不孕症試管嬰兒中心:蔡鋒博醫師,陳昭雯醫師 客服電話：0911905889 地址: 50044 彰化市中正路1段392號 電話:04-7260678(10 lines);047260988;047298888 Fax: 04-7225626 e-mail: ok7260678@gmail.com 博元婦產科官網--:http://www.babymaker.com.tw; 博元 YouTube Channel--看博元' YouTube影片- 進入網址：http://www.youtube.com/7260678 請輸入您想了解的主題，如:試管嬰兒、如：多囊性卵巢，可看有關影片 !! 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