A total of 521 patients less than 20 years of age were included in this study. 92 had non-neoplastic lesions, 382 had benign neoplasms, and 47 had malignant tumors. The primary presenting symptoms and signs were abdominal pain and menstrual disorder.
A total of 521 patients less than 20 years of age were included in this study. 92 had non-neoplastic lesions, 382 had benign neoplasms, and 47 had malignant tumors. The primary presenting symptoms and signs were abdominal pain and menstrual disorder.
A total of 521 patients less than 20 years of age were included in this study. 92 had non-neoplastic lesions, 382 had benign neoplasms, and 47 had malignant tumors. The primary presenting symptoms and signs were abdominal pain and menstrual disorder.
Ovarian Masses in Children and Adolescents - An Analysis of 521 Clinical Cases
Mingxing Zhang MD, Wei Jiang MD, PhD, Guiling Li MD, PhD*, Congjian Xu MD, PhD* Obstetrics and Gynecology Hospital, Fudan University, Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Shanghai, China a b s t r a c t Objective: To analyze the clinical characteristics of ovarian masses in children and adolescents. Materials and Methods: We performed a retrospective analysis of patients less than 20 years of age who were treated at the Obstetrics and Gynecology Hospital of Fudan University between March 2003 and January 2012. Medical records were reviewed for age at operation, including presentation of symptoms and signs; the levels of tumor markers; imaging examinations; pathologic ndings; the size of masses; treatment; and outcome. Data management and descriptive analyses were performed using SPSS 16.0. Results: A total of 521 patients were included in this study. Among them, 92 had non-neoplastic lesions, 382 had benign neoplasms, and 47 had malignant tumors. The mean age of the patients was 16.3 2.2 years. The primary presenting symptoms and signs were abdominal pain (39.5%), menstrual disorder (31.1%), abdominal swelling (5.4%), and an enlarged abdominal perimeter (3.3%). Malignant tumors tended to be larger than benign neoplasms (17.3 8.6 cm vs 9.0 5.7 cm; P 5 .000). There was no age difference between patients with benign neoplasms (16.3 2.1 y) and those with malignant tumors (15.7 2.5 y). The operations included salpingo-oophorectomy, ovarian cystectomy, and oophorectomy. Two patients with malignant tumors had bilateral salpingo-oophorectomy, and 2 patients who had tumor metastasis underwent a total abdominal hysterectomy and bilateral salpingo-oophorectomy. Forty-one cases of malignant tumors received postoperative chemotherapy. Conclusions: Germ cell tumors are the most common malignancy, and mature teratomas are the most common benign neoplasms in children and adolescents. Abdominal pain and menstrual disorder are the main reasons for doctors visit. Although examination by ul- trasound is the preferred auxiliary in the diagnosis of ovarian pathology, it could not distinguish between benign and malignant tumors. However, tumor size and tumor markers are helpful to identify the properties of masses. Surgery is usually better for treatment, and it is preferable to attempt conservative, fertility-sparing surgery in adolescents. Postoperative chemotherapy is necessary for malignant tumors. Key Words: Ovarian masses, Children, Adolescents Introduction Ovarian masses represent the most frequent tumors of the female genital tract in children and adolescents. 1 The incidence of ovarian masses has been estimated at 2.6 cases per 100,000 girls each year, and malignant ovarian tumors make up approximately 1% of all childhood can- cers. 2 Childhood ovarian masses represent a heterogeneous group of lesions with many etiologies. Up to 64% of these masses are reported to be neoplastic. Less than 20% of such neoplasms are derived from the surface epithelium of the ovary, whereas the majority of these neoplasms arise from germ cells. 3,4 Although benign neoplasms greatly outnumber malignant ones in this age group and although their clinical symptoms and signs are non-specic, it is critical to determine the possibility of malignancy at an early stage by currently available multi-modal diagnostic methods. Most ovarian masses discovered in infants, chil- dren and adolescents are removed surgically. Operative procedures involving the ovary in young patients can compromise future fertility, due either to removal of the ovary or to formation of adhesions. Laparoscopic ap- proaches are used to adequately assess and resect ovarian tumors that are benign. 5,6 However, the use of laparoscopy or minimally invasive techniques remains controversial in children with ovarian malignancies. 7 This retrospective study reviews the clinical practice and outcome of the operative treatment of ovarian masses in children and adolescents at the Obstetrics and Gynecology Hospital of Fudan University over the past 9 years. Materials and Methods We searched the pathology database in our hospital to identify all patients who had ovarian tissue submitted for pathologic analysis from March 2003 to January 2012. Five hundred twenty-one patients were identied and had medical records available. Thirteen patients, including 8 patients with malignant ovarian tumors and 5 with benign diseases, were primarily treated elsewhere and had path- ologic material submitted for consultation. Among the 13 patients, 7 patients had second or third operations at our hospital, of which 2 malignant cases were due to distant metastasis and 5 benign cases were due to recurrence in situ or other sites. All patients were less than 20 years old. The retrospective data from the hospital medical records The authors indicate no conicts of interest. * Address correspondence to: Guiling Li and Congjian Xu, Department of Gyne- cology, Obstetrics and Gynecology Hospital of Fudan University, 419 Fang-Xie Road, Shanghai, 200011, P. R. China; Phone: 86-21-63455050; fax: 86-21- 63455600 E-mail addresses: guilingli@fudan.edu.cn (G. Li), xucongjian@gmail.com (C. Xu). 1083-3188/$ - see front matter 2013 North American Society for Pediatric and Adolescent Gynecology. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jpag.2013.07.007 included age at operation, presenting symptoms and signs, and the levels of tumor markers (CA 125, CA199, carci- noembryonic antigen (CEA), human chorionic gonadotropin (b-hCG,) a-fetoprotein). We reviewed all imaging exami- nations including the results of ultrasonography and computed tomography (CT) scans. We reviewed all opera- tion records, and, when available, we recorded the sizes of all masses as documented at surgery or in the pathology record. The study was approved by the Ethics Committee of Obstetrics and Gynecology Hospital of Fudan University. Statistical analyses were performed using Students t test as appropriate. A P value of .05 or less was regarded as statistically signicant. All continuous data are expressed as the mean SD. Results Five hundred twenty-one patients underwent 524 op- erations for ovarian mass removal at our hospital during the past 9 years. Among the 524 operations, 434 surgeries, up to 82 percent of all operations, were operated by means of a laparoscope. The principal pathology was in the right ovary in 241 (46%) patients, the left ovary in 201 (38%) patients, and 82 (16%) patients had bilateral disease. The patients ranged in age from 9 years to 19 years, with a mean age of 16.3 2.2 years at the time of surgery. We found no difference in the age of presentation between patients who had benign neoplasms (16.3 2.1 y) and those who had malignant tumors (15.7 2.5 y; P 5 .115; Table 1). However, there was a signicant difference in tumor size between patients who had benign neoplasms (9.0 5.7 cm) and those with malignant tumors (17.3 8.6 cm; P 5 .000; Table 1). Ultrasonography (US) was performed in 495 (95%) pa- tients to dene the size of the lesion and the gross morphologic nature of the tumor. Only 29 (5.5%) patients had abdominal CT scans, and 6 (1.1%) had magnetic reso- nance imaging, where further evaluation of the nature of the ovarian tumor and abdominal organs was necessary. Overall, there were 48 patients who had ovarian torsion, and 20 had an ovarian rupture. However, only 14 patients received a diagnosis of torsion or rupture based on US. Benign Diseases Four hundred seventy-four patients had benign diseases and 47 patients had malignant tumors. A list of all tumor types is included in Table 2. The primary presenting symptoms and signs that led to a visit to the doctor included abdominal pain (n 5 187; 39.5%), menstrual disorder (n 5 156; 32.9%), abdominal swelling (n 518; 3.8%), an enlarged abdominal perimeter (n 5 14; 3.0%), precocious puberty (n 5 4; 0.8%), or premenarchal (n 5 4; 0.8%). In 78 patients, pelvic masses were found through physical examinations during the follow-up of other diseases, and in the other 13 patients, the masses were incidentally found by self-palpation (Table 3). Ultrasonography was performed in 453 (96%) patients to dene the size of the lesion and gross morphologic nature of the tumor such as a solid mass (n 5 20, 6%), a complex mass (n 5 158, 34%), or a cyst (n 5 275, 60%). The charac- teristics of ultrasonographic performance of benign tumors are clear boundary and cystic or complex mass. Most of blood supply distributes around the lesion. a-fetoprotein (AFP) was done in 197 patients, and the level raised in 4 of them.b-HCG was done in 32 patients, and none of them had a rise. CA125 was done in 213 patients, and in 53 cases it raised, 30 turned out to be benign neo- plasms and other cases were non-neoplasms. CA199 was done in 251 patients, and in 141 of them it raised included 109 benign neoplasms and 10 non-neoplasms. CEA was done in 161 patients, and none of them had a rise. In the group with benign diseases, 481 operations in total were performed for 474 patients. Seven patients (including 4 cases that were primarily treated elsewhere) underwent 2 separate operations, and 2 patients (including 1 patient who was primarily treated elsewhere) underwent 3 separate operations. Among patients with benign lesions, 48 had unilateral salpingo-oophorectomy. Of the 48 pa- tients, 37 had adnexal torsion or ovarian torsion and 11 patients had other conditions. Malignant Tumors Patients whose pathology ndings showed malignancy are listed in Table 2. Of the malignant group, 19 (40.4%) patients had acute or chronic abdominal pain, 10 (21.3%) patients had abdominal Table 1 Comparison of Characteristic of Benign and Malignant Neoplasms Benign Neoplasms (n 5 382) Malignant Neoplasms (n 5 47) P-Value Age at presentation (y) 16.3 2.1 15.7 2.5 .115 Tumor size (cm) 9.0 5.7 17.3 8.6 .000 Table 2 Pathologic Findings of 521 Patients Pathology No. of Patients Percent of Total Non-neoplastic 92 17.7 Ovarian torsion (without an associated tumor) 8 1.5 Corpus luteal cyst 9 1.7 Follicular cyst 27 5.2 Simple ovarian cyst 16 3.1 Endometrioma 32 6.1 Neoplastic: benign 382 73.3 Mature teratoma 270 51.8 Cystadenoma 86 16.5 Fibrothecoma 4 0.8 Struma ovarii 3 0.6 Sclerosing stromal tumor 3 0.6 Ovarian theca cell tumor 1 0.2 Fibroma 1 0.2 Ovary sex cord tumor with annular tubules 1 0.2 Borderline cystadenoma 13 2.5 Neoplastic: malignant 47 9 Immature teratoma 19 3.6 Invasive mucinous cystadenocarcinoma 8 1.5 Yolk sac tumor 5 1.0 Dysgerminoma 4 0.8 Mixed germ cell tumor 4 0.8 Sertoli-Leydig cell tumor 4 0.8 Juvenile granulosa cell tumor 1 0.2 Gonadoblastoma 2 0.4 M. Zhang et al. / J Pediatr Adolesc Gynecol xxx (2013) 1e5 2 swelling, 3 (6.4%) patients had a palpable abdominal mass, 6 (12.8%) patients had a menstrual disorder, 3 (6.4%) patients had an enlarged abdominal perimeter, 2 (4.2%) patients were premenarchal, 1 (2.1%) patient had vomiting, and 3 (6.4%) patients found masses incidentally (Table 3). Forty-two of these patients had an ultrasonography and 13 were complex masses, 21 were cysts, and 8 were solid masses. The characteristics of ultrasonographic perfor- mance of malignant tumors are irregular shape, unclear boundary, and solid or predominantly solid mixed mass. And most of blood supply distributes in the interior of solid mass. Among the 31 patients who had an AFP test, 21 had increased AFP levels. b-HCG increased in only 1 patient with mixed germ cell tumor. CA125 was tested in 32 patients, and it increased in 21 cases. CA199 was analyzed in 23 pa- tients, and 12 patients had increased levels. CEA was analyzed in 27 patients, and in 1 patient with immature teratomas of left ovary the level had elevated. There were 43 operations for 47 patients; 8 patients were rst treated in other hospitals, and 2 patients were operated on twice in our hospital. The malignant lesions included 32 (68%) germ cell tumors, 8 (17%) epithelial tumors (Table 4), and 7 (15%) sex-cord stromal tumors (Table 4). Of the 19 cases of immature teratomas, 5 patients were treated with ovarian cystectomy and the remaining patients underwent unilateral salpingo-oophorectomy. In addition, only 8 patients underwent pelvic lymph node dissection, 5 underwent omentectomy, and 2 underwent appendectomy. Data regarding the stages of immature teratomas was available in only 13 patients; 10 were staged Ia, and 3 were staged Ic. All but 2 patients received postoperative chemotherapy, including 7 patients who received cisplatin, bleomycin, and vinblastine, 9 who received cisplatin, etoposide, and bleomycin (PEB), and 1 who received vincristine, cytoxan, and actinomycin D. The course of chemotherapy varied from 1 cycle to 7 cycles, with a mean of 3.7 cycles. Three patients lost to follow-up, and all others are alive and well. The mean time of follow-up was 3.77 3.33 years. We also reviewed the treatment and outcome of other malignant germ cell tumors (Table 5). One patient with dysgerminoma had an oophorectomy at another hospital, followed by 6 cycles of chemotherapy (cisplatin, etopo- side, and bleomycin) at our hospital. Two patients with gonadoblastomas had bilateral salpingo-oophorectomy, and 2 patients who had tumor metastasis underwent a total abdominal hysterectomy and bilateral salpingo- oophorectomy. Discussion Ovarian tumors account for approximately 1% of all tu- mors in children and adolescents. Less than 5% of malignant ovarian tumors occur in this age group. Thirty percent of all ovarian neoplasms occurring during childhood and adolescence are maliganant. 3 In our study, 91% of ovarian masses were benign, and only 9% of ovarian masses were malignant, which is consistent with recent reports. 2,8 However, Brown et al 9 reported that 33% of ovarian masses in patients between the ages of 8 and 18 years were malignant. Of the malignant group, 68% were germ cell tumors, and only 17% were surface epithelial neoplasms, which is consistent with other studies. 10-12 Symptoms and signs are varied and non-specic. 13,14 Based on our study, for both benign and malignant dis- eases, the most common symptom was abdominal pain. While different frompatients with benign diseases, patients with malignant tumors presented abdominal swelling more often, rather than menstrual disorders. Therefore, parents should pay attention when their children have menstrual changes (cycles, period, and dysmenorrhea), acute or chronic abdominal pain, an increasing abdominal girth, or abdominal swelling. A sonogram during physical examina- tion is essential for identifying problems. Analysis of symptoms and signs cannot, however, distinguish between benign and malignant lesions. The classication of ovarian masses is complex, 15 as most ovarian masses in children are benign diseases. For these reasons, it is difcult to make the correct preoperative diagnosis. In distinguishing patients with benign disease from those with malignancy, we found that age (P 5 .115) was not useful, whereas imaging characteristics, tumor size, and tumor markers were important. Malignant lesions tended to be larger (P 5 .000) in our analysis, which was consistent with previous ndings. 16 Ultrasound has been found to be a helpful diagnostic tool for ovarian masses. 17 Of the 26 solid ovarian masses identied by ultrasound, 8 were malignant. Solid ovarian masses identied by ultrasound were more likely to be malignant. 18 However, both malig- nant and benign neoplasms can appear cystic, in which case, AFP is helpful to preoperatively distinguish these le- sions. The clinical application of serum AFP concentration is of great benet not only as diagnostic aid but also in monitoring the efcacy of any treatment modality, such as chemotherapy, radiotherapy or surgical resection. 19,20 In this study, AFP was raised in 25 cases and 21 turned out to have malignant tumors. The treatment of ovarian masses in children and adoles- cents is generally conservative, whether expectant, medical, or surgical. For the surgical treatment of benign masses, the preservation of ovarian tissue and function is very impor- tant, and cystectomy by laparoscopic approach is advo- cated. 11 Given the high rate of relapse of borderline mucinous or serous cystadenoma, doctors in our hospital usually remove unilateral adnexa. However, in this study there were only 4 patients who decided to have unilateral Table 3 Presenting Symptoms, Signs, and Indications in 521 Patients Presenting Symptoms/Signs No. of Patients (%) Benign (n 5 474) Malignant (n 5 47) Abdominal pain 187 (39.5) 19 (40.4) Abdominal swelling 18 (3.8) 10 (21.3) Enlarged abdominal perimeter 14 (3.0) 3 (6.4) Menstrual disorder 156 (32.9) 6 (12.8) Physical examination 78 (16.5) 0 Precocious puberty 4 (0.8) 0 Premenarchal 4 (0.8) 2 (4.2) Palpable abdominal mass 0 3 (6.4) Vomiting 0 1 (2.1) Incidental nding 13 (2.7) 3 (6.4) M. Zhang et al. / J Pediatr Adolesc Gynecol xxx (2013) 1e5 3 salping-oophorectomy. And the other 9 patients had cys- tectomy for parent demands. Two of the 9 patients had a recurrence. On these grounds, it is suggested that patients with borderline tumors can have conservative cystectomy. But we need more data to support this conclusion. Of the other 461 benign diseases, there were only 7 pa- tients who did not have cyst torsion and undergo salpingo- oophorectomy. After detailed reading of medical records, we think some factors may drive doctors to take such measures. These inuencing factors are patients age, tumor size, and remaining functional ovarian tissue, and adhesion formation. For example, a younger patient with a giant mass growing in a short time came for help. During surgery, we found that the affected ovary had no remaining formal functional tissue, and pelvic adhesion had formed. Then we usually removed the ovary completely. For suspected malignancies, a conservative surgical treatment approach with unilateral salpingo-oophorectomy and staging is appropriate. 11 In a past study, a postoperative ultrasound revealed that the affected ovary resumed its normal size and volume despite the attenuated appearance of the ovarian cortex at the time of surgery. 21 Moreover, Table 4 Treatment and Outcome of Patients with Invasive Mucinous Cystadenocarcinomas and Sex Cord-Stromal Tumors Patient No. Age (y) Diagnosis Operation Stage Chemotherapy Outcome: F/U (yr) 1 17 Invasive Mucinous Cystadenocarcinomas LSO, appendectomy Not staged TP, six cycles NED, 5 2 17 Invasive Mucinous Cystadenocarcinomas RSO, appendectomy* Not staged No NED, 2.5 3 16 Invasive Mucinous Cystadenocarcinomas LSO, appendectomy Not staged No NED, 0.5 4 19 Invasive Mucinous Cystadenocarcinomas Left cystectomy a No Loss to FU 5 18 Invasive Mucinous Cystadenocarcinomas LSO Not staged PC, one cycle NED, 7 6 16 Invasive Mucinous Cystadenocarcinomas RSO, appendectomy, omentectomy, PLND, interval TAHLSO c TP, eight cycles NED, 3.5 7 16 Invasive Mucinous Cystadenocarcinomas LSO, omentectomy c TP, 3 cycles NED, 0 8 16 Invasive Mucinous Cystadenocarcinomas RSO a No NED, 4 9 18 SLCT RSO Not staged PEB, 4 cycles NED, 2.5 10 19 SLCT Right cystectomy Not staged PVB, 1 cycle NED, 8 11 15 SLCT LSO Not staged TP, 6 cycles NED, 8 12 17 SLCT LSO Not staged CAP, 6 cycles NED, 8 13 18 JGCT LSO Not staged PEB, 4 cycles NED, 3 14 17 Gonadoblastoma BSO Not staged PVB, 3 cycles NED, 4.5 15 14 Gonadoblastoma BSO Not staged PEB, 4 cycles NED, 2 CAP, cytoxan, adriamycin, cisplatin: F/U, follow-up; JGCT, Juvenile granulosa cell tumor; LSO, left salpingo-oophorectomy; NED, no evidence of disease; PC, cytoxan and cisplatin; PEB, cisplatin, etoposide, and bleomycin; PLND, pelvic lymph node dissection; PVB, cisplatin, bleomycin, and vinblastine; RSO, right salpingo-oophorectomy; SLCT, Sertoli-Leydig cell tumor; TAHBSO, total abdominal hysterectomy and bilateral salpingo-oophorectomy; TP, cisplatin and paclitaxel; TP, cisplatin and paclitaxel * Patient who was treated in other hospital primarily. Table 5 Treatment and Outcome of 13 Patients with Malignant Germ Cell Tumors Patient No. Age (yr) Diagnosis Operation Stage Chemotherapy Recurrence Outcome: F/U (yr) 1 16 YST, Turner's syndrome RSO, PLND, omentectomy a PEB, 6 cycles No NED, 0.5 2 17 YST LSO*, omentectomy Not staged PEB, 6 cycles Yes @ 1 year Loss to FU 3 12 YST Not quiet clear* Not quiet clear PVB, 10 cycles Yes @ 1 year, staged c, cytoreductive surgery, part transverse colon and small intestinal resection and anastomosis Died after one year 4 16 YST RSO, omentectomy a PVB, 6 cycles No Loss to FU 5 15 YST TAHBSO, PLND c PVB, 6 cycles No Loss to FU 6 12 Dysgerminoma RSO a PEB, 4 cycles No NED, 2.25 7 10 Dysgerminoma RSO, appendectomy* a PEB, 6 cycles No NED, 1.5 8 9 Dysgerminoma RSO c PEB, 6 cycles No NED, 4.5 9 19 Dysgerminoma Left oophorectomy* Not staged PEB, 6 cycles No NED, 1.5 10 13 MGCT RSO* Not staged VAC*, 1 cycle PEB, 1 cycle Yes @ 2 mon, cystectomy surgery, appendectomy, omentectomy Loss to FU 11 15 MGCT RSO, omentectomy c PEB No NED, 1 12 16 MGCT LSO, omentectomy c PEB, 5cycles No NED, 5.5 13 15 MGCT RSO c PEB, 6cycles No NED, 0.25 F/U, follow-up; LSO, left salpingo-oophorectomy; MGCT, mixed germ cell tumor; mon, month; NED, no evidence of disease; PEB, cisplatin, etoposide, and bleomycin; PLND, pelvic lymph node dissection; PVB, cisplatin, bleomycin, and vinblastine; RSO, right salpingo-oophorectomy; TAHBSO, total abdominal hysterectomy and bilateral salpingo- oophorectomy; VAC, vincristine, cytoxan, and actinomycin D; y, year; YST, yolk sac tumor * Patient who was treated in other hospital primarily. M. Zhang et al. / J Pediatr Adolesc Gynecol xxx (2013) 1e5 4 it was reported that chemotherapy based on cisplatin is very efcient, with a 5-year overall survival of non- seminomatous GCT at 85%-95%. 22 In this study, only 7 pa- tients received cystectomy; all of the other patients were treated with unilateral or bilateral salpingo-oophorectomy, with or without pelvic lymph node dissection. The 7 cases included 5 immature terotomas, 1 invasive mucinous cys- tadenocarcinoma and 1 Sertoli-Leydig cell tumor. The reason why they underwent cystectomy was family mem- bers demands (3 cases) and that the pathologic histology of intraoperative frozen section indicated mature teratomas (2 cases). And in addition, 2 patients with immature teratomas primarily operated in other hospitals, so we did not know clearly about why they underwent cystectomy. Two of 5 patients with immature teratomas who underwent cys- tectomy had recurrences twice in the following 3 years after rst operation. The recurrence rate was much higher than that of those who underwent unilateral salpingo- oophorectomy. And the other 2 patients with malignant lesions while underwent cystectomy lost to follow-up. In view of the above, we do not suggest conservative cys- tectomy for any malignant lesions. Most patients with malignant tumors received postoperative chemotherapy. In our experience, the PEB regimen is most commonly used in germ cell tumors, and the paclitaxel combined with plat- inum (TP) protocol is generally selected for surface epithe- lial tumors. There are limitations to our study. It was retrospective in design, and certain data were unavailable, including stages of some patients, and patients who were lost to follow-up. Currently, there are no studies of ultrasound assessment of the ovarian reserve in these patients after ovarian cys- tectomy or unilateral salpingo-oophorectomy. Long-term follow-up is needed to fully assess the effects of ovary- conserving surgery on future fertility and ovarian function in this population. In addition, long-term follow-up of postoperative adhesion formation and its effect on fertility should be studied. Conclusion Germ cell tumors are the most common malignancy; epithelial cell tumors are less likely, and mature teratomas are the most common benign neoplasms in children and adolescents. Abdominal pain and menstrual disorder are the main reasons for doctors visit. Although examination by ultrasonogram is the preferred auxiliary in the diagnosis of ovarian pathology, it could not distinguish between benign and malignant tumors. However, tumor size and tumor markers are helpful to identify the properties of masses. Surgery is usually better for treatment, and it is preferable to attempt conservative, fertility-sparing surgery in adolescents. Postoperative chemotherapy is necessary for malignant tumors. References 1. 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