The management of mature cystic teratomas in children and adolescents: a retrospective analysis

Claire L. Templeman1, S.Paige Hertweck1, James P. Scheetz2, Sally E. Perlman1 and Mary E. Fallat3,4

1 Divisions of Pediatric Gynecology, Department of Obstetrics and Gynecology, 2 Diagnostic Sciences, Department of Dentistry and 3 Pediatric Surgery, Department of Surgery, University of Louisville, Louisville, Kentucky, USA


    Abstract
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Mature cystic teratomas (MCT) are the most common ovarian tumours seen in children and adolescents. Fifty-two patients <21 years of age had surgical removal of an MCT, 14 of whom were approached laparoscopically. Compared with laparotomy, those patients managed laparoscopically had a significantly shorter hospital stay. Intra-operative tumour spillage occurred in 27 (52%) patients; there were no cases of chemical peritonitis. Available follow-up data on 34 (65%) patients revealed seven pregnancies occurring at a median of 70 months (46–123) postoperatively, including four in patients with intraoperative MCT spill. There were no cases of tumour recurrence during the follow-up period among the 27 (52%) patients managed with ovarian cystectomy. These results demonstrate that some of the conclusions regarding the contemporary management of MCT in adults are applicable to children and adolescents.

Key words: adolescents/children/ovarian/teratoma


    Introduction
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Teratomas are neoplasms containing tissue from all three germ cell layers. Most are mature cystic teratomas (MCT) with predominantly ectodermal derivatives such as hair and teeth. Collectively, teratomas constitute half of all ovarian neoplasms in children (Azizkhan and Caty, 1996Go) and 1% of these are malignant immature teratomas (O'Connor, 1996Go). Traditional management of children with MCT has been oophorectomy via laparotomy (Carney, 1972; Mahour et al., 1976Go; Azizkhan and Caty, 1996Go). However, acceptable management in adults is ovarian cystectomy approached by laparoscopy, with laparotomy generally reserved for cases of large MCT tumours or those suspected of malignancy (Bollen et al., 1992Go; Canis et al., 1994; Lin et al., 1995Go). The aim of this study was to examine the contemporary surgical management of MCT in children and adolescents.


    Materials and methods
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
The international coding and diagnosis (ICD-9) code specific for ovarian dermoid cyst was used to identify patients at Kosair Children's Hospital, Norton Hospital and University of Louisville Hospital, Louisville, Kentucky during the time period June 1980 to February 2000. Only patients <21 years old with a surgical pathology report confirming the diagnosis of MCT (dermoid cyst) of the ovary were included in this retrospective study. Fifty-two patients fulfilled the entry criteria.

The medical records were searched for age, presenting symptoms, investigations, operative reports, postoperative hospital stay and complications. In addition, any subsequent hospital admissions or clinic visits were reviewed for evidence of postoperative complications, tumour recurrence, pregnancy or subsequent abdominal surgery. If follow-up details were not found in the hospital records, the attending surgeon's office was contacted and any records available reviewed. The patient was deemed lost to follow-up if there was no information available following the original operation and postoperative care. All postoperative pregnancies were verified by ultrasound and outcome confirmed by review of medical records or labour and delivery database.

For the purposes of further analysis, girls were defined as <=15 years and adolescents as >15 years of age. To assess the possible effects of time on surgical management, two time periods were considered: June 1, 1980 to June 30, 1989 and July 1 1989 to February 1, 2000. These time periods were chosen because they reflect the popularity of laparoscopy during the last decade. Tumour size was recorded as the largest diameter noted on preoperative imaging. Surgeon was categorized as gynaecologist or paediatric, surgical approach as laparoscopy or laparotomy, and surgical procedure as cystectomy or oophorectomy. Laparoscopic cyst dissection was accomplished by aqua or blunt dissection in all cases and removal from the abdomen was achieved by endobag. The ovarian capsule was left unsutured following tumour removal. Intra-operative spill was managed with copious saline irrigation until the lavage was clear. Additional surgery was defined as any other surgery performed at the time of MCT removal. However, if a biopsy of the contralateral ovary was performed during the operation, this was recorded separately. Operative time (in minutes) was recorded from the nursing and anaesthesia record in each chart, and hospital stay (in hours) was recorded from the time of surgery to the time of patient discharge. Since the initial diagnosis of chemical peritonitis is clinical, it was suspected in any patient with postoperative fever and ileus.

Statistical analysis was performed using SPSS 10.0 (SPSS Inc, Chicago, IL, USA). Categorical data were analysed using {chi}2 and Fisher's exact test. Logistic regression was used where the dependent variable was dichotomous. Student's t-test was used for normally distributed data. Mean values are reported with the SD. P <= 0.05 was considered significant and all reported P values are two-sided.


    Results
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 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Fifty-two patients <21 years of age underwent surgery for the removal of a MCT. The median age was 16 years (range 1.3–20). Table IGo demonstrates the presentation, investigation and mean tumour size in girls compared with adolescents.


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Table I. Presentation, investigation and management of girls and adolescents with mature cystic teratomas
 
The most common presentation in girls was abdominal pain and in adolescents it was a palpable adnexal mass. The most common investigation in both groups was ultrasound. The mean size of a MCT in this series was 8.5 ± 4.4 cm and two (3.8%) patients had bilateral tumours.

Fourteen patients (27%) underwent laparoscopic excision of their MCT, median age 16 years (range 4–19 years) with the remainder approached by laparotomy (see Figures 1 and 2GoGo). Overall, laparoscopy was performed more commonly in the recent time period (70% compared with 9.5%, P = 0.008) and patients had smaller tumours than those undergoing laparotomy (5.5 ± 2.4 cm compared with 9.6 ± 4.4 cm, P < 0.001). Significant predictive factors for a laparoscopic approach included tumour size (P = 0.001), time period (P = 0.004) and surgeon (P = 0.04). Patients who had smaller tumours removed by gynaecologists in the more recent time period were the group approached laparoscopically. Twenty-five patients (48%) had tumour removal by cystectomy with the remainder removed by oophorectomy. All patients approached laparoscopically were managed with cystectomy. There was no significant difference in the incidence of cystectomy over time (65% compared with 41%). The only significant predictive factor for cystectomy was MCT size (P = 0.002). Table IGo compares the surgical procedures in girls with adolescents.



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Figure 1. Preoperative ultrasound of an 8 cm mature cystic teratoma in a 4 year old girl.

 


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Figure 2. Postoperative ultrasound at 6 months following laparoscopic removal of an 8 cm mature cystic teratoma in a 4 year old girl.

 
Intra-operative rupture of the MCT occurred in 27 (52%) patients and there were no cases of chemical peritonitis. Rupture was more common with laparoscopy than laparotomy (92.8% compared with 36.8%, P <= 0.001) and in patients managed by cystectomy rather than oophorectomy (92% compared with 14.8%, P < 0.001). In a regression analysis of predictive factors for rupture (including surgical approach, surgical procedure, type of surgeon and size of tumour) only surgical procedure was significant (P = 0.006).

Of the 21 patients (40.4%) who had additional surgery at the time of MCT excision, 18 (85.7%) had elective appendectomy alone, two had ovarian cystectomies for cystadenomas in the contralateral ovary and one had closure of an umbilical hernia. Two patients had appendectomy with concurrent lysis of adhesions and para-ovarian cystectomy respectively. Significant predictive factors for additional surgery included surgeon type (P = 0.001) and earlier time period of presentation (P = 0.007). Specifically, additional surgery, typically appendectomy, was more commonly performed in the earlier time period by paediatric surgeons rather than gynaecologists. Twelve patients (23%) had a biopsy of the contralateral ovary at the time of surgery. This occurred more frequently in the earlier time period (39% compared with 10%, P = 0.01) and although this was more commonly performed by gynaecologists than paediatric surgeons, the difference was not statistically significant (24% compared with 20%).

The mean operating time was 97.0 ± 33.9 min. There was no significant difference between laparoscopy and laparotomy (116.0 ± 51.0 compared with 90.0 ± 21.5 min). The mean postoperative stay was 64.4 ± 31.8 h with significantly shorter stays among patients approached laparoscopically compared with laparotomy (26.8 ± 20.0 compared with 78.3 ± 22.7 h, P < 0.001). Regression analysis (including surgical approach, surgeon and additional surgery) showed that surgical approach (P < 0.001) was the only significant predictive factor of postoperative stay. Perioperative complications occurred in five patients, including four wound infections (two post-laparotomy and two post-laparoscopy) and one bladder injury at the time of suprapubic port placement during laparoscopy.

Follow-up data were available on 34 (65%) patients. The median follow-up time was 28 months (range 1.2–123). The median time for follow-up in those patients managed with cystectomy was 26 months (range 1.2–88). There were seven postoperative pregnancies occurring at a median of 70 months (range 46–123) following surgery. Median age of those who became pregnant was 19 years (range 16–20). Four (57%) patients had had intraoperative MCT spillage, six (86%) had additional surgery at the time of MCT removal and three (43%) had contralateral ovarian biopsy. All seven patients had term deliveries, four vaginally and three by Caesarean section. Six patients had second-look procedures including two for pain at 71 and 66 months respectively, one for bilateral ovarian masses at 12 months and three at the time of Caesarean section. Findings included mild adhesions (as described by the attending surgeon) in four patients whose initial surgery was oophorectomy without cyst spillage. The adhesions were at the site of contralateral ovarian wedge biopsy in one patient and the site of previous oophorectomy in the other three patients. Final pathology in the patient with bilateral ovarian masses revealed a haemorrhagic cyst and a corpus luteum, respectively.

Twenty-one patients had a documented pelvic ultrasound following surgery. Indications included abdominal pain (n = 10), elective (n = 6), palpable mass on pelvic exam (n = 4) and voiding difficulty (n = 1 patient). There were no reported postoperative MCT recurrences or germ cell tumours. However, in one patient who had multiple, large, bilateral MCT removed at laparoscopy, pelvic ultrasound at 6 weeks revealed a 1 cm mass consistent with a MCT. This was thought to be a residual tumour rather than recurrence.


    Discussion
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 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Conservative ovarian surgery in childhood and adolescence is important for the development of normal puberty and future fertility. Mature cystic teratomas constitute half of the benign ovarian masses in this population (Azizkhan and Caty, 1996Go) making the appropriate management of this tumour a vital concern to surgeons caring for patients in this age group.

Pre-operative and intraoperative criteria that have been historically used to predict malignancy in adnexal cystic masses include: adnexal masses with extra-ovarian spread, ultrasonically suspicious masses >8 cm in diameter, a thick cyst wall, a lengthened utero-ovarian ligament or numerous vessels starting from the mesovarium with a comb-like pattern, peritoneal metastases and external ovarian or intracystic vegetations (Canis et al., 1994). Taken together, these criteria have a 100% sensitivity for predicting malignancy but result in a 4% rate of unnecessary laparotomy (Canis et al., 1994). After careful exclusion of an obvious malignancy, ovarian cystectomy has become an accepted option for MCT in adults. If the surgeon is endoscopically experienced, a laparoscopic approach may be considered (Lin et al., 1995Go). However, there has been concern about the impact of laparoscopy on the incidence of intraoperative MCT spill with the subsequent risk of chemical peritonitis and adhesion formation (Nezhat et al., 1999Go). In children with an MCT, oophorectomy has traditionally been performed due to concern about occult germ cell malignancy along with the viability of ovarian tissue and potential for MCT recurrence after cystectomy. At present, experience with a laparoscopic approach in children with MCT is limited to case reports (Cohen et al., 1996Go; Garcia et al., 1996Go; Jawad, 1998; Liu et al., 1998Go). The aim here was to address some of these management concerns in children and adolescents.

The results show that abdominal pain and torsion as presenting symptoms were more common among young girls. Adolescent tumours were more likely to be detected on pelvic examination. Ultrasound was the most commonly used diagnostic test and this is appropriate given that the positive predictive ability of ultrasound approaches 100% when two or more characteristic findings for MCT, such as shadowing echodensity and regionally bright echodensity are present (Patel et al., 1998Go).

A laparoscopic approach to the management of MCT in adults has now become accepted practice among many surgeons (Luxman et al., 1996Go; Yuen et al., 1997Go; Morgante et al., 1998Go). A consistent benefit to the patient is a shorter hospital stay (Howard, 1995Go; Lin et al., 1995Go; Morgante et al., 1998Go; Zanetta et al., 1999Go). A shorter hospital stay was also demonstrated among our patients approached laparoscopically, suggesting that the benefit afforded adults is also applicable to children. Until recently, inadequate instrumentation made this approach difficult in children and this is reflected in our series where laparoscopy was confined almost entirely to the more recent time period. Among our patients, surgeon type was predictive of operative approach. This may be explained by the greater experience of gynaecologists with laparoscopic adnexal surgery. Our results suggest that young patients particularly suited to a laparoscopic approach are those with smaller tumours (all <=8 cm, mean 5.5 cm in our series).

The diagnosis of chemical peritonitis is suspected in the presence of postoperative fever and ileus associated with granulomatous deposits on the abdominal peritoneum and adhesion formation (Huss et al., 1996Go). This concern has been addressed in the adult literature and chemical peritonitis has been found to occur with an estimated incidence of 0.2% following laparoscopic excision of an MCT (Nezhat et al., 1999Go) if spillage is managed by immediate copious lavage (Zanetta et al., 1999Go). In our series, there were no cases of chemical peritonitis, confirming that spill in children can be managed in the same way as adults with similar expectations for a successful outcome.

Intraoperative tumour spillage also raises the concern of postoperative adhesion formation. This issue is confounded in adults because few patients have had second-look procedures. Also, many patients undergoing MCT removal have had concurrent reproductive surgery, including resection of endometriosis, tubal adhesiolysis or myomectomy (Nezhat et al., 1989Go; Bollen et al., 1992Go) all of which may themselves promote adhesion formation. Concurrent surgery among our patients was almost entirely elective appendectomy (85.7%) and this has been shown not to affect future fertility (Andersson et al., 1999Go). In our series, postoperative intrauterine pregnancy occurred in seven (20.6%) patients, four of whom had intraoperative spill of MCT contents and six who had additional surgery at the time of MCT removal. As in adults (Canis et al., 1992Go), this suggests that even if tumour spillage does promote adhesion formation, future fertility is possible.

Biopsy of the contralateral ovary was performed in 12 patients, typically by gynaecologists in the earlier time period. This was likely to be due to concerns about the presence of MCT in the contralateral ovary. However, ovarian wedge biopsy is not without complication and may result in haemorrhage, infection, and adhesion formation (Toaff et al., 1976Go). It is unlikely to be positive if the contralateral ovary is normal in appearance since the chance of an occult MCT is 1.1% (Doss et al., 1977Go; Ayhan et al., 1991Go). Therefore, since ultrasound is a good predictor of MCT presence, preoperative ultrasound in combination with careful inspection of the contralateral ovary at the time of surgery offers a safe alternative to wedge biopsy (Commerci et al., 1994Go).

In adults, the reported incidence of recurrent MCT following cystectomy is 3–4% (Anteby et al., 1994Go; Chapron et al., 1994Go) and usually occurs in patients under 40 years of age (Anteby et al., 1994Go). Also, in younger patients with multiple or bilateral MCT there is a 2–3% incidence of the subsequent development of germ cell tumours (Borenstein et al., 1982Go; Yanai-Inbar and Scully, 1987Go; Anteby et al., 1994Go). In our series there were no reported cases of recurrence among the 19 patients (of a total of 25) managed with cystectomy in whom follow-up data were available. However, this may be due to insufficient follow-up time since recurrences and germ cell tumours may occur months to many years following surgery (Chapron et al., 1994Go).

This study demonstrates that some of the conclusions regarding the contemporary management of MCT in adults are applicable to children and adolescents. In particular, the benefit of shorter hospital stay achieved in adults with a MCT approached laparoscopically extends to our population. Chemical peritonitis may be avoided and future fertility is possible if intraoperative MCT spill is managed with copious saline irrigation.

In the absence of specific literature investigating MCT recurrence in children, recommendations for postoperative surveillance are empirical. Given the sensitivity of ultrasound in the detection of MCT, annual imaging in prepubertal and young adolescents followed by annual pelvic examinations in older adolescents seems appropriate.


    Notes
 
4 To whom correspondence should be addressed at: Kosair Children's Hospital, P.O. Box 35070, Louisville, KY 40232-5070, USA. E-mail: mefall01{at}athena.louisville.edu Back


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 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
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Submitted on May 19, 2000; accepted on August 15, 2000.