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Noninflammatory Ovarian Masses in Girls and Young Women

From the Division of Pediatric Gynecology, Department of Obstetrics and Gynecology, and the Division of Pediatric Surgery, Department of Surgery, University of Louisville School of Medicine and Kosair Children’s Hospital, Louisville, Kentucky.

Address reprint requests to: S. Paige Hertweck, MD Department of Obstetrics and Gynecology University of Louisville 550 Jackson Street Louisville, KY 40492

	Abstract

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Objective: We reviewed the presentation, treatment, and pathologic diagnoses of girls and young women less than 21 years old with noninflammatory ovarian masses that required surgery and established whether treatment had changed over time.

Methods: We retrospectively reviewed charts of all girls and young women under 21 years old with International Classification of Diseases, 9th Revision (ICD-9) codes specific for noninflammatory ovarian masses treated at our institution from June 1980 to July 1998 (n = 140).

Results: The median age at surgery was 15 years (range 2 days–21 years). Ovarian cysts occurred in 57.9% (81 of 140) of patients, benign tumors (including mature cystic teratomas) in 30% (42 of 140), malignant tumors in 7.9% (11 of 104), and torsed but normal ovaries in 4.3% (six of 140) of the study sample. Patients older than 15 years were more likely to have ovarian cysts and benign tumors than younger patients (P = .019). There were no malignancies among girls with neonatal cysts. The incidence of ovarian torsion was 17.8% (25 of 140). Patients with ovarian cysts, mature cystic teratomas, and normal ovaries were more likely to have torsion than those with other benign or malignant tumors (P < .001). Operative approach and surgical procedure were compared before and after July 1, 1989. Laparoscopy was performed more commonly after July 1, 1989 (P = .009). However, patient age (P < .001) rather than time of surgery (P = .83) was the most important predictive factor in a multivariate analysis for use of laparoscopy. In addition, multivariate analysis revealed that patient age (P = .02) rather than time of surgery (P = .79) was also predictive of surgeon type (gynecologist or pediatric surgeon).

Conclusion: The most frequent cause of an ovarian mass requiring surgery in a girl or young woman under 21 years of age is an ovarian cyst, which justifies consideration of a laparoscopic approach. Patient age rather than time of surgery predicted operative approach and surgeon type. Caution should be exercised in patients over age 12 months with a complex mass on ultrasound and clinical evidence of hormonal activity, as these masses are usually malignant.

Malignant ovarian tumors in children and adolescents are rare, accounting for 0.9% of all malignancies in this age group.¹ However, the improved resolution of ultrasound has resulted in more frequent identification of benign ovarian pathology in girls of all ages, including infants.² The increasing use of laparoscopic techniques and conservative ovarian surgery in adults has provided new options in pediatric patients, where future reproductive function is of prime concern. The aim of this study was to review our experience with noninflammatory ovarian masses in patients under 21 years of age that required surgery. In particular, we wished to establish whether treatment has changed over time with the advent of more conservative surgical techniques.

	Materials and Methods

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The International Classification of Diseases, 9th Revision (ICD-9) codes specific for noninflammatory ovarian masses were used to identify patients who received care at Kosair Children’s Hospital and Norton Hospital in Louisville, Kentucky between June 1980 and July 1998. This retrospective case series included patients 21 years old or younger who required operative intervention and removal of ovarian tissue. One hundred forty patients met these criteria. The records were reviewed for age at presentation, presenting symptoms, diagnostic studies, operative approach, surgical procedure, pathology findings, and surgeon type (gynecologist or pediatric surgeon). For purposes of further analysis, girls were defined as patients 15 years or younger, and pathologic diagnosis was divided into the following five categories: ovarian cyst, benign tumor, mature cystic teratoma (dermoid tumor), malignant tumor, and normal ovary. Operative approach and surgical procedure were compared during two periods, June 1, 1980 to June 30, 1989 (period 1) and July 1, 1989 to July 31, 1998 (period 2). The size of the ovarian cyst or tumor was recorded by two methods in all cases, including largest diameter on ultrasound and an envelope measure, calculated by the product of the two largest diameters on ultrasound.

Statistical analysis was performed using SPSS 8.0 (SPSS Inc., Chicago, IL). Categoric data were analyzed using ² test, Fisher exact test, and Monte Carlo simulation as appropriate. Normally distributed data were analyzed using Student t test, analysis of variance and covariance, and logistic regression. Mean values are reported with the standard deviation (SD). Statistical significance for all tests was set at P .05. All reported P values are two-sided.

	Results

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The median age at surgery was 15 years (range 2 days–21 years). Patients requiring surgery during period 2 were significantly younger than those during period 1. Table 1 shows the comparison between the two periods in terms of age, pathology, operative approach and procedure, surgeon type, and ovarian torsion. Table 2 details presenting signs, symptoms, and diagnostic studies performed. Abdominal pain was the most common presenting symptom during both periods, occurring in 62% (41 of 66) of patients during period 1 and 77% (57 of 74) of patients during period 2 (P = .055). Because of the wide age range at surgery and the varied nature of the presenting symptoms, many patients had more than one diagnostic test, although pelvic ultrasound was the most common. Three patients presented with hirsutism and virilism; the underlying pathology was Sertoli-Leydig tumor in each case. Precocious puberty was the presenting condition in two patients, one of whom had a granulosa cell tumor and the other a dysgerminoma. Three ovarian masses were diagnosed by antenatal ultrasound. In a 9-month-old girl, the presenting symptom was an inguinal hernia containing a torsed adnexa.

Ovarian torsion occurred in 17.8% (25 of 140) of patients in this study. The median age of patients with ovarian torsion was 12 years (range 3 days–21 years). All 25 patients presented with abdominal pain and 20 (80%) had associated vomiting. Abdominal or pelvic ultrasound showed complex ovarian masses in 78.3% (18 of 23) of patients who had imaging studies. Laparotomy was the most common surgical approach (76%, 19 of 25 patients) and salpingo-oophorectomy (60%, 15 of 25 patients) the most common surgical procedure. Detorsion alone was done in two patients. The most frequent pathologic diagnosis in patients with torsion was an ovarian cyst in 48% (12 of 25 patients), followed by a dermoid tumor in 28% (seven of 25 patients), and a normal ovary in 24% (six of 25 patients). Patients with these pathologic diagnoses were significantly more likely to have torsion than patients with other tumors (benign or malignant) (P < .001). There was no difference in size of ovarian mass in patients with torsion (8.1 ± 4.1 cm) compared with those without (7.1 ± 5.5 cm) (P = .57).

Mature cystic teratomas were the most common benign ovarian tumor among patients in our study with an incidence of 21.4% (30 of 140). Among girls, the incidence was 18% (13 of 72), and in young women over 15 years old it was 25% (17 of 68). Complex ovarian masses were seen on ultrasound examination in all cases. We compared operative approach and surgical procedure for mature cystic teratomas diagnosed before and after July 1, 1989. Our results show a significant increase in the use of laparoscopy in period 2 (0% compared with 33.3%, P = .018). Although the use of ovary-sparing tumor excision (cystectomy) was also more common during period 2, the difference was not statistically significant (P = .09).

Eight patients with ovarian masses were under 12 months old (mean 66 days, range 8–270 days). Three ovarian masses were diagnosed antenatally, and the remainder of patients presented with either a palpable mass or with abdominal distension and vomiting. All but one patient had an ultrasound. One infant had an inguinal hernia containing a torsed ovary. There was one case of torsion in an infant with a large follicular cyst. There were no benign or malignant tumors in this group, and seven of eight patients had large simple follicular cysts of mean diameter 7.7 cm (range 6–10 cm). All infants were operated on using laparotomy, except for the infant with an inguinal hernia and a 4-month-old infant who had laparoscopy. Most infants (five of eight) had oophorectomies and three had ovarian cystectomies.

The surgical treatment of all ovarian masses over time was assessed in our study by comparing operative approach and surgical procedure before and after July 1, 1989. A laparoscopic approach was statistically more likely to be used after July 1, 1989 (Table 1). However, when patient age and time of surgery were combined in a logistic regression analysis, patient age (P < .001) rather than time of surgery (P = .83) was predictive of operative approach. This is demonstrated by 98% (53 of 54) of all laparoscopies being performed in patients 12.5 years old or older. Although more ovarian cystectomies were done during period 2, the difference was not statistically significant (P = .27). To evaluate for possible confounding factors in surgical treatment over time, we assessed surgeon type during the two periods. Pediatric surgeons were more likely than gynecologists to operate during period 2 (Table 1). However, when age (15 years and younger compared with older than 15 years) and time of surgery were combined in logistic regression analysis, patient age (P = .02) rather than time of surgery (P = .79) was predictive of surgeon type.

	Discussion

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The aim of this study was to examine over time the treatment of ovarian masses in girls and young women. We found that patient age, rather than time of surgery, was the most important factor influencing operative approach and surgeon type in this population. Pediatric surgeons operated more frequently during period 2 than period 1, and this is reflective of the younger mean age of the patients in that group. In addition, although laparoscopy was significantly more frequent during recent years, this increase was confined to postmenarchal young women in whom gynecologists were more likely to operate. Pathology was also an important factor, as ovarian malignancies were more common in our patients 15 years old or younger, with ovarian cysts and benign tumors more likely in older patients.

Although ovarian neoplasms in children are rare, the diagnosis should be considered in any female patient presenting with abdominal pain or mass. Among our patients, 70% presented with abdominal pain and 35.7% with a palpable mass. Abdominal distension and vomiting were additional prominent symptoms among infants. The incidence of ovarian malignancy among patients requiring ovarian surgery in the first decade of life has been reported to vary from 9.6%³ to 82%.⁴ This discrepancy is likely a result of the nature of the referral institution as more children with malignancies will be referred to tertiary centers. However, we found that the malignancy rate varied depending on the age group examined and was highest (11.1%) among patients between age 12 months and 15 years. In children and adolescents with ovarian neoplasms, the frequency of germ-cell tumors is reported to vary from 67–85%.⁵ In our series it was 69%. Unusual presenting symptoms, such as virilism and precocious puberty in conjunction with a mass, were indicators of malignancy in our study, although these symptoms collectively accounted for less than 5% of initial presentations among our patients.

The surgical treatment of mature cystic teratomas is currently debated. Laparotomy and oophorectomy or cystectomy have been the most accepted forms of treatment. However, recent literature for adult populations suggests that laparoscopic excision is a safe procedure, particularly when an endobag is used to remove the tumor from the abdomen.^6–8 There appears to be no increase in recurrence rate when compared with laparotomy.⁹ The decision to use this approach in children is likely to depend upon the laparoscopic skills of the particular surgeon. At present there is no long-term follow-up information on reproductive function in children or adolescents who have had laparoscopic cystectomy for mature cystic teratoma.

Recent studies using high-resolution ultrasound suggest that ovarian enlargement detected on ultrasound is most likely caused by a benign cyst.¹⁰ Our results confirm that, as benign ovarian cysts associated with persistent abdominal pain were the most frequent reason for surgical intervention in our series. Among infants less than 12 months old, the abnormality was almost exclusively a follicular cyst. It is well established that neonates can have small simple ovarian cysts less than 4 cm as a result of maternal (estrogen), placental (hCG), or fetal hormones (FSH).^11,12 In a series of 64 infants with antenatally diagnosed ovarian cysts (mean diameter 4 cm), Sakala et al¹³ found that 64% involuted postpartum. In 90% of cases this process was complete by 3 months of age; however, a small number of cysts did not involute until the infant was 12 months old. The indications for surgical intervention include complex appearance on ultrasound (the presence of fluid debris, retracting clot, or solid components),¹¹ increasing cyst size, or an infant that becomes symptomatic with a distended abdomen, vomiting, or anemia.¹³ All five neonates in our series had large cysts (mean 7.7 cm diameter) that were not decreasing in size. Additionally, two infants had a large solid- or complex-appearing mass on ultrasound that required intervention. Subsequent pathology in those two patients revealed ovarian torsion and hemorrhage into a follicular cyst. It was reported previously that persistence of a neonatal ovarian cyst suggests a cyst accident such as hemorrhage or torsion.¹⁴

Ovarian torsion is most common in the first 3 decades of life.¹⁵ Among our patients with torsion, all ovarian masses were either mature cystic teratomas or ovarian cysts. There were no malignancies. This is consistent with results of Quint and Smith,³ who found no ovarian malignancy among 18 premenarchal girls with ovarian torsion. Six patients with ovarian torsion in our series had enlarged but normal ovaries, which has also been reported.¹⁶ We could not relate torsion to ovarian size in our study because of inadequate power (only 25 patients had torsion). However, it could also be because all patients in our study had enlarged ovaries. Alternatively, torsion might be related to another factor, such as ovarian volume, shape, or the length of the ovarian ligament, rather than ovarian size. The treatment of ovarian torsion traditionally has been by oophorectomy because of possible embolization after detorsion.¹⁷ Oophorectomy was the most common procedure among our patients. However, ovarian cystectomy was done in five patients and detorsion alone in two. These more conservative procedures were all done after 1989, consistent with more recent literature supporting detorsion as an alternative approach.^17,18

The overall approach to symptomatic ovarian masses among children and adolescents in our institution has become more conservative, which is appropriate, as the most common cause of symptomatic ovarian enlargement in our series was a benign cyst. If ovarian cystectomy is contemplated, caution should be exercised in patients over 12 months of age with complex or solid ovarian masses accompanied by evidence of hormonal activity. In our experience these tumors are often malignant. Ovarian size alone did not distinguish between benign and malignant tumors among our patients. Before an operative approach is chosen, it is important to consider the clinical presentation, tumor marker profile, and other imaging signs that indicate malignancy.

	Footnotes

 
The authors gratefully acknowledge the contribution of Dr. Jane Goldsmith for assistance with statistical analysis.

PII S0029-7844(00)00929-7

Received September 27, 1999. Received in revised form February 24, 2000. Accepted March 9, 2000.

	References

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2. Murray S, London S. Management of ovarian cysts in neonates, children, and adolescents. J Pediatr Adolesc Gynecol 1995;8:64–70.

3. Quint EH, Smith YR. Ovarian surgery in premenarchal girls. J Pediatr Adolesc Gynecol 1999;12:27–30.[Medline]

4. Haefner HK, Roberts JA, Schmidt RW. The university experience of clinical and pathological findings of ovarian neoplasms in children and adolescents. J Pediatr Adolesc Gynecol 1992;5:182–6.

5. Breen J, Maxson WS. Ovarian tumours in childhood and adolescence. Clin Obstet Gynecol 1977;20:607–23.[Medline]

6. Rosen DM, Lam AM, Carlton MA, Cario GM. The safety of laparoscopic treatment for ovarian dermoid tumours. Aust N Z J Obstet Gynaecol 1998;38:77–9.[Medline]

7. Luxman D, Cohen JR, David MP. Laparoscopic conservative removal of ovarian dermoid cysts. J Am Assoc Gynecol Laparosc 1996;3:409–11.[Medline]

8. Lin P, Falcone T, Tulandi T. Excision of ovarian dermoid cysts by laparoscopy and by laparotomy. Am J Obstet Gynecol 1995;173: 769–71.[Medline]

9. Nitke S, Goldman GA, Fisch B, Kaplan B, Ovadia J. The management of dermoid cysts: A comparative study of laparoscopy and laparotomy. Isr J Med Sci 1996;32:1177–9.[Medline]

10. Diamond M, Baxter J, Peerman C. Occurrence of ovarian malignancy in childhood and adolescence: A community wide evaluation. Obstet Gynecol 1988;17:858–62.

11. Brandt M, Luks F, Filiatrault D, Garel L, Desjardins JG, Youssef S. Surgical indications in antenatally diagnosed ovarian cysts. J Pediatr Surg 1991;26:276–9.[Medline]

12. Croitoru D, Aaraon L, Laberge J, Neilson IR, Guttman FM. Management of complex ovarian cysts presenting in the first year of life. J Pediatr Surg 1991;26:1366–8.[Medline]

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14. Nussbaum AR, Sanders RC, Hartman DS, Dudgeon DL, Parmly TH. Neonatal ovarian cysts: Sonographic-pathologic correlation. Radiology 1988;168:817–21.[Abstract/Free Full Text]

15. Warner MA, Fliescher AC, Edell SL, Thieme GA, Bundy AL, Kurtz AB. Uterine adnexal torsion: Sonographic findings. Radiology 1985;154:773–5.[Abstract/Free Full Text]

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17. Oelsner G, Bider D, Goldenberg M, Admon D, Mashiach S. Long-term follow-up of the twisted ischemic adnexa managed by detorsion. Fertil Steril 1993;60:976–9.[Medline]

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