Obstetrics & Gynecology:
Access to Conservative Surgical Therapy for Adolescents With Benign Ovarian Masses
Berger-Chen, Sloane MD; Herzog, Thomas J. MD; Lewin, Sharyn N. MD; Burke, William M. MD; Neugut, Alfred I. MD, PhD; Hershman, Dawn L. MD; Wright, Jason D. MD
From the Departments of Obstetrics and Gynecology and Medicine, Columbia University College of Physicians and Surgeons, the Department of Epidemiology, Mailman School of Public Health, and the Herbert Irving Comprehensive Cancer Center, New York, New York.
Corresponding author: Jason D. Wright, MD, Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Columbia University College of Physicians and Surgeons, 161 Fort Washington Avenue, 8th Floor, New York, NY 10032; e-mail: firstname.lastname@example.org.
Financial Disclosure The authors did not report any potential conflicts of interest.
OBJECTIVE: To perform a population-based analysis to determine possible factors associated with use of laparoscopy and ovarian-conserving cystectomy.
METHODS: Women and girls aged 18 years or younger with benign ovarian masses who underwent surgery from 2000 to 2010 and were recorded in a commercial database were analyzed. Patients were classified based on the surgical approach (open compared with laparoscopy) and procedure (oophorectomy compared with cystectomy). Use of laparoscopy and performance of cystectomy were characterized using multivariable logistic regression models accounting for patient, surgeon, and hospital characteristics.
RESULTS: A total of 2,126 patients, including 1,425 (67.0%) who underwent laparotomy and 701 (33.0%) who had laparoscopy, were identified. Laparoscopy increased from 32.1% in 2000 to 57.9% by 2010. In a multivariable model, African American women and girls (odds ratio [OR] 0.49, 95% confidence interval [CI] 0.37–0.65) and patients in the Northeast (OR 0.65, 95% CI 0.46–0.94) were less likely to undergo laparoscopy, whereas treatment at a high-volume hospital (OR 1.35, 95% CI 1.04–1.75) was associated with use of laparoscopy. Cystectomy was performed in 57.1% in 2000 and increased to 61.4% in 2010. The only significant predictors of cystectomy were age and the specialty of the treating physician; patients aged 13–16 years (OR 1.34, 95% CI 1.03–1.75) were more likely to undergo cystectomy than were younger patients, whereas patients treated by surgeons (OR 0.51, 95% CI 0.38–0.68) were less likely to undergo cystectomy than were those treated by gynecologists.
CONCLUSION: The treatment of adolescents with benign ovarian masses is highly variable. In addition to patient characteristics, both physician and hospital factors strongly influenced treatment.
LEVEL OF EVIDENCE: II
Adnexal masses in adolescents are rare. Although precise population-based estimates are lacking, it is estimated that ovarian masses arise in approximately 2.6 per 100,000 girls younger than 18 years of age.1,2 The vast majority of these ovarian masses are either cysts or benign neoplasms. Malignant ovarian tumors are found in approximately 10% of adolescents with adnexal masses.1,3–5 Among adolescents with invasive malignancies, ovarian germ cell tumors predominate.1,3,6
Given the low frequency with which ovarian masses are seen in adolescents, evidence-based recommendations to guide treatment are largely lacking. Traditional treatment consists of unilateral oophorectomy. Although appropriate for most malignancies to avoid spillage and extirpate the entire tumor, there is growing recognition that less aggressive treatment is adequate for benign neoplasms.3,6–10 Ovarian-conserving cystectomy has proven safe for adolescents and reproductive-aged women and is now recommended as the procedure of choice by many gynecologic surgeons.3,6,8–13
The past decade also has seen an increase in the use of laparoscopic surgery for the treatment of adnexal masses. For adult women, randomized studies have shown that laparoscopic surgery is associated with reduced perioperative morbidity, shorter postoperative recovery, and improved cosmesis.14,15 Given these findings, laparoscopic surgery has also gained increased acceptance and popularity in adolescents.6,10,11,16–19
Despite the controversy surrounding the management of adnexal masses in adolescents, few data are available to describe the care these patients receive. The objective of our study was to examine the patterns of care of adolescents with benign adnexal masses. Specifically, we performed a population-based analysis to determine the possible patient, physician, and hospital characteristics associated with use of minimally invasive surgery and ovarian-conserving cystectomy in adolescents treated throughout the United States.
MATERIALS AND METHODS
We used the Perspective database. Perspective is a nationwide database originally developed to measure resource use and quality. The sampling frame of Perspective includes more than 500 acute-care hospitals throughout the United States.20 Perspective collects data on demographics, disease characteristics, procedures, and all billed services. The database is validated and has been used in a number of outcomes studies.21,22 In 2006, Perspective recorded approximately 5.5 million hospital discharges, which represents approximately 15% of nationwide hospitalizations.20,22 A study exemption was obtained from the Columbia University institutional review board.
We analyzed adolescents aged 18 years or younger who underwent surgery for a benign ovarian neoplasm (International Classification of Diseases, 9th Revision [ICD-9] code 220) between 2000 and 2010. Patients were stratified based on the primary procedure performed as having undergone either ovarian cystectomy (ICD-9 code 65.22, 65.24, 65.25, or 65.29) or oophorectomy (ICD-9 codes 65.3x–65.6x). Patients who had ICD-9 codes for both cystectomy and oophorectomy were included in the oophorectomy group. Each procedure was further classified based on the mentioned ICD-9 coding as either an open or laparoscopic surgery.
Demographic data analyzed included age (younger than 13, 13–16, 17–18 years), race (white, African American, other), insurance status (commercial, Medicaid, or other or unknown), and year of diagnosis (2000–2003, 2004–2006, 2007–2010). The hospitals in which patients were treated were characterized based on location (metropolitan, nonmetropolitan), region of the country (Northeast, Midwest, West, South), size (less than 400 beds, 400–600 beds, and more than 600 beds), and teaching status (teaching, nonteaching).
We recorded the specialty of the attending surgeon of the procedure. We classified procedure physicians into the following groups: gynecologists (all obstetricians and gynecologists including gynecologic oncologists), surgeon (general surgery or any surgical subspecialty), and other or unknown. For each surgeon and hospital, we determined the total number of ovarian procedures performed on adolescents during the study period. Because not all physicians and hospitals contributed data for the entire study period, we calculated annualized procedure volumes. The annualized procedure volume was estimated by dividing the total number of patients who underwent a procedure by the number of years a given surgeon or hospital contributed at least one procedure. The volumes were then divided into low- and high-volume strata.
Frequency distributions between categorical variables were compared using chi-squared tests. The primary outcomes of interest were performance of laparoscopy and ovarian-conserving cystectomy. The association between patient, physician, and hospital characteristics and the outcomes of interest were assessed using multivariable logistic regression models. Results are reported with odds ratios (ORs) and 95% confidence intervals (CIs). All analyses were performed with SAS 9.2. All statistical tests were two-sided.
A total of 2,126 patients, including 1,425 (67.0%) who underwent laparotomy and 701 (33.0%) who underwent laparoscopy, were identified (Table 1). Use of laparoscopy increased with time from 32.1% in 2000 to 57.9% in 2010 (P<.001) (Fig. 1). Laparoscopic surgery was performed in 37.1% of white patients compared with 22.5% of African American patients (P<.001). Likewise, 35.0% of adolescents with commercial insurance had a laparoscopic procedure compared with 29.9% of those with Medicaid (P=.008). Patients operated on by gynecologists were more likely to have laparoscopy than were those treated by surgeons (35.0% compared with 29.3%) (P=.006). Area of residence, physician procedure volume, and hospital volume had no effect on use of laparoscopy (P>.05).
The rate of ovarian-conserving cystectomy was 57.1% in 2000, decreased to 48.4% in 2001, and then gradually rose to 61.4% by 2010 (P=.17) (Fig. 2). Cystectomy was performed in 55.4% of white adolescents compared with 45.0% of African Americans (P=.002). Similarly, 54.9% of patients with commercial insurance had a cystectomy compared with 48.4% of those with Medicaid (P=.008). Adolescents treated at nonteaching hospitals, small facilities, low-volume hospitals, by low-volume physicians, and at institutions in the Midwest were more likely to undergo cystectomy (P<.05 for all). Cystectomy was performed by 57.6% operated on by gynecologists compared with 37.3% of patients treated by surgeons (P<.001).
In a multivariable model, African American patients (OR 0.49, 95% CI 0.37–0.65) and those in the Northeast (OR 0.65, 95% CI 0.46–0.94) were less likely to undergo laparoscopy, whereas treatment in 2007–2010 (OR 2.43, 95% CI 1.90–3.11) and surgery at a high-volume hospital (OR 1.35, 95% CI 1.04–1.75) were associated with performance of a laparoscopic procedure (Table 2). The only significant predictors of cystectomy were age and the specialty of the treating physician; patients aged 13–16 years (OR 1.34, 95% CI 1.03–1.75) were more likely to undergo cystectomy than were younger patients, whereas those treated by surgeons (OR 0.51, 95% CI 0.38–0.68) were less likely to undergo cystectomy than were patients treated by gynecologists. Patients treated laparoscopically were more likely to undergo cystectomy (OR 2.23, 95% CI 1.83–2.71).
Our findings suggest that the treatment of adolescents with benign ovarian masses is highly variable. Young women and girls with benign ovarian tumors frequently still undergo laparotomy, and many are treated with oophorectomy. In addition to patient characteristics, both physician and hospital characteristics strongly influence the care these patients receive.
We were encouraged to note that the use of laparoscopy increased over the past decade and approached 60% by 2010. Among adolescents, a number of reports have suggested that laparoscopic surgery is safe for the management of adnexal masses.6,10,11,17–19 For many surgical procedures, sociodemographic characteristics exert substantial influence on access to laparoscopy.23–28 Appendectomy, hysterectomy, cholecystectomy, and colectomy are all more likely to be performed laparoscopically in white compared with African American patients.23–28 Similarly, insurance status plays a major role in access to laparoscopy; in one report patients with private insurance were more than 50% more likely to undergo a laparoscopic procedure than those with Medicaid.24 We noted that race and insurance status were two of the most important predictors of access to laparoscopy.
Despite the widespread use of ovarian cystectomy in adult women, uptake among adolescents has been slow; almost 40% of those aged younger than 18 years still underwent oophorectomy. These findings are somewhat surprising because adolescents have a very low risk of malignancy and young women and girls are the most likely to derive benefit from ovarian conservation.1,4–6 There is increasing recognition of the possible sequela of unilateral oophorectomy. Women with a single ovary have decreased ovarian reserve, and those who are treated for infertility have higher gonadotropin requirements and may have lower clinical pregnancy rates.29 Additionally, young women and girls who have undergone oophorectomy remain at risk for pathology in the contralateral ovary, which, if removed, would result in premature menopause. The balance of evidence suggests that ovarian cystectomy should be the procedure of choice whenever it is deemed safe and technically feasible.
There was substantial variation in practice patterns based on the specialty of the attending surgeon. Compared with those treated by general surgeons, patients operated on by gynecologists were more likely to undergo a laparoscopic procedure as well as cystectomy. In a series of 82 women and girls aged 18 years or younger, Bristow and colleagues noted that gynecologists were more than eight times more likely to perform ovarian-conserving surgery than surgeons.6 A similar series noted that postmenarchal patients less likely to undergo oophorectomy and that patients treated by gynecologic oncologists were more likely to undergo complete surgical staging for cancers.12 The etiology of the disparate patterns of care is likely multifactorial. Even at high-volume centers, ovarian surgery in adolescents is rare. Data from the pediatric surgery department of one tertiary center showed that ovarian operations accounted for only 0.2% of the overall caseload per year.3 Similar trends are likely for gynecologists and there is now increased emphasis on training specialists in pediatric gynecology. Regardless of the underlying cause of our findings, our data suggest that adolescents should be referred to clinicians with expertise in the management of ovarian masses.
Although our study benefits from the inclusion of a large number of adolescents from across the United States, we recognize a number of important limitations. Perhaps most importantly, we lacked data on the characteristics of the masses and the final pathology of these lesions. Undoubtedly, operative planning was influenced by the size of the masses as well as their morphology on imaging. Some of the differences in treatment we noted were likely the result of this difference in case mix. Our data set lacks detail on body mass index, habitus, and surgical history. We cannot exclude the possibility that some patients' procedures were misclassified. To minimize bias, we included only patients with benign ovarian neoplasms and used well-recognized ICD-9 procedural codes. Although we were able to examine surgeon specialty, many important physician characteristics including age, gender, and year of graduation from medical school were lacking in our data set. Finally, despite the fact that we included data from over a 10-year period, the power of our study may have been limited to detect some differences in treatment between the groups.
Our findings shed light on the patterns of care for adolescents with ovarian masses. Although the use of laparoscopy and cystectomy increased with time, our data suggest that there are still large numbers of patients, particularly minorities and those who lack commercial insurance, without access to these treatments. These data have important implications for patients, providers, and payors. Our work suggests that ovarian conservation among adolescents who undergo adnexal surgery may be an important quality. Further work to promote educational interventions and multidisciplinary treatment planning for adolescents with ovarian pathology should be encouraged so all young women and girls who require intervention have access to high-quality care.
1. Skinner MA, Schlatter MG, Heifetz SA, Grosfeld JL. Ovarian neoplasms in children. Arch Surg 1993;128:849–53.
2. Lindfors O. Primary ovarian neoplasms in infants and children. A study of 81 cases diagnosed in Finland and Sweden. Ann Chir Gynaecol Fenn Suppl 1971;177:1–66.
3. Cass DL, Hawkins E, Brandt ML, Chintagumpala M, Bloss RS, Milewicz AL, et al.. Surgery for ovarian masses in infants, children, and adolescents: 102 consecutive patients treated in a 15-year period. J Pediatr Surg 2001;36:693–9.
4. Diamond MP, Baxter JW, Peerman CG Jr, Burnett LS. Occurrence of ovarian malignancy in childhood and adolescence: a community-wide evaluation. Obstet Gynecol 1988;71:858–60.
5. Quint EH, Smith YR. Ovarian surgery in premenarchal girls. J Pediatr Adolesc Gynecol 1999;12:27–9.
6. Bristow RE, Nugent AC, Zahurak ML, Khouzhami V, Fox HE. Impact of surgeon specialty on ovarian-conserving surgery in young females with an adnexal mass. J Adolesc Health 2006;39:411–6.
7. Milingos S, Protopapas A, Drakakis P, Liapi A, Loutradis D, Rodolakis A, et al.. Laparoscopic treatment of ovarian dermoid cysts: eleven years' experience. J Am Assoc Gynecol Laparosc 2004;11:478–85.
8. Seckin B, Ozdener T, Tapisiz OL, Batioglu S. Laparoscopic treatment of ovarian cysts in adolescents and young adults. J Pediatr Adolesc Gynecol 2011;24:300–3.
9. Savasi I, Lacy JA, Gerstle JT, Stephens D, Kives S, Allen L. Management of ovarian dermoid cysts in the pediatric and adolescent population. J Pediatr Adolesc Gynecol 2009;22:360–4.
10. Shapiro EY, Kaye JD, Palmer LS. Laparoscopic ovarian cystectomy in children. Urology 2009;73:526–8.
11. Brandt ML, Helmrath MA. Ovarian cysts in infants and children. Semin Pediatr Surg 2005;14:78–85.
12. Eskander RN, Bristow RE, Saenz NC, Saenz CC. A retrospective review of the effect of surgeon specialty on the management of 190 benign and malignant pediatric and adolescent adnexal masses. J Pediatr Adolesc Gynecol 2011;24:282–5.
13. Islam S, Yamout SZ, Gosche JR. Management and outcomes of ovarian masses in children and adolescents. Am Surg 2008;74:1062–5.
14. Mais V, Ajossa S, Piras B, Marongiu D, Guerriero S, Melis GB. Treatment of nonendometriotic benign adnexal cysts: a randomized comparison of laparoscopy and laparotomy. Obstet Gynecol 1995;86:770–4.
15. Yuen PM, Yu KM, Yip SK, Lau WC, Rogers MS, Chang A. A randomized prospective study of laparoscopy and laparotomy in the management of benign ovarian masses. Am J Obstet Gynecol 1997;177:109–14.
16. Mayer JP, Bettolli M, Kolberg-Schwerdt A, Lempe M, Schlesinger F, Hayek I, et al.. Laparoscopic approach to ovarian mass in children and adolescents: already a standard in therapy. J Laparoendosc Adv Surg Tech A 2009;19(suppl 1):S111–5.
17. Templeman C, Fallat ME, Blinchevsky A, Hertweck SP. Noninflammatory ovarian masses in girls and young women. Obstet Gynecol 2000;96:229–33.
18. Jawad AJ, Al-Meshari A. Laparoscopy for ovarian pathology in infancy and childhood. Pediatr Surg Int 1998;14:62–5.
19. Cohen Z, Shinhar D, Kopernik G, Mares AJ. The laparoscopic approach to uterine adnexal torsion in childhood. J Pediatr Surg 1996;31:1557–9.
20. Lagu T, Rothberg MB, Nathanson BH, Pekow PS, Steingrub JS, Lindenauer PK. The relationship between hospital spending and mortality in patients with sepsis. Arch Intern Med 2011;171:292–9.
21. Lindenauer PK, Pekow P, Wang K, Mamidi DK, Gutierrez B, Benjamin EM. Perioperative beta-blocker therapy and mortality after major noncardiac surgery. N Engl J Med 2005;353:349–61.
22. Lindenauer PK, Pekow PS, Lahti MC, Lee Y, Benjamin EM, Rothberg MB. Association of corticosteroid dose and route of administration with risk of treatment failure in acute exacerbation of chronic obstructive pulmonary disease. JAMA 2010;303:2359–67.
23. Csikesz NG, Tseng JF, Shah SA. Trends in surgical management for acute cholecystitis. Surgery 2008;144:283–9.
24. Guller U, Jain N, Curtis LH, Oertli D, Heberer M, Pietrobon R. Insurance status and race represent independent predictors of undergoing laparoscopic surgery for appendicitis: secondary data analysis of 145,546 patients. J Am Coll Surg 2004;199:567–75.
25. Ricciardi R, Selker HP, Baxter NN, Marcello PW, Roberts PL, Virnig BA. Disparate use of minimally invasive surgery in benign surgical conditions. Surg Endosc 2008;22:1977–86.
26. Abenhaim HA, Azziz R, Hu J, Bartolucci A, Tulandi T. Socioeconomic and racial predictors of undergoing laparoscopic hysterectomy for selected benign diseases: analysis of 341487 hysterectomies. J Minim Invasive Gynecol 2008;15:11–5.
27. Kemp JA, Finlayson SR. Nationwide trends in laparoscopic colectomy from 2000 to 2004. Surg Endosc 2008;22:1181–7.
28. Wu JM, Wechter ME, Geller EJ, Nguyen TV, Visco AG. Hysterectomy rates in the United States, 2003. Obstet Gynecol 2007;110:1091–5.
29. Lass A. The fertility potential of women with a single ovary. Hum Reprod Update 1999;5:546–50.
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