Obstetrics & Gynecology:
Trends in Bilateral Oophorectomy at the Time of Hysterectomy for Benign Disease
Novetsky, Akiva P. MD, MS; Boyd, Leslie R. MD; Curtin, John P. MD, MBA
From the New York University School of Medicine Department of Obstetrics and Gynecology, and the Division of Gynecologic Oncology, New York University, New York, New York.
See related article on page 1271.
Funded in part by a Young Investigator Award grant from the American Society of Clinical Oncology (L.R.B.).
Corresponding author: Akiva Novetsky, 462 First Avenue, Room 9N1, New York, NY 10016; e-mail: email@example.com.
Financial Disclosure The authors did not report any potential conflicts of interest.
OBJECTIVE: To identify patient characteristics associated with bilateral oophorectomy or removal of remaining ovary at the time of benign hysterectomy, and to estimate trends in the performance of oophorectomy from 2001 to 2006.
METHODS: This was a cross-sectional analysis using the New York State Department of Health Statewide Planning and Research Cooperative System. Women aged 18 years or older undergoing hysterectomies for benign gynecologic conditions were included. We evaluated factors associated with oophorectomy on both univariable and multivariable analyses and assessed for changes in performance of oophorectomy over the course of the study.
RESULTS: Forty-seven percent of 144,877 hysterectomies included oophorectomy. Women who underwent oophorectomy were older and were more likely to have a family history of breast or ovarian cancer, a personal history of breast cancer, ovarian cysts, or endometriosis. Women who underwent vaginal or laparoscopic hysterectomy or had uterine prolapse were less likely to undergo oophorectomy. Both race and insurance status were associated with performance of oophorectomy. From 2001 to 2006, there was an 8% absolute decrease in the performance of oophorectomy at the time of benign hysterectomy for women of all ages, with a 10.4% decrease in women aged younger than 55 (P for trend <.001).
CONCLUSION: Age, route of hysterectomy, and concomitant gynecologic diagnoses influence oophorectomy rate. From 2001 to 2006, a significant decrease in the performance of oophorectomy at the time of benign hysterectomy was noted in women aged younger than 55 years. Recent studies of complications of hormone therapy and prophylactic oophorectomy may have influenced patients' and physicians' decision-making, leading to lower oophorectomy rates.
LEVEL OF EVIDENCE: II
Hysterectomy is the most common major surgery performed among nonpregnant women, with 600,000 performed annually in the United States.1 The majority are performed for benign uterine conditions, allowing the option of ovarian retention.2 Between 1965 and 1999, the percentage of benign hysterectomies performed with a concomitant oophorectomy increased from 25% to 55%.3
Ovarian cancer is the most common cause of cancer death attributable to gynecologic malignancies, with an estimated 21,880 new cases and 13,850 deaths in the United States in 2009.4 One in 70 women (1.4%) will have ovarian cancer develop in her lifetime and the majority of cases are diagnosed as advanced cancer. It has been estimated that between 4% and 14% of women with ovarian cancer diagnosed will have undergone previous hysterectomy.5 Approximately 1,000 cases of ovarian cancer could be prevented annually if concomitant prophylactic oophorectomy was performed with benign hysterectomy for all women older than age 40 years.6 A recent study showed a decreased incidence of ovarian cancer with performance of bilateral salpingo-oopherectomy in women undergoing benign hysterectomy without a family history of ovarian cancer from 0.33% to 0.02%.7 If performed before menopause, then prophylactic oophorectomy causes the loss of ovarian function, leading to menopausal symptoms. The effect of oophorectomy on cardiovascular and bone health is the subject of much debate. Some studies have suggested a deleterious effect of bilateral salpingo-oopherectomy and early menopause on cardiovascular and bone health,8–10 whereas others have found no correlation between menopausal status and these outcomes.7,11 Thus, despite its potential benefit in decreasing epithelial ovarian cancer, routine prophylactic oophorectomy at the time of hysterectomy in premenopausal women has remained controversial.
Prophylactic oophorectomy at the time of hysterectomy is a complex decision requiring that the patient and physician consider multiple factors. In 1999, the American College of Obstetricians and Gynecologists stated, “prophylactic oophorectomy should be based not only on the patient's age but also on other factors that weigh individual risk for developing ovarian cancer against the loss of ovarian function.”12 In 2008, they changed their recommendation to, “strong consideration should be given to retaining normal ovaries in premenopausal women who are not at increased genetic risk of ovarian cancer.”13 Our objective was to evaluate patient characteristics associated with oophorectomy at the time of benign hysterectomy and to estimate trends in the performance of oophorectomy from 2001 to 2006.
MATERIALS AND METHODS
The study protocol was submitted to the researchers' institutional review board and was granted exempt status. Hysterectomies were identified using the New York State Department of Health Statewide Planning and Research Cooperative System. This is a comprehensive data reporting system, established in 1979, that collects patient and treatment information for every hospital discharge and emergency department admission. New York State mandates reporting by every hospital. This database has been used extensively in research. A PubMed search for “Statewide Planning and Research Cooperative System” yielded more than 35 articles that used this database.
Demographic data for each entry in the database are available, including age, gender, race or ethnicity, type of insurance (private, Medicare, Medicaid, self-pay, or uninsured), postal code of residence, reason for admission by diagnosis-related group codes, primary and secondary (up to 24) diagnoses, primary and secondary (up to 20) procedures, dates of procedure, and length of stay. The version of the database obtained by the researchers was de-identified, omitting the patient names, dates of birth, and medical record numbers.
Clinical predictors of hysterectomy, including vaginal bleeding (626.2, 626.4, 626.7, 626.8), endometriosis (617), family history of breast or ovarian cancer (V16.3, V16.41), ovarian cyst (220, 620), personal history of breast cancer (174, V10.3), and pelvic organ prolapse (618), were identified using their respective International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) codes.
Cases were identified in the years 2001 to 2006, utilizing ICD-9-CM procedure codes 68.3–68.5 (hysterectomy). Each admission that resulted in hysterectomy was included in the study. The cases were further analyzed for presence of bilateral oophorectomy or bilateral salpingo-oophorectomy, including removal of the remaining ovary, utilizing ICD-9-CM procedure codes 65.5 and 65.6, respectively. Hysterectomies performed for gynecologic malignancies (ICD-9-CM diagnosis codes 179–185) and obstetric indications (ICD-9-CM diagnosis codes 640–679) were excluded.
Statistical analyses were performed using Pearson χ2 and Student t test. A logistic regression model to assess the associations between demographic and clinical factors with undergoing bilateral salpingo-oopherectomy at the time of hysterectomy was created. All of these were included in the multivariable model. An interaction between age at the time of hysterectomy and insurance type was noted during the analysis and was confirmed by formal tests of interaction. To account for this interaction, the multivariable model is presented stratified by age. We hypothesized that a significant decrease in the performance of bilateral salpingo-oopherectomy would be found throughout the course of the study. P for trend was calculated using Cuzick nonparametric test for trend across ordered groups.14 All statistical analyses were performed using STATA 9 software.
From 2001 to 2006, a total of 144,877 hysterectomies were performed for benign gynecologic conditions. Of these, 67,610 (46.7%) had a concomitant oophorectomy. Table 1 shows the demographic information for patients in this study. The women undergoing hysterectomy averaged 48.1 years of age. The majority of women undergoing hysterectomy were white (64.1%), had private insurance (80.3%), had a preoperative diagnosis of fibroids (65.7%), and underwent abdominal hysterectomy (70.1%).
Figure 1 demonstrates the rate of oophorectomy over the course of the study. From 2001 through 2006, there was an absolute decrease of 7.7% in the performance of oophorectomy (P for trend <.001). A significant decrease in oophorectomy rates at the time of hysterectomy was noted for all modes of hysterectomy (P for trend <.001, .01, and <.001 for abdominal, vaginal, and laparoscopic hysterectomies, respectively). After stratification by age, the trend of decreased performance of oophorectomy remained only in women younger than age 55 years (P for trend <.001).
Women who underwent abdominal and laparoscopic hysterectomies were more likely to undergo oophorectomy at the time of hysterectomy (53.9% and 50.4%, respectively) as compared with those undergoing vaginal hysterectomy (17.0%, P<.001). Overall, older women were more likely to undergo oophorectomy. The average age of women undergoing oophorectomy was 5 years older than those who retained their ovaries (50.7±9.8 years compared with 45.8±10.8 years, respectively, P<.001).
Health insurance was associated with performance of oophorectomy (Table 2). An interaction was noted between age at oophorectomy (younger than 55 compared with 55 years or older) and health insurance type (P<.001 for test of interaction). Oophorectomy was most commonly performed in women younger than age 55 years who had Medicare (P<.001), whereas in women 55 years of age or older, oophorectomy was most commonly performed in those who self-paid or had federal (non-Medicare) insurance (P<.001).
A logistic regression model was created to analyze the effects of multiple predictors of oophorectomy found on univariable analysis (Table 3). Women with a family history of breast or ovarian cancer, a personal history of breast cancer, presence of ovarian cysts, or age 55 years or older were associated with the greatest odds of concomitant oophorectomy. Women undergoing vaginal hysterectomy had an 88% relative reduction in their rate of oophorectomy.
Figure 2 demonstrates the adjusted odds ratio for having undergone oophorectomy over each year of the study, after stratification by age (younger than 55 compared with 55 years or older) and controlling for the predictors of oophorectomy. Only in women younger than age 55 years was there a decline in the incidence of oophorectomy over the course of the study (P for trend <.001, compared with P for trend=.16 for women 55 years of age or older). In women younger than 55 years, there was a consistent decrease in the rate of oophorectomy throughout the course of the study after 2002, although no significant change in the rate of oophorectomy was seen between 2001 and 2002 (P=.18). Between the years 2003 and 2005, the rate of oophorectomy continued to decrease annually, with an annual decline of 1.1–1.5% per year. Between 2005 and 2006, a 4% decline in oophorectomy rate was seen.
We found an 8% reduction in the total number of oophorectomies performed over the study period. After controlling for multiple factors associated with oophorectomy, only women aged younger than 55 had a significant reduction in their likelihood of undergoing oophorectomy, with an absolute decrease of 10.4% and a relative reduction of 35%. Lowder et al15 showed a significant increase in the proportion of oophorectomies performed at the time of benign hysterectomy from 1979 to 2004. Our study found an even larger decrease than that reported by Whiteman et al,16 who demonstrated a 5.5% absolute decrease in the performance of oophorectomy from 2000 to 2004. This difference may be attributable to lower rates of bilateral salpingo-oopherectomy in the Northeast.17
As expected, women who underwent a vaginal hysterectomy were significantly less likely to undergo oophorectomy, despite data that oophorectomy can safely be performed in more than 85% of vaginal hysterectomies.18–20 Surprisingly, despite good visibility of the peritoneal cavity, women undergoing laparoscopic hysterectomy had a 16% relative reduction in bilateral salpingo-oopherectomy performance.
A previous study by Jacoby et al17 reported that oophorectomy was more common in white women and those who were uninsured or had Medicaid insurance. Whereas on univariate analysis it appeared that older African American women were the most likely to undergo bilateral salpingo-oopherectomy, on multivariate analysis white women of all ages were most likely to undergo bilateral salpingo-oopherectomy. This apparent contradiction may reflect access to surgeons who performed minimally invasive hysterectomies (34.8% compared with 15.1% for white and African American women, respectively) and a prevalence of fibroids (58.3% compared with 87.2% for white and African American women, respectively). It is unclear why African American women had the lowest rates of bilateral salpingo-oopherectomy, although it may relate to a general mistrust of the medical system leading to lower rates of an elective surgery.21,22
In contrast to the study by Jacoby et al, we found that younger women with Medicare and older women who self-paid for insurance were most likely to undergo bilateral salpingo-oopherectomy. Both of these groups include women who may be more willing to undergo bilateral salpingo-oopherectomy secondary to long-term medical problems or an inability to afford future surgeries.
Over the course of the study, women younger than age 55 years had a significant decline in oophorectomy rates. The largest declines occurred between 2002 and 2003 and between 2005 and 2006 (decreases of 2.5% and 3.4%, respectively). In July 2002, the results of the combined estrogen and progestin arm of the Women's Health Initiative were released, concluding that the overall health risks of combined hormone therapy (HT) exceeded the benefits.23 Since that time, recommendations for the use of HT have changed,24 resulting in a decrease in its use,25,26 with a 40% decrease in HT prescriptions by July 2003. Compared with the first 7 months of 2002, we found a 2.2% absolute decrease in oophorectomy rate in the 5 months after the release of the results of the Women's Health Initiative study (P=.001). After controlling for relevant confounders, a 9.6% relative decrease in oophorectomy performance was seen in 2002 in the months after the release of the Women's Health Initiative study (P=.001). Despite the results of the Women's Health Initiative trial being limited to combined estrogen and progesterone, both combined and estrogen alone HT decreased after the results of these data.27 The decrease in bilateral salpingo-oopherectomy observed may be a result of practitioners' unwillingness to prescribe HT, leading to an increase in ovarian retention.
The largest decline in oophorectomy rate occurred between 2005 and 2006. A 15% relative decrease, compared with the previous year, was noted in women younger than 55 years old. The reason for the decrease in oophorectomy rate is similarly unclear but may be related to accumulating evidence as to the risks of oophorectomy. In 2005, Parker et al28 published their first article based on a Markov decision analytic model describing morbidity and mortality after oophorectomy demonstrating a benefit from ovarian conservation in women younger than age 65 years. The greatest benefit was seen in women 50–54 years old and decreased with increasing age. At no age was higher mortality seen in women who chose ovarian conservation. This article may have influenced patients' and physicians' decision-making in favor of ovarian retention, leading to the lower rates of oophorectomy seen in our cohort.
In 2009, a study using the Nurse's Health Study cohort evaluated women 30–55 years of age who underwent oophorectomy at the time of benign hysterectomy. They demonstrated a decreased risk of breast and ovarian cancer but an increased risk of all-cause mortality, fatal and nonfatal coronary heart disease, and lung cancer.29 In contrast, a recent article by Jacoby et al7 concluded that bilateral salpingo-oopherectomy may not have an adverse effect on cardiovascular health, hip fractures, or overall mortality. The effect that these studies will have on the performance of prophylactic oophorectomy is yet to be determined.
Our study has several important limitations. Our study is based on all hysterectomies performed in the state of New York and may not be generalizable to other populations. Although compliance with the database is mandatory for all acute care hospitals in New York State, the accuracy of the reported data are not validated. Specifically, surgical procedures require accurate coding, both for the primary procedure (in this case, hysterectomy) and for all secondary procedures (including oophorectomy) to be captured for this project. Our rates of family history of breast or ovarian cancer and personal history of breast cancer are significantly lower than would have been expected, likely because of incomplete coding. Complete coding might have allowed us to account for additional cases of oophorectomy secondary to personal or family history.
In summary, this study has demonstrated that there has been a significant decrease in the performance of oophorectomy at the time of benign hysterectomy in women younger than age 55 years. Despite increasing recognition of genetic susceptibility to ovarian and breast cancer and the benefit of prophylactic surgery,30–32 we still identified a significantly decreased rate of bilateral salpingo-oopherectomy. Although there is no conclusive evidence linking the publication of the Women's Health Initiative study to this decrease, we postulate that patients and providers have demonstrated an unwillingness to induce surgical menopause without HT. If evidence of the detrimental affects of performing prophylactic oophorectomy at the time of benign hysterectomy increases, then we anticipate that rates of oophorectomy will continue to decline.
1. Wu JM, Wechter ME, Geller EJ, Nguyen TV, Visco AG. Hysterectomy rates in the United States, 2003. Obstet Gynecol 2007;110:1091–5.
2. Merrill RM. Hysterectomy surveillance in the United States, 1997 through 2005. Med Sci Monit 2008;14:CR24–31.
3. Keshavarz H, Hillis S, Kieke B, Marchbanks P. Hysterectomy surveillance—United States, 1994–1999. Morb Mortal Wkly Rep CDC Surveill Summ 2002;51(5):1–8.
4. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225–49.
5. Sightler SE, Boike GM, Estape RE, Averette HE. Ovarian cancer in women with prior hysterectomy: a 14-year experience at the University of Miami. Obstet Gynecol 1991;78:681–4.
6. Averette HE, Nguyen HN. The role of prophylactic oophorectomy in cancer prevention. Gynecol Oncol 1994;55:S38–41.
7. Jacoby VL, Grady D, Wactawski-Wende J, Manson JE, Allison MA, Kuppermann M, et al.. Oophorectomy vs ovarian conservation with hysterectomy: cardiovascular disease, hip fracture, and cancer in the Women's Health Initiative Observational Study. Arch Intern Med 2011;171:760–8.
8. Colditz GA, Willett WC, Stampfer MJ, Rosner B, Speizer FE, Hennekens CH. Menopause and the risk of coronary heart disease in women. N Engl J Med 1987;31:1105–10.
9. van Der Voort DJ, van Der Weijer PH, Barentsen R. Early menopause: increased fracture risk at older age. Osteoporos Int 2003;14:525–30.
10. Ossewaarde ME, Bots ML, Verbeek AL, Peeters PH, van der Graaf Y, Grobbee DE, et al.. Age at menopause, cause-specific mortality and total life expectancy. Epidemiology 2005;16:556–62.
11. Atsma F, Bartelink ML, Grobbee DE, van der Schouw YT. Postmenopausal status and early menopause as independent risk factors for cardiovascular disease: a meta-analysis. Menopause 2006;13:265–79.
12. Prophylactic oophorectomy. ACOG Practice Bulletin No. 7. American College of Obstetricians and Gynecologists. Int J Gynecol Obstet 1999;67:193–9.
13. Elective and risk-reducing salpingo-oophorectomy. ACOG Practice Bulletin No. 89. American College of Obstetritions and Gynecologists. Obstet Gynecol 2008;111:231–41.
14. Cuzick J. A Wilcoxon-type test for trend. Stat Med 1985;4:87–90.
15. Lowder JL, Oliphant SS, Ghetti C, Burrows LJ, Meyn LA, Balk J. Prophylactic bilateral oophorectomy or removal of remaining ovary at the time of hysterectomy in the United States, 1979–2004. Am J Obstet Gynecol 2010;202:538.e1–9.
16. Whiteman MK, Hillis SD, Jamieson DJ, Morrow B, Podgornik MN, Brett KM, et al.. Inpatient hysterectomy surveillance in the United States, 2000–2004. Am J Obstet Gynecol 2008;198:34.e1–7.
17. Jacoby VL, Vittinghoff E, Nakagawa S, Jackson R, Richter HE, Chan J, et al.. Factors associated with undergoing bilateral salpingo-oophorectomy at the time of hysterectomy for benign conditions. Obstet Gynecol 2009;113:1259–67.
18. Davies A, O'Connor H, Magos AL. A prospective study to evaluate oophorectomy at the time of vaginal hysterectomy. Br J Obstet Gynaecol 1996;103:915–20.
19. Sheth SS. Adnexectomy for benign pathology at vaginal hysterectomy without laparoscopic assistance. BJOG 2002;109:1401–5.
20. Sizzi O, Paparella P, Bonito C, Paparella R, Rossetti A. Laparoscopic assistance after vaginal hysterectomy and unsuccessful access to the ovaries or failed uterine mobilization: changing trends. JSLS 2004;8:339–46.
21. LaVeist TA, Nickerson KJ, Bowie JV. Attitudes about racism, medical mistrust, and satisfaction with care among African American and white cardiac patients. Med Care Res Rev 2000;57(Suppl 1):146–61.
22. Brandon DT, Isaac LA, LaVeist TA. The legacy of Tuskegee and trust in medical care: is Tuskegee responsible for race differences in mistrust of medical care? J Natl Med Assoc 2005;97:951–6.
23. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, et al.. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321–33.
24. Recommendations for estrogen and progestogen use in peri-and postmenopausal women: October 2004 position statement of The North American Menopause Society. Menopause 2004;11(6Pt1):589–600.
25. Buist DS, Newton KM, Miglioretti DL, Beverly K, Connelly MT, Andrade S, et al.. Hormone therapy prescribing patterns in the United States. Obstet Gynecol 2004;104(5Pt1):1042–50.
26. Ettinger B, Grady D, Tosteson AN, Pressman A, Macer JL. Effect of the Women's Health Initiative on women's decisions to discontinue postmenopausal hormone therapy. Obstet Gynecol 2003;102:1225–32.
27. Hersh AL, Stefanick ML, Stafford RS. National use of postmenopausal hormone therapy: annual trends and response to recent evidence. JAMA 2004;291:47–53.
28. Parker WH, Broder MS, Liu Z, Shoupe D, Farquhar C, Berek JS. Ovarian conservation at the time of hysterectomy for benign disease. Obstet Gynecol 2005;106:219–26.
29. Parker WH, Broder MS, Chang E, Feskanich D, Farquhar C, Liu Z, et al.. Ovarian conservation at the time of hysterectomy and long-term health outcomes in the nurses' health study. Obstet Gynecol 2009;113:1027–37.
30. Kauff ND, Satagopan JM, Robson ME, Scheuer L, Hensley M, Hudis CA, et al.. Risk-reducing salpingo-oophorectomy in women with a BRCA1 or BRCA2 mutation. N Engl J Med 2002;346:1609–15.
31. Scheuer L, Kauff N, Robson M, Kelly B, Barakat R, Satagopan J, et al.. Outcome of preventive surgery and screening for breast and ovarian cancer in BRCA mutation carriers. J Clin Oncol 2002;20:1260–8.
32. Schmeler KM, Lynch HT, Chen LM, Munsell MF, Soliman PT, Clark MB, et al.. Prophylactic surgery to reduce the risk of gynecologic cancers in the Lynch syndrome. N Engl J Med 2006;354:261–9.
This article has been cited 1 time(s).
American Journal of EpidemiologyInvited Commentary: Reproductive Organ Surgeries and Breast Cancer Risk-Apples, Oranges, or Fruit Cocktail?American Journal of Epidemiology
© 2011 by The American College of Obstetricians and Gynecologists.
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Looking for ABOG articles? Visit our ABOG MOC II collection. The selected Green Journal articles are free through the end of the calendar year.
ACOG MEMBER SUBSCRIPTION ACCESS
If you are an ACOG Fellow and have not logged in or registered to Obstetrics & Gynecology, please follow these step-by-step instructions to access journal content with your member subscription.
Data is temporarily unavailable. Please try again soon.
Readers Of this Article Also Read