Advertisement

National trends of adnexal surgeries at the time of hysterectomy for benign indication, United States, 1998–2011

Published:April 29, 2015DOI:https://doi.org/10.1016/j.ajog.2015.04.031

      Objective

      We sought to investigate the most recent national trends of bilateral salpingectomy (BS) and bilateral salpingo-oophorectomy (BSO) at the time of hysterectomy performed for benign indications.

      Study Design

      We conducted a national cross-sectional analysis of all inpatient discharges for women aged ≥18 years who underwent a hysterectomy for benign indications from 1998 through 2011 using the largest publicly available all-payer inpatient database in the United States. We scanned International Classification of Diseases, Ninth Revision codes for an indication of specific bilateral adnexal surgeries, including BSO and BS. Joinpoint regression was used to characterize and estimate 14-year national trends in performing BSO and BS at the time of hysterectomy for benign indications, overall and in population subgroups.

      Results

      During the study period, there were approximately 428,523 inpatient hysterectomy procedures performed annually for benign indications. Of these, >53% had no adnexal surgery performed during the same hospitalization, whereas 43.7% and 1.3% of those discharges had BSO and BS procedures, respectively. The rate of BSO was directly correlated with increasing age for patients <65 years. Conversely, we observed an inverse relationship between BS and patient age, with the BS rate among women aged <25 years twice that of women aged ≥45 years. From 1998 through 2001, there was a 2.2% increase in the rate of BSO per year (95% confidence interval, 0.4–4.0); however, this was followed by a consistent 3.6% (95% confidence interval, –4.0 to –3.3) annual decline in the BSO rate, from 49.7% in 2001 to 33.4% in 2011. National rates of BS among women undergoing hysterectomy for benign indications increased significantly throughout the study period, with an estimated 8% annual increase from 1998 through 2008, followed by a sharp 24% increase annually during the last 4 years of the study period. The BS rate nearly quadrupled in 14 years.

      Conclusion

      The type of adnexal surgery performed concomitantly with hysterectomy for benign indications has undergone a significant shift since 2001. Significantly more BS and less BSO procedures are being performed among gynecologic surgeons in the United States.

      Key words

      Adnexal surgery at the time of hysterectomy performed for benign indications is a crucial component of preoperative patient counseling and decision making. These concurrent surgeries, which include oophorectomy or salpingectomy, are typically performed with the aim of reducing the possibility of ovarian cancer in the future. Ovarian cancer represents a challenging health problem with 225,500 new cases and 140,200 deaths worldwide in 2008.
      • Jemal A.
      • Bray F.
      • Center M.M.
      • Ferlay J.
      • Ward E.
      • Forman D.
      Global cancer statistics.
      So far there is no effective screening method for ovarian cancer. Despite surgical and medical advances, the prognosis associated with ovarian cancer is poor, with a 5-year overall survival of 45%.
      • Tanner E.J.
      • Long K.C.
      • Visvanathan K.
      • Fader A.N.
      Prophylactic salpingectomy in premenopausal women at low risk for ovarian cancer: risk-reducing or risky?.
      Concomitant oophorectomy, while an important consideration for patients undergoing hysterectomy for benign indications, is usually a difficult decision because of other potential health consequences that result from a surgically induced menopause. Compared with ovarian conservation, bilateral oophorectomy at the time of hysterectomy for benign disease is associated with 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.
      • Parker W.H.
      • Broder M.S.
      • Chang E.
      • et al.
      Ovarian conservation at the time of hysterectomy and long-term health outcomes in the nurses' health study.
      Recently, studies have confirmed the belief that most pelvic serous carcinomas originate from the distal fallopian tube.
      • Kindelberger D.W.
      • Lee Y.
      • Miron A.
      • et al.
      Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship.
      • Carlson J.W.
      • Miron A.
      • Jarboe E.A.
      • et al.
      Serous tubal intraepithelial carcinoma: its potential role in primary peritoneal serous carcinoma and serous cancer prevention.
      • Dietl J.
      Revisiting the pathogenesis of ovarian cancer: the central role of the fallopian tube.
      Therefore, there has been an increasing discussion among gynecologists on the need to prophylactically remove the fallopian tubes at the time of a hysterectomy. Despite the absence of any formal guidelines, this emerging evidence has prompted a change in surgical practice patterns regarding performance of salpingectomy, as opposed to oophorectomy, at the time of simple hysterectomy.
      • Salvador S.
      • Gilks B.
      • Kobel M.
      • Huntsman D.
      • Rosen B.
      • Miller D.
      The fallopian tube: primary site of most pelvic high-grade serous carcinomas.
      • Schenberg T.
      • Mitchell G.
      Prophylactic bilateral salpingectomy as a prevention strategy in women at high-risk of ovarian cancer: a mini-review.
      Currently, there are no studies evaluating practice pattern changes among gynecologic surgeons in the United States. Therefore, the objective of this study is to investigate the most recent national trends of bilateral salpingectomy (BS) and bilateral salpingo-oophorectomy (BSO) performed at the time of a hysterectomy procedure for benign indications. We hypothesize that there has been a significant change in the rate of oophorectomy and salpingectomy in recent years due to this emerging evidence. Our secondary aim is to describe any differences in the rates and trends stratified by socioeconomic, demographic, and hospital characteristics.

      Materials and Methods

      Study design and data source

      After obtaining exempt status from University of South Florida Institutional Review Board, a cross-sectional analysis of all inpatient hospital discharges from 1998 through 2011 was conducted using the National Inpatient Sample (NIS), the largest publicly available all-payer inpatient database in the United States, made available by the Healthcare and Cost Utilization Project (HCUP).
      Each year, HCUP stratifies all nonfederal community hospitals from participating states by 5 major hospital characteristics: type of ownership, geographic region, rural/urban setting, number of beds, and teaching status. HCUP then selects a 20% systematic random sample of hospitals, and all inpatient discharges from selected hospitals are included in the NIS.

      Study population and identification of adnexal surgeries

      The study population consisted of inpatient discharges for women aged ≥18 years who underwent a hysterectomy for ≥1 of the following benign indications: uterine leiomyoma, carcinoma in situ of cervix uteri, uterine prolapse, hypertrophy of the uterus, endometrial hyperplasia, cervical dysplasia, dysmenorrhea, menstruation disorders, or other specified disorders of uterus. Discharges in which the woman underwent a radical abdominal or vaginal hysterectomy, a pelvic exenteration, or in which there was a diagnosis of a malignant neoplasm of the female reproductive system were excluded. We also excluded discharges in which obstetrical procedure was performed (Figure 1). All clinical diagnoses and surgical procedures were identified using International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) diagnosis and procedure codes. After identifying the study population, we scanned procedure codes in each woman's discharge record for an indication of specific bilateral adnexal surgeries, including BSO, BS without oophorectomy, and bilateral oophorectomy without salpingectomy. We also considered a small proportion of surgical procedures in which the remaining tube and/or ovary was removed. Unilateral procedures were not considered. Discharges for women without any indication of adnexal surgeries were classified as “no procedure.” The complete list of ICD-9-CM codes used to characterize each indication and procedure is presented in the Appendix; Supplementary Table 1.
      Figure thumbnail gr1
      Figure 1Inclusion and exclusion criteria used to determine study population
      Flow diagram representing final determination of all inpatient discharges in which hysterectomy was performed due to benign indications, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 1998 through 2011. Flowchart representing entire population of inpatient discharges nationwide and how exclusion criteria were applied to determine final study population.
      ICD-9, International Classification of Diseases, Ninth Revision.
      aExcludes rehabilitation and long-term acute care hospitals; bSpecific diagnosis and procedure code lists are available in the , .
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.

      Sociodemographic, clinical, and hospital characteristics

      Patient-level sociodemographic factors were extracted from the NIS databases. Patient age in years was classified into 6 categories: 18-24, 25-34, 35-44, 45-54, 55-64, and ≥65. Relative median household income (in quartiles) served as a proxy for each woman’s socioeconomic status and was estimated by HCUP using the patient's ZIP code or residence. We grouped the primary payer for hospital admission into 3 categories: government (Medicare/Medicaid), private (commercial carrier, private health maintenance organization, and preferred provider organization), and other sources (eg, self-pay and charity). Clinical characteristics included the type of hysterectomy performed (laparoscopic, vaginal, or abdominal), the benign indication(s) for the hysterectomy, and whether the patient had a genetic susceptibility to or a personal or family history of breast or ovarian cancer. We also considered several hospital characteristics including US region (Northeast, Midwest, South, or West), location (urban vs rural), and teaching status (teaching, or a ratio of full-time equivalent interns and residents to nonnursing home beds ≥0.25, vs nonteaching).

      Data analysis

      We used descriptive statistics including frequencies, percentages, and rates to describe the national prevalence of hysterectomies due to benign indications, the relative rates of adnexal surgeries among those discharges, and the distribution of sociodemographic, clinical, and hospital characteristics across the study population. To compute national estimates, we weighted all analyses with discharge-level weights provided with the NIS databases.
      Joinpoint regression was used to investigate and describe 14-year national trends in performing salpingectomy and oophorectomy at the time of hysterectomy for benign indications. Joinpoint regression first models annual trend data by fitting a straight line (ie, 0 joinpoints).
      • Kim H.J.
      • Fay M.P.
      • Feuer E.J.
      • Midthune D.N.
      Permutation tests for joinpoint regression with applications to cancer rates.
      Then, a Monte Carlo permutation test is used to examine whether a model with 1 joinpoint is statistically significantly better than the null. If it is, the joinpoint is incorporated into the model. Additional joinpoints are considered in a similar manner until the optimal fitting model is determined. In the final model, each joinpoint reflects a significant change (increase or decrease) in the trend, and an annual percent change (APC) is calculated to describe how the rate changes within each time interval. Also, the average APC (AAPC) is calculated. The AAPC weights the APCs for each time interval to produce a single number that best describes the trend of each procedure over the entire study period. Due to the rarity of some adnexal procedures, we focus our results on trends of BSO and BS, overall and among patient- and hospital-level subgroups. To account for design changes in the NIS during the study period, we used HCUP-supplied NIS trends files that consistently define trend weights and data elements over time.

      Houchens RL, Elixhauser A. Using the HCUP Nationwide Inpatient Sample to estimate trends (updated for 1988-2004). HCUP methods series report no 2006-05 online. US Agency for Healthcare Research and Quality; Aug. 18, 2006. Available at: http://www.hcup-us.ahrq.gov/reports/methods.jsp. Accessed Nov. 30, 2014.

      All statistical analyses were weighted to account for the complex sampling design of the NIS. Analyses were performed using SAS software, version 9.4 (SAS Institute Inc, Cary, NC) and the Joinpoint Regression Program, version 4.1.1.1 (National Cancer Institute, Washington, DC).

      Song X, Friedman B. Calculate cost adjustment factors by APR-DRG and CCS using selected states with detailed charges. HCUP methods series report no. 2008-04. US Agency for Healthcare Research and Quality. Available at: http://www.hcup-us.ahrq.gov/reports/methods.jsp. Accessed Nov. 30, 2014.

      Statistical tests were 2-sided with a 5% type I error rate.

      Results

      Of the >63 million inpatient discharge records for female patients aged >18 years in the NIS from 1998 through 2011, 1,231,120 (1.9%) had documentation of a hysterectomy being performed for benign, nonobstetrical indications (Figure 1). This translated into a national estimate of 428,523 such procedures being done in the United States each year during the study period.
      Of these, >53% of hysterectomies had no adnexal surgery performed during the same hospitalization, whereas 43.7% and 1.3% of those discharges had BSO and BS procedures, respectively (Figure 2). All other adnexal procedures including removal of the remaining ovary, removal of the remaining tube, and bilateral oophorectomy without salpingectomy were very rare procedures with prevalence of <1% or just >1% collectively. Therefore, we restrict the presentation of our results below to BSO, BS, and the “no procedure” groups.
      Figure thumbnail gr2
      Figure 2Distribution of the type of adnexal surgery during benign hysterectomy in US, 1998-2011
      Distribution of primary surgical outcome among inpatient discharges in which hysterectomy was performed due to benign indications, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 1998 through 2011. All inpatient hospitalizations for hysterectomy due to benign indications in the United States over 14-year period by type of concomitant adnexal surgery. Frequencies represent average annual number of discharges from 1998 through 2011 in which each surgical procedure was performed, among all discharges in the United States in which there was hysterectomy performed due to benign indications.
      BO, bilateral oophorectomy; BS, bilateral salpingectomy; BSO, bilateral salpingo-oophorectomy; mixed, combination of bilateral procedure and “removal of remaining procedure”; no procedure, all discharges in which no bilateral or “removal of other” procedures were performed; RO, oophorectomy, remaining ovary; RS, salpingectomy, remaining tube; RSO, salpingo-oophorectomy, remaining tube/ovary.
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      Table 1 describes the distribution of our study population by patient-level sociodemographic and hospital characteristics, and by type of adnexal surgery received. Women aged 35-54 years comprise >75% of all women who underwent a hysterectomy for benign indications in the United States. Patient age was the factor most strongly associated with the primary outcome (P < .0001). The rate of BSO was directly correlated with increasing age for patients aged <65 years, with >60% of women aged 45-64 years undergoing BSO, compared to <20% of women aged <35 years. Conversely, we observed an inverse relationship between BS and patient age, with the BS rate among women <25 years twice that of women aged ≥45 years. As expected, the regional breakdown tended to mirror the underlying age distribution of patients with the highest BSO rates in the South (oldest patient mix) and the lowest in the Northeast (youngest patient mix). The rates of BSO and BS were relatively comparable among subgroups of all other sociodemographic and hospital characteristics available and investigated.
      Table 1Distribution of selected patient sociodemographic and hospital characteristics
      CharacteristicOverall
      Only selected bilateral procedures were included in this figure; bilateral oophorectomies and those procedures in which “removal of other tube/ovary” was documented were excluded due to their relative infrequency. “No procedure” category includes all discharges in which no bilateral or “removal of other” procedures were performed. “Overall” column includes all procedures; therefore, procedure-specific frequencies in each row will add to less than “overall” totals
      Primary outcome
      Only selected bilateral procedures were included in this figure; bilateral oophorectomies and those procedures in which “removal of other tube/ovary” was documented were excluded due to their relative infrequency. “No procedure” category includes all discharges in which no bilateral or “removal of other” procedures were performed. “Overall” column includes all procedures; therefore, procedure-specific frequencies in each row will add to less than “overall” totals
      BSOBSNo procedureP value
      Calculated from Rao-Scott modified χ2 test assessing whether there is statistical association between primary outcome status and each characteristic
      n
      Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      %
      Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      n
      Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      %
      Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      n
      Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      %
      Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      n
      Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      %
      Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      Age at admission, y< .0001
       18–2423,7220.4407917.24682.018,85979.5
       25–34577,6369.6111,54819.310,0901.8447,14877.4
       35–442,382,00139.7699,08029.436,2701.51,610,30867.6
       45–542,146,88735.81,310,04361.021,9931.0777,49236.2
       55–64459,3387.7301,06165.532690.7146,82032.0
       ≥65409,7336.8195,66147.829550.7204,88650.0
      Primary payer< .0001
       Government
      Includes Medicare and Medicaid
      1,026,08117.1427,14541.613,4721.3568,92355.5
       Private4,538,98975.72,002,10244.155,1951.22,407,72153.1
       Other
      Includes self-pay, no charge, and other payers.
      434,2487.2192,22444.363781.5228,87052.7
      Household income< .0001
       Lowest quartile1,451,33924.2645,94944.519,2101.3763,61452.6
       Second quartile1,553,48125.9684,28844.118,8161.2824,05353.1
       Third quartile1,493,85424.9638,03342.718,3811.2813,18454.4
       Highest quartile1,387,95623.1602,83243.417,0351.2745,82753.7
      Hospital region< .0001
       Northeast910,60215.2353,10838.812,9561.4529,43858.1
       Midwest1,417,75223.6635,52744.818,1101.3737,38452.0
       South2,466,67641.11,121,24645.529,4811.21,280,38651.9
       West1,204,28720.1511,59142.514,4981.2658,30654.7
      Hospital location.0037
       Urban5,055,68784.62,195,08343.464,0291.32,716,30853.7
       Rural923,68615.5418,42645.310,8361.2477,62951.7
      Hospital teaching status.4345
       Teaching2,443,49440.71,060,75143.431,7321.31,312,07153.7
       Nonteaching3,535,87958.91,552,75843.943,1341.21,881,86653.2
      Among inpatient discharges in which hysterectomy was performed due to benign indications, by primary outcome status, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 1998 through 2011.
      BS, bilateral salpingectomy; BSO, bilateral salpingo-oophorectomy.
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      a Only selected bilateral procedures were included in this figure; bilateral oophorectomies and those procedures in which “removal of other tube/ovary” was documented were excluded due to their relative infrequency. “No procedure” category includes all discharges in which no bilateral or “removal of other” procedures were performed. “Overall” column includes all procedures; therefore, procedure-specific frequencies in each row will add to less than “overall” totals
      b Weighted to estimate national frequency; sum of all groups may not add up to total due to missing data. Percentages in “overall” column are column percentages to show distribution of study population; percentages for each primary outcome are row percentages to show breakdown of primary outcome within each population subgroup
      c Calculated from Rao-Scott modified χ2 test assessing whether there is statistical association between primary outcome status and each characteristic
      d Includes Medicare and Medicaid
      e Includes self-pay, no charge, and other payers.
      Women with a personal or family history, or a genetic susceptibility, to breast and ovarian cancer experienced significantly higher rates of adnexal procedures, ranging from 55.2% (family history of breast cancer) to 94.3% (genetic susceptibility to breast cancer) (Figure 3). The route of hysterectomy seems to have an impact on the rate of BS. During years in which more specific ICD-9-CM codes permitted complete differentiation of hysterectomies according to route (2007 through 2011), laparoscopic hysterectomy was associated with statistically significantly higher rates of BS (4.2% in 2011) compared to abdominal (2.6%) or vaginal (1.7%) hysterectomies (Figure 4). Nonlaparoscopic vaginal hysterectomies were much less likely to be accompanied by any adnexal surgery (16.7% in 2011) than laparoscopic (40.3%) or abdominal (45.2%) procedures.
      Figure thumbnail gr3
      Figure 3Distribution of type of adnexal surgery according to indication of hysterectomy
      Distribution of primary surgical outcome among inpatient discharges in which hysterectomy was performed, among patients with most common benign indications and personal or family risk factors for breast and ovarian cancer, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 1998 through 2011. Distribution of primary study outcome (type of concomitant adnexal surgery) overall and across major benign indications for hysterectomy and personal/family history factors. Only selected bilateral procedures were included in this figure; bilateral oophorectomies and those procedures in which “removal of other tube/ovary” was documented were excluded due to their relative infrequency. “No procedure” category includes all discharges in which no bilateral or “removal of other” procedures were performed. Length of each bar represents proportion of all bilateral salpingo-oophorectomy (BSO), bilateral salpingectomy (BS), and “no procedures” each specific type accounted for within each sample subgroup (eg, women with uterine leiomyoma); however, numbers listed within each bar represent actual rate of that surgical outcome (percent of all discharges for hysterectomy). These may not add to 100% due to omission of “removal of other tube/ovary” and bilateral oophorectomy procedures. X-axis, proportion of all hysterectomies falling within one primary surgical outcome included in this figure; Y-axis, subset of hysterectomies with documented indication or characteristic.
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      Figure thumbnail gr4
      Figure 4Distribution of type of adnexal surgery according to route of hysterectomy
      Distribution of primary surgical outcome among inpatient discharges in which hysterectomy was performed, by type/route of hysterectomy, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 2007 through 2011. Temporal changes in distribution of primary study outcome (type of concomitant adnexal surgery) by route of hysterectomy. Primary surgical outcome was statistically significantly associated with type/route of hysterectomy (Rao-Scott modified χ2 test: P < .0001). Only selected bilateral procedures were included in this figure; bilateral oophorectomies and those procedures in which “removal of other tube/ovary” was documented were excluded due to their relative infrequency. “No procedure” category includes all discharges in which no bilateral or “removal of other” procedures were performed. Length of each bar represents proportion of all bilateral salpingo-oophorectomy (BSO), bilateral salpingectomy (BS), and “no procedures” each specific type accounted for within each sample subgroup (eg, women undergoing laparoscopic hysterectomy in 2007); however, numbers listed within each bar represent actual rate of that surgical outcome (percent of all discharges for hysterectomy). These may not add to 100% due to omission of “removal of other tube/ovary” and bilateral oophorectomy procedures. Only years 2007 through 2011 were included due to inability to differentiate fully between type/route of hysterectomy using International Classification of Diseases, Ninth Revision codes available prior to Oct.1, 2006. X-axis, type/route of hysterectomy; Y-axis, proportion of all hysterectomies falling within one primary surgical outcome included in this figure.
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      We observed significant changes in the trends of adnexal procedures in our study population during the study period (Figure 5). From 1998 through 2001, there was a 2.2% increase in the rate of BSO per year (95% confidence interval, 0.4–4.0); however, this was followed by a consistent 3.6% (95% confidence interval, –4.0 to –3.3) annual decline in the BSO rate, from 49.7% in 2001 to 33.4% in 2011. National rates of BS among women undergoing hysterectomy for benign indications increased significantly throughout the study period, with an 8% annual increase from 1998 through 2008, followed by a sharp 24% annual increase during the last 4 years of the study period. The BS rate nearly quadrupled in 14 years. The trend of declining BSO rates were fairly consistent across all women aged 25-64 years, although APCs were more pronounced in premenopausal and perimenopausal women (APC –5.8 and –4.9, respectively) (Figure 6, A). Similarly, the increasing BS rates were observed in every age group <65 years (Figure 6, B). The rate of BS among women aged 25-34 years doubled in just 4 years.
      Figure thumbnail gr5
      Figure 5National trends of BSO and BS during benign hysterectomy in US, 1998-2011
      Trends in bilateral salpingo-oophorectomy (BSO) and bilateral salpingectomy (BS) among inpatient discharges in which hysterectomy was performed due to benign indications, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 1998 through 2011. The 14-year temporal trends in BSO and BS during study period. Circular markers indicate observed annual rate, whereas solid lines represented trends estimated by joinpoint regression. X-axis, year of discharge; Y-axis, percentage of hysterectomies in which procedure was performed (axis is split to account for substantial differences in rates across procedure types).
      APC, annual percent change, point estimate (95% confidence interval).
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      Figure thumbnail gr6
      Figure 6National trends of BSO and BS according to age group
      Trends in A, bilateral salpingo-oophorectomy (BSO) and B, bilateral salpingectomy (BS) among inpatient discharges in which hysterectomy was performed due to benign indications, by patient age at admission, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 1998 through 2011. The 14-year temporal trends in BSO and BS, by patient age, during study period. Only annual percent change, point estimate (APC) statistically significantly different from 0 were included in figure. Circular, filled markers indicate significant change in trend. X-axis, year of discharge; Y-axis, percentage of hysterectomies in which procedure was performed (note that y-axes for 2 panels are on different scales).
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      We further examined BSO and BS trends in all sociodemographic subgroups and in discharges of all hospital types. BSO trends (small increase into the early 2000s followed by an annual decline between 2-6%) and BS trends (consistent 6-20% annual increase) were consistent in nearly every subgroup (Supplementary Tables 2 and 3). It is noteworthy to observe that an increasing rate of BS was 2 times higher in hospitals in the Northeast (AAPC 12.3%) compared to those in the South (AAPC 6.2%), and in urban hospitals (AAPC 12.3%) compared to rural ones (AAPC 6.2%).

      Comment

      In this study, a significant change in the type of adnexal surgeries performed at the time of hysterectomy for benign indication was found. It is evident from our study that the number of concurrent BSO has consistently and significantly declined since 2001. On the other hand, the number of concomitant BS has steadily increased since early 2000 with exponential and significant increase since 2008. This significant shift in practice pattern is in line with current evidence suggesting the fallopian tube as the origin of ovarian cancer, and attempts to eliminate the increased risk of all-cause mortality, and fatal and nonfatal coronary heart disease seen in some patients undergoing oophorectomy during hysterectomy.
      • Parker W.H.
      • Broder M.S.
      • Chang E.
      • et al.
      Ovarian conservation at the time of hysterectomy and long-term health outcomes in the nurses' health study.
      The lifetime risk of developing ovarian cancer in the general population is 1 in 70 or 1.4%.
      American College of Obstetrics and Gynecology
      Elective and risk-reducing salpingo-oophorectomy. ACOG Practice bulletin no. 89.
      The fimbria is believed to be the source of nearly half of primary peritoneal serous carcinoma.
      • Carlson J.W.
      • Miron A.
      • Jarboe E.A.
      • et al.
      Serous tubal intraepithelial carcinoma: its potential role in primary peritoneal serous carcinoma and serous cancer prevention.
      The role of the fallopian tube in the pathogenesis of ovarian cancer has been studied extensively.
      • Seidman J.D.
      • Zhao P.
      • Yemelyanova A.
      “Primary peritoneal” high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer.
      • Sieh W.
      • Salvador S.
      • McGuire V.
      • et al.
      Tubal ligation and risk of ovarian cancer subtypes: a pooled analysis of case-control studies.
      • Kurman R.J.
      • Shih Ie M.
      The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory.
      In agreement with the link between ovarian cancer and fallopian tubes, gynecological surgeons have demonstrated a significant shift toward the performance of more BS during hysterectomy done for benign indications as opposed to BSO.
      In women at the highest risk for ovarian cancer, such as carriers of BRCA mutation, prophylactic BSO on completion of childbearing reduces the risk of ovarian cancer dramatically; and reduces the risk of breast cancer by 50%.
      • Tanner E.J.
      • Long K.C.
      • Visvanathan K.
      • Fader A.N.
      Prophylactic salpingectomy in premenopausal women at low risk for ovarian cancer: risk-reducing or risky?.
      While there is clear recommendation for a prophylactic BSO for those patients, ovarian preservation in premenopausal low-risk populations should strongly continue to be considered as seen in this study.
      American College of Obstetrics and Gynecology
      Elective and risk-reducing salpingo-oophorectomy. ACOG Practice bulletin no. 89.
      BSO offers the greatest risk reduction for breast and ovarian cancer among BRCA mutation carriers. However, when considering quality-adjusted life expectancy, BS with delayed oophorectomy is a cost-effective strategy and may be an acceptable alternative.
      • Kwon J.S.
      • Tinker A.
      • Pansegrau G.
      • et al.
      Prophylactic salpingectomy and delayed oophorectomy as an alternative for BRCA mutation carriers.
      In patients at average risk for ovarian cancer, the potential benefit of cancer risk reduction with elective BSO should be balanced with the consequences of premature loss of estrogen production.
      • Asante A.
      • Whiteman M.K.
      • Kulkarni A.
      • Cox S.
      • Marchbanks P.A.
      • Jamieson D.J.
      Elective oophorectomy in the United States: trends and in-hospital complications, 1998-2006.
      Due to the aforementioned risks of oophorectomy, young premenopausal women at low risk for ovarian cancer are not generally recommended to undergo BSO at time of hysterectomy unless clinically indicated.
      • Tanner E.J.
      • Long K.C.
      • Visvanathan K.
      • Fader A.N.
      Prophylactic salpingectomy in premenopausal women at low risk for ovarian cancer: risk-reducing or risky?.
      While there are currently no clear recommended national guidelines with respect to this surgical practice, it is clearly seen in this adequately powered study that gynecologic surgeons have gradually adopted this practice. Given that the steepest transition point between less BSO and more BS during hysterectomy for benign indications was mid 2000 (Figure 5), it will be interesting to see if the overall incidence and survival from ovarian cancer will change positively in the future.
      About 51% of women who had hysterectomy from 1988 through 1993 underwent concurrent BSO,
      • Lepine L.A.
      • Hillis S.D.
      • Marchbanks P.A.
      • et al.
      Hysterectomy surveillance–United States, 1980-1993.
      while this rate has now decreased to 43.7% according to our current study. Additionally, there was a negative trend for BSO that was more pronounced in premenopausal women. In a study by Asante et al
      • Asante A.
      • Whiteman M.K.
      • Kulkarni A.
      • Cox S.
      • Marchbanks P.A.
      • Jamieson D.J.
      Elective oophorectomy in the United States: trends and in-hospital complications, 1998-2006.
      it was shown that the rate of BSO during hysterectomy performed for benign indications has initially increased in the period 1998 through 2001 then decreased from 2002 through 2006, and it was assumed that the change in the trend was attributed to the fact that Women’s Health Initiative early termination results were published in 2002.
      • Asante A.
      • Whiteman M.K.
      • Kulkarni A.
      • Cox S.
      • Marchbanks P.A.
      • Jamieson D.J.
      Elective oophorectomy in the United States: trends and in-hospital complications, 1998-2006.
      That finding was confirmed in our study; the only difference is that the reversed trend started in 2001 as opposed to 2002 as previously reported.
      • Asante A.
      • Whiteman M.K.
      • Kulkarni A.
      • Cox S.
      • Marchbanks P.A.
      • Jamieson D.J.
      Elective oophorectomy in the United States: trends and in-hospital complications, 1998-2006.
      Although one of the earliest publications associating the fallopian tubes with the development of ovarian cancer was in 2001 by Dietl
      • Dietl J.
      Revisiting the pathogenesis of ovarian cancer: the central role of the fallopian tube.
      and Piek et al,
      • Piek J.M.
      • van Diest P.J.
      • Zweemer R.P.
      • et al.
      Dysplastic changes in prophylactically removed fallopian tubes of women predisposed to developing ovarian cancer.
      by 2008 and 2009, the evidence supporting the tubal hypothesis of ovarian cancer and associated increased long-term health risk with BSO
      • Parker W.H.
      • Broder M.S.
      • Chang E.
      • et al.
      Ovarian conservation at the time of hysterectomy and long-term health outcomes in the nurses' health study.
      led to calls for BS to be added to hysterectomies performed for benign reasons in women at average population risk of ovarian cancer.
      • Kindelberger D.W.
      • Lee Y.
      • Miron A.
      • et al.
      Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship.
      • Salvador S.
      • Gilks B.
      • Kobel M.
      • Huntsman D.
      • Rosen B.
      • Miller D.
      The fallopian tube: primary site of most pelvic high-grade serous carcinomas.
      • Schenberg T.
      • Mitchell G.
      Prophylactic bilateral salpingectomy as a prevention strategy in women at high-risk of ovarian cancer: a mini-review.
      • Seidman J.D.
      • Zhao P.
      • Yemelyanova A.
      “Primary peritoneal” high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer.
      This universal swift change in practice pattern is evident in our study (Figure 5).
      To change current recommendations safely, we need prospective evidence that the strategy of a staged approach is not inferior to upfront risk-reducing BSO to reduce the risk of cancer in BRCA carriers. A randomized controlled trial comparing these strategies is unfortunately not feasible.
      • Schenberg T.
      • Mitchell G.
      Prophylactic bilateral salpingectomy as a prevention strategy in women at high-risk of ovarian cancer: a mini-review.
      Despite the absence of prospective evidence that BS decreases the incidence of ovarian cancer, the British Columbia Ovarian Cancer Prevention Project encourages prophylactic BS and estimates up to a 50% reduction in ovarian cancer deaths after 20 years, and up to 20% through BS at time of hysterectomy, up to 20% through BS instead of tubal ligation, and up to 20% through risk-reducing BSO in patients with BRCA mutations.
      • Morelli M.
      • Venturella R.
      • Mocciaro R.
      • et al.
      Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
      Since 2010, an educational initiative aimed for gynecologic surgeons in the province of British Columbia, Canada, has resulted in a shift in surgical paradigm for the uptake of BS during hysterectomy procedures in that province.
      • McAlpine J.N.
      • Hanley G.E.
      • Woo M.M.
      • et al.
      Opportunistic salpingectomy: uptake, risks, and complications of a regional initiative for ovarian cancer prevention.
      Concomitant BS during hysterectomy does not seem to increase perioperative morbidity. In a clinical trial conducted by Findley et al,
      • Findley A.D.
      • Siedhoff M.T.
      • Hobbs K.A.
      • et al.
      Short-term effects of salpingectomy during laparoscopic hysterectomy on ovarian reserve: a pilot randomized controlled trial.
      which only included 30 patients, the conclusion was that BS at the time of laparoscopic hysterectomy with ovarian preservation is a safe procedure that does not appear to have any short-term deleterious effects on ovarian reserve. Although this study was underpowered and followed up patients for only 3 months, it provided encouraging results. In another retrospective study by Morelli et al,
      • Morelli M.
      • Venturella R.
      • Mocciaro R.
      • et al.
      Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
      that included 79 patients, they found no significant differences in perioperative outcomes or ovarian reserve modification between patients who underwent total laparoscopic hysterectomy with and without BS. It is important to note that larger studies with longer follow-up periods are needed.
      The strengths of this study include the fact that we used the HCUP-NIS database that is a sample of hospitals designed to approximate a 20% sample of all US community hospitals. All discharges are retained for each sampled hospital. The NIS is a yearly database and includes roughly 1000 hospitals with about 7 million discharge records.
      • Steiner C.
      • Elixhauser A.
      • Schnaier J.
      The healthcare cost and utilization project: an overview.
      Nevertheless, the major weakness of our study is that the NIS database does not include outpatient procedures; hence some of the hysterectomies performed in the outpatient setting were not sampled. However, according to Russo et al,
      • Russo A.
      • Elixhauser A.
      • Steiner C.
      • Wier L.
      Hospital-based ambulatory surgery, 2007. Statistical brief no. 86.
      only 13.8% of hysterectomy procedures were done as an outpatient procedure during 2007. Further studies are needed to investigate if the proportion of outpatient hysterectomy is increasing in recent years and if there is a difference in the trends of concomitant adnexal surgery. Despite this limitation, a universal shift in the type of adnexal surgeries being performed during hysterectomy for benign indications in the United States is evident from this study. Whether this change in practice pattern would effectively reduce the burden of ovarian cancer while allowing women to preserve ovarian function, or whether the trends for ovarian preservation will increase the need for subsequent surgery for benign adnexal indications will remain to be seen through subsequent studies.

      Appendix

      Supplementary Table 1List of ICD-9 diagnosis and procedure codes used to identify selected clinical conditions and procedures
      Condition/procedureICD-9-CM diagnosis code, or ICD-9 procedure code
      Code suffix “x” represents all possible codes that follow stated code prefix. Unless otherwise specified, codes were available for entire study period (1998 through 2011)
      Hysterectomy procedures
      Ability to differentiate all included hysterectomies by route (laparoscopic, nonlaparoscopic abdominal, nonlaparoscopic vaginal) was not possible until Oct. 1, 2006 since 68.31 and 68.39 codes were not implemented until Oct. 1, 2003 and 68.41 and 68.49 codes until Oct. 1, 2006
      68.3x, 68.4x, 68.5x
       Laparoscopic68.31, 68.41, 68.51
       Nonlaparoscopic abdominal68.39, 68.49
       Nonlaparoscopic vaginal68.59
      Diagnoses indicating benign indications
       Uterine leiomyoma218.0–218.2, 218.9
       Carcinoma in situ of cervix uteri233.1
       Uterine prolapse618.1–618.4, 618.89
       Hypertrophy of uterus621.2
       Endometrial hyperplasia621.31–621.33
       Other specified disorders of uterus621.8
       Cervical dysplasia622.11, 622.12
       Dysmenorrhea625.3
       Menstruation disorders626.2, 626.4, 626.6, 626.8, 626.9, 627.0
      Exclusion criteria (diagnoses)
       Malignant neoplasm of cervix uteri180x
       Malignant neoplasm of placenta181x
       Malignant neoplasm of body of uterus182x
       Malignant neoplasm of ovary and other uterine adnexa183x
       Malignant neoplasm of other/unspecified female genital organs184x
      Exclusion criteria (procedures)
       Radical abdominal hysterectomy68.6x
       Radical vaginal hysterectomy68.7x
       Pelvic evisceration68.8
       Delivery or obstetrical operation72x, 73x, 74x, 75x
      Procedural outcomes
       Bilateral salpingo-oophorectomy65.61, 65.63
       Bilateral salpingectomy66.51
       Bilateral oophorectomy65.51, 65.53
       Removal of remaining ovary and tube65.62, 65.64
       Removal of remaining tube66.52
       Removal of remaining ovary65.52, 65.54
      Other clinical factors
       Personal history of breast cancerV10.3
       Family history of breast cancerV16.3
       Family history of ovarian cancerV16.41
       Genetic susceptibility to breast cancer
      Codes not available until October 1, 2004.
      V84.01
       Genetic susceptibility to ovarian cancer
      Codes not available until October 1, 2004.
      V84.02
      ICD-9, International Classification of Diseases, Ninth Revision; ICD-9-CM, International Classification of Diseases, Ninth Revision, Clinical Modification.
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      a Code suffix “x” represents all possible codes that follow stated code prefix. Unless otherwise specified, codes were available for entire study period (1998 through 2011)
      b Ability to differentiate all included hysterectomies by route (laparoscopic, nonlaparoscopic abdominal, nonlaparoscopic vaginal) was not possible until Oct. 1, 2006 since 68.31 and 68.39 codes were not implemented until Oct. 1, 2003 and 68.41 and 68.49 codes until Oct. 1, 2006
      c Codes not available until October 1, 2004.
      Supplementary Table 2Time-specific and average APC in rates of bilateral salpingo-oophorectomy
      CharacteristicFirst time segmentAnnual percent change (95% CI)Second time segmentAnnual percent change (95% CI)Average annual percent change (95% CI)
      Overall1998 through 20012.2 (0.4–4.0)
      Statistically significantly different from 0.
      2001 through 2011−3.6 (−4.0 to −3.3)
      Statistically significantly different from 0.
      −2.3 (−2.7 to −1.9)
      Statistically significantly different from 0.
      Age at admission, y
       18–241998 through 2011−0.2 (−2.0 to 1.6)n/an/a−0.2 (−2.0 to 1.6)
       25–341998 through 20016.0 (2.0–10.3)
      Statistically significantly different from 0.
      2001 through 2011−3.2 (−3.9 to −2.5)
      Statistically significantly different from 0.
      −1.1 (−2.0 to −0.2)
      Statistically significantly different from 0.
       35–441998 through 20012.5 (0.0–5.1)2001 through 2011−5.8 (−6.3 to −5.3)
      Statistically significantly different from 0.
      −3.9 (−4.5 to −3.4)
      Statistically significantly different from 0.
       45–541998 through 2002−0.2 (−1.2 to 0.8)2002 through 2011−4.9 (−5.3 to −4.4)
      Statistically significantly different from 0.
      −3.5 (−3.8 to −3.1)
      Statistically significantly different from 0.
       55–641998 through 20012.4 (1.1–3.7)
      Statistically significantly different from 0.
      2001 through 2011−1.9 (−2.2 to −1.7)
      Statistically significantly different from 0.
      −1.0 (−1.3 to −0.7)
      Statistically significantly different from 0.
       ≥651998 through 20013.2 (−0.2 to 6.6)2001 through 2011−0.4 (−1.0 to 0.2)0.4 (−0.4 to 1.2)
      Primary payer
       Government
      Includes Medicare and Medicaid
      1998 through 20012.8 (0.6–5.0)
      Statistically significantly different from 0.
      2001 through 2011−2.4 (−2.8 to −2.0)
      Statistically significantly different from 0.
      −1.2 (−1.7 to −0.7)
      Statistically significantly different from 0.
       Private1998 through 20011.9 (0.0–3.9)2001 through 2011−3.9 (−4.3 to −3.5)
      Statistically significantly different from 0.
      −2.6 (−3.0 to −2.1)
      Statistically significantly different from 0.
       Other
      Includes self-pay, no charge, and other payers
      1998 through 20022.3 (−0.2 to 4.9)2002 through 2011−4.5 (−5.3 to −3.6)
      Statistically significantly different from 0.
      −2.4 (−3.3 to −1.6)
      Statistically significantly different from 0.
      Household income
       Lowest quartile
      Category had 2 joinpoints estimated by best fitting model. The third time segment was from 2009-2011 and had an APC of −7.7 (−15.0 to 0.1)
      1998 through 20013.0 (0.4–5.8)
      Statistically significantly different from 0.
      2001 through 2009−2.7 (−3.5 to −1.9)
      Statistically significantly different from 0.
      −2.2 (−3.3 to −1.0)
      Statistically significantly different from 0.
       Second quartile1998 through 20021.0 (−0.3 to 2.4)2002 through 2011−3.5 (−4.0 to −3.1)
      Statistically significantly different from 0.
      −2.2 (−2.6 to −1.7)
      Statistically significantly different from 0.
       Third quartile1998 through 20011.8 (−0.4 to 4.0)2001 through 2011−4.0 (−4.4 to −3.6)
      Statistically significantly different from 0.
      −2.7 (−3.2 to −2.2)
      Statistically significantly different from 0.
       Highest quartile1998 through 20011.0 (−0.5 to 2.4)2001 through 2011−4.2 (−4.5 to −3.9)
      Statistically significantly different from 0.
      −3.0 (−3.4 to −2.7)
      Statistically significantly different from 0.
      Hospital region
       Northeast1998 through 2004−1.4 (−2.4 to −0.5)
      Statistically significantly different from 0.
      2004 through 2011−4.8 (−5.8 to −3.7)
      Statistically significantly different from 0.
      −3.3 (−3.9 to −2.6)
      Statistically significantly different from 0.
       Midwest1998 through 20020.2 (−1.8 to 2.2)2002 through 2011−3.4 (−4.0 to −2.8)
      Statistically significantly different from 0.
      −2.3 (−2.9 to −1.7)
      Statistically significantly different from 0.
       South1998 through 20013.9 (1.2–6.7)
      Statistically significantly different from 0.
      2001 through 2011−3.2 (−3.7 to −2.7)
      Statistically significantly different from 0.
      −1.6 (−2.2 to −1.0)
      Statistically significantly different from 0.
       West1998 through 20010.6 (−3.0 to 4.3)2001 through 2011−4.8 (−5.5 to −4.0)
      Statistically significantly different from 0.
      −3.5 (−4.4 to −2.7)
      Statistically significantly different from 0.
      Hospital location
       Urban1998 through 20011.9 (0.3–3.4)
      Statistically significantly different from 0.
      2001 through 2011−3.8 (−4.1 to −3.5)
      Statistically significantly different from 0.
      −2.5 (−2.9 to −2.2)
      Statistically significantly different from 0.
       Rural1998 through 20013.5 (−1.6 to 8.9)2001 through 2011−2.5 (−3.4 to −1.7)
      Statistically significantly different from 0.
      −1.2 (−2.3 to 0.0)
      Hospital teaching status
       Teaching1998 through 20021.2 (−0.9 to 3.3)2002 through 2011−3.9 (−4.6 to −3.2)
      Statistically significantly different from 0.
      −2.4 (−3.1 to −1.7)
      Statistically significantly different from 0.
       Nonteaching1998 through 20012.0 (−0.9 to 4.9)2001 through 2011−3.7 (−4.2 to −3.2)
      Statistically significantly different from 0.
      −2.4 (−3.1 to −1.8)
      Statistically significantly different from 0.
      Among inpatient discharges in which hysterectomy was performed due to benign indications, by selected patient and hospital characteristics, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 1998 through 2011.
      APC, annual percent change; CI, confidence interval; n/a, subgroups for which no statistically significant change in trend occurred during study period.
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      a Includes Medicare and Medicaid
      b Includes self-pay, no charge, and other payers
      c Category had 2 joinpoints estimated by best fitting model. The third time segment was from 2009-2011 and had an APC of −7.7 (−15.0 to 0.1)
      d Statistically significantly different from 0.
      Supplementary Table 3Time-specific and average APC in rates of bilateral salpingectomy
      CharacteristicFirst time segmentAPC (95% CI)Second time segmentAPC (95% CI)Average APC (95% CI)
      Overall1998 through 20088.0 (5.6–10.5)
      Statistically significantly different from 0.
      2008 through 201123.8 (4.3–46.8)
      Statistically significantly different from 0.
      11.4 (7.4–15.7)
      Statistically significantly different from 0.
      Age at admission, y
       18241998 through 201110.7 (4.5–17.3)
      Statistically significantly different from 0.
      n/an/a10.7 (4.5–17.3)
      Statistically significantly different from 0.
       25–341998 through 20084.6 (0.8–8.6)
      Statistically significantly different from 0.
      2008 through 201130.9 (4.7–63.6)
      Statistically significantly different from 0.
      10.2 (4.7–15.9)
      Statistically significantly different from 0.
       35–44
      35–44-y age group had 2 joinpoints estimated by best fitting model. The third time segment was from 2009-2011 and had an APC of 26.2 (12.1–42.0)
      1998 through 2000−5.3 (−25.4 to 20.2)2000 through 20087.9 (4.4–11.4)
      Statistically significantly different from 0.
      9.6 (5.3–14.1)
      Statistically significantly different from 0.
       45–541998 through 201114.7 (11.7–17.7)
      Statistically significantly different from 0.
      n/an/a14.7 (11.7–17.7)
      Statistically significantly different from 0.
       55–641998 through 20119.6 (4.0–15.5)
      Statistically significantly different from 0.
      n/an/a9.6 (4.0–15.5)
      Statistically significantly different from 0.
       ≥651998 through 200620.3 (11.1–30.2)
      Statistically significantly different from 0.
      2006 through 2011−0.8 (−14.0 to 14.4)11.7 (4.8–19.0)
      Statistically significantly different from 0.
      Primary payer
       Government
      Includes Medicare and Medicaid
      1998 through 201110.9 (9.0–12.8)
      Statistically significantly different from 0.
      n/an/a10.9 (9.0–12.8)
      Statistically significantly different from 0.
       Private1998 through 20088.0 (5.8–10.2)
      Statistically significantly different from 0.
      2008 through 201125.7 (7.3–47.1)
      Statistically significantly different from 0.
      11.8 (8.0–15.7)
      Statistically significantly different from 0.
       Other
      Includes self-pay, no charge, and other payers
      1998 through 20118.3 (5.3–11.3)
      Statistically significantly different from 0.
      n/an/a8.3 (5.3–11.3)
      Statistically significantly different from 0.
      Household income
       Lowest quartile1998 through 20119.4 (7.2–11.6)
      Statistically significantly different from 0.
      n/an/a9.4 (7.2–11.6)
      Statistically significantly different from 0.
       Second quartile1998 through 20119.9 (7.5–12.3)
      Statistically significantly different from 0.
      n/an/a9.9 (7.5–12.3)
      Statistically significantly different from 0.
       Third quartile1998 through 20088.0 (5.8–10.3)
      Statistically significantly different from 0.
      2008 through 201129.0 (9.4–52.1)
      Statistically significantly different from 0.
      12.6 (8.6–16.7)
      Statistically significantly different from 0.
       Highest quartile1998 through 201111.7 (9.3–14.1)
      Statistically significantly different from 0.
      n/an/a11.7 (9.3–14.1)
      Statistically significantly different from 0.
      Hospital region
       Northeast1998 through 201113.3 (9.8–16.8)
      Statistically significantly different from 0.
      n/an/a13.3 (9.8–16.8)
      Statistically significantly different from 0.
       Midwest1998 through 20116.5 (4.3–8.8)
      Statistically significantly different from 0.
      n/an/a6.5 (4.3–8.8)
      Statistically significantly different from 0.
       South1998 through 201110.6 (8.1–13.1)
      Statistically significantly different from 0.
      n/an/a10.6 (8.1–13.1)
      Statistically significantly different from 0.
       West1998 through 201110.3 (7.2–13.5)
      Statistically significantly different from 0.
      n/an/a10.3 (7.2–13.5)
      Statistically significantly different from 0.
      Hospital location
       Urban1998 through 20088.8 (6.0–11.6)
      Statistically significantly different from 0.
      2008 through 201124.8 (2.6–51.9)
      Statistically significantly different from 0.
      12.3 (7.6–17.2)
      Statistically significantly different from 0.
       Rural1998 through 20116.2 (3.8–8.7)
      Statistically significantly different from 0.
      n/an/a6.2 (3.8–8.7)
      Statistically significantly different from 0.
      Hospital teaching status
       Teaching1998 through 20088.5 (7.1–10.0)
      Statistically significantly different from 0.
      2008 through 201126.1 (13.3–40.2)
      Statistically significantly different from 0.
      12.4 (9.8–15.0)
      Statistically significantly different from 0.
       Nonteaching1998 through 20119.7 (7.2–12.2)
      Statistically significantly different from 0.
      n/an/a9.7 (7.2–12.2)
      Statistically significantly different from 0.
      Among inpatient discharges in which hysterectomy was performed due to benign indications, by selected patient and hospital characteristics, Healthcare Cost and Utilization Project–Nationwide Inpatient Sample, 1998 through 2011.
      APC, annual percent change; CI, confidence interval; n/a, subgroups for which no statistically significant change in trend occurred during study period.
      Mikhail. National trends of adnexal surgeries. Am J Obstet Gynecol 2015.
      a 35–44-y age group had 2 joinpoints estimated by best fitting model. The third time segment was from 2009-2011 and had an APC of 26.2 (12.1–42.0)
      b Includes Medicare and Medicaid
      c Includes self-pay, no charge, and other payers
      d Statistically significantly different from 0.

      References

        • Jemal A.
        • Bray F.
        • Center M.M.
        • Ferlay J.
        • Ward E.
        • Forman D.
        Global cancer statistics.
        CA Cancer J Clin. 2011; 61: 69-90
        • Tanner E.J.
        • Long K.C.
        • Visvanathan K.
        • Fader A.N.
        Prophylactic salpingectomy in premenopausal women at low risk for ovarian cancer: risk-reducing or risky?.
        Fertil Steril. 2013; 100: 1530-1531
        • Parker W.H.
        • Broder M.S.
        • Chang E.
        • et al.
        Ovarian conservation at the time of hysterectomy and long-term health outcomes in the nurses' health study.
        Obstet Gynecol. 2009; 113: 1027-1037
        • Kindelberger D.W.
        • Lee Y.
        • Miron A.
        • et al.
        Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship.
        Am J Surg Pathol. 2007; 31: 161-169
        • Carlson J.W.
        • Miron A.
        • Jarboe E.A.
        • et al.
        Serous tubal intraepithelial carcinoma: its potential role in primary peritoneal serous carcinoma and serous cancer prevention.
        J Clin Oncol. 2008; 26: 4160-4165
        • Dietl J.
        Revisiting the pathogenesis of ovarian cancer: the central role of the fallopian tube.
        Arch Gynecol Obstet. 2014; 289: 241-246
        • Salvador S.
        • Gilks B.
        • Kobel M.
        • Huntsman D.
        • Rosen B.
        • Miller D.
        The fallopian tube: primary site of most pelvic high-grade serous carcinomas.
        Int J Gynecol Cancer. 2009; 19: 58-64
        • Schenberg T.
        • Mitchell G.
        Prophylactic bilateral salpingectomy as a prevention strategy in women at high-risk of ovarian cancer: a mini-review.
        Front Oncol. 2014; 4: 21
      1. Healthcare Cost and Utilization Project (HCUP). HCUP databases. Overview of the Nationwide Inpatient Sample (NIS). Agency for Healthcare Research and Quality, Rockville, MD2011
        • Kim H.J.
        • Fay M.P.
        • Feuer E.J.
        • Midthune D.N.
        Permutation tests for joinpoint regression with applications to cancer rates.
        Stat Med. 2000; 19: 335-351
      2. Houchens RL, Elixhauser A. Using the HCUP Nationwide Inpatient Sample to estimate trends (updated for 1988-2004). HCUP methods series report no 2006-05 online. US Agency for Healthcare Research and Quality; Aug. 18, 2006. Available at: http://www.hcup-us.ahrq.gov/reports/methods.jsp. Accessed Nov. 30, 2014.

      3. Song X, Friedman B. Calculate cost adjustment factors by APR-DRG and CCS using selected states with detailed charges. HCUP methods series report no. 2008-04. US Agency for Healthcare Research and Quality. Available at: http://www.hcup-us.ahrq.gov/reports/methods.jsp. Accessed Nov. 30, 2014.

        • American College of Obstetrics and Gynecology
        Elective and risk-reducing salpingo-oophorectomy. ACOG Practice bulletin no. 89.
        Obstet Gynecol. 2008; 111: 231-241
        • Seidman J.D.
        • Zhao P.
        • Yemelyanova A.
        “Primary peritoneal” high-grade serous carcinoma is very likely metastatic from serous tubal intraepithelial carcinoma: assessing the new paradigm of ovarian and pelvic serous carcinogenesis and its implications for screening for ovarian cancer.
        Gynecol Oncol. 2011; 120: 470-473
        • Sieh W.
        • Salvador S.
        • McGuire V.
        • et al.
        Tubal ligation and risk of ovarian cancer subtypes: a pooled analysis of case-control studies.
        Int J Epidemiol. 2013; 42: 579-589
        • Kurman R.J.
        • Shih Ie M.
        The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory.
        Am J Surg Pathol. 2010; 34: 433-443
        • Kwon J.S.
        • Tinker A.
        • Pansegrau G.
        • et al.
        Prophylactic salpingectomy and delayed oophorectomy as an alternative for BRCA mutation carriers.
        Obstet Gynecol. 2013; 121: 14-24
        • Asante A.
        • Whiteman M.K.
        • Kulkarni A.
        • Cox S.
        • Marchbanks P.A.
        • Jamieson D.J.
        Elective oophorectomy in the United States: trends and in-hospital complications, 1998-2006.
        Obstet Gynecol. 2010; 116: 1088-1095
        • Lepine L.A.
        • Hillis S.D.
        • Marchbanks P.A.
        • et al.
        Hysterectomy surveillance–United States, 1980-1993.
        MMWR CDC Surveill Summ. 1997; 46: 1-15
        • Piek J.M.
        • van Diest P.J.
        • Zweemer R.P.
        • et al.
        Dysplastic changes in prophylactically removed fallopian tubes of women predisposed to developing ovarian cancer.
        J Pathol. 2001; 195: 451-456
        • Morelli M.
        • Venturella R.
        • Mocciaro R.
        • et al.
        Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere.
        Gynecol Oncol. 2013; 129: 448-451
        • McAlpine J.N.
        • Hanley G.E.
        • Woo M.M.
        • et al.
        Opportunistic salpingectomy: uptake, risks, and complications of a regional initiative for ovarian cancer prevention.
        Am J Obstet Gynecol. 2014; 210: 471.e1-471.e11
        • Findley A.D.
        • Siedhoff M.T.
        • Hobbs K.A.
        • et al.
        Short-term effects of salpingectomy during laparoscopic hysterectomy on ovarian reserve: a pilot randomized controlled trial.
        Fertil Steril. 2013; 100: 1704-1708
        • Steiner C.
        • Elixhauser A.
        • Schnaier J.
        The healthcare cost and utilization project: an overview.
        Eff Clin Pract. 2002; 5: 143-151
        • Russo A.
        • Elixhauser A.
        • Steiner C.
        • Wier L.
        Hospital-based ambulatory surgery, 2007. Statistical brief no. 86.
        Healthcare Cost and Utilization Project (HCUP) Statistical Briefs, Rockville, MD2006