Original Article Trends of Bilateral Salpingectomy During Vaginal Hysterectomy With and Without Laparoscopic Assistance Performed for Benign Indications in the United States Emad Mikhail, MD*, Jason L. Salemi, PhD, MPH, Allison Wyman, MD, Hamisu M. Salihu, MD, PhD, Anthony N. Imudia, MD, and Stuart Hart, MD From the Department of Obstetrics and Gynecology, University of South Florida, Morsani College of Medicine, Tampa, Florida (Drs. Mikhail, Wyman, Salihu, Imudia, and Hart), and Department of Family and Community Medicine, Baylor College of Medicine, Houston, Texas (Drs. Salemi and Salihu). ABSTRACT Study Objective: To estimate the recent temporal trends of concurrent bilateral salpingectomy (BS) during vaginal hysterectomy (total vaginal hysterectomy [TVH] and laparoscopic-assisted vaginal hysterectomy [LAVH]) in the United States. Design: A cross-sectional analysis was conducted using data from the Healthcare Cost and Utilization Project Nationwide Inpatient Sample, including all female patients 18 years and older whose inpatient discharge record indicated a TVH or LAVH performed for benign indications between January 1, 1998, and December 31, 2011. Joinpoint regression was used to identify statistically significant changes in overall and subgroup temporal trends of TVH and LAVH as well as concomitant BS during the 14-year study period (Canadian Task Force Classification II). Setting: Not applicable. Patients: All patients who underwent TVH and LAVH from 1998 to 2011 registered in the Healthcare Cost and Utilization Project Nationwide Inpatient Sample database. Interventions: Not applicable. Measurements and Main Results: Regarding TVH, between 1998 and 2001, there was a steep negative trend with an annual percentage change of 25.2 (95% confidence interval [CI], 28.8 to 22.2). From 2001 to 2011, the negative trend was still observed but with a more gradual 2% annual decrease (95% CI, 22.4 to 21.3). Conversely, the rate of LAVH increased at a rate of 4.4% each year (95% CI, 3.7–5.0). From 1998 to 2004, the national rate of BS during TVH increased sharply with an annual increase of 42.8% (95% CI, 22.7–66.3). Beginning in 2004, the BS rate during TVH decreased and remained stable. During LAVH, the rate of concomitant BS increased an estimated 15% each year during the entire study period (95% CI, 11.9–17.8). Conclusion: The proportion of annual LAVH with concomitant BS procedures performed across the nation is on the rise while TVH is declining with a stable rate of concomitant BS. Journal of Minimally Invasive Gynecology (2016) -, -–- Ó 2016 AAGL. All rights reserved. Keywords: Laparoscopic-assisted vaginal hysterectomy; Salpingectomy; Temporal trends; Vaginal hysterectomy Bilateral salpingectomy (BS) at the time of hysterectomy performed for benign indications should be an important Dr. Hart was a speaker and consultant for Medtronic. The authors declare that they have no conflict of interest. A preliminary version of these data was presented at the American Association of Gynecologic Laparoscopists Global Congress on Minimally Invasive Gynecology, November 15-19, 2015, Las Vegas, NV. Corresponding author: Emad Mikhail, MD, Department of Obstetrics and Gynecology, University of South Florida, 2 Tampa General Circle, Tampa, FL 33606. E-mail: emikhail@health.usf.ed Submitted May 4, 2016. Accepted for publication July 12, 2016. Available at www.sciencedirect.com and www.jmig.org 1553-4650/$ - see front matter Ó 2016 AAGL. All rights reserved. http://dx.doi.org/10.1016/j.jmig.2016.07.009 component of preoperative patient counseling. Recently, it became generally accepted that most pelvic serous carcinomas originate from the distal fallopian tube [1–3]. It is worth noting that recently 2 large population-based retrospective studies have shown a decreased risk for ovarian cancer for women who underwent salpingectomy or tubal ligation [4,5]. This belief has warranted gynecologic surgeons to begin counseling patients about the potential benefits of the removal of the fallopian tubes during hysterectomy, particularly in women at a population risk of ovarian cancer who are not undergoing a concomitant oophorectomy [6]. Recent studies have shown that the rate of BS during hysterectomy performed for benign 2 Journal of Minimally Invasive Gynecology, Vol -, No -, -/- 2016 indications, regardless of the route of hysterectomy, quadrupled between 1998 and 2011 [7]. Although vaginal hysterectomy remains the preferred and the recommended route of hysterectomy for benign disease [8,9], the use of a vaginal approach for hysterectomy performed for benign indication decreased from 22% in 2003 to 2005 to 18% in 2009 [10]. Researchers have attributed this decrease in the rate of vaginal hysterectomy to various reasons [11], but it remains unknown how this decline could impact the recommended uptake of concomitant BS during benign hysterectomy. It is possible that the performance of fewer vaginal hysterectomies will negatively impact the uptake of concomitant BS during vaginal hysterectomy, and, thus, laparoscopic use might be needed to facilitate the performance of BS as part of the hysterectomy. Therefore, to fill this gap in knowledge, we sought to estimate the temporal trends of gynecologic surgeons’ performance of concomitant bilateral salpingectomy during vaginal hysterectomy (total vaginal hysterectomy [TVH] and laparoscopic-assisted vaginal hysterectomy [LAVH]) in the United States. Our study will add to the existing body of evidence that attempts to identify and explain changing practice patterns among gynecologists in the United States. Material and Methods A cross-sectional analysis was conducted using data from the Healthcare Cost and Utilization Project Nationwide Inpatient Sample (NIS), the largest publicly available all-payer inpatient database in the United States [12]. Each year, the NIS stratifies all nonfederal community hospitals from participating states (1049 hospitals in 46 states in 2011) into groups based on 5 major hospital characteristics: rural/urban location, number of beds, geographic region, teaching status, and ownership. Within each stratum, a 20% sample of hospitals is drawn using a systematic random sampling technique [13]. All discharges are retained for each sampled hospital. The NIS is generated annually and, in 2011, included over 1000 hospitals and approximately 7 million discharge records [14]. The study population includes all female patients aged 18 years and older whose inpatient discharge record indicated a vaginal hysterectomy that was performed for benign indications between January 1, 1998, and December 31, 2011. Hysterectomies for nonbenign indications were excluded. Discharges with diagnoses or procedures indicative of ovarian disease, tubal disease, pelvic adhesions, and endometriosis were also excluded. Please review Appendix 1 for details of the inclusion and exclusion criteria. We then classified vaginal hysterectomies into 2 groups based on whether laparoscopic assistance was included (LAVH) or not (TVH). We only included LAVH and TVH because these are the routes in question; analyses including other routes (e.g., total laparoscopic hysterectomy or robotic-assisted total laparoscopic hysterectomy) or supracervical hysterectomy are beyond the scope of this study. We subclassified LAVH and TVH discharges by the type of adnexal surgery performed at the time of hysterectomy, specifically BS (Fig. 1). All clinical diagnoses and surgical procedures were identified using International Classification of Diseases, Ninth Revision, Clinical Modification diagnosis and procedure codes. Fig. 1 A flow diagram representing the final determination of all inpatient discharges in which a hysterectomy was performed because of benign indications and subsequent classification by hysterectomy route and adnexal surgery (Healthcare Cost and Utilization Project NIS, 1998–2011).ICD-9 5 International Clasification of Diseases, Ninth Edition; LAVH 5 laparoscopically-assisted vaginal hysterectomy TVH 5 total vaginal hysterectomy. a Excludes rehabilitation and long-term acute care hospital. b See Appendix 1 for specific diagnosis and procedure code lists. Mikhail et al. 3 Salpingectomy Trends During Vaginal Hysterectomy Descriptive statistics were used to describe the distribution of selected patient sociodemographic and hospital characteristics across women in the United States by type of hysterectomy (TVH vs LAVH) and by receipt of concomitant BS. Sociodemographic characteristics considered include age, race, income, reason for hysterectomy, hospital characteristics, and primary payer. We then estimated and compared the temporal trends of TVH and LAVH as well as the trends in the rates of BS between these 2 groups. To generate nationally representative estimates of rates and trends, we used sampling weights provided by the Health- care Cost and Utilization Project to account for the complex sampling design of the NIS. Differences in sociodemographic and hospital characteristics across groups were compared using the Rao-Scott modified chi-square test, which also accounts for the weighted analysis. Joinpoint regression was used to identify statistically significant changes in the temporal trends described earlier. Joinpoint regression analysis is a statistical method that illustrates changing trends over successive segments of time and the amount of increase or decrease within each distinct time segment. This analysis involves fitting a series of joined Table 1 Distribution of selected patient sociodemographic and hospital characteristics among inpatient discharges in which a vaginal hysterectomy was performed because of benign indications (Healthcare Cost and Utilization Project Nationwide Inpatient Sample, 1998–2011) TVH (n 5 1 349 439) n* Age at admission (years) 18–24 25–34 35–44 45–54 55–64 R65 Race/ethnicity Non-Hispanic white Non-Hispanic black Hispanic Other Missing Primary payer Governmentz Private Otherx Household income Lowest quartile 2nd quartile 3rd quartile Highest quartile Hospital region Northeast Midwest South West Hospital location Urban Rural Hospital teaching status Teaching Nonteaching LAVH (n 5 655 293) %* n* %* 6792 149 486 456 792 363 471 160 320 212 579 0.5 11.1 33.9 26.9 11.9 15.8 3579 86 035 268 416 222 032 47 666 27 565 0.5 13.1 41.0 33.9 7.3 4.2 777 041 76 315 103 291 45 795 346 996 57.6 5.7 7.7 3.4 25.7 392 221 46 020 38 631 21 712 156 710 59.9 7.0 5.9 3.3 23.9 316 757 945 169 87 513 23.5 70.0 6.5 87 778 527 052 40 463 13.4 80.4 6.2 310 081 359 891 344 067 311 819 23.0 26.7 25.5 23.1 150 613 174 399 165 991 150 991 23.0 26.6 25.3 23.0 184 309 355 330 494 733 315 067 13.7 26.3 36.7 23.3 76 861 153 187 280 932 144 313 11.7 23.4 42.9 22.0 1 110 454 234 503 82.6 17.4 541 782 110 742 83.0 17.0 533 065 811 892 39.5 60.2 236 416 416 108 36.1 63.5 p valuey ,.001 ,.001 ,.001 .999 ,.001 .644 .010 LAVH 5 laparoscopic-assisted vaginal hysterectomy; TVH 5 total vaginal hysterectomy. * Weighted to estimate national frequency; the sum of all groups may not add up to the total because of missing data. Percentages for each primary outcome are column percentages to show the distribution of that characteristic in the 2 outcome groups. y p value calculated from a Rao-Scott modified chi-square test assessing whether there is a statistical association between the hysterectomy route and each characteristic. z Includes Medicare and Medicaid. x Includes self-pay, no charge, and other payers. 4 Journal of Minimally Invasive Gynecology, Vol -, No -, -/- 2016 Fig. 2 Trends in inpatient discharges in which a vaginal hysterectomy was performed because of benign indications by method of hysterectomy (Healthcare Cost and Utilization Project NIS, 1998–2011). X-axis denotes year of discharge; Y-axis denotes percentage of hysterectomies in which route was used. APC 5 annual percent change, point estimate (95% confidence interval); LAVH 5 laparoscopic-assisted vaginal hysterectomy; TVH 5 total vaginal hysterectomy. straight lines and choosing the best-fitting point or points, called joinpoints, where there is a statistically significant change (increase or decrease) in the rate. Each joinpoint in the final model represents a statistically significant change in trend. Then, the magnitude and statistical significance of the change between each distinct time segment are characterized by the annual percent change [15]. All statistical analyses were performed using SAS software, version 9.4 (SAS Institute, Cary, NC) and the Joinpoint Regression Program, version 4.1.1.1 (National Cancer Institute, Washington, DC). Statistical tests were 2 sided with a 5% type I error rate. Results During the 14-year study period, there were an estimated 1 169 700 discharges among women aged 18 and older who underwent a hysterectomy for benign indications, with 23.7% and 11.6% undergoing TVH and LAVH, respectively (Fig. 1). When estimated nationally, there was an average of over 143 000 discharges in which a vaginal hysterectomy was performed each year. The distribution of patient sociodemographic and hospital characteristics was compared among women receiving TVH versus LAVH. Several characteristics were statistically significantly (p , .001) associated with the route of hysterectomy including age, race, and primary payer (Table 1). Nearly 28% of women receiving TVH were 55 and older compared with less than 12% of women receiving LAVH. TVH discharges were also more likely to be paid for by government insurance (23.5%) compared with LAVH (13.4%). Certain hospital characteristics were also found to be signif- icantly associated with the route of hysterectomy, including hospital region and teaching status. About 43% of LAVH procedures were performed in the South compared with only 36.7% of TVH. For both TVH and LAVH, more than 80% of procedures were performed in urban hospitals, and more than 60% were performed in nonteaching hospitals (Table 1). There was a statistically significant decrease in the rate of TVH throughout the study period. Between 1998 and 2001, there was a steep negative trend with an annual percent change of 25.2 (95% confidence interval [CI], 28.8 to 22.2). From 2001 to 2011, the negative trend was still observed but with a more gradual 2% annual decrease (95% CI, 22.4 to 21.3). Conversely, the rate of LAVH among hysterectomies increased steadily throughout the study period, at a rate of 4.4% each year (95% CI, 3.7– 5.0) (Fig. 2). For both TVH and LAVH for benign indications, slightly less than 1% had a BS performed during the hysterectomy. We observed statistically significant differences in the distribution of age and race/ethnicity between TVH and LAVH groups during which BS was also performed. Over 60% of women receiving BS during TVH were 45 years and older, whereas over 75% of women receiving BS during LAVH were less than 45 years old (p , .001). One quarter of patient discharge records had missing race/ethnicity because of some states’ reporting protocols. However, among those with reported race and ethnicity, women undergoing BS during TVH were slightly more likely to be non-Hispanic white (73.4% vs 71.0%); those undergoing BS during LAVH were more likely to be non-Hispanic black (12.5% vs 9.1%, p 5 .029). The distribution of hospital characteristics was similar between BS during TVH and LAVH (Table 2). The national rate of BS during TVH changed significantly during the study period. Initially, from 1998 to 2004, BS during TVH increased sharply from less than 2 per 1000 discharges to 14 per 1000 discharges; with an estimated 42.8% annual increase (95% CI, 22.7–66.3). Beginning in 2004, the BS rate among TVH remained stable through 2011. Among LAVH, the rate of BS increased nearly 15% each year during the entire study period (95% CI, 11.9–17.8) (Fig. 3). Discussion A decreasing rate of TVH for benign indications was observed throughout the study period, but the rate of decline was less steep between 2001 and 2011. On the other hand, we observed a consistent increase in the rate of LAVH throughout the 14-year study period. Despite the position statements from the American College of Obstetricians and Gynecologists and the American Association of Gynecologic Laparoscopists endorsing vaginal hysterectomy as the preferred route of hysterectomy for benign disease [8,9], a negative trend was observed for TVH performed across the nation. Interestingly, the performance of Mikhail et al. 5 Salpingectomy Trends During Vaginal Hysterectomy Table 2 Distribution of selected patient sociodemographic and hospital characteristics among inpatient discharges in which a vaginal hysterectomy and bilateral salpingectomy were performed because of benign indications (Healthcare Cost and Utilization Project Nationwide Inpatient Sample, 1998–2011) Age at admission (years) 18–24 25–34 35–44 45–54 55–64 R65 Race/ethnicity Non-Hispanic white Non-Hispanic black Hispanic Other Missing Primary payer Governmentz Private Otherx Household income Lowest quartile 2nd quartile 3rd quartile Highest quartile Hospital region Northeast Midwest South West Hospital location Urban Rural Hospital teaching status Teaching Nonteaching Bilateral salpingectomy during TVH (n 5 11 551) Bilateral salpingectomy during LAVH (n 5 5700) n* %* n* %* 43 1054 3458 4052 1545 1398 0.4 9.1 29.9 35.1 13.4 12.1 92 1280 2945 1254 92 38 1.6 22.5 51.7 22.0 1.6 0.7 6393 797 1114 409 2837 55.4 6.9 9.7 3.5 24.6 3,359 591 537 244 969 58.9 10.4 9.4 4.3 17.0 2426 8200 924 21.0 71.0 8.0 941 4384 375 16.5 76.9 6.6 2931 2715 2794 2789 25.4 23.5 24.2 24.2 1483 1618 1211 1269 26.0 28.4 21.3 22.3 1184 2840 4790 2736 10.3 24.6 41.5 23.7 728 1737 2263 972 12.8 30.5 39.7 17.1 9748 1793 84.5 15.5 4384 1316 76.9 23.1 5119 6422 44.3 55.6 2145 3555 37.6 62.4 p valuey ,.001 .029 .051 .386 .351 .342 .189 * Weighted to estimate national frequency; the sum of all groups may not add up to the total because of missing data. Percentages for each primary outcome are column percentages to show the distribution of that characteristic in the 2 outcome groups. y p value calculated from a Rao-Scott modified chi-square test assessing whether there is a statistical association between the hysterectomy route and each characteristic. z Includes Medicare and Medicaid. x Includes self-pay, no charge, and other payers. concomitant BS has been increasing annually during LAVH compared with an increased performance of BS during TVH that was evident until 2004 followed by a stable rate. The question that arises is why the vaginal route for hysterectomy is underused despite its proven advantages. Researchers report that fewer than 20% of hysterectomies are performed using the vaginal approach [16]. In 2008, Julian [17] noted that few graduating residents felt comfortable performing vaginal hysterectomy. Surveys indicate that only 27.8% of residents in 2010 felt comfortable performing vaginal hysterectomy independently compared with 79% before 2008 [18,19]. The Society of Gynecologic Surgeons’ Education Committee identifies 3 critical factors associated with the underutilization of vaginal hysterectomy: (1) inadequate surgical training resulting from diminished cases in residency, (2) difficulty maintaining surgical skills in practice as a result of low surgical volumes, and (3) increased marketing and awareness of alternative hysterectomy techniques that result in vaginal hysterectomy appearing less attractive as 6 Journal of Minimally Invasive Gynecology, Vol -, No -, -/- 2016 Fig. 3 Trends in BS at the time of vaginal hysterectomy by method of hysterectomy (Healthcare Cost and Utilization Project NIS, 1998–2011). X-axis denotes year of discharge; Y-axis denotes percentage of hysterectomy subtype in which bilateral salpingectomy was performed. APC 5 annual percent change, point estimate (95% confidence interval); LAVH 5 laparoscopic-assisted vaginal hysterectomy; TVH 5 total vaginal hysterectomy. a surgical option [11]. It appears from the results of this study that the decline in the number of TVHs could be the result of greater use of LAVH, which allows for easier performance of BS. The role of the fallopian tube in the pathogenesis of ovarian cancer has been studied extensively [20–22]. Recent studies have shown that national rates of BS among women undergoing hysterectomy for benign indications increased significantly, with an 8% annual increase from 1998 to 2008 followed by a more pronounced 24% annual increase from 2008 to 2011 [7]. The American College of Obstetricians and Gynecologists continues to emphasize minimally invasive approaches for hysterectomy and favors the vaginal approach even if salpingectomy is planned by stating that ‘‘The approach to hysterectomy should not be influenced by the theoretical benefit of salpingectomy. Surgeons should continue to observe and practice minimally invasive techniques. A vaginal hysterectomy should not be changed to a laparoscopic hysterectomy simply to perform concurrent salpingectomy [6].’’ Adherence to this recommendation is not justified by the findings of this study. It appears that soon after the initial report of the role of fallopian tubes in the pathogenesis of ovarian cancer, surgeons made every effort to perform concomitant BS during TVH, but this practice pattern was only maintained until 2004. The change in practice pattern could be caused by greater use of LAVH as an alternative surgical approach. Specifically, the trends of BS during TVH were lacking behind the general trend, as evident in this study. Despite an initial increase during 1998 to 2004, the rate did not change significantly between 2004 and 2011. On the other hand, a sustained increasing rate of BS during LAVH was observed throughout the study period. Knowing that pelvic adhesions significantly predicted the ability to perform salpingectomy during vaginal hysterectomy (odds ratio 5 6.3; 95% CI, 2.8–14.3) [23], all records with any of the following diagnoses were excluded from the analysis: benign neoplasm of ovary, polycystic ovaries, salpingitis, oophoritis, pelvic peritoneal adhesions, endometriosis of ovary, fallopian tube, ovarian cyst, and congenital anomalies of ovaries or the fallopian tubes (Appendix 1). These exclusions enabled us to ascertain that the declining trend of concurrent BS during TVH was not caused by pelvic adhesive disease. Surgical experience in performing vaginal adnexectomy is considered very important to successfully complete the procedure. Some authors report a success rate of 95% (158/166) excluding cases with malignancy and limited adnexal mobility [24]. In a study published by Robert et al [23], an 88% success rate was shown in performing concomitant salpingectomy in all women presenting for vaginal hysterectomy. They also reported that surgical experience continued to grow throughout their study period; 50% of the salpingectomies not performed for technical reasons occurred in the first 50 hysterectomies performed by each surgeon [23]. In addition, some researchers propose that laparoscopic assistance is not necessary for prophylactic oophorectomy during vaginal hysterectomy by experienced vaginal surgeons in patients without associated problems, such as endometriosis, adhesions, or adnexal masses [25]. It is to be noted that both of these studies describe the practice of experienced vaginal surgeons. On the other hand, findings in the current study show a national trend that better reflects the general gynecologic surgery practice patterns, which demonstrate a shift toward more laparoscopicassisted vaginal surgeries as opposed to traditional TVH. Concomitant BS during laparoscopic hysterectomy does not seem to increase perioperative morbidity. In a clinical trial conducted by Findley et al [26] that 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. In another retrospective study by Morelli et al [27] 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. Similar studies are needed for patients undergoing TVH. The strengths of this study include the use of a large, national database that includes a sample of hospitals designed to represent all US community hospitals. The NIS is a yearly database and includes roughly 1000 hospitals with about 7 million discharge records [14]. Nevertheless, one of the weaknesses of the study is that the NIS database does not include outpatient procedures; hence, hysterectomies performed in the outpatient setting were not sampled. However, according to Russo et al [28], only 13.8% of hysterectomy procedures were performed as an outpatient (as opposed to Mikhail et al. Salpingectomy Trends During Vaginal Hysterectomy inpatient) procedure in 2007. We acknowledge that a larger proportion of hysterectomy procedures are likely performed on an outpatient basis nowadays, and a significant proportion of them might be vaginal hysterectomy, which can impact the trends in this study. Despite various organizational efforts to promote the vaginal route for hysterectomy, it is evident in this study that the overall trend for TVH is still declining. However, it is promising to find that the 25.2% annual change during 1998 to 2001 changed to 21.9% between 2001 and 2011. Because of the significant decline in the rate of concomitant BS during TVH, efforts are needed to train gynecologic surgeons on the performance of vaginal salpingectomy if the use of laparoscopic assistance is not considered a good alternative minimally invasive surgical approach to compensate for this training deficiency. Conclusion If the uptake of BS during TVH is lacking behind national trends, laparoscopic assistance might be needed to complete the salpingectomy component. Emphasis on surgical training for vaginal salpingectomy is needed to bridge the gap and to help gynecologic surgeons provide their patients with the proposed added benefit of BS. References 1. Kindelberger DW, 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. 2. Carlson JW, Miron A, Jarboe EA, 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. 3. Dietl J. Revisiting the pathogenesis of ovarian cancer: the central role of the fallopian tube. Arch Gynecol Obstet. 2014;289:241–246. 4. Falconer H, Yin L, Gronberg H, Altman D. Ovarian cancer risk after salpingectomy: a nationwide population-based study. J Natl Cancer Inst. 2015;107. 5. Madsen C, Baandrup L, Dehlendorff C, Kjaer SK. Tubal ligation and salpingectomy and the risk of epithelial ovarian cancer and borderline ovarian tumors: a nationwide case-control study. Acta Obstet Gynecol Scand. 2015;94:86–94. 6. Committee opinion no. 620: salpingectomy for ovarian cancer prevention. Obstet Gynecol. 2015;125:279–281. 7. Mikhail E, Salemi JL, Mogos MF, Hart S, Salihu HM, Imudia AN. National trends of adnexal surgeries at the time of hysterectomy for benign indication, United States, 1998-2011. Am J Obstet Gynecol. 2015;213: 713.e1–713.e13. 8. ACOG Committee Opinion No. 444: choosing the route of hysterectomy for benign disease. Obstet Gynecol. 2009;114:1156–1158. 9. Worldwide AAMIG. AAGL position statement: route of hysterectomy to treat benign uterine disease. J Minim Invasive Gynecol. 2011;18:1–3. 10. Cohen SL, Vitonis AF, Einarsson JI. Updated hysterectomy surveillance and factors associated with minimally invasive hysterectomy. JSLS. 2014;18. 7 11. Moen M, Walter A, Harmanli O, et al. Considerations to improve the evidence-based use of vaginal hysterectomy in benign gynecology. Obstet Gynecol. 2014;124:585–588. 12. HCUP. Agency for Healthcare Research and Quality. Healthcare Cost and Utilization Project (HCUP). 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Am J Obstet Gynecol. 2008;198: 567.e1–567.e4. 19. Burkett D, Horwitz J, Kennedy V, Murphy D, Graziano S, Kenton K. Assessing current trends in resident hysterectomy training. Female Pelvic Med Reconstr Surg. 2011;17: 210–214. 20. Seidman JD, 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. 21. 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. 22. Kurman RJ, Shih IeM. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol. 2010;34: 433–443. 23. Robert M, Cenaiko D, Sepandj J, Iwanicki S. Success and complications of salpingectomy at the time of vaginal hysterectomy. J Minim Invasive Gynecol. 2015;22:864–869. 24. Sheth SS. Adnexectomy for benign pathology at vaginal hysterectomy without laparoscopic assistance. BJOG. 2002;109: 1401–1405. 25. Agostini A, Vejux N, Bretelle F, et al. Value of laparoscopic assistance for vaginal hysterectomy with prophylactic bilateral oophorectomy. Am J Obstet Gynecol. 2006;194:351–354. 26. Findley AD, Siedhoff MT, Hobbs KA, et al. Short-term effects of salpingectomy during laparoscopic hysterectomy on ovarian reserve: a pilot randomized controlled trial. Fertil Steril. 2013;100: 1704–1708. 27. 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. 28. Russo A, Elixhauser A, Steiner C, Wier L. Hospital-based ambulatory surgery, 2007: statistical brief #86. Healthcare Cost and Utilization Project (HCUP) Statistical Briefs. Rockville, MD: Agency for Healthcare Research and Quality; 2006. 7.e1 Journal of Minimally Invasive Gynecology, Vol -, No -, -/- 2016 Appendix 1 List of International Classification of Diseases, Ninth Revision (ICD-9-CM) diagnosis and procedure codes used to identify selected clinical conditions and procedures Condition/procedure ICD-9-CM diagnosis code or ICD-9 procedure code* Hysterectomy procedures Vaginal hysterectomy Total vaginal hysterectomy (TVH) Laparoscopically assisted vaginal hysterectomy (LAVH) Abdominal hysterectomy Diagnoses indicating benign indications Uterine leiomyoma Other benign neoplasm of uterus Carcinoma in situ of cervix uteri Uterine prolapse Hypertrophy of uterus Endometrial hyperplasia Other specified disorders of uterus Cervical dysplasia Dysmenorrhea Menstruation disorders Exclusion criteria (diagnoses) Malignant neoplasm of cervix uteri Malignant neoplasm of placenta Malignant neoplasm of body of uterus Malignant neoplasm of ovary and other uterine adnexa Malignant neoplasm of other/unspecified female genital organs Secondary malignant neoplasm of ovary Benign neoplasm of ovary Polycystic ovaries Salpingitis and oophoritis Pelvic peritoneal adhesions Endometriosis of ovary, fallopian tube Ovarian cyst Congenital anomalies of ovaries, fallopian tubes Exclusion criteria (procedures) Radical abdominal hysterectomy Radical vaginal hysterectomy Pelvic evisceration Delivery or obstetrical operation Procedural outcomes Bilateral salpingectomy Other adnexal procedures (salpingo-oophorectomy, oophorectomy, other salpingectomy) 68.3x, 68.4x, 68.5x 68.5x 68.59 68.51 68.3x, 68.4x 218.0-218.2, 218.9 219.0-219.1, 219.8-219.9 233.1 618.1-618.4, 618.89 621.2 621.31-621.34 621.8 622.11, 622.12 625.3 626.2, 626.4, 626.6, 626.8, 626.9, 627.0 180x 181x 182x 183x 184x 198.6 220 256.4 614.0-614.2 614.6 617.1-617.2 620.0-620.2 752.0-752.1 68.6x 68.7x 68.8 72x, 73x, 74x, 75x 66.51 65.3x, 65.4x, 65.5x, 65.6x, 66.4x, 66.59, 66.6x ICD-9, International Classification of Diseases, Ninth Revision. * The code suffix ‘‘x’’ represents all possible codes that follow the stated code prefix. Unless otherwise specified, codes were available for the entire study period (1998–2011).