Effect of tubal sterilization technique on risk of serous epithelial ovarian and primary peritoneal carcinoma

doi:10.1016/j.ygyno.2014.10.005

Gynecologic Oncology

Volume 135, Issue 3, December 2014, Pages 423-427

https://doi.org/10.1016/j.ygyno.2014.10.005 Get rights and content

Highlights

•
Tubal sterilization reduces the risk of serous epithelial ovarian (EOC) and peritoneal cancer (PPC) by 41%.
•
Excisional tubal sterilization reduces the risk of serous EOC and PPC by 65%.
•
Prospective studies on the impact of salpingectomy on serous EOC and PPC development are needed.

Abstract

Objective

To determine the effect of excisional tubal sterilization on subsequent development of serous epithelial ovarian cancer (EOC) or primary peritoneal cancer (PPC).

Methods

We performed a population-based, nested case–control study using the Rochester Epidemiology Project. We identified all patients with a diagnosis of serous EOC or PPC from 1966 through 2009. Each case was age-matched to 2 controls without either diagnosis. Odds ratios (ORs) and corresponding 95% CIs were estimated from conditional logistic regression models. Models were adjusted for prior hysterectomy, prior salpingo-oophorectomy, oral contraceptive use, endometriosis, infertility, gravidity, and parity.

Results

In total, we identified 194 cases of serous EOC and PPC during the study period and matched them with 388 controls (mean [SD] age, 61.4 [15.2] years). Fourteen cases (7.2%) and 46 controls (11.9%) had undergone tubal sterilization. Adjusted risk of serous EOC or PPC was slightly lower after any tubal sterilization (OR, 0.59 [95% CI, 0.29–1.17]; P = .13). The rate of excisional tubal sterilization was lower in cases than controls (2.6% vs 6.4%). Adjusted risk of serous EOC and PPC was decreased by 64% after excisional tubal sterilization (OR, 0.36 [95% CI, 0.13–1.02]; P = .054) compared with those without sterilization or with nonexcisional tubal sterilization.

Conclusions

We present a population-based investigation of the effects of excisional tubal sterilization on the risk of serous EOC and PPC. Excisional methods may confer greater risk reduction than other sterilization methods.

Introduction

Epithelial ovarian cancer (EOC) will be newly diagnosed in approximately 21,980 women in 2014 and account for 14,270 deaths, making it the most lethal gynecologic cancer in the United States [1]. Serous EOC accounts for approximately 70% to 75% of EOC subtypes and has a high propensity to metastasize beyond the reproductive tract [2], [3]. In a recent report, 67% of ovarian cancers among BRCA1 and BRCA2 mutation carriers were of serous histology [4]. At least 20% of ovarian carcinomas appear to be hereditary [5], and, in high-risk patients, risk-reducing salpingo-oophorectomy (RRSO) is recommended [6]. However, most women with EOC have no identifiable risk factors or precursor lesions [7], and few effective screening tools exist for early diagnosis [7].

Bilateral tubal sterilization has been associated with a decreased risk of sporadic and hereditary EOC [8], [9]. Risk reduction theories have suggested that tubal sterilization decreases ovarian blood supply or interrupts the pathway for environmental carcinogens from the lower genital tract to reach the ovaries [8], [10], [11]. However, the exact mechanism of risk reduction remains unclear, and more recent literature has suggested that the fallopian tube may be a source of serous EOC and primary peritoneal cancer (PPC). Within the BRCA1/2 population, a substantial proportion of clinically occult serous malignancies (2%–17%) have been identified in the fallopian tube during RRSO [12], [13], [14], [15] and histopathologic assessment suggests that the fimbriated portion of the tube is the most common site of origin [16]. In addition, prospective assessment of the “section and extensively examine the fimbriae” (SEE-FIM) protocol has identified up to 75% of pelvic serous carcinomas to have endosalpinx involvement. Over 70% of these cases also have tubal intraepithelial carcinoma (TIC) and more than 90% of TICs are identified in the distal fallopian tubes and involve the fimbriae [17]. Kim and colleagues provided further evidence of the tube as the source of EOC in their Dicer–Pten double knock out (DKO) mouse model. In Dicer–Pten DKO mice that underwent bilateral oophorectomy, with fallopian tubes remaining intact, high grade serous cancers developed. In contrast, among mice that underwent bilateral salpingectomy, with ovaries remaining intact, high grade serous cancers did not develop [2].

Given the increasing evidence indicating the fallopian tube as a primary site of serous EOC carcinogenesis, we sought to determine whether excisional tubal sterilization techniques account for the observed decrease in risk of serous EOC and PPC development among women who have undergone tubal sterilization.

Section snippets

Materials and methods

A population-based, case–control study was designed using the Rochester Epidemiology Project (REP). The REP is a research infrastructure that links the medical records of virtually all persons who have resided in Olmsted County, Minnesota, between January 1, 1966, and the present. As of 2010, the REP contained information on 502,820 persons and their respective medical records from 65 different health care facilities in Olmsted County, including Mayo Clinic, Olmsted Medical Center, and

Demographics and cancer characteristics

During the study period, 194 cases of serous EOC and PPC were diagnosed in women residing in Olmsted County; these cases were matched with 388 controls. Mean (SD) age was 61.4 (15.2) years in both groups (Table 1). Mean body mass index was similar in cases and controls (27.9 [7.0] vs 27.0 [5.8] kg/m²), and most patients were white (83.5% vs 87.6%). The rate of prior breastfeeding was the same for both groups (13.9%), but breastfeeding data were available for less than half the patients. The

Discussion

Existing epidemiologic literature on the effect of reproductive factors on EOC development have described 34% to 67% decreases in risk after tubal sterilization [8], [9], [10], [11], [23], [24], [25]. However, the specific tubal sterilization techniques and their impact on EOC development have not been previously detailed. Given the increasing evidence that a large proportion of serous cancers arise from the distal fallopian tube [26], [27], [28], sterilization procedures that remove a portion

Conflict of interest statement

The authors report no conflict of interest.

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Cited by (91)

Risk of ovarian cancer after salpingectomy and tubal ligation: Prospects on histology and time since the procedure
2023, Gynecologic Oncology
Recent theories propose that most epithelial ovarian cancer (EOC), depending on histological type, originate from other gynecological tissues and involve the ovary secondarily. According to these theories, any protective effect of salpingectomy and tubal ligation may vary by histological type. The study aim was to examine the association between salpingectomy and tubal ligation, respectively, and risk of EOC, with a focus on associations specific for histological types.
We identified EOC cases and matching controls in national registries and gathered information on surgical procedures and potential confounders. Conditional logistic regression was used to estimate odds ratio (OR) with 95% confidence interval (CI) of EOC related to salpingectomy and tubal ligation, respectively, overall and stratified by histological type. Furthermore, we investigated the association according to timing of the procedures.
Our study comprised 16,822 EOC cases. Each case was matched with 40 controls. There was an overall EOC risk reduction after unilateral (OR = 0.73; 95% CI: 0.60–0.87) and bilateral salpingectomy (OR = 0.46; 95% CI: 0.31–0.67). A slight risk reduction was seen among women with previous tubal ligation (OR = 0.91; 95% CI: 0.83–0.99). For salpingectomy, the risk reduction increased with increasing time since the surgical procedure and was only present among women younger than 50 years at salpingectomy. Unilateral and bilateral salpingectomy was associated with a risk reduction for most histological types.
The association between previous salpingectomy and reduced risk of several histological subtypes of EOC supports the suggested theories about the site of origin of EOC and may be of clinical importance.
Racial and ethnic differences in the adoption of opportunistic salpingectomy for ovarian cancer prevention in the United States
2022, American Journal of Obstetrics and Gynecology
Clinicians in the United States have rapidly adopted opportunistic salpingectomy for ovarian cancer prevention. However, little is known about racial and ethnic differences in opportunistic salpingectomy adoption. Surgical innovations in gynecology may be adopted differentially across racial and ethnic groups, exacerbating current disparities in quality of care.
This study aimed to evaluate racial and ethnic differences in opportunistic salpingectomy adoption across inpatient and outpatient settings and assess the effect of national guidelines supporting opportunistic salpingectomy use on these differences.
A sample of 650,905 women aged 18 to 50 years undergoing hysterectomy with ovarian conservation or surgical sterilization from 2011 to 2018 was identified using the Premier Healthcare Database, an all-payer hospital administrative database, including more than 700 hospitals across the United States. The association between race and ethnicity and opportunistic salpingectomy use was examined using multivariable-adjusted mixed-effects log-binomial regression models accounting for hospital-level clustering. Models included race and ethnicity by year of surgery (2011–2013 [before guideline] and 2014–2018 [after guideline]) interaction term to test whether racial and ethnic differences in opportunistic salpingectomy adoption changed with the release of national guidelines supporting opportunistic salpingectomy use.
From 2011 to 2018, 82,792 women underwent hysterectomy and opportunistic salpingectomy (non-Hispanic White, 60.3%; non-Hispanic Black, 18.8%; Hispanic, 12.2%; non-Hispanic other race, 8.7%) and 23,398 women underwent opportunistic salpingectomy for sterilization (non-Hispanic White, 64.7%; non-Hispanic Black, 10.8%; Hispanic, 16.7%; non-Hispanic other race, 7.8%). The proportion of hysterectomy procedures involving an opportunistic salpingectomy increased from 6.3% in 2011 to 59.7% in 2018 (9.5-fold increase), and the proportion of sterilization procedures involving an opportunistic salpingectomy increased from 0.7% in 2011 to 19.4% in 2018 (27.7-fold increase). In multivariable-adjusted models, non-Hispanic Black (risk ratio, 0.94; 95% confidence interval, 0.92–0.97), Hispanic (risk ratio, 0.98; 95% confidence interval, 0.95–1.00), and non-Hispanic other race women (risk ratio, 0.93; 95% confidence interval, 0.90–0.96) were less likely to undergo hysterectomy and opportunistic salpingectomy than non-Hispanic White women. A significant interaction between race and ethnicity and year of surgery was noted in non-Hispanic Black compared with non-Hispanic White women (P<.001), with a reduction in differences in hysterectomy and opportunistic salpingectomy use after national guideline release (risk ratio_2011–2013, 0.80 [95% confidence interval, 0.73–0.88]; risk ratio_2014–2018, 0.98 [95% confidence interval, 0.95–1.01]). Moreover, non-Hispanic Black women were less likely to undergo an opportunistic salpingectomy for sterilization than non-Hispanic White women (risk ratio, 0.91; 95% confidence interval, 0.88–0.95), with no difference by year of surgery (P=.62). Stratified analyses by hysterectomy route and age at surgery revealed similar results.
Although opportunistic salpingectomy for ovarian cancer prevention has been rapidly adopted in the United States, our findings suggested that its adoption has not been equitable across racial and ethnic groups. Non-Hispanic Black, Hispanic, and non-Hispanic other race women were less likely to undergo opportunistic salpingectomy than non-Hispanic White women even after adjusting for sociodemographic, clinical, procedural, hospital, and provider characteristics. These differences persisted after the release of national guidelines supporting opportunistic salpingectomy use. Future research should focus on understanding the reasons for these differences to inform interventions that promote equity in opportunistic salpingectomy use.
Female permanent contraception trends and updates
2022, American Journal of Obstetrics and Gynecology
Permanent contraception remains one of the most popular methods of contraception worldwide. This article has reviewed recent literature related to demographic characteristics of users, prevalence of use and trends over time, surgical techniques, and barriers to obtain the procedure. We have emphasized the patient’s perspective as a key element of choosing permanent contraception. This review has incorporated sections on salpingectomy, hysteroscopy, unmet need, impact of policies at religiously affiliated institutions, and reproductive coercion.
Reply to a question regarding ovarian cancer prevention with partial salpingectomy vs complete
2021, American Journal of Obstetrics and Gynecology
Paradigm shift from tubal ligation to opportunistic salpingectomy at cesarean delivery in the United States
2021, American Journal of Obstetrics and Gynecology
Citation Excerpt :
Because data over the past 2 decades have continued to support the tubal hypothesis implicating the distal fallopian tube in the pathogenesis of high-grade serous epithelial ovarian cancer, opportunistic salpingectomy has emerged as a potential means to reduce the risk of ovarian cancer.1,2 In retrospective studies, bilateral salpingectomy is associated with a 42% to 65% reduction in ovarian cancer risk.3–7 Opportunistic salpingectomy has subsequently been widely adopted at the time of routine gynecologic surgery, such that performance of opportunistic salpingectomy at benign hysterectomy increased more than 10-fold over the past 2 decades to nearly 60% in 2015.8,9
Opportunistic salpingectomy is now recommended at the time of routine gynecologic surgery to reduce the risk of future ovarian cancer, and performance of opportunistic salpingectomy has increased markedly at the time of benign hysterectomy. Salpingectomy has also been suggested to be feasible at the time of cesarean delivery in women desiring sterilization; however, uptake has not been previously studied on a national level.
This study aimed to examine recent population trends in the utilization and characteristics of salpingectomy at the time of cesarean delivery in the United States.
This is a population-based retrospective observational study querying the National Inpatient Sample between October 2015 and December 2018. The primary outcome measure was the temporal trend of bilateral salpingectomy at cesarean delivery, assessed with linear segmented regression with log transformation utilizing 3-month time increments. The secondary outcome measures included patient characteristics associated with bilateral salpingectomy, assessed with a multinomial regression model, and surgical outcome (hemorrhage, blood transfusion, hysterectomy, and oophorectomy) at the time of bilateral salpingectomy vs bilateral tubal ligation, assessed with generalized estimating equation in a propensity score-matched model.
There were 3,813,823 women at the age of 15 to 49 years who had cesarean deliveries included, of whom 397,260 (10.4%) had bilateral salpingectomy and 203,400 (5.3%) had bilateral tubal ligation overall. During the time period studied, performance of bilateral salpingectomy among women undergoing cesarean delivery significantly increased from 4.6% to 13.2% (odds ratio for the fourth quarter of 2018 vs the fourth quarter of 2015, 2.69; 95% confidence interval, 2.63–2.75; Figure panel). In contrast, performance of bilateral tubal ligation among women undergoing cesarean delivery significantly decreased from 11.3% to 2.4% (odds ratio, 0.20; 95% confidence interval, 0.19–0.21). By the third quarter of 2016, the number of women who had bilateral salpingectomy exceeded those who had bilateral tubal ligation at cesarean delivery (8.6% vs 7.3%). Increasing the utilization of bilateral salpingectomy did not vary across age groups; the salpingectomy rate increased from 7.5% to 21.1% among women at the age of ≥35 years and from 3.8% to 10.7% among women at the age of <35 years (both, P<.001). In a propensity score matched model, women in the bilateral salpingectomy group were more likely to have hemorrhage (3.8% vs 3.1%; odds ratio, 1.24; 95% confidence interval, 1.15–1.33), blood product transfusion (2.1% vs 1.8%; odds ratio, 1.16; 95% confidence interval, 1.04–1.30), hysterectomy (0.8% vs 0.4%; odds ratio, 2.28; 95% confidence interval, 1.84–2.82), and oophorectomy (0.3% vs 0.2%; odds ratio, 2.02; 95% confidence interval, 1.47–2.79) than those in the bilateral tubal ligation group. When restricted to the nonhysterectomy cases, the bilateral salpingectomy group had a higher rate of hemorrhage (3.4% vs 3.0%; odds ratio, 1.16; 95% confidence interval, 1.06–1.26) and oophorectomy (0.3% vs 0.1%; odds ratio, 1.75; 95% confidence interval, 1.22–2.50) than the bilateral tubal ligation group.
In the United States, the utilization of bilateral salpingectomy at the time of cesarean delivery increased rapidly between 2015 and 2018, replacing tubal ligation as the most common type of sterilization performed with cesarean delivery. The higher surgical morbidity in the bilateral salpingectomy group than the bilateral tubal ligation group observed in this study warrants further investigation.
Frequency and characteristics associated with opportunistic salpingectomy at cesarean delivery: A retrospective chart review
2021, Contraception
To identify the frequency and characteristics associated with total salpingectomy (TS) versus occlusion or partial salpingectomy (PS) at the time of cesarean delivery.
We performed a retrospective chart review of cesarean deliveries with a concurrent permanent contraception procedure, from July 1, 2014 to June 30, 2019 at 2 hospitals (community hospital and tertiary care academic center) within a single healthcare system. We assessed the proportion of TS versus PS at cesarean, and secondarily compared operative times between the 2 procedures.
We identified 2110 procedures during the 5-year period. Surgeons performed TS in 302 (14%, 95% confidence interval [CI] 13%–16%) cases, and the annual rate varied from 14% to 18% over the study period (p = 0.14). Factors associated with increased likelihood of TS rather than PS included public insurance/self-pay (adjusted odds ratio, aOR 2.8, 95% CI 2.0–4.1), delivery at the community hospital (aOR 4.8, 95% CI 3.0–7.7), parity of 5 or more (aOR 2.2, 95% CI 1.1–4.4), and presence of an obstetrician/gynecologist for cesarean delivery (aOR 2.9, 95% CI 1.6–5.4). The total operative time for TS and PS differed at the academic center (90 vs 68 minutes, p < 0.001) but not at the community hospital (55 vs 54 minutes, p = 0.5).
This study highlights provider and institutional characteristics associated with TS compared to PS at the time of cesarean delivery, which may inform future programs aimed at increasing utilization of TS at cesarean delivery.
Access to TS at the time of cesarean delivery may provide pregnant women with a very effective permanent contraception method at a convenient time of concurrent cesarean. This study identifies patient factors that may influence access to TS as part of obstetrical care.

View all citing articles on Scopus

^☆: Presented at the 2013 Society of Gynecologic Oncology Annual Meeting on Women's Cancer, Los Angeles, California, March 9–12, 2013.

^☆☆: The Rochester Epidemiology Project (REP) is supported by the National Institute on Aging of the National Institutes of Health under award number R01AG034676. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. This work was also supported in part by the Office of Women's Health Research Building Interdisciplinary Careers in Women's Health (BIRCWH award K12 HD065987). The funding sources played no role in the design, conduct, or reporting of this study.

¹: Present address: Altru Health System, Department of Obstetrics & Gynecology, 1000 South Columbia Road, Grand Forks, ND 58201, United States.

View full text

Effect of tubal sterilization technique on risk of serous epithelial ovarian and primary peritoneal carcinoma☆,☆☆

Highlights

Abstract

Objective

Methods

Results

Conclusions

Introduction

Section snippets

Materials and methods

Demographics and cancer characteristics

Discussion

Conflict of interest statement

Gynecol Oncol

Fertil Steril

Gynecol Oncol

Ann Epidemiol

Mol Oncol

Mod Pathol

Gynecol Oncol

Cancer statistics, 2014

CA Cancer J Clin

High-grade serous ovarian cancer arises from fallopian tube in a mouse model

Proc Natl Acad Sci U S A

Lessons from BRCA: the tubal fimbria emerges as an origin for pelvic serous cancer

Clin Med Res

Pathology of breast and ovarian cancers among BRCA1 and BRCA2 mutation carriers: results from the Consortium of Investigators of Modifiers of BRCA1/2 (CIMBA)

Cancer Epidemiol Biomarkers Prev

Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality

JAMA

Management updates for women with a BRCA1 or BRCA2 mutation

Mol Diagn Ther

Association of oral contraceptive use, other contraceptive methods, and infertility with ovarian cancer risk

Am J Epidemiol

Reproductive and hormonal factors, and ovarian cancer risk for BRCA1 and BRCA2 mutation carriers: results from the International BRCA1/2 Carrier Cohort Study

Cancer Epidemiol Biomarkers Prev

Underlying mechanisms of ovarian cancer risk reduction after tubal ligation

Acta Obstet Gynecol Scand

Epidemiological and molecular aspects of ovarian cancer risk

J Cancer Res Clin Oncol

Occult carcinoma in prophylactic oophorectomy specimens: prevalence and association with BRCA germline mutation status

Am J Surg Pathol