Risk-Reducing Salpingectomy with Benign Hysterectomy and Permanent Sterilization: A Survey of Obstetrician

Abstract

Objective: The goal of this research was to determine the willingness among obstetrician–gynecologists to offer risk-reducing salpingectomy at the time of benign hysterectomy or permanent sterilization. Materials and Methods: A voluntary and anonymous survey survey was administered to obstetrician–gynecologists at an urban academic and affiliated community hospital in 2012. The survey assessed provider demographics and knowledge about ovarian cancer prevention. Providers were then given a brief summary of the emerging data that ovarian cancer may emerge from Fallopian tubes and were surveyed on willingness to offer risk-reducing salpingectomy at the time of hysterectomy or permanent sterilization to patients who would otherwise undergo ovarian conservation. Results: Ninety-one providers completed the survey (75% response rate). Significantly more physicians were willing to offer risk-reducing salpingectomy at the time of hysterectomy rather than at the time of permanent sterilization (96% versus 56%, p<0.05). Willingness to offer salpingectomy at the time of permanent sterilization was associated with younger provider age and greater provider surgical experience. Conclusions: Obstetrician–gynecologists will offer risk-reducing salpingectomy at the time of benign hysterectomy in women who elect ovarian conservation. However, providers are less willing to offer risk-reducing salpingectomy at the time of permanent sterilization and the physician's age and level of surgical experience affects the likelihood of recommending this intervention. (J GYNECOL SURG 30:285)

Introduction

One in 70 women will develop ovarian cancer, and the majority of cases are diagnosed at an advanced stage.¹ The recently reported Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial evaluated annual screening in the general asymptomatic population of women ages 55–74 and found that there was no reduction in mortality from ovarian cancer with annual screening, compared to usual care.² As high-grade serous cancers are rarely confined to the ovary at the time of diagnosis and effective screening modalities do not exist, there is a great deal of interest in the prevention and identification of precursor lesions.

Until recently, the prevailing theory regarding the origin of ovarian serous tumors has been that they arise from the ovarian surface epithelium and epithelial inclusions within the cortex. However, pathologic examination of the ovaries and Fallopian tubes of women with BRCA mutations who are undergoing risk-reducing salpingo-oophorectomy has challenged this theory and suggests the Fallopian tubes as the sites of origin for many ovarian, Fallopian-tube, and primary-peritoneal carcinomas.³ Approximately 10% of patients with the BRCA mutation have malignant or premalignant lesions at the time of risk-reducing salpingo-oophorectomy, and the majority of these lesions are located in the Fallopian tubes.^4–7 This theory has since been investigated beyond the BRCA population, and the Fallopian tube origin may also hold true for cases of sporadic ovarian cancer in the general population.^4,5,8 In addition, tubal ligation has been associated with a reduction in the risk of ovarian cancer in the general population^9–11 and in the population with the BRCA1 mutation,¹² which may support a tubal origin of disease further.

As attempts to demonstrate effective screening for ovarian cancer have so far been largely unsuccessful, disease prevention through surgical intervention is an exciting prospect. Approximately 600,000 women undergo hysterectomy annually in the United States, and the majority of procedures are performed for benign indications by general obstetrician–gynecologists.¹³ In most premenopausal women, the ovaries are conserved for hormone production and the Fallopian tubes are left in situ. It has been estimated that between 4% and 14% of women who developed ovarian cancer underwent a prior hysterectomy. This implies that routine bilateral salpingo-oophorectomy at the time of hysterectomy could prevent more than 1000 cases of ovarian cancer annually.¹⁴ However, there is evidence suggesting that oophorectomy increases a woman's risk for coronary artery disease and osteoporosis, and that the protective effect of having ovaries might continue even after menopause because of androgen production.¹⁵ While 14,000 women die each year from ovarian cancer, nearly 490,000 women die from heart disease and 48,000 women die within 1 year after hip fracture. Based on this data, mathematical modeling of a hypothetical cohort of perimenopausal women undergoing hysterectomy predicts that by the time women reach age 80, 47 fewer women will have died from ovarian cancer, but 838 more women will have died from coronary artery disease and 158 more will have died from hip fracture complications.^15–20 Many physicians are now counseling perimenopausal and even postmenopausal patients for ovarian conservation at the time of hysterectomy.

On September 15, 2011, the Society of Gynecologic Oncology of Canada (GOC) issued the following statement on salpingectomy and ovarian cancer prevention:

1. Due to its cancer prevention potential, it is recommended that physicians discuss the risks and benefits of bilateral salpingectomy with patients undergoing hysterectomy or requesting permanent, irreversible contraception.

2. Given that the total benefits and risks of this practice change have not been defined, a national ovarian cancer prevention study focused on fallopian tube removal is a GOC priority.²¹

In November of 2013 the Society of Gynecologic Oncology (SGO) released a clinical practice statement entitled “Salpingectomy for Ovarian Cancer Prevention” supporting that salpingectomy may be an appropriate and feasible strategy for ovarian cancer–risk reduction. Specifically, the statement recommended that, for women at an average risk of ovarian cancer, risk-reducing salpingectomy should be discussed and considered at the time of abdominal or pelvic surgery, hysterectomy, or in lieu of tubal ligation.²² However, the acceptability of offering this procedure to patients among obstetrician–gynecologists in the United States remains unclear. The objective of the current study was to evaluate the willingness among obstetrician–gynecologists to offer risk-reducing salpingectomy at the time of benign hysterectomy or surgical sterilization.

Materials and Methods

Attending physicians and residents in the department of obstetrics and gynecology at an urban academic institution and the affiliated community hospital were surveyed from January 2012 through March 2012. Surveys were mailed to the offices of the attending physicians and distributed to residents during a residency-program meeting. Participation was voluntary and anonymous, and no incentive was offered. Institutional review board approval was obtained prior to initiating this study.

The survey instrument was used to obtain physician demographics and practice patterns, such as age, years in practice, surgical volume, type of surgeries performed annually (minimally invasive versus abdominal versus vaginal) and patient population. Physician awareness of the current data regarding ovarian cancer and Fallopian-tube cancer was assessed. The following brief summary of the existing literature on this topic was provided:

• Pathologic examination of Fallopian tubes and ovaries from BRCA-positive patients undergoing prophylactic bilateral salpingo-oophorectomy (BSO) has shown that 10% of these patients will have a malignant or premalignant lesion at the time of surgery.^4–7

• The majority of lesions found on BRCA-positive patients undergoing prophylactic BSO are found in the fimbriated end of the Fallopian tube rather than in the ovary.^4–7

• Fallopian tubes have been identified as the sites of primary serous carcinomas in the general population (non-BRCA mutation carriers) as well.^4,5,8

• Fallopian-tube epithelial cells can transform into pathologically/immune-phenotypically high-grade serous carcinomas.²³

After reading the review, physicians were queried about their willingness to offer salpingectomy at the time of benign hysterectomy or surgical sterilization. The questions were dichotomous and completed on a printed form. Electronic questionnaires were not utilized.

Data analysis was performed using IBM SPSS Statistics 19.0.0 (Armonk, NY). Pearson's χ² test of independence or Fisher's exact test was used to compare proportions as appropriate. A Kolmogorov–Smirnov test was used to evaluate outcome variable distributions for normality. Normally distributed outcome variables were analyzed with an independent sample t-test and a one-way analysis of variance, while non–normally distributed outcome variables were analyzed with Kruskal-Wallis H and Mann-Whitney U tests as appropriate. The Type I error threshold was set at a p-value of <0 .05 for all tests.

Results

The surveys were distributed to 122 attending physicians and residents. Ninety-one surveys were completed and returned (a 75% response rate). Seventy-nine percent of respondents were attending obstetrician–gynecologists, 16% were residents, and 9% did not provide informations on their positions. Sixty-eight percent of the participating attending physicians were employed at academic hospitals and 24% at affiliated community hospitals. Twenty-three percent of physicians had <5 years in practice, 16% had 5–10 years, 21% had 11–20 years, and 40% had >20 years.

Among respondents, laparotomy was the most common approach for hysterectomy (53% abdominal, 21% laparoscopic or robotic-assisted, and 8% vaginal). Fifty-four percent of physicians performed <5 hysterectomies annually and 19% performed >20 hysterectomies annually. Fifty-two percent of physicians performed <5 permanent sterilizations annually and 7% performed >20 permanent sterilizations annually. Laparoscopic bilateral tubal ligation was the most common method of permanent sterilization (43% laparoscopic bilateral tubal ligation, 25% postpartum tubal ligation, and 21% hysteroscopically placed permanent birth control). See Table 1.

Table 1.

Physician Demographics

Parameter	N^a	%
Physician age
20–29 years	13	14
30–39 years	21	23
40–49 years	21	23
50–59 years	19	21
≥60 years	13	14
No answer	4	4
Physician gender
Male	35	38
Female	48	53
No answer	8	9
Physician race
African American	4	4
Asian	17	19
Caucasian	51	56
Hispanic	2	2
Other	7	8
No answer	10	11
Physician position
Attending	72	79
Resident	15	16
No answer	4	4
Physician years in practice
<5 years	21	23
5–10 years	15	16
11–20 years	19	21
>20 years	36	40
No answer	0	0
Practice type
Primary gynecology	23	25
Primary obstetrics	13	14
Mixed gynecology & obstetrics	47	52
No answer	8	9
Hospital affiliation
Academic hospital	62	68
Community hospital	22	24
No answer	7	8
Predominant patient age
21–39 years	47	52
40–49 years	18	20
50–59 years	3	3
>60 years	10	11
No answer	13	14
# of hysterectomies performed annually
<5 hysterectomies	49	54
5–10 hysterectomies	15	16
11–20 hysterectomies	5	5
>20 hysterectomies	17	19
No answer	5	5
Method of hysterectomy
Abdominal	48	53
Laparoscopic/robotic	19	21
Vaginal	7	8
No answer	17	19
# of permanent sterilizations performed annually
<5 sterilizations	47	52
5–10 sterilizations	22	24
11–20 sterilizations	13	14
>20 sterilizations	6	7
No answer	3	3
Method of sterilization
Hysteroscopically placed permanent birth control	19	21
Laparoscopic bilateral tubal ligation	39	43
Postpartum tubal ligation	23	25
No answer	10	11

N=91 respondents.

Among the physicians surveyed, 70% reported already being aware of the literature suggesting that ovarian cancer may arise in the Fallopian tube. None of the physicians routinely offered bilateral salpingectomy to patients who elected ovarian conservation at the time of hysterectomy. Seventy percent of physicians routinely recommended BSO to postmenopausal women undergoing benign hysterectomy. Far fewer physicians recommended BSO for premenopausal and perimenopausal women (ages 30–35, 1%; ages 36–40, 10%; ages 41–45, 3%; ages 46–50, 30%; ages 50–55, 68%). However, after respondents were provided with a summary of the available data supporting the Fallopian tube as a possible site of origin of serous ovarian cancer, 96% of physicians reported that they would offer patients undergoing hysterectomy for benign indications a risk-reducing salpingectomy. Willingness to offer salpingectomy at the time of hysterectomy was not significantly associated with physician age, type of practice, surgical volume, or method of hysterectomy (Table 2).

Table 2.

Physician Willingness to Offer Risk-Reducing Salpingectomy at the Time of Benign Hysterectomy

	Not willing to offer (N^a=4)		Willing to offer (N=87)
Factor	N	%	N	%	p-Value
Physician age
20–29 years	0	0	13	100	0.07
30–39 years	0	0	21	100
40–49 years	0	0	21	100
50–59 years	1	5	18	95
≥60 years	2	15	11	85
No answer	1	25	3	75
Physician gender
Male	2	6	33	94	0.01
Female	0	0	48	100
No answer	2	25	6	75
Attending vs. resident
Attending	3	4	69	96	0.09
Resident	0	0	15	100
No answer	1	25	3	75
Years in practice
<10 years	0	0	36	100	0.13
≥10 years	4	7	51	93
No answer	0	0	0	0
Practice type
Primary gynecology	2	9	21	91	0.33
Primary obstetrics	0	0	13	100
Mixed gynecology & obstetrics	1	2	46	98
No answer	1	12	7	88
Academic vs. community hospital
Academic hospital	1	2	61	98	0.14
Community hospital	2	9	20	91
No answer	1	14	6	86
# of hysterectomies performed annually
≤10	2	3	62	97	0.75
>10	1	5	21	95
No answer	1	20	4	80
Method of hysterectomy
Abdominal	3	6	45	94	0.76
Laparoscopic/robotic	0	0	19	100
Vaginal	0	0	7	100
No answer	1	6	16	94

N=91 respondents.

Significantly more physicians were willing to offer risk-reducing salpingectomy at the time of hysterectomy than at the time of permanent sterilization (96% versus 56%, p<0.05). Willingness to offer salpingectomy at the time of permanent sterilization was associated with younger provider age (92% in ages 20–29, 52% in ages 30–39, 43% in ages 40–49, 67% in ages 50–59, and 31% in ages >60; p=0.01). Resident physicians were significantly more likely to offer risk-reducing salpingectomy than were attending physicians (93% residents versus 48% attending physicians, p<0.005). Greater provider surgical experience was associated with increased likelihood of offering salpingectomy at the time of sterilization (43% of providers performing <10 hysterectomies per year versus 86% of physicians performing >10 hysterectomies, p<0.001). The number of surgical sterilizations performed annually and the method of sterilization utilized were not associated with willingness to offer risk-reducing salpingectomy at the time of surgical sterilization (Table 3).

Table 3.

Physician Willingness to Offer Risk-Reducing Salpingectomy at the Time of Permanent Sterilization

	Not willing to offer (n=40)		Willing to offer (n=50)
Factor	N	%	N	%	p-Value
Physician age
20–29 years	1	8	12	92	0.03
30–39 years	10	48	11	52
40–49 years	12	57	9	43
50–59 years	6	33	12	67
≥60 years	9	69	4	31
No answer	2	50	2	50
Physician gender
Male	15	44	19	56	0.95
Female	21	44	27	56
No answer	4	50	4	50
Attending vs. resident
Attending	37	52	34	48	0.005
Resident	1	7	14	93
No answer	2	50	2	50
Years in practice
<10 years	12	33	24	67	0.06
≥10 years	28	52	26	48
No answer	0	0	0	0
Practice type
Primary gynecology	10	43	13	57	0.43
Primary obstetrics	8	62	5	38
Mixed gynecology & obstetrics	20	43	26	57
No answer	2	25	6	75
Academic vs. community hospital
Academic hospital	25	41	36	59	0.6
Community hospital	11	50	11	50
No answer	4	57	3	43
# of hysterectomies performed annually
≤10	36	57	27	43	<0.001
>10	3	14	19	86
No answer	1	20	4	80
# of permanent sterilizations performed annually
<5 sterilizations	26	55	21	45	0.24
5–10 sterilizations	8	36	14	64
11–20 sterilizations	4	33	8	67
>20 sterilizations	1	17	5	83
No answer	1	33	2	67
Method of permanent sterilization
Hysteroscopically placed permanent birth control	6	33	12	67	0.65
Laparoscopic tubal ligation	19	49	20	51
Postpartum tubal ligation	10	43	13	57
No answer	5	50	5	50

N=90 respondents; 1 respondent did not respond to this question.

Discussion

This study evaluated the willingness among obstetrician–gynecologists to change their practice patterns and offer risk-reducing salpingectomy at the time of benign hysterectomy or permanent sterilization. Among the physicians surveyed, 70% recommended BSO to postmenopausal women undergoing benign hysterectomy, and as expected, far fewer obstetrician–gynecologists recommended BSO for premenopausal women. However, after reading literature on risk-reducing salpingectomy, most obstetrician–gynecologists reported that they would offer patients a risk-reducing salpingectomy with a benign hysterectomy. The mode of surgery (laparotomy versus minimally invasive surgery), the length of time the physician has been in practice, and surgical volume did not affect this decision.

The obstetrician–gynecologists in the current study were less willing to perform risk-reducing salpingectomy at the time of permanent sterilization. The current authors hypothesized that this might be related to the type of permanent sterilization most commonly performed by the physicians, as salpingectomy cannot be performed with hysteroscopically placed permanent birth control and might be technically difficult at the time of postpartum tubal procedures. However, willingness to offer salpingectomy at the time of surgical sterilization was not associated with the method of sterilization favored by the physician. Willingness to offer salpingectomy at the time of permanent sterilization was, however, associated with younger provider age and greater provider surgical experience. This finding may be explained by the fact that surgeons who perform a larger volume of hysterectomies are more comfortable operating on the adnexa and, therefore, are more willing to offer salpingectomy, a procedure that can be technically more difficult than tubal ligation and hysteroscopically placed permanent birth control.

The study was comprised of physicians in a single geographic region, making the results potentially difficult to generalize. Future studies should be conducted to explore possible answers to this question among larger groups from many institutions throughout the United States. Another important limitation of this study was that the intervention focused on—risk-reducing salpingectomy—has yet to be evaluated in a prospective manner, and its role in ovarian cancer prevention remains theoretical. Furthermore, there are no available data on the potential adverse outcomes associated with including bilateral salpingectomy during a hysterectomy or permanent sterilization procedure. There is some evidence that bilateral tubal ligation is associated with surgical menopause and early natural menopause²⁴ and whether or not this is also true for salpingectomy remains unclear. The low volume of surgical procedures reported by the surveyed physicians (54% performed <5 hysterectomies annually and 52% performed <5 permanent sterilizations annually) represents another limitation which may limit the extrapolation of this study's results to the general population of obstetrician–gynecologists.

Conclusions

The data from the current study suggest that obstetrician–gynecologists will offer risk-reducing salpingectomy at the time of benign hysterectomy in women who elect ovarian conservation. However, providers are less willing to offer risk-reducing salpingectomy at the time of permanent sterilization, and physician age and level of surgical experience affects the likelihood of recommending this intervention. If the Fallopian tube is the precursor site for ovarian cancer, patients will have the option to reduce their risk of ovarian cancer while maintaining the protective effects of ovarian function with salpingectomy at the time of hysterectomy. The strength of the emerging data regarding the origin of ovarian cancer and the clinical practice statement put forth by the SGO indicates that the current surgical conventional protocol should be reconsidered and bilateral salpingectomy should be discussed with patients at the time of hysterectomy or permanent sterilization. Additional studies are necessary to investigate this topic further, including a case-control study to evaluate potential adverse effects of salpingectomy and a randomized controlled trial to determine if salpingectomy alters the incidence of ovarian cancer.

Footnotes

Acknowledgments

This project was supported by the Foundation for Women's Wellness—Women's Health Fellowship Award 2013.

Disclosure Statement

The authors report no conflicts of interest.

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Risk-Reducing Salpingectomy with Benign Hysterectomy and Permanent Sterilization: A Survey of Obstetrician–Gynecologists

Abstract

Abstract

Introduction

Materials and Methods

Results

Discussion

Conclusions

Footnotes

Acknowledgments

Disclosure Statement

References