Once considered an innocent bystander, the fallopian tube is now thought to play an important role in development of one of the most deadly gynecologic cancers. Several studies evaluating risk-reducing salpingo-oophorectomy specimens in women who are BRCA gene mutation carriers implicate the fallopian tube as the most common site of occult carcinomas. Serous tubal intraepithelial carcinomas (STIC), which representative preinvasive fallopian tube pathology, are also identified in these patients, and believed to be a part of the pathway of malignant transformation that results in high-grade serous carcinomas (HGSCs).1-3 Gene expression and molecular profiling studies demonstrate that ovarian HGSCs more closely resemble fallopian tube epithelium than ovarian surface epithelium.4-6 TP53 mutations are extremely common in both STIC lesions and ovarian HGSCs, and more importantly, the particular mutations in these 2 lesions have been shown to be identical.7
While much of the evidence supporting the fallopian tube as the origin of HGSC is derived from high-risk patients, several studies demonstrate that this is also the case for the remainder of the population at baseline risk, including some research that shows a decreased risk of ovarian cancer in women who have undergone tubal ligation.8-11
Patients with germline BRCA mutations are particularly predisposed to ovarian cancer. However, 85%–90% of ovarian HGSCs arise in patients without a currently identified genetic susceptibility.12 Nearly 70% of those cancers are thought to arise from the fallopian tube, implying a potential role for salpingectomy as a means for ovarian cancer risk reduction in the general population.4,12 While it remains to be determined whether the risks outweigh the benefits of performing a bilateral salpingectomy as a stand-alone procedure in an average-risk patient, bilateral salpingectomy certainly should be considered in patients who are already undergoing hysterectomy for other indications. The operative safety of salpingectomy in this setting has been demonstrated in a large retrospective cohort study of more than 40,000 women.13
Hysterectomy remains one of the most common surgical procedures, with approximately 600,000 of these surgeries performed annually in the United States. Approximately 90% of hysterectomies are performed for benign indications, the most common of which are related to symptoms of uterine leiomyomas.14,15 In the general population, the lifetime risk of ovarian cancer is approximately 1 in 70 women and approximately 22,000 women are diagnosed annually in the United States.16
Bilateral oophorectomy, when performed concurrently with hysterectomy for benign disease, has been demonstrated to increase risk of all-cause mortality and coronary artery disease. Parker and colleagues’ report that estrogen replacement therapy in the setting of oophorectomy may mitigate these negative long-term effects was an observational study which limits our understanding of the reasons behind estrogen use or non-use in some patients. Moreover, concerns remain about patient compliance with hormone therapy.17,18
The potential long-term risks of oophorectomy, in conjunction with data supporting the fallopian tube as a precursor lesion of HGSC, may make bilateral salpingectomy at the time of a hysterectomy with ovarian preservation a procedure with a more optimized risk-benefit ratio.
While the safety of risk-reducing salpingectomy at the time of hysterectomy has been demonstrated in retrospective studies,19,20 one frequently raised concern is the potential decline in ovarian function after salpingectomy. A retrospective study and a randomized controlled trial (RCT) both have demonstrated preservation of normal ovarian function after salpingectomy at the time of hysterectomy, as measured by surrogate markers of ovarian function, such as serum anti-mullerian hormone (AMH), follicle-stimulating hormone (FSH), and estradiol levels.9,21,22 However, the long-term effects on ovarian function are less well described in the literature.
In January 2015, the American College of Obstetricians and Gynecologists (ACOG) published a Committee Opinion that underscores the potential benefits of salpingectomy at the time of hysterectomy in patients who are not undergoing oophorectomy. ACOG also states that bilateral salpingectomy can be considered as a method of sterilization in patients seeking permanent contraception, but that RCTs are needed to evaluate bilateral salpingectomy as an approach to decreasing risk of ovarian cancer.23
Similar recommendations have been published by our European colleagues, such as the AGO’s Kommission OVAR, which recommends preoperative counseling about opportunistic salpingectomy at the time of hysterectomy, including the potential risks and benefits.24 Like ACOG, AGO reports a lack of sufficient evidence to justify a universal recommendation for opportunistic salpingectomy. The Society of Gynecologic Oncology (SGO) put forth a Clinical Practice Statement in November 2013 stating that, for women at average risk of ovarian cancer, salpingectomy should be considered at the time of hysterectomy or at the time of other pelvic surgery.25 SGO reaffirmed this recommendation in a 2015 publication.26
In light of these data, many providers and institutions are now offering patients opportunistic salpingectomies at the time of hysterectomy. Here we suggest techniques for bilateral salpingectomy at the time of hysterectomy, including abdominal, laparoscopic, and vaginal approaches.
In general, we recommend that salpingectomy at the time of abdominal hysterectomy be performed prior to hysterectomy because it allows for complete removal of the entire fallopian tube without the need to re-isolate any surgical pedicle. The ampullary portion of the fallopian tube is grasped with a Babcock clamp and elevated.
Fenestrations should be made within the mesosalpinx, isolating the small vessels that lie between the ovary and fallopian tube. These vessels are branches of the ovarian and uterine arteries and may provide additional blood supply to the ovaries. Small clamps, such as Kelly or tonsil clamps, are placed across these vessels, favoring the tubal side of the mesosalpinx, in order to preserve as much ovarian blood supply as possible. Each pedicle is then transected and ligated.
Alternatively, a monopolar electrosurgery device with coagulation current or an electrosurgical vessel sealing device can be used. These devices should be placed immediately adjacent to the tube in order to cauterize and transect the mesosalpinx.
Be sure to incorporate the entire fimbriated distal portion of the tube, which sometimes requires careful dissection of tubal adhesions or distal tubal cysts off the ovary and its blood supply. At the cornual segment of the fallopian tube, take care to avoid entry into the uterine myometrium, as this region can be particularly vascular. Once detached from the mesosalpinx, the fallopian tubes can be left attached to the uterus as the hysterectomy is then performed and can be removed en bloc with the uterus.
Both traditional and robotic approaches to laparoscopy allow for bilateral salpingectomy at the time of hysterectomy. A grasper should be used to hold onto the infundibular portion of the fallopian tube and to provide gentle traction toward the anterior abdominal wall. This allows for better exposure and visualization of the plane between the ovary and fallopian tube. Any laparoscopic instrument that allows for electrosurgical vessel sealing and transection of tissue can be used to dissect across the mesosalpinx.
Alternatively, a monopolar electrosurgery device can be used to cauterize the mesosalpinx before transection with endoscopic scissors. Again, transect the mesosalpinx as close to the fallopian tube as possible while ensuring that the tube is entirely removed. As in the open approach, the fallopian tubes can be left attached to the uterus while the hysterectomy is performed and removed as a single unit once the hysterectomy is complete.
Salpingectomy at the time of vaginal hysterectomy is often the most challenging of these procedures. In this situation, the hysterectomy is performed as usual up to the level of the “triple pedicles.” At that point, the first triple pedicle—incorporating the utero-ovarian ligaments, the fallopian tubes, and the round ligaments—is clamped and transected from the uterus. A large clamp, such as a Zeppelin, Heaney, or long Pean, should be used. Then place gentle upward traction on the uterus to keep the operative field clear of intraperitoneal contents.
Next evaluate the feasibility of transvaginal salpingectomy by gently turning the clamp on the triple pedicle in order to make an anatomic assessment. In a technique described by Kho and colleagues, the round ligament can first be divided to allow better mobilization of the adnexa and access to the proximal fallopian tube.27 The challenge from this point is to incorporate the entire fallopian tube into the salpingectomy specimen. Leaving the triple pedicle clamped rather than suture-ligating it allows for the clamp to become a handle with which gentle traction and manipulation of the tube can be performed.
Once identified, the fimbriated end of the fallopian tube should be brought into the operative field with a Babcock clamp. Transection of the mesosalpinx begins with freeing the fimbriated end from the ovary. Again, this can be done by clamping, transecting, and ligating isolated vascular pedicles of the mesosalpinx, or with monopolar cautery or an electrosurgical vessel sealing device. In our experience, an electrosurgical vessel sealing device allows for more dexterity and easier sealing and transection of the mesosalpinx during vaginal surgery than individually clamping, cutting, and ligating each pedicle.
Once the isthmic portion of the tube is reached, place a second large clamp just cephalad to the large clamp that contains the triple pedicle. This second clamp should incorporate only the utero-ovarian ligament and the round ligament, leaving the fallopian tube free. The first large clamp can then be removed, allowing for completion of the salpingectomy while the utero-ovarian ligament and the round ligament remain clamped at all times. Then remove the fallopian tube in its entirety. Clamp and transect the contralateral triple pedicle, and remove the uterus before performing contralateral salpingectomy. A surgical sponge on a Forester clamp can be used to gently push the intraperitoneal contents out of the operative field. Complete the contralateral salpingectomy in a similar fashion after removing the uterus.
Salpingectomy at the time of hysterectomy with ovarian preservation will likely become more common as growing evidence implicates the fallopian tube as the site of origin of high-grade serous ovarian cancer. Operative considerations include removal of the fallopian tube in its entirety and preservation of ovarian blood supply. The techniques described here allow for removal of the fallopian tubes while respecting these considerations.
Salpingectomy can be performed safely at the time of hysterectomy via an open abdominal, minimally invasive, or transvaginal approach.
1. Rhiem K, Foth D, Wappenschmidt B, et al. Risk-reducing salpingo-oophorectomy in BRCA1 and BRCA2 mutation carriers. Arch Gynecol Obstet. 2011;283(3):623-627.
2. Mingels MJ, Roelofsen T, van der Laak JA, et al. Tubal epithelial lesions in salpingo-oophorectomy specimens of BRCA-mutation carriers and controls. Gynecol Oncol. 2012;127(1):88-93.
3. Powell CB, McLennan J, Crawford B, et al. Risk-reducing salpingo-oophorectomy (RRSO) in BRCA mutation carriers: experience with a consecutive series of 111 patients using a standardized surgical-pathological protocol. Int J Gynecol Cancer. 2011;21(5):846-51.
4. Kurman, RJ. Origin and molecular pathogenesis of ovarian high-grade serous carcinoma. Ann Oncol. 2013;24(10):16-21.
5. Jazaeri AA, Bryant JL, Park H, et al. Molecular requirements for transformation of fallopian tube epithelial cells into serous carcinoma. Neoplasia. 2011;13(10):899-911.
6. Perets R, Wyant G, Muto K, et al. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten Models. Cancer Cell. 2013;24(6):751-765.
7. Kuhn E, Kurman RJ, Vang R et al. TP53 mutations in serous tubal intraepithelial carcinoma and concurrent pelvic high-grade serous carcinoma-evidence supporting the clonal relationship of the two lesions. J Pathol. 2012; 226:421–426.
9. Rabban JT, Garg K, Crawford B, Chen LM, Zaloudek CJ. Early detection of high-grade tubal serous carcinoma in women at low risk for hereditary breast and ovarian cancer syndrome by systematic examination of fallopian tubes incidentally removed during benign surgery. Am J Surg Pathol. 2014;38(6):729-742.
10. Cibula D, Widschwendter M, Majek O, Dusek L. Tubal ligation and the risk of ovarian cancer: review and meta-analysis. Hum Reprod Update. 2011;17(1):55-67.
11. Rice MS, Murphy MA, Tworoger SS. Tubal ligation, hysterectomy and ovarian cancer: A meta-analysis. J Ovarian Res. 2012;5(1):13.
12. Levine, DA. Genetics and Biology of Gynecologic Cancers. In: Karlan BY, Bristow RE, Li, AJ, eds. Gynecologic Oncology: Clinical Practice & Surgical Atlas. 1st ed. China: McGraw-Hill; 2012.
13. McAlpine JN, Hanley GE, Woo MM, et al. Opportunistic salpingectomy: uptake, risks, and complications of a regional initiative for ovarian cancer prevention. Am J Obstet Gynecol. 2014;210(5):471e1-11.
14. Hoffman BL, Schorge JO, Schaffer JI, et al. Surgeries for Benign Gynecologic Conditions. In: Hoffman BL, Schorge JO, Schaffer JI, Halvorson LM, Bradshaw KD, Cunningham FG, Calver LE, eds. Williams Gynecology. 2nd ed. New York: McGraw-Hill; 2012.
15. Wieslander CK, Wong KS. Therapeutic Gynecologic Procedures. In: DeCherney AH, Nathan L, Laufer N, Roman AS, editors. CURRENT Diagnosis & Treatment: Obstetrics & Gynecology. 11th ed. New York: McGraw-Hill; 2013.
16. Siegel R, Naishadam D, Jemal A. Cancer Statistics, 2013. CA Cancer J Clin. 2013;63(1):11-30.
19. Vorwergk J, Radosa MP, Nicolaus K, et al. Prophylactic bilateral salpingectomy (PBS) to reduce ovarian cancer risk incorporated in standard premenopausal hysterectomy: complications and re-operation rate. 2014; J Cancer Res Clin Oncol. 140(5):859–865.
20. 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(3):448-451.
21. 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(6):1704-1708.
22. Sezik M, Ozkaya O, Demir F, Sezik HT, Kaya H. Total salpingectomy during abdominal hysterectomy: effects on ovarian reserve and ovarian stromal blood flow. J Obstet Gynaecol Res. 2007;33(6):863–869.
23. American College of Obstetricians and Gynecologists. Salpingectomy for ovarian cancer prevention. Committee Opinion No. 620. Obstet Gynecol. 2015;125:279–281.
24. Pölcher M, Hauptmann S, Fotopoulou C, Schmalfeldt B, et al. Opportunistic salpingectomies for the prevention of a high-grade serous carcinoma: a statement by the Kommission Ovar of the AGO. Arch Gynecol Obstet. 2015;292(1):231-234.
25. Society of Gynecologic Oncology. SGO Clinical Practice Statement: Salpingectomy for Ovarian Cancer Prevention. https://www.sgo.org/clinical-practice/guidelines/sgo-clinical-practice-s.... Accessed March 9, 2016.
27. Kho RM, Magrina JF. Round ligament technique and use of a vessel-sealing device to facilitate complete salpingectomy at the time of vaginal hysterectomy. J Minim Invasive Gynecol. 2015;22(6):1084-1087.