Prophylactic bilateral salpingectomy (PBS) to reduce ovarian cancer risk incorporated in standard premenopausal hysterectomy: complications and re-operation rate.

Purpose Hysterectomy for benign conditions can be combined with bilateral salpingectomy to prevent re-intervention for malignant or benign fallopian tube pathologies. The objective of this study was to evaluate the benefit of prophylactic bilateral salpingectomy (PBS) in standard hysterectomy in premenopausal women.

This retrospective cohort study included all premenopausal patients at our institution who underwent laparoscopically assisted vaginal hysterectomy (LAVH) without oophorectomy for benign pathologies between 2001 and 2007 [PBS group (LAVH + PBS), 2006–2007; non-PBS group (LAVH without PBS), 2001–2005]. Electronic and paper-based files as well as questionnaire responses were analyzed. In 2010, a survey on patients of a non-BRCA background with and without PBS was requested to complete a standardized questionnaire. Data were analyzed for differences between both subgroups regarding surgical outcome and adnexal pathologies as reported in the postoperative follow-up.

Surgical outcomes of 540 patients (PBS: 127; non-PBS: 413) revealed no difference between groups. No preneoplastic or malignant lesions were diagnosed in the fallopian tubes. Follow-up (non-PBS 92 months, PBS 55 months; p < 0.01) responses from 295 (54.6 %) patients showed a higher incidence of benign adnexal pathologies in the non-PBS group (26.9 vs. 13.9 %; p = 0.02). The rate of LAVH-related surgical re-intervention was higher in the non-PBS group (12.56 vs. 4.16 %; p = 0.04). No malignant neoplasm was reported in the cohort.

PBS did not increase the complication rate and reduced the incidence of adnexal pathologies requiring surgical re-intervention. Prospective trials should clarify the impact of PBS on cancer mortality.

Ovarian cancer, Prophylactic salpingectomy, Hysterectomy, Risk-reducing bilateral salpingo-oophorectomy, Premenopausal women

Hysterectomy is one of the most frequently performed surgical procedures in women of reproductive age: In Germany, approximately 150.000 hysterectomies were performed in 2006 (Statistisches Bundesamt 2011). In 2004, one-third of all women, residing in the USA, could expect to have undergone hysterectomy by the end of their menopause (Whiteman and al 2008). Currently, a debate is ongoing about the clinical benefit of a concurrent removal of the fallopian tubes in premenopausal women without the background of a BRCA mutation undergoing hysterectomy, referred to as elective, opportunistic, or prophylactic bilateral salpingectomy (PBS). In prophylactically removed fallopian tubes from BRCA mutation carriers, precursor lesions of serous cancer with a “p53 signature” have been described (Crum et al. 2007). Mutations of the p53 gene are most frequent in serous ovarian cancers and have initially been described in serous cancer derived from fallopian tube by our group p53 (Runnebaum et al. 1994). Serous tubal intraepithelial carcinoma (STIC, see Fig. 1b) lesions recently hypothesized to play a pivotal role in the pathogenesis of at least some serous fallopian tube, ovarian, and peritoneal cancers, which could originate in tubal remnants after hysterectomy (Piek et al. 2001; Jarboe et al. 2009). Thus, the routine removal of the fallopian tubes at the time of hysterectomy might prevent the subsequent manifestation of such cancers (Dietl et al. 2011). In a recent survey among US teaching hospitals, 54 % of the responding practioners stated to perform PBS to reduce the risk of tubal malignancy (75 % of responders) or of repeat operation (49 % of responders) (Gill and Mills 2013). Of the practioners who do not perform PBS during hysterectomy (45 %), most believe there is no benefit (69 %) or believe there is a risk of reduced ovarian function by compromising ovarian perfusion. A recent study on salpingectomy with hysterectomy in a laparoscopic approach did not demonstrate a negative impact of salpingectomy on ovarian function (Morelli et al. 2013). In our department, laparoscopically assisted vaginal hysterectomy (LAVH) for benign uterine pathologies has been routinely combined with concomitant PBS in premenopausal patients since October 2005. In the absence of macroscopic pathology, department policy did not entail fallopian tube removal in standard hysterectomy from January 2001 through September 2005. This policy has changed since then to PBS as an institutional standard. Within the context of the scientific debate about PBS, the aim of this study was to evaluate the clinical rationale for this procedure in premenopausal women undergoing hysterectomy by comparing intra- and postoperative outcomes in patients undergoing LAVH with (2006–2007) and without (2001–2005) PBS in our department.

Study design and patient selection This retrospective single-center cohort study was conducted at the Department of Gynecology and Obstetrics, Jena University Hospital, to evaluate the clinical benefit of concomitant PBS in premenopausal women without a particular BRCA background undergoing LAVH. Our institution serves as a tertiary university referral center. LAVH has been one standard surgical method for hysterectomy to treat benign uterine disorders at our hospital since the early nineties. Since October 2005, LAVH has been complemented with PBS in premenopausal patients. All patients undergoing PBS were specifically counseled about the procedure. All premenopausal women who underwent LAVH without oophorectomy to treat benign uterine pathologies between January 2001 and August 2007 were identified by searching the hospital’s electronic database (ISHMed; SAP, Walldorf, Germany). Patients’ paper-based and electronic charts were reviewed to determine eligibility for study inclusion according to the following criteria: (1) age 40–55 years and premenopausal, as defined by the World Health Organization; (2) presence of a benign gynecological condition leading to hysterectomy; (3) American Society of Anesthesiologists physical status classification of I–II (Owens et al. 1978), and (4) completion of hysterectomy as intended, with no conversion to laparotomy. Included patients were classified into the non-PBS group (LAVH without PBS, January 2001–December 2005) and the PBS group (LAVH and PBS, January 2006–August 2007). Surgical procedure and postoperative management Preoperatively, patients underwent gynecological examination and transvaginal ultrasound. Basic laboratory tests included the measurement of preoperative hemoglobin concentrations. All surgical procedures were performed in the Department of Gynecology and Obstetrics, Jena University Hospital. LAVH was performed according to the technique described by Childers and Surwit (1992). When performed, concomitant laparoscopic salpingectomy was carried out at the beginning of the surgical procedure in the following manner: After the induction of capnoperitoneum and placement of one 10-mm umbilical optic trocar and three 5-mm working trocars (one suprapubic, two iliac), the salpinx was grasped with an atraumatic tubal forceps and the fimbria attached to the ovarian surface was slightly electrocoagulated and sharply dissected. The mesosalpinx was gradually electrocoagulated precisely close to the tube and sharply dissected from the fimbrial portion to the tubal isthmus, close to the tubal serosa, to avoid heat development near the ovarian blood supply. The peritoneal cavity was re-inspected laparoscopically after closure of the vaginal cuff in all patients to assure adequate hemostasis, and an intra-abdominal drain (French, 18 gauges) was placed through one of the 5-mm iliac trocars for postoperative monitoring. The duration of surgery was calculated from the time of Verres needle placement until closure of the trocar sites at the end of the procedure. All patients received intraoperative antibiotic prophylaxis (1.5 g cefuroxime and 0.5 g metronidazole, injected intravenously). Low-molecular weight heparin (enoxaparin, 40 mg daily) was administered subcutaneously in the postoperative period for the entire length of each patient’s hospitalization. Intra- and postoperative complications were defined according to the revised Clavien-Dindo classification (Dindo et al. 2004). Patients were discharged at the resumption of full daily activity; the duration of hospitalization was calculated from the first operative day until the day of discharge. Follow-up data collection In June 2011, a questionnaire was mailed to all patients included in the study. Patients were asked to provide information about the indication(s) and procedure(s) used for any further required surgical or medical treatment following hysterectomy. Particularly, patients were asked whether they had been treated for a benign pathology of the ovary or salpinx (hydrosalpinx, pyosalpinx, salpingitis, ovarian cysts, adnexitis, tubal, or ovarian torsion) or diagnosed with a malignant neoplasia (ovarian or peritoneal cancer) since their hysterectomy. Questionaires were double analyzed by two examiners (NB and MPR) in order to determine whether subsequent reported surgical interventions were related to the initial hysterectomy. Statistical analysis Data were collected and processed using an Excel database (Microsoft, Redmond, WA, USA). Differences between groups were examined by calculating standard deviations and means for the categories duration of surgery, intra- and postoperative complications, postoperative hospital stay, benign and malignant adnexal pathologies observed in the study’s follow-up as well as subsequent surgical interventions related to the initial hysterectomy. Unpaired two-sample t tests or Fisher’s exact tests for categorical data were hence performed. p values <0.05 were considered to indicate statistical significance. All statistical calculations were conducted with QuickCalcs software (GraphPad, La Jolla, CA, USA).

The study sample comprised 540 women (PBS group, n = 127; non-PBS group, n = 413, see Table 1). The non-PBS group included 22 patients who underwent unilateral salpingectomy during LAVH. Mean patient ages at the time of surgery in the non-PBS and PBS groups were 46.23 [standard deviation (SD), 4.58] and 46.42 (SD, 5.15) years, respectively (p = 0.69). The most frequent indications for hysterectomy, with multiple indications for some patients, were symptomatic leiomyoma of the uterus (88 %), uterine bleeding disorders (37 %), and adenomyosis uteri (9 %). No significant difference in indications was observed between groups. Table 1. | PBS group | Non-PBS group | p | ||| |---|---|---|---|---|---| | I. Retrospective patient’s data analysis | ||||| | n | n | |||| | Patients | 127 | 413 | | Mean | SD | Mean | SD | || |---|---|---|---|---|---| | Patient’s age at time of surgery (years) | 46.42 | 5.15 | 46.23 | 4.58 | 0.69 | | Duration of surgery (min) | 142.97 | 63.31 | 139.72 | 49.31 | 0.55 | | n | n | |||| |---|---|---|---|---|---| | Surgical complications | 24 | 73 | 0.79 | || | Clavien-Dindo grade I–II complications | 20 | 45 | 0.16 | || | Clavien-Dindo grade III complicationsa | 4 | 28 | 0.19 | | Mean | SD | Mean | SD | || |---|---|---|---|---|---| | Postoperative hospitalization (days) | 4.93 | 1.51 | 5.11 | 1.82 | 0.31 | | II. Patient’s survey | ||||| |---|---|---|---|---|---| | n | n | |||| | Returned questionnaires | 72 (57 %) | 223 (54 %) | | Mean | SD | Mean | SD | || |---|---|---|---|---|---| | Follow-up (months) | 55.21 | 7.92 | 92.32 | 16.96 | <0.01 | | n | n | |||| |---|---|---|---|---|---| | Benign adnexal pathologies | 10 | 60 | 0.02 | || | Surgical interventions related to hysterectomy | 3 | 28 | 0.04 | || | Malignant pathologies ovary/peritoneum | 0 | 0 | b | Bold values indicate statistical significance aNo grade IV or V complications did occur bNot applicable A total of 97 complications (Clavien-Dindo grade I, n = 40; grade II, n = 33; grade III, n = 24) were recorded in the whole study cohort (overall complication rate, 17.96 %). The incidence of complications overall and severe complications (Clavien-Dindo grade ≥III) in particular did not differ between groups. Severe complications (Clavien-Dindo grade ≥III) comprised seven urinary tract lesions requiring postoperative suprapubic urinary catheter placement, five cases of pelvic abscess formation treated by laparoscopic lavage, six cases of postoperative hemorrhage, and six cases of vaginal vault dehiscence. All other observed surgical complications (Clavien-Dindo grades I and II) were minor postoperative events, such as increased wound pain, urinary tract infection, and abdominal bloating. No grade IV or V complication occurred. The mean duration of postoperative hospitalization was 5.04 (SD 1.51) days, with no significant difference between groups. Histopathological examination revealed that removed uteri were benign in all but two patients in the non-PBS group, in whom endometrioid adenocarcinoma of the uterus was diagnosed. These two patients were excluded from follow-up data evaluation in June 2011. No premalignant (Fig. 1) or malignant lesion was detected in fallopian tubes removed electively from patients in the PBS group. A total of 295/540 (non-PBS, n = 223; PBS, n = 72; response rate, 54.63 %) patients returned completed follow-up questionnaires. Given the study design, the mean follow-up interval was significantly longer in the non-PBS group [92.32 (SD, 16.96) months] than in the PBS group [55.2 (SD, 7.92) months; p < 0.01]. No patient reported the occurrence of malignant neoplasia of the ovary or peritoneum in the follow-up period. Sixty (26.91 %) women in the non-PBS group reported the postoperative occurrence of adnexal pathologies requiring medical or surgical treatment. These pathologies comprised 33 cases of ovarian cysts, eight cases of hydrosalpinx, one case of pyosalpinx (Fig. 1d), and 18 cases of adnexitis. Ten (13.88 %) women in the PBS group reported adnexal pathologies (ovarian cysts, n = 9; adnexitis, n = 1). The rates of observed benign adnexal pathologies following hysterectomy differed significantly between groups (p = 0.02). In the non-PBS group, 28 surgical interventions were related to initial hysterectomies. Twelve cases of ovarian cysts were treated by uni- or bilateral salpingo-oophorectomy, 15 cases of adnexitis were treated by laparoscopic pelvic lavage and postoperative antibiotic therapy, nine cases of hydrosalpinx were treated by laparoscopic bilateral salpingectomy, one case of pyosalpinx was treated by unilateral laparoscopic adnexectomy, and one case of vaginal prolapse was treated by vaginal anterior and posterior colporrhaphy. In the PBS group, three ovarian cysts were treated by laparoscopic bilateral oophorectomy. The rate of hysterectomy-related surgical interventions reported by patients was significantly higher in the non-PBS group than in the PBS group (12.56 vs. 4.16 %; p = 0.04).

The surgical removal of fallopian tubes in patients undergoing hysterectomy is technically simple and can be rapidly performed, as the salpinx and uterus compose an embryologic unit derived from the Müllerian duct (Strandell et al. 2001). Surgical outcomes, including operation time, the occurrence of perioperative complications, and duration of postoperative hospitalization, did not differ between the PBS group and non-PBS group and were comparable to those reported previously in perimenopausal patients undergoing LAVH (Devendra and Tay 2002). Overall surgical morbidity rate was 17.96 % in the study cohort, which appeared high in a non-risk population of premenopausal women with benign uterine pathologies. The complication rate can be related to the classification system used to assess perioperative complications: Surgical morbidity was classified using the Clavien-Dindo system, a standardized, patient-oriented approach with a low threshold for the inclusion of surgical complications, defined as any deviation from an ideal postoperative course (Dindo et al. 2004). Previous assessments using the Clavien-Dindo system have yielded similarly high estimates of surgical morbidity in laparoscopic hysterectomy (11.21–18.39 %) compared with non-standardized evaluations (Radosa et al. 2013). Severe complications of Clavien-Dindo grade ≥III were infrequent in both, PBS and non-PBS patients. In our opinion, the similar surgical morbidity rates in the two study groups support the consideration of PBS as a technically safe addition to hysterectomy in premenopausal patients. Preservation of the fallopian tubes in premenopausal women significantly elevated the risk of developing symptomatic benign tubal or ovarian pathologies, which were approximately twofold more prevalent in the non-PBS group than in the PBS group and were responsible for the majority of subsequent procedure-related re-laparoscopies in this cohort. These findings could be biased by the significant difference in follow-up intervals between our groups due to the comparison of two historic patient cohorts. Published studies on the subject have previously found comparable results: Repasy et al. (2009) reported that clinically relevant benign salpingeal pathologies occurred in 35.5 % of patients undergoing hysterectomy with salpinx preservation. Morse and et al. (2002) observed a 7.8 % life-time risk of hydrosalpinx development in a mixed cohort of patients undergoing hysterectomy or tubal sterilization. Other studies have suggested that patients undergoing hysterectomy with fallopian tube preservation are at increased risk of surgical re-intervention due to infectious adnexal pathology, compared with patients undergoing removal of the uterus with concurrent bilateral salpingectomy (Morse et al. 2006; Singla 2007; Timor-Tritsch et al. 2010; Rezvani and Shaaban 2011). Dietl et al. (2011) hypothesized that this increased risk was due to the origination of urogenital infections in the blind-ended fallopian tube remnants. Guldberg et al. observed a twofold increased risk of benign pathologies of the fallopian tube with need for surgical revision in a large Danish patient cohort, who underwent hysterectomy without BES. The authors hence recommended BES in patients undergoing hysterectomy, regardless of their respective menopausal state (Guldberg et al. 2013). It has been hypothesized that concurrent PBS in premenopausal women undergoing hysterectomy for benign uterine pathology could reduce the subsequent life-time risk for developing a serous epithelial cancer of the tubes, the ovaries, or the peritoneum: Accumulated data indicate that the fallopian tubes are a likely origin site of serous epithelial cancers of the ovary, fallopian tube, and peritoneum (Callahan et al. 2007; Crum et al. 2007; Kindelberger et al. 2007). Several surgical specimens from prophylactic salpingo-oophorectomies performed in women with BRCA1 or BRCA2 germ line mutations exhibited serous intraepithelial carcinomas originating in the distal ends of the fallopian tubes (Piek et al. 2001). The coexistence of invasive serous ovarian cancer and serous tubal intraepithelial carcinoma (STIC) has been determined in 50 % of adnexal specimens from patients with sporadic, non-BRCA-associated serous ovarian cancer (Kindelberger et al. 2007; Przybycin et al. 2010). Histopathological examination of fallopian tubes from our patients via conventional microscopy and immunohistochemistry of paraffin-embedded specimens revealed no tubal malignancy. This result could be biased by a lack of sensitivity of this examination method for the detection of occult cancerous lesions (Mingels and al 2013). The use of a histopathological sectioning protocol focusing on the morphology of the entire fallopian tube and intensive examination of the fimbria mucosa as the SEE-FIM, as well as those involving immunohistochemical detection of p53 and Ki-67 (MIB-1), could enhance the detection rate of early tubal carcinomas (Medeiros et al. 2006; Callahan et al. 2007). A long-term follow-up study found that bilateral total or partial salpingectomy reduced the risk of serous epithelial ovarian or peritoneal cancer by approximately one-third in premenopausal women carrying BRCA germ line mutations (Cibula et al. 2011). Our evaluation did not demonstrate this beneficial effect of PBS in a non-BRCA mutation carrier population, as no patient reported the development of malignant neoplasia during follow-up. This finding should be interpreted with caution, as the majority of our patients had not reached the peak age of sporadic epithelial ovarian cancer prevalence (~65 years) (Chornokur et al. 2013) at the time of follow-up. A substantially longer follow-up period may have contributed to the assessment of the ability of concurrent PBS to reduce the incidence of serous ovarian, peritoneal, or tubal cancer in our study cohort. One argument against PBS, especially in women of reproductive age, is the potential risk of iatrogenic ovarian blood supply impairment, which can reduce ovarian function due to the close anatomical association of the blood supply and nervous system of the adnexal structures. Although this study did not specifically address this issue, recently published studies have challenged the clinical relevance of PBS-induced ovarian blood supply impairment in patients undergoing hysterectomy. Doppler sonography revealed no significant difference between pre- and postoperative ovarian blood supply, or even postoperative improvement, in patients who underwent hysterectomy with concomitant PBS (Dar et al. 2000; Sezik et al. 2007; Strandell et al. 2001). Nahas et al. (2003) hypothesized that this finding was related physiologically to the redistribution effects of arterial blood flow in areas supplying the uterus and ovaries, which induces functional hypertrophy of the ovaries. Ghezzi et al. (2009) assessed ovarian hormonal secretion in patients undergoing hysterectomy with and without PBS and found comparable serum follicle-stimulating and luteinizing hormone levels at 6 months postoperatively. Similar results have been recently reported by Morelli et al. (2013). Still, no data have been reported regarding effect on the time of menopause. In summary, our findings underline the clinical benefits of PBS in premenopausal women undergoing hysterectomy for benign uterine pathology: The procedure itself can easily be integrated into the surgical steps of a laparoscopic uterus extirpation, without significant changes in terms of perioperative morbidity or duration of surgery. In the sequel of a standard hysterectomy, PBS may substantially reduce the rate of adnexal pathology. Since no ovarian or peritoneal cancer was reported in the follow-up of this study, this finding was conceivably biased by a not sufficiently long follow-up period. Prospective studies are warranted to assess the clinical impact of PBS in standard premenopausal hysterectomy on cancer mortality. Conflict of interest None. Footnotes J. Vorwergk and M. P. Radosa have contributed equally to this work.

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