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ORIGINAL ARTICLE
Year : 2018  |  Volume : 14  |  Issue : 3  |  Page : 543-548

Comparing surgical outcome and ovarian reserve after laparoscopic hysterectomy between two methods of with and without prophylactic bilateral salpingectomy: A randomized controlled trial


1 Department of Obstetrics and Gynecology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
2 Department of Obstetrics and Gynecology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran
3 Department of Epidemiology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

Date of Web Publication12-Jun-2018

Correspondence Address:
Dr. Safoura Rouholamin
Shahid Beheshti Hospital, Motahari Street, Isfahan
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.193114

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 > Abstract 


Background: This study aimed to compare the surgical outcome and ovarian reserve in premenopausal women undergoing laparoscopic hysterectomy (without oophorectomy) for benign cause between two methods of with and without prophylactic bilateral salpingectomy.
Materials and Methods: In a prospective randomized clinical trial, 62 premenopausal women with benign indication underwent a laparoscopic hysterectomy. Patients were then randomized to undergo hysterectomy with bilateral salpingectomy (Group 1; n = 15) or without bilateral salpingectomy (Group 2; n = 15). We evaluated the impact of bilateral salpingectomy on surgical outcome and ovarian reserve using serum levels of anti-Mullerian hormone (AMH) and follicle stimulating hormone (FSH) that were measured preoperatively and at 3 months postoperatively (P < 0.001).
Results: Baseline characteristics such as age, uterine size, body mass index, and preoperative AMH and FSH levels were similar between the two study groups. The average operative time, estimated blood loss, uterine size, uterine weight, and intraoperative complication were similar between two groups. The mean AMH levels were not significantly different at baseline (1.44 ng/mL vs. 1.2 ng/mL) and at 3-month postoperatively (1.13 ng/mL vs. 0.97 ng/mL) among women with salpingectomy versus no salpingectomy. At 3-month follow-up, in both groups, postoperative AMH levels were significantly lower and FSH levels were significantly higher than before surgery.
Conclusion: Prophylactic bilateral salpingectomy at the time of laparoscopic hysterectomy neither has a negative effect on ovarian reserve nor increases the surgical risk. Therefore, we may recommend gynecologic surgeons to perform prophylactic bilateral salpingectomy during laparoscopic hysterectomy to conserve both ovaries.

Keywords: Anti-Mullerian hormone levels, laparoscopic hysterectomy, ovarian reserve, prophylactic salpingectomy


How to cite this article:
Asgari Z, Tehranian A, Rouholamin S, Hosseini R, Sepidarkish M, Rezainejad M. Comparing surgical outcome and ovarian reserve after laparoscopic hysterectomy between two methods of with and without prophylactic bilateral salpingectomy: A randomized controlled trial. J Can Res Ther 2018;14:543-8

How to cite this URL:
Asgari Z, Tehranian A, Rouholamin S, Hosseini R, Sepidarkish M, Rezainejad M. Comparing surgical outcome and ovarian reserve after laparoscopic hysterectomy between two methods of with and without prophylactic bilateral salpingectomy: A randomized controlled trial. J Can Res Ther [serial online] 2018 [cited 2020 Jul 8];14:543-8. Available from: http://www.cancerjournal.net/text.asp?2018/14/3/543/193114




 > Introduction Top


Of all gynecologic cancers, ovarian malignancies have a high mortality, and most of the patients have advanced stage disease at diagnosis.[1] Unfortunately, the value of ultrasonography and tumor markers for screening the epithelial ovarian cancer have not established and are associated with false-positive test results that lead to unnecessary surgery and surgical complications.[2],[3] Prophylactic salpingo-oophorectomy in hereditary ovarian cancers (high-risk women) is well documented and considered as the most effective way to reduce the risk of this cancer.[4] However, most epithelial ovarian cancers are sporadic (low-risk women) and only 5–10% are hereditary.[5] Recent evidence has suggested that the majority of high-grade pelvic serous carcinomas may actually be originated from the distal  Fallopian tube More Details.[6],[7],[8] Therefore, to decline the risk of ovarian cancer, performing salpingectomy during hysterectomy has been suggested. One of the theoretical concerns about salpingectomy during hysterectomy is the decreased blood supply to the ovary that leads to the risk of premature ovarian failure or early menopause. In this case, the benefit of prophylactic salpingectomy would be considered because of increased risk of cardiovascular disease due to early menopause.[9] If tubes are dissected (along with the fallopian tube) with caution to utero-ovarian vascularity, dilemma of menopausal age will be eliminated.

Ovarian reserve describes the number and quality of the follicles in the ovaries at any given time. There are many tests to measure ovarian reserve.[10] Among these markers, anti-Mullerian hormone (AMH) is accepted to be the most reliable marker because is neither dependent on the menstrual cycle nor affected by the use of hormone.[11],[12]

There has been a debate about the effect of salpingectomy on ovarian reserve. Some of previous studies have concluded that salpingectomy has no negative effect on ovarian function, and others have shown that salpingectomy is associated with decreased ovarian reserve.[13],[14]

Therefore, we designed a prospective randomized study to compare the surgical outcome and ovarian reserve after laparoscopic hysterectomy between two methods of with and without bilateral salpingectomy. We evaluated ovarian reserve by assaying AMH and follicle stimulating hormone (FSH) levels before surgery and at 3 months after laparoscopic hysterectomy.


 > Materials and Methods Top


Ethical statement

This prospective randomized study was conducted at the university hospital from October 2013 to March 2015. The study protocol was approved by the Institutional Review Board of university hospital. Informed written consent was taken from all the participants before enrollment in the study.

Study design and population

During a 2-year period from October 2013 through March 2015, a total of 62 women were screened to select thirty women who met the inclusion criteria and randomly assigned to one of two treatment groups.

The inclusion criteria were as follows: Age <45 years, no symptom of menopause, and candidate of total laparoscopic hysterectomy (TLH) for abnormal uterine bleeding related to benign pathology (both ovaries were preserved).

Exclusion criteria were as follows: Age ≤45 years, family history of gynecologic or breast cancer, prior ovarian surgery, imaging findings suggestive of the ovarian cyst at vaginal ultrasonography, history of oral contraceptive pill or other hormonal agent for the past three cycles, and performing laparoscopic adnexectomy due to suspected ovarian malignancy.

Serum AMH and FSH levels were determined on the 3rd day of the menstrual cycle before the operation and rechecked at 3 months after surgery.

Sample size calculation

This study had 80% power to determine the difference between two groups if their true clinical difference was 1.25.

Study intervention

Among 62 patients, 32 eligible cases were randomized into one of the two treatment groups. Patients were randomly assigned into two groups as Group 1 (with bilateral salpingectomy; n = 15) and Group 2 (without bilateral salpingectomy = 15), using a computer-designed randomization method that was provided by a statistician.

Random number sequence was stratified with a 1:1 Allocation using random block sizes of 6. The randomization sequence was protected in a sealed envelope until the operation. The operators and patients were not aware of the assignment. Whenever a patient was found to be qualified for participating in the study, the numbered envelope was opened to determine the surgical technique to undergo with or without bilateral salpingectomy.

The surgical procedure was performed by a team of expert surgeons for the treatment of endometriosis at the Laparoscopic Center of Tehran Medical University, Tehran, Iran. TLH was performed under general anesthesia. After the establishment of pneumoperitoneum with the Veress needle through a 10 mm subumbilical vertical incision, a 10 mm laparoscope was introduced. Then, two to three additional 5 mm trocars were placed for operative instruments. Intra-abdominal CO2 pressure was set at 13–15 mmHg.

In Group 1, TLH was done and fallopian tubes were divided in the proximal tubal isthmus that was followed by preserving both adnexa. In Group 2, patients underwent TLH (both ovaries were reserved), and complete removal of the both fallopian tubes was performed using bipolar electrosurgery (40W current; Richard Wolf, Germany). Resection of the mesosalpinx was done as close to the fallopian tube as possible to avoid injury to the ovarian vessels. For each patient, time of surgery (minute), average blood loss, uterine size, uterine weight, body mass index (BMI), drains inserted after surgery, and history of previous tubal sterilization and complication rate were recorded.

The aim of this study was to compare ovarian reserve by measuring AMH and FSH levels between two groups. All hormonal measurements were performed in the same reference laboratory. Venous blood samples were obtained and sera were extracted by centrifugation. Serum FSH level was measured by enzyme-linked fluorescent assay (ELFA; VIDAS, bioMerieux S.A., France) according to the manufacturer's instructions. Serum AMH level was measured by a commercially available enzyme-linked immunosorbent assay kit (Beckman Coulter Inc., Ireland) and reported as nanograms per milliliter with the detection limit of 0.16 ng/mL. The values of intra- and inter-assay coefficient of variation were 4.18% and 4.74% for FSH and >12.3% and >14.2% for AMH, respectively.

Statistical analysis

Baseline differences between two groups were tested using t-tests for continuous variables and Chi-square statistics for categorical variables.

The responses of primary and secondary end points (postoperative AMH and postoperative FSH) were analyzed using linear regression model, with treatment group as main effects, and BMI, age, parity, and the baseline values of a relevant variable as the covariates. The value of P = 0.05 was considered statistically significant. All statistics were generated using running Stata version 13.0 software packages (Stata, College Station, TX, USA).


 > Results Top


Patient characteristics

Among 62 patients, 32 eligible cases were randomized into one of the two treatment groups [Figure 1]. Baseline demographic and illness characteristics did not differ significantly between the two study arms. The background characteristics of the patients included in the intention-to-treat group are shown in [Table 1].
Figure 1: Flowchart showing participant recruitment

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Table 1: Baseline demographics and disease characteristics

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Surgical outcome

The mean ± standard deviation was estimated for blood loss, based on American Society of Anesthesiologists scores, while surgical time, uterine size, and uterine weight were similar between the groups. There were no significant differences in terms of intraoperative complications between both groups. One patient in each group had intraoperative bleeding, so they needed a transfusion of 2 units of packed cells to correct blood loss because of large uterus. There was no bladder or bowel damage in both groups. In both group, no surgery was converted to laparotomy [Table 2].
Table 2: Surgical outcome

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Hormonal assay

As presented in [Figure 2], the AMH levels showed a decreased trend for two groups during study, and there was no significant difference between them. Basic descriptive statistics, crude, and standardized regression coefficients are shown in [Table 3].
Figure 2: Serum AMH concentrations between two groups before and after treatment

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Table 3: The results of a multiple linear regression model for anti-Mullerian hormone

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For AMH level, the model was statistically significant (F (5, 24) = 158.58; P < 0.001), and accounted for approximately 97% of the variance of AMH (R2 = 0.971; adjusted R2 = 0.965).

Similarly, there was no significant difference between two groups regarding FSH levels [Table 4]. The model was statistically significant (F (5, 24) =21.84; P < 0.001) and accounted for approximately 82% of the variance of AMH (R2 = 0.82; adjusted R2 = 0.782).
Table 4: The results of a multiple linear regression model for follicle stimulating hormone

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Comparison of serum hormonal concentrations between the two groups before and after treatment is presented in [Figure 3].
Figure 3: Serum FSH concentrations between two groups before and after treatment

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 > Discussion Top


Hysterectomy is the second most frequently major surgical procedure. The highest rate of hysterectomy is between the ages of 40 and 49 years.[15] Before age 65, premenopausal women undergoing salpingo-oophorectomy at the time of hysterectomy due to benign disease face the increased risk of cardiovascular disease leading to an increase in mortality rate. Thus, ovarian preservation must be strongly considered in these patients.[16] Since majority of high-grade serous carcinomas may be originated from the distal fallopian tube, salpingectomy during hysterectomy has been suggested to protect them from later ovarian cancer and further tubal complication such as hydrosalpinx.[8],[17] Yet the debate about salpingectomy affecting ovarian function has been continued.

Ovarian reserve is marked as the size and quantity of the remaining ovarian follicular pool at any given time. AMH level has been considered as a reliable and useful marker of ovarian reserve than the levels of inhibin B, estradiol (E2), FSH, and luteinizing hormone on day 3 of cycle.[18] We measured AMH and FSH levels at 3 months after the surgery when a complete recovery of ovarian tissue was obtained.

The results of this study did not detect significant difference in AMH and FSH levels at 3 months after hysterectomy in women who received bilateral salpingectomy as compared those who did not receive salpingectomy.

Our surgical techniques also preserved the ovarian blood supply. The fallopian tube is an essential component of the female reproductive system. The blood supply of the tubes comes from branches of uterine artery (ascending branch) and ovarian artery. The attention to blood supply and resection of tubes close to the fallopian tube were essential elements of our technique for adding bilateral salpingectomy to TLH. At the time of bilateral salpingectomy, application of a proper surgical technique to maintain an adequate ovarian blood flow has recommended by previous study.[13] The surgical removal of fallopian tubes in patients undergoing hysterectomy is technically simple and can be rapidly performed. Our findings revealed that surgical outcomes, including operation time, blood loss, and intraoperative complication, did not differ between women who received bilateral salpingectomy compared those who did not receive salpingectomy.

We also found that the serum AMH and FSH levels after TLH, with or without salpingectomy, showed no significant differences.

Two other studies also evaluated the effect of bilateral salpingectomy on ovarian function during total abdominal hysterectomy and concluded that ovarian blood flow and function remained intact after surgery.[13],[19] Comparing these findings with our results reveals that this difference is not due to laparoscopy or laparotomy root of surgery, but it is related to the technique of surgery used.

Similar to our finding, Findley et al. evaluated the serum AMH levels at 4–6 weeks and at 3 months after TLH with or without salpingectomy. They showed postoperative mean AMH levels were not significantly different between two groups and concluded salpingectomy during TLH with ovarian preservation has no deleterious effect on ovarian reserve.[20]

Morelli et al. performed a retrospective study to compare ovarian function after TLH, with and without salpingectomy, when both ovaries were preserved. They concluded that salpingectomy did not show a negative effect on the ovarian function by determining the preoperative and 3-month postoperative levels of AMH and FSH, as well as antral follicle count.[21]

However, Ye et al. reported a decline in ovarian reserve (decreased AMH and increased FSH levels) after salpingectomy in patients seeking in vitro fertilization (IVF).[22] The differences between our results and those of Ye et al. could be attributed to the facts that they did not check AMH levels before salpingectomy and also chose heterogeneous characteristic for the cases.

Grynnerup et al. found lower AMH level and fewer oocytes retrieved in salpingectomized women compared with women with tubal factor infertility, leading to preserve tubes during IVF treatment.[14] This controversy result may be correlated to removal of hydrosalpinx compared to common surgical removal of the tube that is associated with more unintended effects on ovarian vascular supply. Furthermore, resection of the fallopian tube is considered as a difficult procedure to avoid injury to the ovarian vessels that is similar to the study by Gelbaya et al., in which they concluded that follicle count and oocytes retrieved were significantly lower after salpingectomy as compared to the patients undergoing proximal tubal division of hydrosalpinx.[23]

There are some limitations with our study. We needed larger sample size and longer follow-up period of patients through menopause. Moreover, we simultaneously compared ovarian reserve after total abdominal hysterectomy between two methods of with and without salpingectomy in our center, but due to low number of open surgery, we recommend further study.

Our study has some advantages. It was a prospective randomized clinical trial, use of AMH and FSH levels to measure ovarian reserve and no loss-to-follow-up.


 > Conclusion Top


Salpingectomy at the time of laparoscopic hysterectomy with the aim of ovarian preservation neither has negative effect on ovarian reserve nor increases the surgical risk. The procedure can easily be done in the surgical steps of laparoscopic hysterectomy, without changes of perioperative morbidity or duration of surgery. Therefore, we may recommend gynecologic surgeons to perform bilateral salpingectomy during laparoscopic hysterectomy to conserve both ovaries.

Acknowledgments

The authors acknowledge the whole staff of the laparoscopic operation room and gynecologic ward in Women's hospital.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 > References Top

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Whiteman MK, Hillis SD, Jamieson DJ, Morrow B, Podgornik MN, Brett KM, et al. Inpatient hysterectomy surveillance in the United States, 2000-2004. Am J Obstet Gynecol 2008;198:34.e1-7.  Back to cited text no. 1
    
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Einhorn N, Sjövall K, Knapp RC, Hall P, Scully RE, Bast RC Jr., et al. Prospective evaluation of serum CA 125 levels for early detection of ovarian cancer. Obstet Gynecol 1992;80:14-8.  Back to cited text no. 2
    
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Higgins RV, van Nagell JR Jr., Donaldson ES, Gallion HH, Pavlik EJ, Endicott B, et al. Transvaginal sonography as a screening method for ovarian cancer. Gynecol Oncol 1989;34:402-6.  Back to cited text no. 3
    
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Berek JS, Chalas E, Edelson M, Moore DH, Burke WM, Cliby WA, et al. Prophylactic and risk-reducing bilateral salpingo-oophorectomy: Recommendations based on risk of ovarian cancer. Obstet Gynecol 2010;116:733-43.  Back to cited text no. 4
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Whittemore AS, Gong G, Itnyre J. Prevalence and contribution of BRCA1 mutations in breast cancer and ovarian cancer: Results from three U.S. population-based case-control studies of ovarian cancer. Am J Hum Genet 1997;60:496-504.  Back to cited text no. 5
    
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Crum CP, Drapkin R, Miron A, Ince TA, Muto M, Kindelberger DW, et al. The distal fallopian tube: A new model for pelvic serous carcinogenesis. Curr Opin Obstet Gynecol 2007;19:3-9.  Back to cited text no. 6
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Carlson JW, Miron A, Jarboe EA, Parast MM, Hirsch MS, Lee Y, et al. Serous tubal intraepithelial carcinoma: Its potential role in primary peritoneal serous carcinoma and serous cancer prevention. J Clin Oncol 2008;26:4160-5.  Back to cited text no. 7
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Jacoby VL, Grady D, Wactawski-Wende J, Manson JE, Allison MA, Kuppermann M, et al. Oophorectomy vs. ovarian conservation with hysterectomy: Cardiovascular disease, hip fracture, and cancer in the Women's Health Initiative Observational Study. Arch Intern Med 2011;171:760-8.  Back to cited text no. 9
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Fanchin R, Schonäuer LM, Righini C, Guibourdenche J, Frydman R, Taieb J. Serum anti-Müllerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3. Hum Reprod 2003;18:323-7.  Back to cited text no. 10
    
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La Marca A, Stabile G, Artenisio AC, Volpe A. Serum anti-Mullerian hormone throughout the human menstrual cycle. Hum Reprod 2006;21:3103-7.  Back to cited text no. 12
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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;33:863-9.  Back to cited text no. 13
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Grynnerup AG, Lindhard A, Sørensen S. Anti-Müllerian hormone levels in salpingectomized compared with nonsalpingectomized women with tubal factor infertility and women with unexplained infertility. Acta Obstet Gynecol Scand 2013;92:1297-303.  Back to cited text no. 14
    
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Parker WH, Feskanich D, Broder MS, Chang E, Shoupe D, Farquhar CM, et al. Long-term mortality associated with oophorectomy versus ovarian conservation in the nurses' health study. Obstet Gynecol 2013;121:709.  Back to cited text no. 16
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Anderson CK, Wallace S, Guiahi M, Sheeder J, Behbakht K, Spillman MA. Risk-reducing salpingectomy as preventative strategy for pelvic serous cancer. Int J Gynecol Cancer 2013;23:417-21.  Back to cited text no. 17
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Toner JP, Seifer DB. Why we may abandon basal follicle-stimulating hormone testing: A sea change in determining ovarian reserve using antimüllerian hormone. Fertil Steril 2013;99:1825-30.  Back to cited text no. 18
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Nouh A, El Behery M, Alanwar A, Seleim B. Total salpingectomy during abdominal hysterectomy preserves ovarian blood flow and function. Webmed Central Obstet Gynaecol 2010;1:WMC00707.  Back to cited text no. 19
    
20.
Findley AD, Siedhoff MT, Hobbs KA, Steege JF, Carey ET, McCall CA, et al. Short-term effects of salpingectomy during laparoscopic hysterectomy on ovarian reserve: A pilot randomized controlled trial. Fertil Steril 2013;100:1704-8.  Back to cited text no. 20
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21.
Morelli M, Venturella R, Mocciaro R, Di Cello A, Rania E, Lico D, et al. Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: Primum non nocere. Gynecol Oncol 2013;129:448-51.  Back to cited text no. 21
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22.
Ye XP, Yang YZ, Sun XX. A retrospective analysis of the effect of salpingectomy on serum antiMüllerian hormone level and ovarian reserve. Am J Obstet Gynecol 2015;212:53.e1-10.  Back to cited text no. 22
    
23.
Gelbaya TA, Nardo LG, Fitzgerald CT, Horne G, Brison DR, Lieberman BA. Ovarian response to gonadotropins after laparoscopic salpingectomy or the division of fallopian tubes for hydrosalpinges. Fertil Steril 2006;85:1464-8.  Back to cited text no. 23
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