The aim of the present systematic review was to study the effect of bipolar electrocoagulation during ovarian cystectomy on ovarian reserve. We searched Medline (1966–2015), Scopus (2004–2015), ClinicalTrials.gov (2008–2015), and Cochrane Central Register (CENTRAL) databases along with reference lists of electronically retrieved studies. The levels of antimullerian hormone (AMH) and antral follicle count (AFC) at 1, 3, 6, and 12 months following the excision of the benign ovarian cyst were defined as primary outcomes. Eight studies were finally included in our systematic review, which recruited 545 women. A metaanalysis was precluded because of significant heterogeneity in the methodological characteristics of the included studies. Data from the included studies suggest that the use of bipolar coagulation compared with ovarian sutures seems to result in significantly lower AMH and AFC during the first 3 months following the excision of the ovarian cyst. Two studies reported that this effect seems to persist at 6 and 12 months postoperatively. Bipolar electrodiathermy seems to be accompanied by increased damage to ovarian reserve, which is indicated by the lower levels of AMH and AFC. However, definitive results are precluded because of the significant heterogeneity of included studies and the potential bias.
During the last 2 decades, laparoscopy has gained ground in the operative field for the treatment of benign diseases, and today it is thought to be the gold standard for the excision of nonmalignant ovarian cysts. The procedure briefly includes stripping of the ovarian cyst wall, which is followed by appropriate hemostasis by means of bipolar electrocoagulation or simple suturing of the residual ovarian parenchyma. Certain studies have suggested that surgical excision of ovarian cysts and specifically of endometriomas may have a negative impact on ovarian reserve. This observation could be partly explained from inadvertently removed healthy ovarian tissue after excision of endometriomas and other benign ovarian cysts.
Several noninvasive markers have been proposed to assess the ovarian reserve including the serum levels of follicle-stimulating hormone (FSH), serum anti-Müllerian hormone (AMH), luteinizing hormone, estradiol, the luteinizing hormone/FSH ratio, and inhibin B, and sonographic variables such as the mean ovarian diameter, the ovarian volume, the antral follicle count (AFC), and the peak systolic velocity (PSV) of the ovarian artery. Among them the most sensitive seem to be AMH and AFC.
Until today it is not known whether the negative effect of cyst excision on ovarian reserve is exerted through the application of bipolar electrocoagulation, which may potentially destroy the oocytes. The purpose of the present systematic review was to compare bipolar electrocoagulation with ovarian sutures and study its effect on ovarian reserve and fertility outcomes.
Materials and Methods
Study design
The present study was designed according to the Preferred Reporting Items for Systematic Reviews and Metaanalyses guidelines. Eligibility criteria were predetermined by the authors. All prospective and retrospective observational cohort studies that reported treatment outcomes and adverse effects related to bipolar electrocoagulation vs ovarian suture during laparoscopic ovarian cystectomy were included in the present systematic review. Case reports, reviews, and animal studies were excluded. In cases in which data from a particular study sample appeared in more than 1 publication, the article with the most complete follow-up data was used. No language restrictions were used. Any discrepancies between the authors during data collection were resolved by the consensus of all authors.
Literature search and data collection
We systematically searched the literature using the Medline (1966–2015), Scopus (2004–2015), ClinicalTrials.gov (2008–2015), and Cochrane Central Register (CENTRAL) databases as well as the references of the electronically retrieved articles.
Our search strategy included the words bipolar, coagulation, suture, ovarian reserve, AMH, and FSH. We specifically searched PubMed using the MeSH terms (bipolar [All Fields] and (ovarian reserve [MeSH terms] or (ovarian [All Fields] and reserve [All Fields]) or ovarian reserve [All Fields]), (blood coagulation [MeSH terms] or (blood [All Fields] and coagulation [All Fields]) or blood coagulation [All Fields] or coagulation [All Fields] or blood coagulation tests [MeSH terms] or (blood [All Fields] and coagulation [All Fields] and tests [All Fields]) or (blood coagulation tests [All Fields]) and FSH[All Fields].
We also used the terms (blood coagulation [MeSH terms]) or (blood [All Fields] and coagulation [All Fields]) or blood coagulation [All Fields] or coagulation [All Fields] or blood coagulation tests [MeSH terms] or (blood [All Fields] and coagulation [All Fields] and tests [All Fields]) or (blood coagulation tests [All Fields]) and AMH [All Fields] and the terms (blood coagulation [MeSH terms]) or (blood [All Fields] and coagulation [All Fields]) or (blood coagulation [All Fields] or coagulation [All Fields] or blood coagulation tests [MeSH terms]) or (blood [All Fields] and coagulation [All Fields] and tests [All Fields]) or (blood coagulation tests [All Fields]) and (ovarian reserve [MeSH terms]) or (ovarian [All Fields] and reserve [All Fields]) or (ovarian reserve [All Fields]).
Our search strategy is presented in Figure 1 .
Quality assessment
We assessed the methodological quality of all included studies using the Oxford Level of Evidence criteria and the GRADE (Grading of Recommendations Assessment, Development and Evaluation) list. The methodological quality of included randomized controlled trials was also assessed according to the modified Jadad scale using the following criteria: description of the studies as randomized along with details of randomization, description of the studies as double blind, details of the double-blinding procedure, information on withdrawals, and allocation concealment ( Figure 2 ).
Definitions
The levels of AMH, the AFC at 1, 3, 6 and 12 months following the excision of the benign ovarian cyst and the pregnancy rates were predefined as main outcomes. The serum postoperative levels of FSH, estradiol, inhibin, the postoperative ovarian volume, the postoperative PSV, and the postoperative pregnancy rates were predefined as secondary outcomes.
Sutures were described either as intraovarian or parenchymal in all studies. Cases enrolled in the suture group did not receive any form of electric coagulation to achieve adequate hemostasis. In all studies serum samples were collected at day 3 of the menstrual cycle.
Results
Excluded studies
One study was excluded because it compared ovarian cystectomy with ovarian vaporization. Three more studies were excluded because they did not have a control group. Another paper was excluded because it represented a case report, which reported the potential beneficial effect of a gelantine-thrombin-matrix sealant. Finally, 2 more studies were excluded because they compared bipolar electrocoagulation with hemostatic sealant.
Included studies
Eight studies were finally included in our systematic review, which recruited 545 women. Among them, 266 women (48.8%) were treated with bipolar electrocoagulation after the excision of the ovarian cyst, whereas the remaining 279 (51.2%) were treated with hemostatic suturing. In Table 1 , we present the methodological characteristics of these studies. In Table 2 , we present the preoperative levels of serum AMH and FSH. In Table 3 , we present the postoperative outcomes from the studies included in our systematic review.
| Year; first author | Type of study | OLE | n | Age, y | Inclusion criteria | Exclusion criteria | Type of cyst | Cyst size | Hemostasis |
|---|---|---|---|---|---|---|---|---|---|
| 2004; Fedele | Retrospective | 2b | 21 vs 26 | 22 ± 1.5 vs 23 ± 1.9 | Age ≤38 y, previous monolateral gonadectomy with no surgery on the residual ovary, and a follow-up of >12 mo | Irregular menstrual flow (defined as cycle length <25 or >35 d in the 6 mo before surgery) and known endocrine disease | Endometriotic | 1.2 ± 0.4 vs 1.3 ± 0.3 (1) | Bipolar vs suture (2–4 interrupted polyglyconate sutures placed to reaproximate the edges of the ovary) |
| 2009; Li | RCT | 2b | 38 vs 44 | 24 ± 4.2 vs 25 ± 3.9 | Age 18–40 y; uni/bilateral ovarian cyst(s) without clinical and sonographic suspicion of ovarian cancer; regular menstrual cycles defined as a cycle length between 25 and 35 d in the 6 mo before surgery | Prior ovarian surgery; surgical necessity to perform adnexectomy known endocrine disease; postoperative pathologic diagnosis that was not benign ovarian cyst; oral contraceptive use before surgery | Benign ovarian cysts | 6.4 ± 2.1 vs 6.4 ± 2.8 | Bipolar vs suture (3-0 absorbable sutures placed to reapproximate the edges of the ovary) |
| 2011; Mohamed | RCT | 2b | 30 vs 29 | 23 ± 4.1 vs 24 ± 5.2 | No evidence of endocrinologic disorders (normal levels of androstenedione, testosterone, prolactin, FSH, LH, and thyroid-stimulating hormone); no clinical signs or ultrasound evidence suspicious of ovarian malignancy; presence of a unilateral ovarian cyst; regular menstrual cycles (cycle length between 21 and 35 d in the 3 mo before cystectomy) | Previous history of adnexal surgery; polycystic ovary syndrome (Rotterdam); oral contraceptive pill or other hormonal agents within 3 mo postoperative; nonbenign pathology result; endometrioma diagnosed at laparotomy or laparoscopy; cigarette smoking; asthma and use of asthma medications; hypertension; use of any other medication | Benign ovarian cysts | 5.1 ± 2.2 vs 5.6 ± 2.0 (2) | Bipolar vs suture (2-0 polyglactin sutures placed to reapproximate the edges of the ovary) |
| 2011; Coric | RCT | 1b | 22 vs 23 | 30.3 ± 4.4 | Single ovarian endometrioma at least 30 mm; age between 18 and 35 y; regular menstrual bleeding; negative history of any previous gynecological surgical procedures; negative history of hormonal therapy (GnRH or OC) in the last 6 mo | Pregnancy; active PID; genital or extragenital malignancy; combined PCO syndrome and endometriosis; intraoperative diagnosis of another cyst type present; any complication during operation or conversion to laparotomy; GnRH or OC therapy in the follow-up period; pregnancy and irregular attendance of follow-up | Endometriotic | 4.24 (3–6.1) vs 4.28 (3.3–5.9) | Bipolar vs suture (2-0 polyglactin sutures placed to reapproximate the edges of the ovary) |
| 2011; Özgönen | RCT | 2b | 30 vs 30 | 30.1 ± 7.5 vs 30.3 ± 4.6 | 18 and 42 y old | Subsequent ovarian surgery; a very low or high BMI; abnormal menstrual cycles; endocrine disorders; history of previous gynecological operation; history of premature ovarian failure in the family; infertility | Benign ovarian cysts | N/A | Bipolar vs suture (2-0 polyglactin intracorporeal sutures) |
| 2012; Ferrero | RCT | 1b | 50 vs 50 | 31.9 ± 4.0 vs 32.1 ± 3.7 | Women of reproductive age with bilateral endometriomas with largest diameter ≥3 cm | Age ≥40 y; previous ovarian surgery; previous surgery for endometriosis; evidence of polycystic ovary syndrome (Rotterdam), premature ovarian failure, and any other endocrine diseases (such as thyroid dysfunction, hyperprolactinemia or Cushing’s syndrome); bilateral tubal occlusion (hysterosalpingography); uterine malformations; presence of nonendometriotic ovarian cysts; suspicion of malignant ovarian disease; use of hormonal therapies in the 4 mo before inclusion in the study; desire of the patients to use hormonal therapies after surgery | Endometriotic | 7.4 ± 2.9 vs 7.5 ± 2.4 | Bipolar vs suture (2- 0 polyglactin intracorporeal sutures) |
| 2013; Takashima | Retrospective | 2b | 21 vs 23 | 35.35 ± 1.57 vs 36.23 ± 1.89 | No previous history of adnexal surgery; both ovaries present; menstrual cycle range between 25 and 35 d; no clinical signs of hyperandrogenism; BMI in the range of 18–25 kg/m 2 | N/A | Endometriotic | 6.20 ± 0.67 vs 6.70 ± 0.90 | Bipolar vs suture (2-0 monofilament sutures to reapproximate the ovarian parenchyma) |
| 2013; Li | Prospective | 1b | 54 vs 54 | N/A | N/A | N/A | Endometriotic | N/A | Bipolar vs suture (types of sutures were not defined) |
| Year; first author | Preoperative AMH | Preoperative FSH |
|---|---|---|
| 2004; Fedele | N/A | 6.4 (5.5–7.3) vs 5.7 (4.8–6.4) |
| 2009; Li | N/A | N/A |
| 2011; Mohamed | 4.2 ± 1.5 vs 4.6 ± 1.5 | N/A |
| 2011; Coric | N/A | N/A |
| 2013; Özgönen | N/A | 5.72 ± 1.78 vs 5.90 ± 2.03 |
| 2012; Ferrero | 2.3 (0.63–9.45) vs 2.7 (0.68–10.5) | 6.3 (3.7–11.3) vs 6.4 (3.8–11.6) |
| 2013; Takashima | 3.25 ± 1.16 vs 3.48 ± 0.91 | N/A |
| 2013; Li | N/S | N/S |
| Year; author | AMH 1 mo | AMH 3 mo | AMH 6 mo | AMH 12 mo | AFC 1 mo | AFC 3 mo | AFC 6 mo | AFC 12 mo | FSH 1 mo | FSH 3 mo | FSH 6 mo | FSH 12 mo | Pregnancy rates |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 2004; Fedele | N/A | N/A | N/A | N/A | N/A | N/A | N/A | N/A | N/A | 13.7 (5.3–21.9) vs 6.9 (5.9–7.9) | 14.5 (5.6–23.5) vs 6.8 (5.7–8.1) | 15.6 (5.6–25.7) vs 7.3 (5.9–8.7) | N/A |
| 2009; Li unilateral | N/A | N/A | N/A | N/A | 3.4 ± 1.8 vs 3.7 ± 2.1 | 4.2 ± 2.3 vs 5.6 ± 2.4 a | 4.1 ± 2.9 vs 6.2 ± 2.7 a | 3.9 ± 2.5 vs 6.4 ± 1.8 a | S/S | N/S | N/S | N/S | 2 vs 5 |
| 2009; Li bilateral | N/A | N/A | N/A | N/A | 3.1 ± 2.4 vs 3.0 ± 2.1 | 3.7 ± 1.9 vs 4.8 ± 2.3 a | 4.1 ± 2.5 vs 5.9 ± 2.4 a | 4.0 ± 2.1 vs 6.1 ± 2.0 a | S/S | S/S | S/S | S/S | 1 vs 1 |
| 2011; Mohamed | 3.2 ± 0.8 vs 3.7 ± 1.0 a | 2.6 ± 0.7 vs 3.5 ± 1.1 a | 2.4 ± 0.5 vs 3.6 ± 1.1 | N/A | 5.1 ± 1.6 vs 5.8 ± 1.7 a | 4.5 ± 1.6 vs 5.6 ± 1.6 a | 4.3 ± 1.8 vs 5.4 ± 1.6 a | N/A | N/A | N/A | N/A | N/A | 3 (10.0) vs 2 (6.9) |
| 2011; Coric | N/A | N/A | N/A | N/A | 5.0 (2–10) vs 12.0 (9–19) a | N/A | N/A | N/A | N/A | N/A | N/A | N/A | |
| 2013; Özgönen | N/A | N/A | N/A | N/A | 6.9 ± 1.04 vs 7.23 ± 1.38 a | 8.63 ± 1.21 vs 8.60 ± 1.24 | N/A | N/A | 6.63 ± 2.29 vs 5.92 ± 1.49 | 6.96 ± 1.86 vs 6.38 ± 1.92 | N/A | N/A | N/A |
| 2012; Ferrero | N/A | N/S | N/S | N/S | N/A | N/A | N/A | N/A | N/A | S/S | S/S | N/S | 36% vs 30% |
| 2013; Takashima | N/A | 3.16 ± 1.27 vs 2.88 ± 0.83 | N/A | N/A | N/A | N/A | N/A | N/A | N/A | N/A | N/A | N/A | 33.33% vs 30.43% |
| 2013; Li | 1.8 ± 0.9 vs 2.8 ± 1.7 a | 1.8 ± 1.0 vs 2.9 ± 1.6 a | 1.9 ± 1.0 vs 3.0 ± 1.3 a | 2.0 ± 1.0 vs 3.2 ± 1.5 a | N/S | 3.7 ± 1.4 vs 4.8 ± 1.4 a | 4.1 ± 1.4 vs 5.9 ± 1.5 a | 4.0 ± 1.5 vs 6.1 ± 1.5 a | 11.7 ± 4.0 vs 9.3 ± 3.8 a | 9.9 ± 4.0 vs 6.7 ± 3.0 a | 9.5 ± 4.3 vs 6.5 ± 3.2 a | 9.5 ± 3.9 vs 6.4 ± 2.2 a | N/A |
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