Applying the vaginal approach for benign ovarian cystectomy: current evidence and future applications

Vaginal ovarian cystectomy has not gained wide acceptance owing to the potential difficulty in entering the cul-de-sac. We review the current evidence on vaginal approaches to benign ovarian cysts. Outcome measures of interest included time to return to work, patient satisfaction, surgical complications and length of hospital stay. Ten studies were included in this review and involving 525 patients. Vaginal ovarian cystectomy is overall safe and feasible in appropriately selected cases with no evidence of intrapelvic adhesions or endometriosis. These findings will need to be validated in appropriately powered studies, before reliable conclusions can be drawn. Furthermore, we emphasize the importance of ultrasound both preoperatively for case selection optimization and intraoperatively, as a means of guidance during posterior culdotomy.

Vaginal ovarian cystectomy (VOC) refers to the management of ovarian cysts through the vaginal canal [1]. The peritoneal cavity is entered at the pouch of Douglas (POD) or cul-de-sac through an incision at the posterior vaginal fornix allowing access to the pelvic organs [1]. This approach was first described over half a century ago [1] but has not gained wide acceptance by gynecological surgeons. This is secondary to the potential difficulty in entering the peritoneal cavity through the posterior fornix (requiring posterior colpotomy or culdotomy) and its close proximity to the rectum [2]. VOC is not considered the gold standard approach for the management of ovarian cysts and no database exists for clinicians to log their cases for further audit or research analysis. Furthermore, visibility and maneuverability is less when compared with laparotomy or laparoscopy, the latter now being considered the gold standard approach for the management of benign ovarian cysts [2].
Laparoscopic ovarian cystectomy (LOC) is minimally invasive and associated with reduced postoperative pain with a relatively fast recovery period [2,3]. Blind entry laparoscopy using a Veress needle, the preferred entry technique by gynecologists in the UK [4], carries the inherent risk of visceral or vascular injury. General surgeons, by contrast, prefer the open entry technique [5]. Pooled data from 47 randomized trials suggested insufficient evidence to recommend the one entry technique over the other in preventing major visceral or vascular complications [6].
Furthermore, the small abdominal incisions for the insertion of trocars are associated with wound infection, herniation and visible scarring [2,3].
Due to the potential risks associated with LOC, which is driven by a need for alternative minimal access procedures that are economic and is associated with short hospital stay, the interest in VOC has recently been revived. Obviating the need for skin incisions or CO 2 insufflation renders the vaginal approach an attractive alternative option. Over the past decade, a number of studies have been conducted investigating the feasibility of VOC and comparing it with LOC. Few techniques of VOC have been described, with attention to the initial entry in the peritoneal cavity via a posterior culdotomy. This step that can be associated with adverse outcomes secondary to the close proximity to the rectum, particularly in cases of extensive adhesions or endometriosis.
A hybrid vaginal approach for ovarian cystectomy includes natural orifice transluminal endoscopic surgery (NOTES). This combines the benefits of both conventional vaginal and laparoscopic approaches as it avoids visible abdominal scars and allows better visualization and access to the abdominal cavity when compared with conventional VOC [7]. The main challenge of vaginal NOTES is associated with the restriction and conflict between the instruments during single-port surgery [7].
When comparing the different approaches to ovarian cystectomy, the findings are inconsistent when it comes to operating times (OT), rate of cyst spillage, length of hospital stay and degree of postoperative pain. To date, no systematic review has been conducted to clarify the matter. The aim of our study is to critically appraise the evidence and evaluate the feasibility and safety of ovarian cystectomy through the vaginal route, including simple VOC, transvaginal NOTES and other mixed laparoscopic and vaginal approaches. Our secondary aim is to propose a safe, easy and widely accepted step-by-step technique of VOC.

Methods
Search strategy for the identification of eligible studies Institutional review board approval was not necessary as this review did not require any patient identifying information. The systematic search followed PRISMA guidelines [8]. A bibliographic search of English language publications in three computerized databases (PubMed, Science Direct and SciFinder) was conducted. The search was augmented by a snowball strategy, examining the references cited in primary sources and review manuscripts.

Study selection
We reviewed studies where benign ovarian cysts were managed using a vaginal approach. Only studies published in English and in peer-reviewed journals were considered. Because of the scarcity of studies on this topic, any study design was deemed suitable for consideration including nonrandomized and observational studies. Review articles were excluded. There were no exclusions in relation to the country of origin of the study or the date of publication.
The following search terms have been used in all three electronic databases ( The search was conducted by the first author (N Galazis), repeated independently by a second author (S Mappouridou) and cross-checked by a senior author (S Saso). This took place in the first week of September 2019, therefore studies published after this date have not been screened. Our group has conducted numerous literature reviews, therefore we did not seek the assistance of a research librarian for the literature search. The above are summarized in Table 1. The initial search, using the search terms described above, identified a total of 278 records (Medline n = 102, Science Direct n = 79, SciFinder n = 97), where 48 were duplicates. These have been published between 1966 and 2017.

Data extraction
A data extraction spreadsheet was developed and agreed between the authors. The selected studies were comprehensively examined. Relevant data were extracted for each paper and inputted into the spreadsheet by the first  author (N Galazis) and subsequently cross-checked by the second author (S Mappouridou). The information selected included author details, year of publication and country of the study, study aim, sample size, methodology, sample characteristics, outcome measures and conclusions. Disagreements regarding extracted data were resolved by discussion and deliberated on by the most senior author (S Saso). Tables 2 and 3 list the main characteristics of the selected studies.
Outcomes of interest & methodological quality assessment These included OT, length of stay, intra-or postoperative complications, estimated blood loss (EBL), postoperative pain score and rate of cyst spillage. Emphasis was placed on the surgical technique used in each study, particularly of the entry in the peritoneal cavity via the posterior fornix. As mentioned previously, because of the scarcity of relevant studies, nonrandomized studies were also included for the review. For this reason, formal methodological quality assessment of the selected studies was not performed. The above are all summarized in Tables 2 and 3.

Search strategy & study selection
A total of 278 records were screened. The publications screened dated from 1966 to 2017, but the oldest paper included for the final review dated from 2008 [9]. Following an initial screen, 240 studies were excluded due to the title alone and 38 abstracts were retained and examined. From those, 26 abstracts were excluded. They were deemed to be irrelevant to the research question (e.g., ovarian cystectomy was not performed through the vaginal route, not available in English, were animal studies or duplicates). Two papers were included after snowball strategy of other relevant studies [10,11]. Of the 14 full text publications examined, ten met the inclusion criteria [5,[9][10][11][12][13][14][15][16][17]. Of the four studies that were excluded, three were unavailable in English and one was a duplicate study. An overview of the search results and screening process is summarized in the study flow diagram ( Figure 1).

Patient characteristics
The ten studies involved a total of 525 patients, 226 of which underwent VOC via different techniques, while 299 served as controls and had conventional LOC. All studies excluded cases with a possible histological diagnosis of malignant or borderline ovarian tumors. Such exclusion was achieved radiologically by TVUS and, where appropriate MRI and computed tomography (CT), as well as biochemically by checking CA125 in serum. Participants had either simple or complex (albeit benign) ovarian masses such as endometriomas and dermoids, were premenopausal and wished to retain their fertility. Some authors specifically reported suspected adhesional disease and/or obliteration of POD either radiologically or clinically as exclusion criteria [9,13]. One study only included cases of benign ovarian cysts over 10 cm in diameter [14]. Where direct comparison was made between VOC and LOC, there were no significant differences in age and BMI between the two groups. The above are presented in Table 2.

Surgical techniques
Five different surgical approaches have been described in the selected studies. Variations were observed in the technique of entering the POD (blindly, ultrasound [US] or laparoscopic guidance) and the technique of ovarian cystectomy (either by exteriorization of the cyst through the vagina or endoscopic cystectomy). These techniques are summarized below: • Simple VOC: A posterior culdotomy is performed which is further extended digitally to access the ovarian cyst. The cyst is exteriorized vaginally, or aspirated while in the POD before being exteriorized and subsequently enuclated, preserving the healthy ovarian tissue [5]. • Simple VOC with US guidance: A transvaginal US (TVUS) probe with an introducer is placed in the vagina.
A needle passed through the introducer is used to puncture the posterior vaginal fornix and enter the POD [9] or directly enter the cyst [11,16] under US guidance. A balloon is inflated, allowing safe extension of culdotomy, after which the cyst is exteriorized and enuclated as per simple VOC. • Laparoscopically-assisted VOC: Three-port laparoscopy to allow drainage of cyst contents. Posterior culdotomy is performed laparoscopically, after which the collapsed cyst is exteriorized vaginally and enuclated as above. This technique was used for cysts over 10 cm in diameter [14]. • Transvaginal and laparoscopic VOC: Single umbilical laparoscopy at 10 mmHg of CO 2 insufflation guides vaginal culdotomy. Two trocars inserted via the posterior fornix and graspers used to perform cystectomy endoscopically. The specimen is retrieved vaginally using an endopouch [10]. • Vaginal NOTES: Posterior culdotomy is performed and three trocars are introduced in the POD. Two graspers and a scope are used through the three trocars and after pneumoperitoneum is created, the cyst is either enuclated     and retrieved using an endopouch [15,17] or aspirated endoscopically following which it is exteriorized. Enuclation is performed similar to simple VOC [13].

Main findings
Ovarian cystectomy through the vaginal route was associated with reduced postoperative pain and higher satisfaction levels when compared with LOC in two retrospective case-control studies [5,13,15]. Similarly, time to return to work was demonstrated to be significantly reduced in VOC when compared with LOC [5]. Loss of income and productivity due to delayed return to work was calculated to £648 and £1869 for VOC and LOC, respectively [5]. Conversely, when a cost analysis was performed by Wang et al., who compared outcomes of ovarian cystectomy via NOTES versus laparoscopy, no significant difference was observed [13]. Overall, no complications have been reported aside from one case of rectal injury requiring defunctioning colostomy. That was a case of severe endometriosis with obliteration of the POD when culdotomy was performed without US guidance [5].
In all but one case, cystectomies have been completed through the vaginal route, where conversion to laparoscopy was required to achieve hemostasis [11]. Spillage seems to have been avoided or reduced in the selected studies. One case-control study by Yoong et al., involving 49 patients (28 treated vaginally and 21 laparoscopically) reported a significant reduction of cyst spillage (6 vs 35%; p < 0.001) [5]. Furthermore, another case-control study evaluating the feasibility of NOTES, reported draining of the cyst contents under direct vision, before exteriorizing the cyst and dissecting it off the ovary [13].
The mean OT varied between different technique of VOC. Yoong et al. reported a mean OT of 91.7 min with simple VOC versus 78 min with LOC (p < 0.001) [5]. On the contrary, Wang et al. reported a reduction in OT (38 vs 54 min; p < 0.001) with NOTES versus conventional LOC [13]. Tanaka et al. did not report any significant difference in the OT between the two approaches [11]. Finally, Wang et al., who performed laparoscopic-assisted VOC for large ovarian masses (10-27 cm) and Ding et al., who performed NOTES, reported mean OT of 62 and 74 min, respectively [14,15].
Five studies reported their EBL [5,10,[13][14][15]. Yoong et al. reported a statistically significant increase in EBL in the simple VOC group compared with LOC (116 vs 95 ml; p < 0.001) [5]. Wang et al. also demonstrated a statistically significant increase in the EBL between NOTES and LOC (31 vs 21 ml), p = 0.028 [13]. These differences, however, are of no clinical significance. Moreover, Tanaka et al. reported a 5% incidence of dyspareunia and postcoital bleeding a month after VOC, which completely resolved at the 2-month follow-up [12]. Table 3 provides more details on the study characteristics, the different surgical techniques used and results.

Discussion
This review presents the current evidence on the effectiveness of ovarian cystectomy through the vaginal route. The number of studies is limited, which prevents us from drawing definitive and reliable conclusions. However, these preliminary findings demonstrate that VOC could provide a safe and feasible alternative option to the conventional laparoscopic approach. More, large-scale studies will, however, need to be performed before reliable conclusions can be drawn. Only ten studies have been published on this topic, indicating that this approach has not been widely adopted by gynecologists. Various techniques have been described for the treatment of benign ovarian cysts through the vaginal route, ranging from a simple VOC to laparoscopic-assisted VOC and transvaginal NOTES. Each technique requires different skill sets as well as novel equipment. For example, Tanaka et al. have developed culdotomy techniques using a TVUS probe with an introducer for needles, guide wires and catheters [9,11,12].
Accessing the peritoneal cavity safely through the POD and subsequently locating and exteriorising the ovary through a confined surgical field are the main challenges of ovarian cystectomy through the vagina. Tanaka et al. performed TVUS intraoperatively, allowing them to safely enter the POD via a posterior culdotomy and access the affected ovary [9,11,12]. Unguided posterior culdotomy, on the other hand, resulted in a rectal injury requiring major corrective surgery and prolonged hospitalization in a case of severe endometriosis [5]. From the abovementioned, it appears that US guidance improves the safety of VOC by ensuring that there is no bowel adherent to the posterior aspect of the uterus. Furthermore, TVUS has the potential of enhancing visualization and localization of the ovaries during an otherwise blind procedure. The disadvantage of Tanaka et al.'s technique is that TVUS guidance requires specialist equipment including a trans-vaginal probe that can receive guide wires and catheters, which are expensive and not readily available in most hospital settings [9,11,12].
Other approaches -described above -such as laparoscopic-assisted VOC, transvaginal-laparoscopic VOC and vaginal NOTES, involve pneumoperitoneum and abdominal incisions, which defeat the purpose of managing benign ovarian cysts vaginally to minimize postoperative pain and improve recovery. Furthermore, they involve conventional and/or specialist laparoscopic equipment, which are associated with increased operative costs. The main challenge of vaginal NOTES is associated with the restriction and conflict between the instruments during single-port surgery [7]. Moreover, the need to perform surgery from the opposite end of the patient compared with conventional laparoscopy requires different hand-eye coordination and ergonomic skills [18].
An increased incidence of bladder injury has been described in vaginal adnexal surgery, particularly in cases of previous cesarean section [19]. However, this is a concern in extensive/advanced NOTES such as hysterectomy [19]. No bladder injury was reported in the studies where ovarian cystectomies were performed vaginally as the peritoneal cavity was entered through the POD. The ovaries were then immediately accessed without too much manipulation and operating in the anterior pelvic compartment, namely, the uterovesical fold.
Identifying cases at risk of intrapelvic adhesions and endometriosis can be achieved by thorough clinical history and physical examination assessing the mobility, shape of uterus and the presence of endometriotic nodules in the POD and uterosacral ligaments. Furthermore, the use of the International Ovarian Tumour Analysis rules should guide clinicians distinguish benign from borderline and malignant ovarian tumors during preoperative TVUS [20]. Cases suspicious of borderline or malignant ovarian tumors should not be offered the vaginal approach, as the minimal visibility of the rest of the pelvis and abdomen will prevent adequate surgical staging of the disease.
Moreover, preoperative TVUS is the first-line imaging modality for the diagnosis of pelvic endometriosis with high specificity and sensitivity demonstrated in the case of endometriomas [21][22][23][24]. Recent evidence suggests that adhesions can be accurately evaluated by real-time dynamic TVUS, using the sliding sign technique. This can determine whether the uterus and ovaries glide freely over the posterior and anterior organs and tissues [25].

Proposed clinical application
Transabdominal US (TAUS) guidance has been described in other gynecological procedures such as complex hysteroscopic surgery for uterine fibroids and septoplasty [26][27][28][29]. The authors of these papers have found that intraoperative US assisted in safe entry in the endometrial cavity and ensured complete resection of the disease with no complications such as rectal or bladder injury. Ma et al. performed TAUS-guided transvaginal hydrolaparoscopy in women with subfertility [30]. TAUS guidance allowed safe entrance in the POD including cases with retroverted uterus. The authors reported no complications with TAUS guidance, while in the comparison group (transvaginal hydrolaparoscopy without TAUS guidance), there were three cases of bowel perforation and one case of uterine injury [30].
We, therefore, advocate the use of TAUS guidance during posterior culdotomy, and access and retrieval of the affected ovary. An US machine with a trans-abdominal probe is readily available in a modern hospital setting and does not require further specialized equipment or additional costs. From a practical perspective, it allows the surgeon to operate vaginally without having additional equipment (e.g., a TVUS probe and wires) directly into their operating field. TAUS can be performed by a gynecology trainee with adequate experience and when necessary with guidance from the operating surgeon while the patient is in the lithotomy position.
For better sonographic evaluation of the uterus, the urinary bladder can be instilled with sterile water or saline solution up to 300 ml and the catheter clamped. In cases of suspected adhesions during preoperative TVUS or from the clinical history, the POD can be instilled with sterile water or saline up to 500 ml via the cervical OS and through the fallopian tubes. Fluid in the POD acts as a contrast medium and optimizes sonographic views by separating the posterior fornix from the rectum, allowing safe posterior culdotomy and minimizing the risk of bowel injury [26][27][28][29]. Following infiltration of local anesthetic with adrenaline to the posterior fornix, a 1-cm incision is made. The presence of fluid draining will reassure the surgeon of the correct site of the culdotomy. Alternatively, prior to posterior culdotomy, infiltration of the posterior fornix and aspiration of saline will confirm entry in the POD. Insertion of a Simm's speculum through the incision can assist in retracting the rectum posteriorly away from the surgical field. The surgeon can extend the incision laterally using their fingers up to 3 cm to allow access and insertion of instruments. The ovary can be retrieved under TAUS guidance and exteriorized before the cyst is dissected off the healthy ovarian tissue. Doppler US can be used to identify pelvic side wall vasculature and minimize vascular injury. At the end of the procedure, any instilled fluid is drained from the bladder and POD. Our proposed clinical application of TAUS-guided VOC is summarized in Figure 2. Haemostasis is ensured, any instilled fluid is drained from the bladder and POD and culdotomy is sutured routinely

Limitations
This was a thorough review evaluating the safety and feasibility of ovarian cystectomy through the vaginal route. Various techniques and study designs have been described. In addition, a small number of studies and patients have been evaluated in this review which precludes us from drawing reliable conclusions at this stage. However, the findings are promising and provide justification for larger, appropriately powered and standardized studies (ideally randomized-controlled trials) in order to be able to draw definitive conclusions.
Most of the procedures described are relatively novel and therefore, the surgeons performing them may have been at an early phase in their learning curve. In addition, US technology and operators' scanning skills have significantly evolved over the past decade. These statements suggest that the role of intraoperative US may not be fully appreciated with the current improved technology and skillset. By and large, the studies assessed in this review, described procedures performed by experienced surgeons. It would be interesting to evaluate surgical outcomes of VOC with and without intraoperative US according to surgeons' experience and capability, to determine which surgeons would benefit the most from it.
Finally, some studies used specialized equipment and US probes not readily available to most hospital settings, including specialized vaginal US probes [10,12,13]. Therefore, the proposed surgical techniques cannot be easily replicated by surgeons around the world. On the other hand, our proposed technique utilizes standard US probes and equipment that are universally accessible in a modern gynecological setting. A proof-of-concept study, followed by large-scale trials will need to be performed to evaluate this proposed technique.

Conclusion
VOC is an alternative minimally invasive technique for the treatment of benign ovarian cysts in appropriately selected cases based on their risk of intra-pelvic adhesions or endometriosis. Current evidence is promising in terms of patient safety, satisfaction and effectiveness but more studies will need to be conducted before reliable conclusions can be drawn. A variety of techniques have been described in the literature, some requiring specialized equipment. Our proposed modified technique offers an approachable and feasible option that will need to be evaluated in appropriately powered clinical trials.

Future perspective
As the search for alternative, cost-effective and minimally invasive procedures for the management of benign ovarian cysts ensues, we anticipate more experimentation and publications in this topic. This review should therefore act as a point of reference for future research on the subject. Moreover, the improved skills in US scanning should contribute to better selection of patients preoperatively. In addition, intraoperative US as described in our novel approach could be utilized to potentially reduce the risk of visceral injury when entering the cul-de-sac and thus further promote the vaginal approach.

Background
• Vaginal ovarian cystectomy (VOC) refers to the management of ovarian cysts via a culdotomy to access the pouch of Douglas. • Although a well-described procedure, it has never gained wide acceptance among gynecologists.
• We review the current literature to assess the role of VOC as another minimally invasive alternative to laparoscopic ovarian cystectomy. Methods • Thorough the literature search was conducted through various electronic databases.
• Hand-searching through the references of relevant studies was also conducted.
• All study designs were eligible for this review.
• Outcomes of interest included operating time, length of stay, complications, costs, etc.

Results
• Ten studies were included for this review involving a total of 525 patients.
• Various surgical techniques have been used by the different studies, whereby ovarian cysts were removed vaginally. • Overall, the authors reported favorable outcomes with VOC in regard to: postoperative pain, safety, time to return to work. • Other outcomes such as operating time and estimated blood loss were inconclusive when VOC was compared with laparoscopic ovarian cystectomy.

Discussion
• Overall the findings are promising and provide justification for appropriately powered studies before reliable conclusions can be drawn. • VOC could be performed in appropriately selected cases. • Preoperative transvaginal ultrasound plays an important role in case selection.
• Intraoperative transabdominal ultrasound can be a useful adjunct in VOC, particularly in reducing the risk of rectal injury during culdotomy. • A proof-of-concept study should be carried out in the near future.

Conclusion & future perspective
• VOC as an alternative minimally invasive option should be explored further to assess its feasibility, safety and cost-effectiveness.