Minimally Invasive Surgery in Gynecologic Oncology: A Review of Modalities and the Literature

Abstract

Minimally invasive surgery is one of the newest and most exciting areas of development in procedural medicine. This field shows tremendous potential to increase therapeutic benefit while minimizing some of the painful or dangerous side effects of surgical interventions. Minimally invasive surgery has strong historic ties to the field of gynecology and has come a long way as technology and techniques have improved. This has increasingly allowed the application of laparoscopy to more complex procedures and the treatment of gynecologic malignancies. Three laparoscopic approaches, traditional laparoscopy, robotic assisted laparoscopy and laparoendoscopic single-site surgery are reviewed here. We discuss the basic approaches to these three laparoscopic techniques, and then review their applications in gynecologic oncology. We also touch on the evidence behind outcomes associated with their use.

Keywords

cervical carcinoma endometrial carcinoma gynecologic oncology laparoendoscopic single-site surgery laparoscopy minimally invasive surgery ovarian carcinoma robotic surgery

Minimally invasive surgery (MIS) is one of the most exciting frontiers in medicine. Smaller incisions, more advanced technology and newly acquired surgical skills and techniques allow us to offer improved cosmesis, minimal pain, a quicker recovery and better outcomes. Tarasconi performed the first traditional laparoscopic (TL) removal of an organ, a salpingectomy, in 1975 [1]. Gynecologists continued to push the limits of laparoscopy to perform more advanced procedures and surgeries beyond the scope of gynecology, for example, one gynecologist unpopularly performed the first TL appendectomy [2]. The first TL hysterectomy was performed in 1988 by Harry Reich [3]. For many procedures, MIS is now the standard of care. The American Association of Gynecologic Laparoscopists released a position statement that said “surgeons without the requisite training and skills required for the safe performance of vaginal or laparoscopic hysterectomy [on an appropriate patient] should enlist the aid of colleagues who do or should refer” [4].

Novel approaches to laparoscopy have been developed, including laparoendoscopic single-site surgery (LESS) and robotic-assisted laparoscopy (RAL). The first LESS procedure was a bilateral tubal ligation performed by Wheeless in 1969 [5]. Pelosi and Pelosi performed the first LESS appendectomy and LESS supracervical hysterectomy with bilateral salpingoophorectomy (BSO) in 1992 [6,7]. A robotic approach to gynecologic procedures has become increasingly popular since the first RAL hysterectomy with BSO and staging for ovarian cancer was reported [8].

As techniques and technologies continue to improve, it will become feasible to perform more and more procedures less invasively. This is never more pertinent than it is in the gynecologic oncology (GON) cancer survivor who often requires the most extensive procedures but will benefit considerably from a quick recovery and minimized morbidity. In this article we will briefly review the applications of, and evidence behind, the MIS in GON, specifically TL, RAL and LESS.

Description of approaches to laparoscopic MIS

Laparoscopy involves the introduction of ports through a patient's abdominal wall to visualize and manipulate the organs in the abdominal cavity. Maintaining awareness of basic anatomic principles, TL allows for multiple different entry points in the abdominal wall, allowing the surgeon freedom to determine the position and size of the trocars depending on the procedure and obstacles anticipated. The rigid instruments usually have one point of torque at the abdominal wall that affords some indirect tactile feedback, but limits the ease with which complex movements are made. The visualization is 2D, potentially limiting the surgeon's understanding of spatial relations. However, the pneumoperitoneum distends the internal abdomen and the angle and proximity of the scope to the pelvic organs, often allowing for excellent visualization. The TL approach is appropriate in patients who can tolerate insufflation and trendelenberg and who do not require a larger incision for palpation of abdominal contents, removal of a specimen or safe entry.

Robotic assistance can be used for patients who are otherwise TL candidates and can tolerate steep trendelenberg and accommodate four to five abdominal port sites. The midline optic trocar is placed 20–27 cm above the pubic symphysis. Four to five additional trocars are placed laterally to the midline trocar, one remaining open for the bedside human assistant. The robotic system consists of four parts: the surgeon console, the patient side cart, detachable instruments and a 3D visual system. The surgeon sits comfortably at the console and has a 3D view, providing an appreciation for objects in space unique to RAL. The patient side cart accommodates and positions the detachable instruments, each with seven degrees of freedom, enabling versatile and complex movements. Surgeon tremor is filtered out and large movements by the surgeon's hands translate into delicate and precise movements at the site of surgery. The advantages this offers in terms of dexterity, accuracy, visualization, instrumentation and surgeon comfort have caused many to endorse RAL for complex GON procedures [9,10]. However, RAL is also costly, time consuming, bulky and lacks tactile feedback.

LESS involves a hason-like entry at the base of the umbilicus, an anatomically privileged location remote from most vessels and nerves. Advocates argue that it is safer than laparoscopic approaches that require incisions in multiple sites that are more vulnerable to neurovascular injury. Patients who may not be good candidates for LESS include those with greater than two midline vertical incisions in the past, a non-native umbilicus, such as after an abdominoplasty or panniculectomy, advanced carcinoma, or a uterus larger than 16 weeks in size. Morbidly obese patients can also be challenging. For the cancer surgeon, the larger umbilical incision can accommodate larger masses minimizing drainage and manipulation. This may potentially reduce the risk of spillage and contamination of the peritoneal cavity with malignant cells. Furthermore, it is more amenable to palpation of the abdominal contents via a hand-assisted laparoscopic surgery port or by accommodating the surgeon's fingers into the abdomen or some abdominal contents, such as a loop of bowel, briefly up through the incision. The introduction of multiple instruments through a single incision requires the surgeon to overcome awkward posturing and instrument clashing and learn new techniques such as intracorporeal crossing. Intstruments and ports utilized with LESS are illustrated in Tables 1 & 2.

Table 1.

Advanced laparoscopic equipment useful for laparoendoscopic single-site surgery.

LESS instrument	Description
Real Hand™ (Novare Surgical Systems, CA, USA)	Utilizes mechanism to mirror directionality of the surgeon's movements
	Provides tactile feedback
	Offers seven degrees of movement
	Economically designed handle with single-hand locking mechanism
Autonomy™ Laparo-Angle™ (Cambridge Endo, MA, USA)	Offers seven degrees of movement
	Maps the motion of the surgeon's hand
	Offers an axial rotating knob with tip orientation locking mechanism
	Instrument tip moves in tandem with surgeon's palm
Autonomy Laparo-Angle Metzenbaum Scissors (Cambridge Endo)	Utilizes flexible and locking technology, allowing several degrees of motion
Autonomy Laparo-Angle Needle Holder (Cambridge Endo)
	Articulating tool with the ability to lock and allow needle driving while suturing and knot tying
	Requires high precision from surgeon
	Steep learning curve
HD EndoEYE® Camera (Olympus Corporation, Japan)	Offers all-in-one focus
	Economically designed
	Available in 45° scopes

LESS: Laparoendoscopic single-site surgery.

Table 2.

Laparoendoscopic single-site surgery port sites.

Port type	Manufacturer	Advantages	Disadvantages	Trocars
TriPort™ (‘R-Port’)	Advanced Surgical Concepts (Ireland)	Can be deployed through incisions between 12 and 25 mm	Requires umbilical port placement	Three ports: two 5-mm ports, one 12-mm port
		Multiple instruments can pass without loss of pneumoperitoneum	Easily dislodged with loss of pneumoperitoneum
		Straightforward technique for introduction into abdomen	Sheath is easily torn necessitating replacement of device
		Able to use on a variety of abdominal wall thicknesses
		Allows wider distances between instruments in abdomen due to larger angles of distraction
AirSeal®	SurgiQuest (CT, USA)	Allows for passage of multiple/large instruments, extracorporeal knot tying and specimen removal without loss of pneumoperitoneum	Long fulcrum associated with 12-mm port limiting instrument movement	One 12-mm
		Maintains exposure during suctioning	Noise associated with pressure barrier	AirSeal port
		Automatic smoke evacuation
		Provides ability to utilize ports of different shapes and sizes
SILS™ port	Covidien (Ireland)	Compressibility of port allows for expansion of access ports to ‘custom fit’ the space being used		Allows up to three instruments: three 5-mm vs two 5-mm and one 12-mm cannula
		Flexible channels for instruments
Uni-X™	Pnavel Systems (NJ, USA)	Allows for simultaneous use of three 5-mm instruments	Requires fascial fixation sutures	Three 5-mm instruments
		Wide range of motion	Curved, articulating instruments preferred when using multiple instruments through one incision
Hunt cannula/trocar	Apple Medical (CT, USA)	Threaded cannula precedes need for fascial sutures	Each port requires separate fascial puncture	Three or four ports: 5 mm or smaller
			Nonadjustable
GelPort®	Applied Medical (CA, USA)	Creates ‘flexible fulcrums’ that allow greater movement	Can create multiple fascial punctures through single incision during instrument placement	Three to five ports: 5–10 mm
		Minimal interference between instruments

Applications of MIS in GON

The data is in favor of TL simple hysterectomies with BSO and pelvic and para-aortic lymph node dissection (PPALND) in the surgical staging of clinically early endometrial cancer. The largest randomized controlled trial to evaluate this was LAP-2, a Gynecologic Oncology Group Study that randomized patients to open or TL endometrial cancer staging and analyzed the safety and quality of life after the procedure. LAP-2 demonstrated improved safety and quality of life in patients who underwent TL staging without any detrimental effect on detection of advanced disease [11,12]. Given the promising results of TL, one could extrapolate that RAL endometrial cancer staging does similarly well, but there is only observational data to support this. The improved visualization, ergonomics and ease of complex, precise maneuvers have led many to speculate that RAL is associated with fewer conversions and is safer and more effective than TL. This has not yet borne out in randomized trials, which are anxiously awaited.

LESS in the treatment of endometrial cancer is novel and good data is lacking. A recent pilot study reported on 20 patients who underwent LESS hysterectomy and BSO for early endometrial cancer with excellent perioperative outcomes and no conversions; staging was not performed [13]. A matched retrospective cohort study of 90 patients demonstrated similar operating times, hospital stays, complication rates and blood loss for patients who underwent LESS, TL or RAL endometrial cancer staging including hysterectomy, BSO and PPALND when indicated [14]. Larger comparative studies, and hopefully randomized controlled trials, will make any advantages of this technique clear.

A recent review of published data comparing RAL to TL radical hysterectomy (RH) with PPALND for early-stage cervical carcinoma concluded that both procedures are feasible, safe, and adequate, but called for more randomized controlled trials. The authors of this review point out the difficulty interpreting the current data given the small numbers for most RAL procedures and that outcomes may improve as surgeons gain experience with this RAL, RH and staging [15]. The amount of vaginal cuff and parametrial tissue obtained at the time of RH appears to be similar between TL and RAL [16]. Many would argue that the complexity of the procedure would make RAL the preferred MIS approach, but this, again, is still speculation.

Laparotomy for ovarian cancer debulking is commonplace, especially given the extensive nature of most diseases at presentation. However, in well-selected, early-stage disease, attempting an MIS approach is an acceptable approach [17,18]. While TL debulking is not always feasible, the use of exploratory laparoscopy to diagnose, triage and debulk appropriate patients is an option. In one report of 32 patients with the International Federation of Gynecology and Obstetrics stage 2C or greater ovarian cancer who were evaluated with TL prior to their debulking procedure, 17 patients were laparoscopically debulked, 88.2% of whom were cytoreduced to less than 0.5 cm. Notably, comorbid medical conditions, not technical inability, accounted for the two that were not optimally cytoreduced [19]. The first RAL hysterectomy with BSO on a human was part of a RAL ovarian cancer staging including PPALND and an infracolic omentectomy [8]. In a retrospective case–control analysis comparing TL, RAL and open ovarian cancer debulking, Magrina et al. conclude that RAL or TL is preferable for tumor excision and one additional major procedure, but as more procedures are required for debulking, benefit from a MIS approach is lost and laparotomy is preferred [20]. A LESS approach to surgical treatment of early-stage ovarian carcinoma has been described, but comparative data are not available [21].

Lymph node dissections are commonplace in the surgical treatment of gynecologic malignancies. Lymph node counts are a common indicator of surgical adequacy. Randomized controlled trial data from LAP-2 demonstrated that while lymph nodes were less likely to be removed in the TL group, TL detects advanced endometrial cancer in patients with early clinical disease at the same rate as laparotomy [11]; data are otherwise rather inconsistent. The interpretation of lymph node counts obtained in nonrandomized, comparative studies is problematic as these observational studies are riddled with biases owing to a particular surgeon's skill level, preference for a method, the extent to which a disease dictates the approach used, and techniques and technology available at the time of the study. Some comparative studies demonstrate a greater lymph node yield for RAL procedures [22 –26], others favor an open procedure [27 –30] and others favor TL [31]. Still, many studies have failed to show a difference in numbers of lymph nodes obtained between modalities [9,20,32 –40]. Comparative data are considerably lacking, but LESS lymphadenectomies appear to yield similar lymph node counts to other techniques, with one series reporting a median pelvic lymph node count of 14, ranging from seven to 19, and a median para-aortic node count of six, ranging from two to 14 [41]. This may be more challenging in obese patients, but a lateral position with the left flank up has been described as a means to work around this [41]. One recent matched retrospective cohort study reports LESS lymph node yields to be similar to RAL and significantly better than TL [14]. Furthermore, extraperitoneal lymph node dissection has been reported and appears to be feasible and safe both via TL [42], RAL [43] and LESS [44,45].

Some of our most extensive procedures can be performed via MIS. Delicate and precise procedures such as fertility-sparing radical trachelectomies or parametrectomies have been performed via advanced laparoscopy and robotics [46,47]. Even the largest, most extensive procedures have met a MIS approach. Pelvic exenteration for gynecologic malignancy has been described in the literature as feasible to perform via TL [48,49] or RAL [50].

Outcome measures of MIS in GON

Observational outcome data should be interpreted with caution. Many of these studies are retrospective or use historic controls, making the influence of changes in practice and outcomes with time being difficult to control for. Furthermore, particularly skilled MIS surgeons, sometimes with more or less training in a given modality, often perform these trials, potentially biasing results. Finally, there is a selection bias that results from the publication process, with success rates more likely to be reported if they are optimistic. Nonrandomized comparative studies are useful for hypothesis generation, but not for drawing conclusions about causality. True differences are elucidated by randomized controlled trials, but these rare studies are cumbersome to perform. Below is a summary of the outcomes data that are available thus far for these three MIS modalities in GON. Table 3 highlights studies comparing RAL and TL in GON.

Table 3.

Robotic-assisted laparoscopy compared with traditional laparoscopy in the surgical management of gynecologic malignancies.

Study (year)	OR time	EBL	Hospital stay	Lymph node counts	Conversions	Intraoperative complications	Postoperative complications	Ref.
Simple hysterectomy and staging for endometrial cancer
Veljovich et al. (2008)	–	–	–	–	–	Not measured	–	[36]
Gehrig et al. (2008)	RAL	RAL	RAL	RAL	–	–	–	[24]
Boggess et al. (2008)	RAL	RAL	RAL	RAL	–	–	–	[22]
Bell et al. (2008)	–	–	–	–	Not measured	–	RAL	[37]
Seamon et al. (2009)	RAL	RAL	RAL	–	RAL	–	–	[34]
Jung et al. (2010)	–	Not measured	–	RAL	–	–	–	[28]
Cardenas-Goicoechea et al. (2010)	TL	RAL	–	–	–	–	–	[35]
Lim et al. (2010)	RAL	RAL	RAL	TL	–	RAL	–	[29]
Lim et al. (2011)	RAL	RAL	RAL	TL	RAL	RAL	RAL	[31]
Radical hysterectomy and staging for cervical cancer
Magrina et al. (2008)	RAL	–	–	–	–	–	–	[51]
Estape et al. (2009)	–	–	–	RAL	Not measured	–	–	[26]
Sert and Abeler (2011)	RAL	RAL	RAL	–	Not measured	–	–	[27]
Tinelli et al. (2011)	RAL	–	–	–	–	–	–	[33]
Ovarian cancer debulking
Magrina et al. (2011)	TL	–	–	–	Not measured	–	–	[20]

–

No significant difference; EBL: Estimated blood loss; OR: Operating room; RAL: Findings favored robotic-assisted laparoscopy; TL: Findings favored traditional laparoscopy.

Success rates & need for conversion

Simple and radical TL and RAL hysterectomies with staging for cancer are now routinely performed. In the LAP-2 trial, in patients with clinical stage 1–2A endometrial cancer, the conversion rate for TL surgical staging to laparotomy was 25.8 %, with the most common reason for conversion being visibility [11]. With rare exceptions [39], most observational studies report a much lower conversion rate of 0.0–6.1% for TL hysterectomies and staging [28,29,31,33,51]. RAL hysterectomies with staging have been reported with conversion rates of 0.0–15.6% [23 –25,28,29,33 –35,38,40,51]. Theoretically, the ergonomic and visual advantages of RAL would lead to fewer conversions compared with TL, but comparative data is inconsistent. However, some studies suggest a more favorable conversion rate for RAL compared with TL [31], especially in obese women [39]. Ovarian carcinoma is still frequently treated via an open approach. A series of TL debulking of apparent stage 1 ovarian cancers with no conversions have been reported [17,52]. Not surprisingly, for patients with more advanced ovarian cancers, much higher conversion rates are reported [19].

In the hands of skilled laparoscopic surgeons, initial LESS performance data is promising. Performing LESS for benign and malignant gynecologic surgeries, Fader et al. reported a 96% success rate, needing to convert one case to TL for adhesions and to laparotomy in two patients because of metastatic ovarian cancer [21]. LESS for extraperitoneal lymph node dissection has been reported with a success rate of 92.9% [44]. Furthermore, an attractive feature of LESS is that when conversion is needed, the surgeon has a choice between inserting additional ports for TL or extending the umbilical incision to perform an exploratory laparotomy.

Operating times

Studies comparing operating room (OR) times for TL, RAL and open GON surgical staging procedures are consistently inconsistent. For simple hysterectomies and staging for endometrial cancer, most comparative studies favor the RAL approach for OR time [22,24,29,31,38], but some have demonstrated no difference [28,37], and at least one favors TL [35]. Most of the RH and staging procedures for cervical cancer favor a RAL over TL with regards to OR time [27,33,51], but some studies show no difference [26]. In early ovarian cancer debulking, the data are still limited and inconsistent comparing TL with laparotomy [17,52]. A retrospective case–control study reported the fastest ovarian cancer debulkings by laparotomy followed by TL and then RAL [20]. Comparative data for OR time for LESS compared with other applications is still incomplete and premature.

Estimated blood loss

The bulk of the endometrial cancer data associates RAL staging with a lower estimated blood loss (EBL) and less blood transfusions compared with open surgery [28,34,38] and TL [35,39]. RAL RH and staging for cervical cancer are associated with less blood loss than laparotomy [23,26,27,30,32,40,51]. However, studies comparing RAL to TL RH are inconclusive with some showing less EBL with RAL [27], but others showing otherwise [23,26,27,30,32,40,51]. TL staging of apparent early-stage ovarian cancers is associated with a lower EBL than laparotomy [17]. RAL ovarian cancer debulking has been associated with a lower EBL than open surgery, but not TL [20]. Again, LESS data is promising in this regard, but most of the comparative data is in benign gynecology. When retrospectively compared with TL, LESS hysterectomies are associated with less blood loss [53]. A recent randomized controlled trial comparing LESS to TL for benign adnexal disease demonstrated that the LESS approach resulted in one-third the blood loss associated with TL, and that LESS provides an advantage over conventional multiaccess laparoscopy in terms of postoperative pain and the need for rescue analgesia, with similar perioperative outcomes [54].

Complication rates

Most data and clinical experience favor MIS for its complication profile compared with laparotomy. Randomized controlled trial data demonstrates similar intraoperative but improved postoperative complication rates with TL endometrial cancer staging compared with laparotomy [11]. Regarding randomized trial data, one could extrapolate from LAP-2 and assume that RAL endometrial cancer staging procedures have fewer complications than laparotomy, and multiple observational studies would support this hypothesis [22,25,28,34,37,38]. This has not been demonstrated in studies comparing open surgery, RAL RH and staging for cervical cancer [26,27,30,32,51]. Fewer complications have been observed in small studies of TL treatment for apparent stage 1 adnexal cancers [17], but this association was not observed in advanced disease [20].

Comparing various MIS modalities, observational studies have mostly found no differences. Some studies have demonstrated a complication profile favoring RAL over TL hysterectomy, BSO and staging for endometrial cancer [27 –29,31,33,35,37], but, more commonly, no difference was observed [22,24,26,39,51]. Similarly, no difference was seen when comparing TL with RAL for staging of cervical [26,27,51] or ovarian cancer [20].

The complication rate for LESS appears low. In one of the largest series of LESS gynecological procedures to date, a review of 74 women who underwent LESS for benign or early-stage cancer, there were no intraoperative complications and only three perioperative complications: a pulmonary embolism, vaginal cuff dehiscence and incisional cellulitis [21]. In benign gynecology, a retrospective study [53] and a randomized controlled trial [54] of LESS have demonstrated no difference in complication rates compared with TL.

Incisional complications

After primary laparotomy for a gynecologic malignancy, incidence of ventral hernia has been reported to be 8.8% [55]. Incisional hernias have an incidence of 0.2–3.1% after major TL procedures [56]. One criticism of the LESS approach has been that the larger umbilical incision may put patients at higher risk for umbilical hernia formation [57]. Thus far, umbilical hernias after LESS seem to be rare and comparable to TL, with a reported incidence of 2.4% [58]. While there are some retrospective data that incisional bowel herniation after laparoscopy tends to occur through ports >10 mm in size [59], there is no evidence that one 1–4 cm incision places the patient at more or less risk for incisional hernia than multiple trocar sites, often including at least one >10 mm. The slightly larger incision may convey risk or allow for a more secure closure. In lieu of stronger comparative data, it seems reasonable to conclude that MIS approaches overall are associated with a lower incisional hernia rate than laparotomy. The ideal MIS modality remains to be determined.

Port-site metastases have an incidence of 0.97–2.3%, but are more likely in women undergoing surgery for disseminated carcinoma, especially in the setting of ascites, synchronous intrabdominal metastases and advanced or recurrent disease [60 –62]. Theoretical causes and means of preventing this have been reviewed, but have not been evaluated in clinical trials [61]. In theory, the risk is minimized with fewer ports, but again, prospective trials comparing TL, RAL and LESS are called for.

Enhanced cosmesis

One of the market-driving forces behind MIS in all surgical fields, including GON, is enhanced cosmesis. Patients have abetter body image after laparoscopy than open endometrial cancer staging [12]. Proponents of LESS claim that the single incision at the umbilicus is cosmetically preferable to multiple incisions. Early critics pointed out that this was based on surgeon assumption not patient preferences [57]. However, recent survey data and randomized controlled trial data from outside of GON indicate that patients and surgeons do prefer LESS scars [54,63]. Further comparative evaluations of the cosmetic outcomes of RAL, TL and LESS in GON are anxiously anticipated.

Improved pain profiles

Improvement in postoperative pain has been demonstrated with the utilization of MIS in GON. Again, the LAP-2 randomized controlled trial data confirm that laparoscopically staged endometrial cancer patients experience less pain than their counterparts that undergo laparotomy [12]. Utilizing one incision in the thinnest portion of the abdominal wall, LESS continues to be promising in this regard. Very low pain scores and narcotic needs have been reported after LESS procedures for both benign and malignant gynecologic disease, with no need for home narcotics being reported by one-third of cancer patients [21]. The benign gynecology literature favors LESS over TL, with favorable pain profiles reported for LESS in a retrospective review of laparoscopically assisted vaginal hysterectomy as well as a randomized controlled trial of adnexal surgery [54,64]. Randomized controlled trials from the cholecystectomy literature support these results [65,66].

Quicker healing

The clinical recovery of patients after MIS is remarkable compared with those who undergo open surgery. Clinical stage 1–2A endometrial cancer patients who were randomized to TL staging had shorter hospital stays, better functioning and quality of life, and earlier resumption of normal activities and return to work in the 6 weeks postoperatively compared with their counterparts who underwent laparotomy [11,12]. Observational retrospective studies repeatedly demonstrate shorter hospital stays associated with RAL simple and radical hysterectomies compared with open surgery [22,23,25 –27,29,30,32,34,37,38,40,51]. Compared with TL, some observational studies have demonstrated shorter hospital stays for RAL simple and RH with staging [22,24,27,29,31,39], but some studies have not demonstrated a significant difference [26,28,33,35,37,51]. Small observational studies have associated shorter hospital stays with TL and RAL compared with open ovarian cancer debulkmg procedures [17,18,20].

Again, data in GON are needed, but in the benign gynecology literature LESS is promising in this regard. LESS hysterectomies are retrospectively associated with shorter hospital stays and earlier diet intake compared with TL [53]. A randomized controlled trial of LESS compared with TL adnexal surgery for benign disease failed to demonstrate any difference in hospital stay, but was small and not powered to demonstrate this [54]. Further comparative data are warranted.

Cancer-related outcomes

Given the novelty of many of these approaches, good long-term data are sparse. It will be some time until long-term outcomes data from the LAP-2 randomized controlled trial are available. Hopefully, minimizing morbidity and enhancing recovery from operative treatment of gynecologic malignancies will improve overall health and enable the cancer survivor to receive adjuvant therapy quicker. However, we must keep in mind that as long as the data are limited, we could be performing harm unknowingly.

In a promising retrospective analysis of clinical stage 1 ovarian cancer patients, patients who underwent TL surgical staging had better short-term postoperative outcomes, no difference in outcomes at 17 months and a shorter interval to adjuvant therapy [18]. However, this was followed by a report later in the same year demonstrating that two patients in the TL group with stage 1A disease recurred and one died of recurrence, causing them to question the oncologic safety of laparoscopic staging [52]. Another recent retrospective study comparing TL, RAL and open RH and staging for early cervical carcinoma demonstrated improved OR times and EBL for RAL; however, they also reported five cervical cancer recurrences with one cervical cancer-related death in the robot-assisted group and no recurrences in the laparoscopy and laparotomy group [27].

It is difficult to interpret these concerning but potentially aberrant results in these small studies. Prospective and randomized trials are necessary to further clarify any real benefit, or harm, conveyed by any MIS approach to the GON patient. Long-term outcome data from LAP-2 and further randomized controlled trials comparing MIS approaches to laparotomy and to each other are eagerly anticipated.

Conclusion & future perspective

MIS has come a long way, both in terms of the technology and approaches available and the skill level of the surgeons who practice it. There are great data available that short-term outcomes are better for early-stage endometrial cancer thanks to the LAP-2 randomized controlled trial. While we extrapolate these results to our other malignancies, further studies such as this one are needed to evaluate MIS approaches in other early-stage gynecologic cancers and in more advanced disease. There is currently an ongoing randomized controlled trial comparing RAL, TL and open RH and staging for cervical cancer [67]. Well-designed randomized controlled trials are the only way we will meaningfully be able to understand the benefits or harms conveyed by MIS procedures compared with open surgery or to each other.

In GON, MIS holds promise for real improvement in outcomes, allowing patients to heal and proceed with adjuvant therapy faster, while tumor burden is still low. Robotics has been embraced by the field, and LESS is an exciting option just beginning to be explored. Thoughtful analysis of cost and savings of various techniques taking into account equipment are needed.

While attempting to better understand the procedures available, new techniques are also on the horizon. The first robotic-assisted LESS hysterectomy and BSO for risk reduction has been reported [68]. This same author has described a cadaveric model for robotic LESS to perform a variety of other GON procedures, including hysterectomy, BSO, modified RH and PPALND dissections [69]. Robotic applications of LESS show promise to eliminate many ergonomic and technical limitations by allowing the surgeon to avoid the awkward posturing and, if desired, correct for on screen handedness when they are intraperitoneally crossed, which may improve performance [70]. Furthermore, we need to continue to evaluate MIS approaches to more advanced procedures, as feasibility may improve as our techniques and technologies do.

MIS shows tremendous promise in GON. We must continue to evaluate current techniques comparatively and develop new ones. The implementation of MIS techniques can help patients heal faster and with less morbidity. Maximizing mobility and quality of life and minimizing the time to recovery and adjuvant therapy is paramount in the field of GON. Further research is needed to determine if these improved outcomes will produce long-term improvements in outcomes.

Executive summary

Background

Laparoscopy has strong historic roots in gynecologic surgery; robotic-assisted laparoscopy (RAL) is becoming increasingly popular and laparoendoscopic single-site surgery (LESS) is a newly re-embraced approach to laparoscopy.

Minimally invasive surgery (MIS) is becoming the standard of care.

Description of approaches to laparoscopic MIS

Traditional laparoscopy (TL) allows for flexibility in terms of size and location of trocar placement and tactile feedback, but can be limited by a 2D view, rigid instruments and challenges accomplishing complex maneuvers.

RAL offers a 3D view, surgeon comfort, ease of precise and complex surgical maneuvers but is costly, time consuming, bulky and lacks tactile feedback.

LESS involves the insertion of instruments through a single 1–4-cm incision at the umbilicus; surgeons must adopt novel laparoscopic skills and adapt to awkward posturing and instrument clashing.

Applications of MIS in gynecologic oncology

Excellent randomized controlled trial data supports the use of TL over laparotomy in the surgical staging of clinically early endometrial cancer. Support for RAL or LESS approaches is based on extrapolation from this and warrants further comparative research.

Further randomized prospective trials are needed to determine the optimal surgical approach to cervical and ovarian cancer.

Outcome measures of MIS in gynecologic oncology

Success rates and need for conversion

– Conversion rates for TL and RAL hysterectomies with staging appear low, but rigorous comparative data is lacking.

– Initial data for LESS appears promising, but, based on the performance of advanced laparoscopic surgeons, may not be generalizable. LESS can be converted to TL or laparotomy.

Operating times

– The studies comparing operating room times for TL, RAL and open gynecologic oncology (GON) procedures are inconsistent, probably depending on surgeon preference and skill.

Estimated blood loss

– MIS is generally associated with a lower estimated blood loss than laparotomy. The MIS approach with the lowest estimated blood loss remains to be determined.

Complication rates

– Excellent data demonstrate improved postoperative complications with TL over open endometrial cancer staging.

– Further research is needed to identify the MIS modality with the fewest complications.

Incisional complications

– Based on reported hernia rates of 0.2–3.1 %, MIS approaches are probably associated with a lower incisional hernia rate than that reported with vertical midline laparotomy (8.8%). Better prospective and comparative data are necessary to determine the MIS approach associated with the lowest incisional hernia rate.

– Port site metastases occur 0.97–2.3% of the time, and no comparative data are available to demonstrate whether TL, RAL or LESS is associated with this complication more or less frequently.

Improved cosmesis

– TL has better cosmetic results than laparotomy for endometrial cancer staging, but further comparative studies are necessary to compare RAL, TL and LESS.

Improved pain profiles

– Randomized controlled data demonstrate less pain after TL endometrial cancer staging than laparotomy.

– Further comparative data in GON are necessary to determine the MIS modality with the best pain profile.

Quicker healing

– Randomized controlled data demonstrate faster recovery after TL compared with open endometrial cancer staging.

– Observational data support that RAL hysterectomies for gynecologic malignancies are associated with quicker healing than open procedures, but randomized trials are still needed.

– More investigation into comparing RAL, TL and LESS in GON are needed.

Cancer-related outcomes

– Long-term outcomes data are lacking. We must continue to evaluate the safety and adequacy of these techniques.

Conclusion & future perspective

MIS is rapidly evolving and has tremendous promise and potential in GON.

TL, RAL and LESS have demonstrated feasibility in a variety of procedures for a variety of gynecologic malignancies, but further randomized controlled trials with long-term follow-up are needed to compare them to the open approach and to each other.

Footnotes

PF Escobar conducts developmental research for Intuitive Surgical (CA, USA). AN Fader is a consultant for Applied Medical (CA, USA). The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

No writing assistance was utilized in the production of this manuscript.

References

Papers of special note have been highlighted as:.

of interest.

of considerable interest.

Tarasconi

. Endoscopic salpingectomy. J. Reprod. Med. 26(10), 541–545 (1981).

Semm

. Endoscopic appendectomy. Endoscopy 15(2), 59–64 (1983).

Sutton

. Hysterectomy: a historical perspective. Baillieres Clin. Obstet. Gynaecol. 11(1), 1–22 (1997).

AAGL Advancing Minimally Invasive Gynecology Worldwide. AAGL position statement: route of hysterectomy to treat benign uterine disease. J. Minim. Invasive Gynecol. 18(1), 1–3 (2011).

Statement released by the American Association of Gynecologic Laparoscopists that highlights the ongoing adoption of minimally invasive surgery as the standard of care .

Wheeless

Jr Thompson

. Laparoscopic sterilization. Review of 3600 cases. Obstet. Gynecol. 42(5), 751–758 (1973).

10.

Pelosi

3rd.

Laparoscopic appendectomy using a single umbilical puncture (minilaparoscopy). J. Reprod. Med. 37(7), 588–594 (1992).

11.

Pelosi

3rd.

Laparoscopic supracervical hysterectomy using a single-umbilical puncture (mini-laparoscopy). J. Reprod. Med. 37(9), 777–784 (1992).

12.

Diaz-Arrastia

Jurnalov

Gomez

. Laparoscopic hysterectomy using a computer-enhanced surgical robot. Surg. Endosc. 16(9), 1271–1273 (2002).

13.

Magrina

. Robotic surgery in gynecology. Eur. J. Gynaecol. Oncol. 28(2), 77–82 (2007).

14.

Mettler

Schollmeyer

Boggess

. Robotic assistance in gynecological oncology. Curr. Opin. Oncol. 20(5), 581–589 (2008).

15.

Walker

Piedmonte

Spirtos

. Laparoscopy compared with laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group study LAP-2. J. Clin. Oncol. 27(32), 5331–5336 (2009).

16.

Highlights the results of the cornerstone Gynecologic Oncology Group randomized controlled trial comparing traditional laparoscopy (TL) with laparotomy for the surgical staging of endometrial cancer .

17.

Kornblith

Huang

Walker

. Quality of life of patients with endometrial cancer undergoing laparoscopic international federation of gynecology and obstetrics staging compared with laparotomy: a gynecologic oncology group study. J. Clin. Oncol. 27(32), 5337–5342 (2009).

18.

Discusses the quality-of-life findings of the LAP-2 randomized controlled trial that compared TL with laparotomy for the surgical staging of endometrial cancer .

19.

Fanfani

Rossitto

Gagliardi

. Total laparoendoscopic single-site surgery (LESS) hysterectomy in low-risk early endometrial cancer: a pilot study. Surg. Endosc. 26(1), 41–46 (2012).

20.

Escobar

Frumovitz

Soliman

. Comparison of single-port laparoscopy, standard laparoscopy, and robotic surgery in patients with endometrial cancer. Ann. Surg. Oncol. doi:10.1245/s10434–011–2136-y (2011) (Epub ahead of print).

21.

This matched retrospective cohort study is one of the only studies comparing outcomes of laparoendoscopic single-site surgery with TL and robotic-assisted laparoscopy (RAL) for the treatment of a gynecologic malignancy .

22.

Kruijdenberg

van den Einden

Hendriks

. Robot-assisted versus total laparoscopic radical hysterectomy in early cervical cancer, a review. Gynecol. Oncol. 120(3), 334–339 (2011).

23.

Sert

Abeler

. Robotic radical hysterectomy in early-stage cervical carcinoma patients, comparing results with total laparoscopic radical hysterectomy cases. The future is now? Int. J. Med. Robot. 3(3), 224–228 (2007).

24.

Chi

Abu-Rustum

Sonoda

. The safety and efficacy of laparoscopic surgical staging of apparent stage I ovarian and fallopian tube cancers. Am. J. Obstet. Gynecol. 192(5), 1614–1619 (2005).

25.

Park

Kim

Suh

. Comparison of laparoscopy and laparotomy in surgical staging of early-stage ovarian and fallopian tubal cancer. Ann. Surg. Oncol. 15(7), 2012–2019 (2008).

26.

Nezhat

DeNoble

Liu

. The safety and efficacy of laparoscopic surgical staging and debulking of apparent advanced stage ovarian, fallopian tube, and primary peritoneal cancers. JSLS 14(2), 155–168 (2010).

27.

Magrina

Zanagnolo

Noble

. Robotic approach for ovarian cancer: Perioperative and survival results and comparison with laparoscopy and laparotomy. Gynecol. Oncol. 121(1), 100–105 (2011).

28.

Fader

Rojas-Espaillat

Ibeanu

. Laparoendoscopic single-site surgery (LESS) in gynecology: a multi-institutional evaluation. Am. J. Obstet. Gynecol. 203(5), 501.e1–6 (2010).

29.

Boggess

Gehrig

Cantrell

. A comparative study of 3 surgical methods for hysterectomy with staging for endometrial cancer: robotic assistance, laparoscopy, laparotomy. Am. J. Obstet. Gynecol. 199(4), 360.e1–9 (2008).

30.

Boggess

Gehrig

Cantrell

. A case–control study of robot-assisted type III radical hysterectomy with pelvic lymph node dissection compared with open radical hysterectomy. Am. J. Obstet. Gynecol. 199(4), 357.e1–7 (2008).

31.

Gehrig

Cantrell

Shafer

. What is the optimal minimally invasive surgical procedure for endometrial cancer staging in the obese and morbidly obese woman? Gynecol. Oncol. 111(1), 41–45 (2008).

32.

Paley

Veljovich

Shah

. Surgical outcomes in gynecologic oncology in the era of robotics: analysis of first 1000 cases. Am. J. Obstet. Gynecol. 204(6), 551.e1–9 (2011).

33.

Estape

Lambrou

Diaz

. A case matched analysis of robotic radical hysterectomy with lymphadenectomy compared with laparoscopy and laparotomy. Gynecol. Oncol. 113(3), 357–361 (2009).

34.

Sert

Abeler

. Robot-assisted laparoscopic radical hysterectomy: comparison with total laparoscopic hysterectomy and abdominal radical hysterectomy; one surgeon's experience at the Norwegian radium hospital. Gynecol. Oncol. 121(3), 600–604 (2011).

35.

Jung

Lee

Kim

. Robot-assisted staging using three robotic arms for endometrial cancer: comparison to laparoscopy and laparotomy at a single institution. J. Surg. Oncol. 101(2), 116–121 (2010).

36.

Lim

Kang

do Park

. Learning curve and surgical outcome for robotic-assisted hysterectomy with lymphadenectomy: case-matched controlled comparison with laparoscopy and laparotomy for treatment of endometrial cancer. J. Minim. Invasive Gynecol. 17(6), 739–748 (2010).

37.

Maggioni

Minig

Zanagnolo

. Robotic approach for cervical cancer: comparison with laparotomy: a case control study. Gynecol. Oncol. 115(1), 60–64 (2009).

38.

Lim

Kang

do Park

. A comparative detail analysis of the learning curve and surgical outcome for robotic hysterectomy with lymphadenectomy versus laparoscopic hysterectomy with lymphadenectomy in treatment of endometrial cancer: a case-matched controlled study of the first one hundred twenty two patients. Gynecol. Oncol. 120(3), 413–418 (2011).

39.

Nam

Kim

. A case–control study of robotic radical hysterectomy and pelvic lymphadenectomy using 3 robotic arms compared with abdominal radical hysterectomy in cervical cancer. Int. J. Gynecol. Cancer 20(7), 1284–1289 (2010).

40.

Tinelli

Malzoni

Cosentino

. Robotics versus laparoscopic radical hysterectomy with lymphadenectomy in patients with early cervical cancer: a multicenter study. Ann. Surg. Oncol. 18(9), 2622–2628 (2011).

41.

Seamon

Bryant

Rheaume

. Comprehensive surgical staging for endometrial cancer in obese patients: comparing robotics and laparotomy. Obstet. Gynecol. 114(1), 16–21 (2009).

42.

Cardenas-Goicoechea

Adams

Bhat

. Surgical outcomes of robotic-assisted surgical staging for endometrial cancer are equivalent to traditional laparoscopic staging at a minimally invasive surgical center. Gynecol. Oncol. 117(2), 224–228 (2010).

43.

Veljovich

Paley

Drescher

. Robotic surgery in gynecologic oncology: program initiation and outcomes after the first year with comparison with laparotomy for endometrial cancer staging. Am. J. Obstet. Gynecol. 198(6), 679.e1–9; discussion 679.e9–10 (2008).

44.

Bell

Torgerson

Seshadri-Kreaden

. Comparison of outcomes and cost for endometrial cancer staging via traditional laparotomy, standard laparoscopy and robotic techniques. Gynecol. Oncol. 111(3), 407–411 (2008).

45.

DeNardis

Holloway

Bigsby

4th . Robotically assisted laparoscopic hysterectomy versus total abdominal hysterectomy and lymphadenectomy for endometrial cancer. Gynecol. Oncol. 111(3), 412–417 (2008).

46.

Seamon

Cohn

Henretta

. Minimally invasive comprehensive surgical staging for endometrial cancer: robotics or laparoscopy? Gynecol. Oncol. 113(1), 36–41 (2009).

47.

Geisler

Orr

Khurshid

. Robotically assisted laparoscopic radical hysterectomy compared with open radical hysterectomy. Int. J. Gynecol. Cancer 20 (3), 438–442 (2010).

48.

Escobar

Fader

Rasool

. Single-port laparoscopic pelvic and para-aortic lymph node sampling or lymphadenectomy: development of a technique and instrumentation. Int. J. Gynecol. Cancer 20(7), 1268–1273 (2010).

49.

Pan

Lin

Wang

. Feasibility of laparoscopic extraperitoneal pelvic lymphadenectomy in gynecologic malignancies. Gynecol. Oncol. 122(2), 281–284 (2011).

50.

Narducci

Lambaudie

Houvenaeghel

. Early experience of robotic-assisted laparoscopy for extraperitoneal para-aortic lymphadenectomy up to the left renal vein. Gynecol. Oncol. 115(1), 172–174 (2009).

51.

Gouy

Kane

Uzan

. Single-port laparoscopy and extraperitoneal para-aortic lymphadenectomy: about fourteen consecutive cases. Gynecol. Oncol. 123(2), 329–332 (2011).

52.

Hahn

Kim

. Single-port laparoscopic pelvic lymph node dissection with modified radical vaginal hysterectomy in cervical cancer. Int. J. Gynecol. Cancer 20(8), 1429–1432 (2010).

53.

Zapardiel

Zanagnolo

Magrina

. Robotic radical parametrectomy in cervical cancer. Gynecol. Obstet. Invest. 72(3), 179–182 (2011).

54.

Kim

Park

Kim

. Fertility-sparing laparoscopic radical trachelectomy for young women with early stage cervical cancer. BJOG 117(3), 340–347 (2010).

55.

Puntambekar

Rajamanickam

Agarwal

. Laparoscopic posterior exenteration in advanced gynecologic malignant disease. J. Minim. Invasive Gynecol. 18(1), 59–63 (2011).

56.

Puntambekar

Kudchadkar

Gurjar

. Laparoscopic pelvic exenteration for advanced pelvic cancers: a review of 16 cases. Gynecol. Oncol. 102(3), 513–516 (2006).

57.

Interesting description of TL exenteration .

58.

Farghaly

. Robotic-assisted laparoscopic anterior pelvic exenteration in patients with advanced ovarian cancer: Farghaly's technique. Eur. J. Gynaecol. Oncol. 31(4), 361–363 (2010).

59.

Interesting description of RAL anterior exenteration .

60.

Magrina

Kho

Weaver

. Robotic radical hysterectomy: comparison with laparoscopy and laparotomy. Gynecol. Oncol. 109(1), 86–91 (2008).

61.

Park

Bae

Lim

. Laparoscopic and laparotomic staging in stage I epithelial ovarian cancer: a comparison of feasibility and safety. Int. J. Gynecol. Cancer 18(6), 1202–1209 (2008).

62.

Yim

Jung

Paek

. Transumbilical single-port access versus conventional total laparoscopic hysterectomy: Surgical outcomes. Am. J. Obstet. Gynecol. 203(1), 26.e1–6 (2010).

63.

Fagotti

Bottoni

Vizzielli

. Postoperative pain after conventional laparoscopy and laparoendoscopic single site surgery (LESS) for benign adnexal disease: a randomized trial. Fertil. Steril. 96(1), 255.e2–259.e2 (2011).

64.

Long

Levinson

Diaz

. Ventral hernia following primary laparotomy for ovarian, fallopian tube, and primary peritoneal cancers. Gynecol. Oncol. 120(1), 33–37 (2011).

65.

Yamamoto

Minikel

Zaritsky

. Laparoscopic 5-mm trocar sheherniation and literature review. JSLS 15(1), 122–126 (2011).

66.

Ramirez

. Single-port laparoscopic surgery: is a single incision the next frontier in minimally invasive gynecologic surgery? Gynecol. Oncol. 114(2), 143–144 (2009).

67.

Gunderson

Knight

Ybanez-Morano

. The risk of umbilical hernia and other complications with laparoendoscopic single-site surgery. J. Minim. Invasive Gynecol. 19(1), 40–45 (2012).

68.

Boike

Miller

Spirtos

. Incisional bowel herniations after operative laparoscopy: a series of nineteen cases and review of the literature. Am. J. Obstet. Gynecol. 172(6), 1726–1731; discussion 1731–1733 (1995).

69.

Nagarsheth

Rahaman

Cohen

. The incidence of port-site metastases in gynecologic cancers. JSLS 8(2), 133–139 (2004).

70.

Ramirez

Wolf

Levenback

. Laparoscopic port-site metastases: etiology and prevention. Gynecol. Oncol. 91(1), 179–189 (2003).

71.

Abu-Rustum

Rhee

Chi

. Subcutaneous tumor implantation after laparoscopic procedures in women malignant disease. Obstet. Gynecol. 103(3), 480–487 (2004).

72.

Park

Olweny

Best

. Patient-reported body image and cosmesis outcomes following kidney surgery: comparison of laparoendoscopic single-site, laparoscopic, and open surgery. Eur. Urol. 60(5), 1097–1104 (2011).

73.

Kim

Lee

Cha

. Single-port-access laparoscopic-assisted vaginal hysterectomy versus conventional laparoscopic- assisted vaginal hysterectomy: a comparison of perioperative outcomes. Surg. Endosc. 24(9), 2248–2252 (2010).

74.

Bresadola

Pasqualucci

Donini

. Elective transumbilical compared with standard laparoscopic cholecystectomy. Eur. J. Surg. 165(1), 29–34 (1999).

75.

Tsimoyiannis

Tsimogiannis

Pappas-Gogos

. Different pain scores in single transumbilical incision laparoscopic cholecystectomy versus classic laparoscopic cholecystectomy: a randomized controlled trial. Surg. Endosc. 24(8), 1842–1848 (2010).

76.

Obermair

Gebski

Frumovitz

. A Phase III randomized clinical trial comparing laparoscopic or robotic radical hysterectomy” with abdominal radical hysterectomy in patients with early stage cervical cancer. J. Minim. Invasive Gynecol. 15(5), 584–588 (2008).

77.

Much-anticipated additional randomized controlled trial that will compare TL with RAL and laparotomy for radical hysterectomy in early cervical cancer .

78.

Escobar

Fader

Paraiso

. Robotic-assisted laparoendoscopic single-site surgery in gynecology: initial report and technique. J. Minim. Invasive Gynecol. 16(5), 589–591 (2009).

79.

Escobar

Kebria

Falcone

. Evaluation of a novel single-port robotic platform in the cadaver model for the performance of various procedures in gynecologic oncology. Gynecol. Oncol. 120(3), 380–384 (2011).

80.

Recent report highlighting the feasibility of multiple gynecologic oncology procedures with the novel laparoendoscopic single-site surgery robotic platform used on a cadaveric model .

81.

Joseph

Goh

Cuevas

. ‘Chopstick’ surgery: a novel technique improves surgeon performance and eliminates arm collision in robotic single-incision laparoscopic surgery. Surg. Endosc. 24(6), 1331–1335 (2010).