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REVIEW article

Front. Med., 05 March 2024
Sec. Obstetrics and Gynecology
This article is part of the Research Topic Changing Backgrounds and Groundbreaking Changes: Gynecological surgery in the third decade of the 21st century Volume II View all 10 articles

Robotic surgery for deep-infiltrating endometriosis: is it time to take a step forward?

Filippo Alberto FerrariFilippo Alberto Ferrari1Youssef YoussefYoussef Youssef2Antoine Naem,
Antoine Naem3,4*Federico FerrariFederico Ferrari5Franco OdicinoFranco Odicino5Harald KrentelHarald Krentel4Gaby Moawad,Gaby Moawad6,7
  • 1Department of Obstetrics and Gynaecology, AOUI Verona, University of Verona, Verona, Italy
  • 2Division of Minimally Invasive Gynecologic Surgery, Department of Obstetrics and Gynaecology-Maimonides Medical Center, Brooklyn, NY, United States
  • 3Faculty of Mathematics and Computer Science, University of Bremen, Bremen, Germany
  • 4Department of Obstetrics, Gynecology, Gynecologic Oncology, and Senology, Bethesda Hospital Duisburg, Duisburg, Germany
  • 5Department of Clinical and Experimental Sciences, Division of Obstetrics and Gynecology, University of Brescia, Brescia, Italy
  • 6Department of Obstetrics and Gynecology, George Washington University, Washington, DC, United States
  • 7The Center for Endometriosis and Advanced Pelvic Surgery, Washington, DC, United States

Endometriosis is a chronic debilitating disease that affects nearly 10% of women of the reproductive age. Although the treatment modalities of endometriosis are numerous, surgical excision of the endometriotic implants and nodules remains the sole cytoreductive approach. Laparoscopic excision of endometriosis was proven to be beneficial in improving the postoperative pain and fertility. Moreover, it was also proved to be safe and efficient in treating the visceral localization of deep endometriosis, such as urinary and colorectal endometriosis. More recently, robotic-assisted surgery gained attention in the field of endometriosis surgery. Although the robotic technology provides a 3D vision of the surgical field and 7-degree of freedom motion, the safety, efficacy, and cost-effectiveness of this approach are yet to be determined. With this paper, we aim to review the available evidence regarding the role of robotic surgery in the management of endometriosis along with the current practices in the field.

1 Introduction

Endometriosis is one of the most common gynecologic diseases affecting nearly 10% of women of the reproductive age (1). Endometriosis is defined by the presence of endometrial-like glands and/or stroma out of the uterus (2, 3). The clinical manifestations of endometriosis could be broadly categorized into endometriosis-associated pain and infertility (4). The most commonly-reported symptoms of endometriosis are chronic pelvic pain, dysmenorrhea, and dyspareunia (5). On the other hand, infertility is reported to affect 30–50% of endometriosis patients (6). Although endometriosis has various forms and manifestations, superficial peritoneal endometriosis, ovarian endometriomas, and deep endometriosis are the three main types of the disease (7). Deep endometriosis has been historically defined as deep infiltrating endometriosis extending 5 mm below the peritoneal surface (8). However, a recent international terminology consensus has argued that measuring depth in millimeters is inaccurate. It is now agreed that any endometrial-like tissue in the abdomen, extending on or under the peritoneal surface, is referred to as deep endometriosis (9). These lesions are typically nodular, capable of invading adjacent structures, and associated with fibrosis, leading to the disruption of the normal anatomy (9). Such lesions usually involve the retro-cervical space, the recto-vaginal septum, the uterosacral ligaments, as well as nearby organs such as the sigmoid colon, rectum, bladder, and ureters (10, 11). It should be noted that bowel endometriosis is a special subtype of deep endometriosis that should be only diagnosed when the muscular layer of the bowel wall is infiltrated with the disease (12, 13). Hormonal suppressive treatments with cyclic oral contraceptive pills, progestins, and gonadotropin-releasing hormones (GnRH) agonists and antagonists were proven to be safe and effective in treating the endometriosis-associated pain (1416). However, those therapies are suppressive rather than cytoreductive, which means, in most cases, the symptoms recur with the suspension of the treatment. This becomes particularly problematic in cases of infertility or when the patient seeks conception. To date, surgical excision of endometriosis is the only cytoreductive approach with promising symptom-relief rates. Furthermore, surgery becomes unavoidable when organ damage is suspected or already detected (4, 17). The basic principles of the endometriosis excisional surgery are the uncomplicated resection of the visualized endometriotic lesions, performing adhesiolysis, and restoring the normal pelvic anatomy (18). Minimally invasive surgery (MIS) is actually the approach of choice since it demonstrated reduced blood loss, postoperative pain, and duration of hospitalization. In fact, the Enhanced Recovery After Surgery (ERAS) program recommends MIS to improve the postoperative patient recovery (19, 20). Nevertheless, the laparoscopic management of advanced and complex cases is challenging due to tissue alterations provoked by adhesions and the endometriosis-associated fibrosis (21). Despite the advantages of laparoscopy compared to open surgery and the development of laparoscopic 3D optics, the laparoscopic approach harbors technical limitations in terms of ergonomics and the limited range of motion (22). Robotic-assisted surgery was developed more than 30 years ago as a United States military project and received the approval of the Food and Drug Administration (FDA) in 2005 (23). Since then, robotic-assisted surgery has been widely implemented and adopted in gynecology (24). Robotic-assisted surgery was recently reported to have shorter operation time and less blood loss than laparoscopic surgery, with comparable outcomes (25). However, the available data in that regard is conflicting and more studies are required to justify this claim. Robotic-assisted surgery with its rapidly evolving technology can overcome much of the laparoscopic limitations, and represents a step forward toward a safer and more precise excision of the disease. Indeed, the EndoWrist® increases the range of motion and the robotic platform 3D vision avoids the problem of an unstable bi-dimensional image totally dependent on the assistant. Nonetheless, its superiority or at least non-inferiority in the management of deep endometriosis remains unclear due to the lack of research in the field. The present review aims to provide an update on the role of robotic-assisted surgery in managing endometriosis and summarize the main scientific findings in the literature.

2 Materials and methods

This work is a narrative review of the role of robotic-assisted surgery in deep-infiltrating endometriosis. A broad scope search of literature was conducted in Scopus, PubMed/Medline, ScienceDirect and the Cochrane Library. A combination of the following keywords was used: deep-infiltrating endometriosis, robotic surgery, robot-assisted laparoscopy. The search was restricted to only include articles in English language. Relevant papers of all types (i.e., original articles, video articles, and case reports) were assessed and included as appropriate.

3 Feasibility of the robotic-assisted surgery

Laparoscopic excisional surgery is the gold standard for the treatment of deep endometriosis. More recently, robotic-assisted surgery became more frequently adopted for the surgical management of endometriosis without clear indications. Available non-comparative studies of women that were operated robotically found a comparable complication rate between robotic-assisted surgery and laparoscopy with a significant reduction of pain symptoms. An improved quality of life at follow-up was also reported (22, 2632). Nonetheless, very few studies that compared the two minimally invasive approaches in patients with r-ASRM stage III/IV endometriosis are available. To the best of our knowledge, there are only one randomized-controlled trial (RCT) (33) and two meta-analyses (34, 35) in that regard.

In 2010, Nezhat et al. (36) published for the first time a retrospective study comparing robotic-assisted surgery and laparoscopy in severe endometriosis. Although the outcomes and complication rates were comparable between the two groups, longer operative time and hospital stay were noted in the robotic group. The mean difference in the operation times was 61 min.

The safety and feasibility of robotic-assisted surgery was further confirmed by several studies that reported comparable outcomes and rates of intra-and postoperative complications (3741).

In a large retrospective study by Nezhat et al. (41), the hospital stay was longer in the robotic-assisted group in contrast to the findings of other reports. In that study, only 23% of patients in the laparoscopy arm stayed overnight in the hospital against all the patients of the robotic arm without any complication in both groups (41). In our opinion, these findings may be related to a standardized protocol of postoperative discharge rather than an actual underlying difference between both approaches.

The total operative time was significantly shorter in the laparoscopy group in the majority of the studies (38, 4042). Dulemba et al. (37) reported a non-significant difference in the length of surgery in accordance the multivariate analysis of Magrina et al. (39), which accounts for the impact of the higher number of procedures and radicality in the robotic group (39). In the same study, the authors reported a higher rate of histological confirmation of endometriosis in the robotic-assisted surgery group compared to the laparoscopic counterpart (80% vs. 56.8%, respectively). This could be attributed to the technology of the robotic platform and its three-dimensional visualization. Improved visualization could logically lead to improved detection of superficial lesions, which is of paramount importance in women reporting pelvic pain suggestive for endometriosis.

For some authors, obesity is a major limiting factor for laparoscopic surgery in terms of some technical aspects and the difficulties to access to the surgical spaces (40). Nonetheless, the available evidence supported the feasibility and safety of robotic-assisted gynecologic surgery in obese patients (4346). In recent years, the wide spread of robotic platforms increased the number of women treated with minimally invasive approach (47, 48). Nezhat et al. (40) speculated that obese patients may benefit from robotic-assisted surgery more than normal-weighted patients. However, their study reported comparable outcomes and a significant higher total operative time in the robotic-assisted surgery arm compared to laparoscopic arm in the obese subgroup (40). Other authors addressed the increased amount of time to the multiple changing in table positioning but the proposal of a hybrid robotic-laparoscopic procedure was not demonstrated to be a time-saving option (38).

In 2017, Soto et al. (33) published a randomized controlled trial (LAROSE trial) enrolling 73 patients randomly assigned to laparoscopy or robotic-assisted surgery (33). To the best of our knowledge, this is the only trial available to date in that regard. Multivariate analysis showed no significant differences in total operative time, intraoperative complications and blood loss between the two groups. Nonetheless, only 33% of the patients had stage III/IV endometriosis and the intraoperative staging was significantly lower in the robotic arm. When taking in consideration the low rate of complications and adverse outcomes as well as the small sample size, the conclusion of the study may not be generalizable.

In a recent meta-analysis by Restaino et al. (35), the safety of robotic-assisted surgery was confirmed with a comparable rate of intra-and post-operative complications. In addition, the authors reported similar estimated blood loss quantities between the two groups. Moreover, robotic-assisted surgery was associated with longer operative time compared to laparoscopic surgery, even when excluding the docking time (35). Nonetheless, the authors concluded that the heterogeneity in outcomes of the included studies and the focus on the peri-operative window did not allow any conclusions on long-term pain relief, quality of life and fertility results (34, 35). Moreover, some of the considered studies enrolled both mild and severe endometriosis (33, 41) while other authors failed to report the stage of the disease, which contributed to the wide heterogeneity in the included population. Those results are in accordance with the results Chen et al. (34).

4 Colorectal endometriosis

Bowel endometriosis is a subgroup of deep endometriosis that involves the recto-sigmoid junction in the majority of the cases (65%), followed by the rectum (15–20%) (40, 49). In the available literature, its incidence was reported to be 4–38% in women with endometriosis and cyclic bowel symptoms, especially dyschezia and hematochezia (50). The surgical management is required after failure of conservative medical therapies and it should be tailored on the patient’s symptoms and disease characteristics. Although clear guidelines are lacking, the choice between segmental resection with anastomosis, discoid resection or nodulectomy (shaving) is mainly based on the size, the depth of the lesions’ invasion, the circumference of the disease and the coexistence of skip lesions (29, 51). In the last years, some authors considered the robotic-assisted surgery in cases of bowel endometriosis to overcome the complexity and technical difficulty of advanced stages allowing a smoother preparation of the rectum with an easier superior rectal artery sparing and simpler handling of the tissue during the anastomosis (23, 29). In a meta-analysis of a total of 3,079 women with recto-sigmoidal endometriosis, the statistical analysis demonstrated a higher rate of major complications for segmental resection (11.8%), followed by discoid resections (7.5%) and the rectal shaving technique (5.5%). In 92% of cases, a minimally invasive approach was used but robotic-assisted surgery was performed only in 1.7% of the patients (49).

In 2011, Nezhat et al. published two successful cases of bowel endometriosis managed with robotic segmental rectal resection and discoid resection demonstrating the feasibility of both approaches (28). In a small comparative study, Lim et al. (52) compared robotic-assisted anterior rectal resection with the open approach. The authors failed to detect any significant differences in total operative time, blood loss and length of hospitalization. A higher number of complications was reported in the laparotomy group, but the difference was not significant (52). In a cohort of 22 consecutive patients, robotic-assisted excision of bowel endometriosis was confirmed to be safe and feasible, with satisfactory short-term results and zero conversions to laparotomy (26).

In a recent prospective cohort study, the comparison between laparoscopy and robotic-assisted surgery did not yield in any differences in blood loss, intra-operative and postoperative complications, and voiding dysfunction rates. The robotic arm had a longer total operative time (221 ± 94 min vs. 163 ± 83 min, p = 0.03), a longer hospital stay (8 ± 4.4 vs. 6.5 ± 2.6 days, p = 0.18), a higher number of grade III complications (according to Clavien Dindo Classification) without reaching the statistical significance (53).

Raimondo et al. (54) published the results of a multicentric prospective cohort study comparing laparoscopy with robotic-assisted surgery. The data of the 44 enrolled women showed no differences in outcomes, complications, operative time (skin to skin) and improvement of symptoms at 12 months of follow-up. A longer operative room time in the robotic arm was reported (296 ± 80 min vs. 241 ± 72 min; p = 0.020). This is also consistent with the findings of Ercoli et al. (26).

5 Diaphragmatic endometriosis

Diaphragmatic endometriosis is a rare form of the disease. The exact incidence and prevalence of diaphragmatic endometriosis are unknown precisely yet. However, the prevalence of diaphragmatic endometriosis was reported to be 1.86–4.7% (55). The preoperative diagnosis is difficult and the management remains controversial (45, 46, 55, 56). It may cause catamenial symptoms or chronic pain. Nonetheless, some cases may be asymptomatic (57, 58).

Ceccaroni et al. reported the portion of the diaphragm behind the right hepatic lobe as the most frequent localization (57). Redwine (56) postulated the existence of sentinel lesion on the anterior part of the diaphragmatic peritoneum which could suggest the presence of more extended localization and may induce the surgeon to a complete retro-hepatic exploration (56). Symptomatic lesions are associated with a deep involvement of the whole thickness of the diaphragm and an association with symptomatic pelvic or bowel disease was reported in the totality of the cases (59, 60).

The management is a real challenge in particular for the rarity of the localization, availability of few case series, lack of guidelines and difficulty in the preoperative diagnosis. Complete surgical resection avoiding the opening of the thoracic cavity is the goal if a full-thickness excision is not required (61). Laparotomic, laparoscopic and robotic approaches were reported in the literature, associated with video-assisted thoracoscopy (VATS) when thoracic symptoms were present (27, 57, 60, 62). Thermal ablation was proposed for the superficial lesions and Ceccaroni et al. favored Argon Beam Coagulator (ABC) than electrocautery (57).

Abo et al. published a case series of 35 patients in which robotic-assisted endometriosis excision was performed over a period of 30 months (27). Among them 8 cases of diaphragmatic localization were reported. No major complications were related to the procedure but the extent of the disease and surgical technique was not described. Recently, Roman et al. published a proposal to standardize the surgical management using robotic surgery reporting the feasibility, safety and reproducibility of this approach (62). Moreover, cases of incidental tension pneumothorax during inspection of the abdomen in patients treated with robotic-assisted surgery is reported and the entire surgical team needs to be aware of this possibility (60, 63).

However, it should be noted that in a recent study of Naem et al. (55) patients with diaphragmatic endometriosis were followed up for a mean duration of 23 months. Although 78.9% of patients reported major postoperative improvement, the postoperative recurrence rates of diaphragmatic endometriosis-related symptoms were higher than expected, with complete pain relief being reported in 25–50% of patients. On the other hand, asymptomatic lesions that were left in situ remained asymptomatic after a follow up period of 6–14 months (55). Therefore, caution should be made before operating diaphragmatic endometriosis, especially in the asymptomatic cases, where treatment seems to be unnecessary, and appropriate patient counseling about what to exactly expect postoperatively should be carried out (55, 64).

6 Urinary endometriosis

The urinary tract is rarely an endometriosis localization occurring in 0.5 to 12% of women with pelvic endometriosis. The prevalence exceeds 50% in patients with deep endometriosis (65, 66). The urinary bladder is the most common site (80%), followed by the ureter (15%), kidney (3%) and urethra (2%) (65, 67). The definition and incidence of bladder endometriosis are different in the literature owing to the variation in the inclusion or exclusion of superficial serosal lesions. Related symptoms frequently include dysuria, hematuria, suprapubic pain and urinary frequency (65). Ureteral endometriosis is less frequent and most commonly affects the left distal ureter (68). It can be classified in extrinsic form when the ureter is involved by an external nodule and intrinsic form if mural invasion is present (68). The symptoms related to ureteral endometriosis may be lower back pain, recurrent urinary tract infections, and hematuria. However, it remains asymptomatic in around 50% of the cases and may lead to an ipsilateral silent kidney (65). When surgery is required, minimally invasive approaches were demonstrated to provide adequate outcomes and acceptable rate of complications in case of urinary tract endometriosis (67, 69). In case of bladder endometriosis, the majority of the authors suggested to perform partial cystectomy to achieve a complete resection of the nodule (65, 67, 68). According to literature, ureteral lesions may be removed with ureterolysis, segmental excision with end-to-end anastomosis or reimplantation (65, 67, 69).

In the literature there are no randomized trials or prospective studies comparing laparotomy with laparoscopy and robotic-assisted surgery in case of urinary tract endometriosis. However, case reports and case series demonstrated the feasibility and safety of the robotic-assisted laparoscopy (22, 27, 29, 65, 66, 68, 7072). A French multicenter retrospective cohort including 232 patients reported the use of robotic surgery in 14.7% of the patients in comparison to laparoscopy and laparotomy in 74.1 and 11.2% of cases, respectively (68). Di Maida et al. (66) published a series of 74 women underwent minimally invasive surgery for urinary tract endometriosis. Twenty-eight (37.8%) were managed with laparoscopy and 46 (62.2%) with robotic-assisted surgery. The authors demonstrated the feasibility of the approach and reported an overall postoperative complication rate of 10.9% in the robotic group, which is consistent with the findings of Giannini et al. (70). A retrospective study compared laparoscopy and robotic-assisted surgery for the treatment of bladder endometriosis with partial cystectomy. No differences in term of surgical outcomes, perioperative complications, blood loss and recurrence rates were observed.

7 Sacral plexus endometriosis

Deep endometriosis involving the sacral plexus and the large nerves of the pelvis is deemed to be rare in gynecology (73). Although the first report of deep endometriosis of the sciatic nerve dates back to 1955 (74), very few data are available regarding its precise prevalence and optimal management. This may be attributed to the lack of awareness of this condition due to the lack of correlation between endometriosis, menstruation, and the resulting neurological symptoms (75). Deep endometriosis may involve the pelvic neural structures mainly in two ways. The first and most common form of neural involvement includes compressing the sciatic nerve and sacral roots due to the posterolateral extension of parametrial and rectovaginal endometriosis, causing intrapelvic nerve entrapment (76). It is noteworthy that rectovaginal nodules tend to involve the sacral roots S2, S3, and S4. While deep nodules of the parametrium with more superior lateral localization tend to involve the sciatic nerve (76). The second form of involvement is the direct infiltration of the nerves with endometriosis. This form is less common and was reported to account for nearly 33.5% of patients with recurrent sciatica (77). Pelvic nerve involvement with endometriosis causes a variety of somatic sensory and motor symptoms, with or without pelvic organ dysfunction (78, 79). In cases of sciatic nerve involvement, the patients often report cyclic sciatica. The term sciatica refers to pain along the distribution of sciatic nerve, usually referring to leg and gluteal pain (79). In addition, foot drop and alteration in the Achill’s tendon reflex may be noticed (76). On the other hand, when the sacral roots are involved with endometriosis the patients suffer from perineal pain, altered sensations in the dermatomes S2 to S4, and pelvic organ dysfunction, such as constipation, vaginal dryness, urinary urgency or bladder atonia (76, 78). It should be noted that such symptoms do not necessarily originate from the sole involvement of the sacral roots, but the involvement of the hypogastric nerves, splanchnic nerves, and inferior hypogastric plexus in the large rectovaginal or parametrial endometriotic nodule (76).

Deep endometriosis involving the sacral roots and sciatic nerves was historically treated with laparoscopic detrapment of the involved structures in the means of neural decompression and shaving at the epineurium level. Less commonly, partial nerve resection was also applied (7678, 80). Furthermore, laparoscopic identification and subsequent excision of peritoneal pockets resulted also in a postoperative resolution of the neurologic pain symptoms (79). The efficacy of such interventions is not estimated precisely yet, but the available reports indicate that pain symptoms tend to be improved postoperatively (76, 80). It should be noted that postoperative bladder dysfunction and the need for self-catheterization was recorded in 5.8% of the operated patients in the series of Roman et al. (76) over a year of follow-up. In the same series, the authors reported that de novo hyperesthesia, hypoesthesia, or allodynia were recorded in 17.2% of patients postoperatively (76).

On this basis, the role of the robotic-assisted surgery, which is basically a subdivision of laparoscopic surgery, is far from being determined. Available reports indicate that robotic surgery with its 3D image and the 7-degree of freedom of the robotic instruments increase the safety and the precision of the neural dissection (81, 82). Other authors used indocyanine green during robotic-assisted surgery for deep endometriosis to examine the vascularization of the hypogastric nerves and inferior hypogastric plexus, and subsequently their viability (83). To date, there are no studies comparing the operative and postoperative outcomes of robotic-assisted surgery compared to laparoscopy in terms of operative time, blood loss, short-and long-term postoperative neurologic symptoms.

8 Discussion

The available literature indicates the feasibility and safety of robotic-assisted surgery in treating deep endometriosis. However, drawing definitive conclusions regarding its superiority or non-inferiority for patients with advanced endometriosis is challenging due to several factors. These include the limited number of studies, their heterogeneity, and the predominance of retrospective designs. Additionally, comprehensive investigations into crucial long-term outcomes such as sustained pain relief, variations in quality of life, and fertility outcomes have been infrequent or inadequately conducted.

Nowadays, minimally invasive approaches are considered the gold standard for the surgical treatment of deep endometriosis and in this setting the robotic-assisted surgery may provide the technology to overcome some of the limitations of laparoscopy allowing a more ergonomic position, three dimensional vision and freedom of wrist movement (40). Some surgeons use robotic-assisted surgery in deep endometriosis claiming an advantage in complex pelvic pathology, obese patients and prior surgical history. However, such studies may be subject to selection bias (23, 29). Several studies demonstrated that the two main limitations to the spread of robotic-assisted surgery are longer operative time and higher costs (23). The increased total operative time is related partially to the phase of docking and intuitively to the specific learning curve of robotic-assisted surgery (84). Moreover, some authors underlined the need for changing the table position and hybrid conventional/robot-assisted laparoscopy in advanced procedures in consideration of the arm maneuverability in the extrapelvic surgical field and absence of interchangeability of the camera between ports (29, 41). Finally, robotic-assisted surgery lacks the tactile feedback and seemed to correlate with longer operative time, making the tissue dissection more difficult and the identification of the lesions limited (85). It should be noted that DaVinci (Intuitive Surgical, United States) has been the main surgical robot used by different surgical specialties worldwide. More recently, the Hugo RAS system (Medtronic, Minneapolis, United States) was introduced and implicated in the management of deep endometriosis (86). The initial experience with this new system indicated its safety in terms of perioperative complications and efficiency in terms of postoperative symptom relief (87, 88). However, the median docking time in one series could be considered long in comparison with the docking time required for DaVinci (87). This could be attributed to the learning curve, since this system is still new and the surgeons may not be very experienced, or due to the multiple bedside arms that should be brought to the operation theater and ducked.

Robotics surgery lead to substantial additional costs compared to laparoscopy, not only for the operative time but also the need of staff training, licenses and maintenance (89). However, recently a trend in cost reduction was registered due to shorter hospital stay, operative time and better resources’ administration compared to initial experiences (90). These findings may suggest avoiding the overestimation of the costs drawback of robotic-assisted surgery and to run studies of suitable design investigating the economic impact in well trained and dedicated team.

One of the major complications of deep endometriosis treatment is the postoperative onset of sexual, rectal and voiding dysfunction that may affected more than 50% of the women (29, 91). Different expert groups described standardized approaches of nerve sparing with a systematic identification of the hypogastric nerves, pelvic splanchnic nerves and pelvic plexus in order to reduce denervation (18, 92, 93). Nonetheless, the preservation of the pelvic autonomic nerves requires not only excellent knowledge of pelvic anatomy, but also great laparoscopic technical skills (92). In this setting, all the latest technical development brought by robotic-assisted surgery may be considered especially helpful to increase the precision of the dissection and to improve autonomic nerve identification and preservation, providing better functional outcomes as demonstrated in the nerve-sparing robotic-assisted prostatectomy (94).

9 Conclusion

In conclusion, the quality of the available studies on robotic-assisted surgery in deep endometriosis is low despite the encouraging findings on peri-operative outcomes. On the other hand, long-term results about pain relief and pregnancy rates are lacking. We strongly believe that future well-designed studies are required to address these topics and to deeply understand possible advantages of robot-assisted surgery in deep endometriosis. Actually, a prospective randomized controlled single-center trial is ongoing (ROBEndo trial) aiming to evaluate the impact of robotic-assisted surgery for severe deep endometriosis at 6, 12 and 24 months postoperatively and we hope it will help to clarify the role robotic approach.

Author contributions

FAF: Conceptualization, Writing – original draft. YY: Resources, Writing – review & editing. AN: Resources, Writing – original draft, Writing – review & editing. FF: Writing – review & editing. FO: Writing – review & editing. HK: Supervision, Writing – review & editing. GM: Conceptualization, Methodology, Supervision, Writing – review & editing.

Funding

The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.

Conflict of interest

GM works with the speakers Bureau at Intuitive Surgical.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

1. Zondervan, KT, Becker, CM, and Missmer, SA. Endometriosis. N Engl J Med. (2020) 382:1244–56. doi: 10.1056/NEJMra1810764

Crossref Full Text | Google Scholar

2. Koninckx, PR, Ussia, A, Adamyan, L, Wattiez, A, Gomel, V, and Martin, DC. Pathogenesis of endometriosis: the genetic/epigenetic theory. Fertil Steril. (2019) 111:327–40. doi: 10.1016/j.fertnstert.2018.10.013

PubMed Abstract | Crossref Full Text | Google Scholar

3. Laganà, AS, and Naem, A. The pathogenesis of endometriosis: are endometrial stem/progenitor cells involved? In: I Virant-Klun , editor. Stem cells in reproductive tissues and organs: From fertility to Cancer. Cham: Springer International Publishing (2022). 193–216.

Google Scholar

4. Becker, CM, Bokor, A, Heikinheimo, O, Horne, A, Jansen, F, Kiesel, L, et al. ESHRE guideline: endometriosis†. Human Reprod Open. (2022) 2022:hoac009. doi: 10.1093/hropen/hoac009

PubMed Abstract | Crossref Full Text | Google Scholar

5. Sourial, S, Tempest, N, and Hapangama, DK. Theories on the pathogenesis of endometriosis. Int J Reprod Med. (2014) 2014:179515:1–9. doi: 10.1155/2014/179515

Crossref Full Text | Google Scholar

6. Macer, ML, and Taylor, HS. Endometriosis and infertility: a review of the pathogenesis and treatment of endometriosis-associated infertility. Obstet Gynecol Clin North Am. (2012) 39:535–49. doi: 10.1016/j.ogc.2012.10.002

PubMed Abstract | Crossref Full Text | Google Scholar

7. Nisolle, M, and Donnez, J. Reprint of: peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities. Fertil Steril. (2019) 112:e125–36. doi: 10.1016/j.fertnstert.2019.08.081

Crossref Full Text | Google Scholar

8. Koninckx, PR, and Martin, DC. Deep endometriosis: a consequence of infiltration or retraction or possibly adenomyosis externa? Fertil Steril. (1992) 58:924–8. doi: 10.1016/S0015-0282(16)55436-3

Crossref Full Text | Google Scholar

9. Tomassetti, C, Johnson, NP, Petrozza, J, Abrao, MS, Einarsson, JI, Horne, AW, et al. An international terminology for endometriosis, 2021. J Minim Invasive Gynecol. (2021) 28:1849–59. doi: 10.1016/j.jmig.2021.08.032

PubMed Abstract | Crossref Full Text | Google Scholar

10. Vercellini, P, Frontino, G, Pietropaolo, G, Gattei, U, Daguati, R, and Crosignani, PG. Deep endometriosis: definition, pathogenesis, and clinical management. J Am Assoc Gynecol Laparosc. (2004) 11:153–61. doi: 10.1016/S1074-3804(05)60190-9

PubMed Abstract | Crossref Full Text | Google Scholar

11. Koninckx, PR, Ussia, A, Adamyan, L, Wattiez, A, and Donnez, J. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril. (2012) 98:564–71. doi: 10.1016/j.fertnstert.2012.07.1061

Crossref Full Text | Google Scholar

12. Chapron, C, Bourret, A, Chopin, N, Dousset, B, Leconte, M, Amsellem-Ouazana, D, et al. Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions. Hum Reprod. (2010) 25:884–9. doi: 10.1093/humrep/deq017

PubMed Abstract | Crossref Full Text | Google Scholar

13. Abrão, MS, Petraglia, F, Falcone, T, Keckstein, J, Osuga, Y, and Chapron, C. Deep endometriosis infiltrating the recto-sigmoid: critical factors to consider before management. Hum Reprod Update. (2015) 21:329–39. doi: 10.1093/humupd/dmv003

PubMed Abstract | Crossref Full Text | Google Scholar

14. Brown, J, Pan, A, and Hart, RJ. Gonadotrophin-releasing hormone analogues for pain associated with endometriosis. Cochrane Database of Syst Rev: Protocols. (2010) 2010:Cd008475. doi: 10.1002/14651858.CD008475

Crossref Full Text | Google Scholar

15. Strowitzki, T, Marr, J, Gerlinger, C, Faustmann, T, and Seitz, C. Dienogest is as effective as leuprolide acetate in treating the painful symptoms of endometriosis: a 24-week, randomized, multicentre, open-label trial. Hum Reprod. (2010) 25:633–41. doi: 10.1093/humrep/dep469

PubMed Abstract | Crossref Full Text | Google Scholar

16. Becker, CM, Johnson, NP, As-Sanie, S, Arjona Ferreira, JC, Abrao, MS, Wilk, K, et al. Two-year efficacy and safety of relugolix combination therapy in women with endometriosis-associated pain: SPIRIT open-label extension study. Hum Reprod. (2024). doi: 10.1093/humrep/dead263

PubMed Abstract | Crossref Full Text | Google Scholar

17. Bourdel, N, Alves, J, Pickering, G, Ramilo, I, Roman, H, and Canis, M. Systematic review of endometriosis pain assessment: how to choose a scale? Hum Reprod Update. (2015) 21:136–52. doi: 10.1093/humupd/dmu046

PubMed Abstract | Crossref Full Text | Google Scholar

18. Uccella, S, Gisone, B, Serati, M, Biasoli, S, Marconi, N, Angeretti, G, et al. Functional outcomes of nerve-sparing laparoscopic eradication of deep infiltrating endometriosis: a prospective analysis using validated questionnaires. Arch Gynecol Obstet. (2018) 298:639–47. doi: 10.1007/s00404-018-4852-z

PubMed Abstract | Crossref Full Text | Google Scholar

19. Nelson, G, Bakkum-Gamez, J, Kalogera, E, Glaser, G, Altman, A, Meyer, LA, et al. Guidelines for perioperative care in gynecologic/oncology: enhanced recovery after surgery (ERAS) society recommendations-2019 update. Int J Gynecol Cancer: Official J Int Gynecol Cancer Society. (2019) 29:651–68. doi: 10.1136/ijgc-2019-000356

PubMed Abstract | Crossref Full Text | Google Scholar

20. Ferrari, F, Forte, S, Sbalzer, N, Zizioli, V, Mauri, M, Maggi, C, et al. Validation of an enhanced recovery after surgery protocol in gynecologic surgery: an Italian randomized study. Am J Obstet Gynecol. (2020) 223:543.e1–543.e14. doi: 10.1016/j.ajog.2020.07.003

Crossref Full Text | Google Scholar

21. ETIC Endometriosis Treatment Italian Club. When more is not better: 10 'don'ts' in endometriosis management. An ETIC (*) position statement. Hum Reprod Open. (2019) 2019. doi: 10.1093/hropen/hoz009

PubMed Abstract | Crossref Full Text | Google Scholar

22. Siesto, G, Ieda, N, Rosati, R, and Vitobello, D. Robotic surgery for deep endometriosis: a paradigm shift. Int J Med Robot + Compr Assist Surg: MRCAS. (2014) 10:140–6. doi: 10.1002/rcs.1518

PubMed Abstract | Crossref Full Text | Google Scholar

23. Hur, C, and Falcone, T. Robotic treatment of bowel endometriosis. Best Pract Res Clin Obstet Gynaecol. (2021) 71:129–43. doi: 10.1016/j.bpobgyn.2020.05.012

Crossref Full Text | Google Scholar

24. Laganà, AS, Garzon, S, D'Alterio, MN, Noventa, M, Stabile, G, Naem, A, et al. Mini-laparoscopy or single-site robotic surgery in gynecology? Let's think out of the box. J Investigative Surg: Official J Acad Surg Res. (2022) 35:440–1. doi: 10.1080/08941939.2020.1857480

PubMed Abstract | Crossref Full Text | Google Scholar

25. Chiou, HY, Chiu, LH, Chen, CH, Yen, YK, Chang, CW, and Liu, WM. Comparing robotic surgery with laparoscopy and laparotomy for endometrial cancer management: a cohort study. Int J Surg (London, England). (2015) 13:17–22. doi: 10.1016/j.ijsu.2014.11.015

PubMed Abstract | Crossref Full Text | Google Scholar

26. Ercoli, A, D'Asta, M, Fagotti, A, Fanfani, F, Romano, F, Baldazzi, G, et al. Robotic treatment of colorectal endometriosis: technique, feasibility and short-term results. Hum Reprod. (2012) 27:722–6. doi: 10.1093/humrep/der444

PubMed Abstract | Crossref Full Text | Google Scholar

27. Abo, C, Roman, H, Bridoux, V, Huet, E, Tuech, JJ, Resch, B, et al. Management of deep infiltrating endometriosis by laparoscopic route with robotic assistance: 3-year experience. J Gynecology Obstetrics Human Reprod. (2017) 46:9–18. doi: 10.1016/j.jgyn.2015.12.003

PubMed Abstract | Crossref Full Text | Google Scholar

28. Nezhat, C, Hajhosseini, B, and King, LP. Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis. JSLS: J Society of Laparoendoscopic Surgeons. (2011) 15:387–92. doi: 10.4293/108680811X13125733356396

PubMed Abstract | Crossref Full Text | Google Scholar

29. Morelli, L, Perutelli, A, Palmeri, M, Guadagni, S, Mariniello, MD, Di Franco, G, et al. Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short-and mid-term surgical and functional outcomes. Int J Colorectal Dis. (2016) 31:643–52. doi: 10.1007/s00384-015-2477-2

PubMed Abstract | Crossref Full Text | Google Scholar

30. Collinet, P, Leguevaque, P, Neme, RM, Cela, V, Barton-Smith, P, Hébert, T, et al. Robot-assisted laparoscopy for deep infiltrating endometriosis: international multicentric retrospective study. Surg Endosc. (2014) 28:2474–9. doi: 10.1007/s00464-014-3480-3

PubMed Abstract | Crossref Full Text | Google Scholar

31. Brudie, LA, Gaia, G, Ahmad, S, Finkler, NJ, Bigsby, GE IV, Ghurani, GB, et al. Peri-operative outcomes of patients with stage IV endometriosis undergoing robotic-assisted laparoscopic surgery. J Robot Surg. (2012) 6:317–22. doi: 10.1007/s11701-011-0314-3

PubMed Abstract | Crossref Full Text | Google Scholar

32. Neme, RM, Schraibman, V, Okazaki, S, Maccapani, G, Chen, WJ, Domit, CD, et al. Deep infiltrating colorectal endometriosis treated with robotic-assisted rectosigmoidectomy. JSLS: J Society of Laparoendoscopic Surgeons. (2013) 17:227–34. doi: 10.4293/108680813X13693422521836

PubMed Abstract | Crossref Full Text | Google Scholar

33. Soto, E, Luu, TH, Liu, X, Magrina, JF, Wasson, MN, Einarsson, JI, et al. Laparoscopy vs. robotic surgery for endometriosis (LAROSE): a multicenter, randomized, controlled trial. Fertil Steril. (2017) 107:996–1002.e3. doi: 10.1016/j.fertnstert.2016.12.033

PubMed Abstract | Crossref Full Text | Google Scholar

34. Chen, Y, Wang, H, Wang, S, Shi, X, Wang, Q, and Ren, Q. Efficacy of ten interventions for endometriosis: a network meta-analysis. J Cell Biochem. (2019) 120:13076–84. doi: 10.1002/jcb.28579

PubMed Abstract | Crossref Full Text | Google Scholar

35. Restaino, S, Bizzarri, N, Tarantino, V, Pelligra, S, Moroni, R, Palmieri, E, et al. Comparison of different near-infrared technologies to detect sentinel lymph node in uterine Cancer: a prospective comparative cohort study. Int J Environ Res Public Health. (2022) 19. doi: 10.3390/ijerph19127377

PubMed Abstract | Crossref Full Text | Google Scholar

36. Nezhat, C, Lewis, M, Kotikela, S, Veeraswamy, A, Saadat, L, Hajhosseini, B, et al. Robotic versus standard laparoscopy for the treatment of endometriosis. Fertil Steril. (2010) 94:2758–60. doi: 10.1016/j.fertnstert.2010.04.031

PubMed Abstract | Crossref Full Text | Google Scholar

37. Dulemba, JF, Pelzel, C, and Hubert, HB. Retrospective analysis of robot-assisted versus standard laparoscopy in the treatment of pelvic pain indicative of endometriosis. J Robot Surg. (2013) 7:163–9. doi: 10.1007/s11701-012-0361-4

PubMed Abstract | Crossref Full Text | Google Scholar

38. Cassini, D, Cerullo, G, Miccini, M, Manoochehri, F, Ercoli, A, and Baldazzi, G. Robotic hybrid technique in rectal surgery for deep pelvic endometriosis. Surg Innov. (2014) 21:52–8. doi: 10.1177/1553350613487804

PubMed Abstract | Crossref Full Text | Google Scholar

39. Magrina, JF, Espada, M, Kho, RM, Cetta, R, Chang, YH, and Magtibay, PM. Surgical excision of advanced endometriosis: perioperative outcomes and impacting factors. J Minim Invasive Gynecol. (2015) 22:944–50. doi: 10.1016/j.jmig.2015.04.016

PubMed Abstract | Crossref Full Text | Google Scholar

40. Nezhat, FR, and Sirota, I. Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis. JSLS: J Society of Laparoendoscopic Surgeons. (2014) 18:e2014.00094. doi: 10.4293/JSLS.2014.00094

PubMed Abstract | Crossref Full Text | Google Scholar

41. Nezhat, CR, Stevens, A, Balassiano, E, and Soliemannjad, R. Robotic-assisted laparoscopy vs conventional laparoscopy for the treatment of advanced stage endometriosis. J Minim Invasive Gynecol. (2015) 22:40–4. doi: 10.1016/j.jmig.2014.06.002

PubMed Abstract | Crossref Full Text | Google Scholar

42. Dubeshter, B, Angel, C, Toy, E, Thomas, S, and Glantz, JC. Current role of robotic hysterectomy. J Gynecol Surg. (2013) 29:174–8. doi: 10.1089/gyn.2012.0113

PubMed Abstract | Crossref Full Text | Google Scholar

43. Bernardini, MQ, Gien, LT, Tipping, H, Murphy, J, and Rosen, BP. Surgical outcome of robotic surgery in morbidly obese patient with endometrial cancer compared to laparotomy. Int J Gynecolog Cancer: Official J Int Gynecolog Cancer Society. (2012) 22:76–81. doi: 10.1097/IGC.0b013e3182353371

PubMed Abstract | Crossref Full Text | Google Scholar

44. Geppert, B, Lönnerfors, C, and Persson, J. Robot-assisted laparoscopic hysterectomy in obese and morbidly obese women: surgical technique and comparison with open surgery. Acta Obstet Gynecol Scand. (2011) 90:1210–7. doi: 10.1111/j.1600-0412.2011.01253.x

PubMed Abstract | Crossref Full Text | Google Scholar

45. Tang, KY, Gardiner, SK, Gould, C, Osmundsen, B, Collins, M, and Winter, WE 3rd. Robotic surgical staging for obese patients with endometrial cancer. Am J Obstet Gynecol. (2012) 206:513.e1–6. doi: 10.1016/j.ajog.2012.01.002

Crossref Full Text | Google Scholar

46. Acholonu, UC Jr, Chang-Jackson, SC, Radjabi, AR, and Nezhat, FR. Laparoscopy for the management of early-stage endometrial cancer: from experimental to standard of care. J Minim Invasive Gynecol. (2012) 19:434–42. doi: 10.1016/j.jmig.2012.02.006

PubMed Abstract | Crossref Full Text | Google Scholar

47. El-Achi, V, Weishaupt, J, Carter, J, and Saidi, S. Robotic versus laparoscopic hysterectomy in morbidly obese women for endometrial cancer. J Robot Surg. (2021) 15:483–7. doi: 10.1007/s11701-020-01133-z

PubMed Abstract | Crossref Full Text | Google Scholar

48. Leitao, MM, Narain, WR, Boccamazzo, D, Sioulas, V, Cassella, D, Ducie, JA, et al. Impact of robotic platforms on surgical approach and costs in the Management of Morbidly Obese Patients with newly diagnosed uterine Cancer. Ann Surg Oncol. (2016) 23:2192–8. doi: 10.1245/s10434-015-5062-6

PubMed Abstract | Crossref Full Text | Google Scholar

49. Balla, A, Quaresima, S, Subiela, JD, Shalaby, M, Petrella, G, and Sileri, P. Outcomes after rectosigmoid resection for endometriosis: a systematic literature review. Int J Colorectal Dis. (2018) 33:835–47. doi: 10.1007/s00384-018-3082-y

PubMed Abstract | Crossref Full Text | Google Scholar

50. Ruffo, G, Sartori, A, Crippa, S, Partelli, S, Barugola, G, Manzoni, A, et al. Laparoscopic rectal resection for severe endometriosis of the mid and low rectum: technique and operative results. Surg Endosc. (2012) 26:1035–40. doi: 10.1007/s00464-011-1991-8

PubMed Abstract | Crossref Full Text | Google Scholar

51. Bourdel, N, Jaillet, L, Bar-Shavit, Y, Comptour, A, Pereira, B, Canis, M, et al. Indocyanine green in deep infiltrating endometriosis: a preliminary feasibility study to examine vascularization after rectal shaving. Fertil Steril. (2020) 114:367–73. doi: 10.1016/j.fertnstert.2020.03.042

PubMed Abstract | Crossref Full Text | Google Scholar

52. Lim, PC, Kang, E, and Park Do, H. Robot-assisted total intracorporeal low anterior resection with primary anastomosis and radical dissection for treatment of stage IV endometriosis with bowel involvement: morbidity and its outcome. J Robot Surg. (2011) 5:273–8. doi: 10.1007/s11701-011-0272-9

PubMed Abstract | Crossref Full Text | Google Scholar

53. Le Gac, M, Ferrier, C, Touboul, C, Owen, C, Arfi, A, Boudy, AS, et al. Comparison of robotic versus conventional laparoscopy for the treatment of colorectal endometriosis: pilot study of an expert center. J Gynecol Obstetrics Human Reprod. (2020) 49:101885. doi: 10.1016/j.jogoh.2020.101885

PubMed Abstract | Crossref Full Text | Google Scholar

54. Raimondo, D, Alboni, C, Orsini, B, Aru, AC, Farulla, A, Maletta, M, et al. Comparison of perioperative outcomes between standard laparoscopic and robot-assisted approach in patients with rectosigmoid endometriosis. Acta Obstet Gynecol Scand. (2021) 100:1740–6. doi: 10.1111/aogs.14170

PubMed Abstract | Crossref Full Text | Google Scholar

55. Naem, A, Andrikos, A, Constantin, AS, Khamou, M, Andrikos, D, Laganà, AS, et al. Diaphragmatic endometriosis-a single-center retrospective analysis of the Patients' demographics, symptomatology, and long-term treatment outcomes. J Clin Med. (2023) 12. doi: 10.3390/jcm12206455

PubMed Abstract | Crossref Full Text | Google Scholar

56. Redwine, DB . Diaphragmatic endometriosis: diagnosis, surgical management, and long-term results of treatment. Fertil Steril. (2002) 77:288–96. doi: 10.1016/S0015-0282(01)02998-3

PubMed Abstract | Crossref Full Text | Google Scholar

57. Ceccaroni, M, Roviglione, G, Farulla, A, Bertoglio, P, Clarizia, R, Viti, A, et al. Minimally invasive treatment of diaphragmatic endometriosis: a 15-year single referral center's experience on 215 patients. Surg Endosc. (2021) 35:6807–17. doi: 10.1007/s00464-020-08186-z

PubMed Abstract | Crossref Full Text | Google Scholar

58. Andres, MP, Arcoverde, FVL, Souza, CCC, Fernandes, LFC, Abrão, MS, and Kho, RM. Extrapelvic endometriosis: a systematic review. J Minim Invasive Gynecol. (2020) 27:373–89. doi: 10.1016/j.jmig.2019.10.004

PubMed Abstract | Crossref Full Text | Google Scholar

59. Visouli, AN, Darwiche, K, Mpakas, A, Zarogoulidis, P, Papagiannis, A, Tsakiridis, K, et al. Catamenial pneumothorax: a rare entity? Report of 5 cases and review of the literature. J Thorac Dis. (2012) 4:17–31. doi: 10.3978/j.issn.2072-1439.2012.s006

PubMed Abstract | Crossref Full Text | Google Scholar

60. Ribeiro, MD, Freire, T, Leite, F, Werebe, E, Cabrera Carranco, R, and Kondo, WW. The importance of early diagnosis and treatment of incidental tension pneumothorax during robotic assisted laparoscopy for diaphragmatic endometriosis: a report of two cases. Facts Views Vis Obgyn. (2021) 13:95–8. doi: 10.52054/FVVO.13.1.010

PubMed Abstract | Crossref Full Text | Google Scholar

61. Bourdel, N, Fava, V, Budianu, MA, Chauvet, P, Canis, M, and Chadeyras, JB. Laparoscopic resection of diaphragmatic endometriosis in 10 steps. J Minim Invasive Gynecol. (2019) 26:1224–5. doi: 10.1016/j.jmig.2019.04.008

PubMed Abstract | Crossref Full Text | Google Scholar

62. Roman, H, Dennis, T, Grigoriadis, G, and Merlot, B. Robotic Management of Diaphragmatic Endometriosis in 10 steps. J Minim Invasive Gynecol. (2022) 29:707–8. doi: 10.1016/j.jmig.2022.03.005

PubMed Abstract | Crossref Full Text | Google Scholar

63. Dunn, T, and Misra, L. Intraoperative Capnothorax during robotic diaphragmatic endometriosis excision. Case Reports in Anesthesiol. (2022) 2022:1–3. doi: 10.1155/2022/5935312

Crossref Full Text | Google Scholar

64. Naem, A, and Laganà, AS. Editorial: minimally invasive surgery as a mean of improving fertility: what do we know so far? Front Surg. (2023) 10:1203816. doi: 10.3389/fsurg.2023.1203816

PubMed Abstract | Crossref Full Text | Google Scholar

65. Nezhat, C, Falik, R, McKinney, S, and King, LP. Pathophysiology and management of urinary tract endometriosis. Nat Rev Urol. (2017) 14:359–72. doi: 10.1038/nrurol.2017.58

PubMed Abstract | Crossref Full Text | Google Scholar

66. Di Maida, F, Mari, A, Morselli, S, Campi, R, Sforza, S, Cocci, A, et al. Robotic treatment for urinary tract endometriosis: preliminary results and surgical details in a high-volume single-institutional cohort study. Surg Endosc. (2020) 34:3236–42. doi: 10.1007/s00464-020-07502-x

PubMed Abstract | Crossref Full Text | Google Scholar

67. Antonelli, A . Urinary tract endometriosis. Urologia. (2012) 79:167–70. doi: 10.5301/RU.2012.9683

Crossref Full Text | Google Scholar

68. Philip, CA, Froc, E, Chapron, C, Hebert, T, Douvier, S, Filipuzzi, L, et al. Surgical Management of Urinary Tract Endometriosis: a 1-year longitudinal multicenter pilot study at 31 French hospitals (by the FRIENDS group). J Minim Invasive Gynecol. (2021) 28:1889–97.e1. doi: 10.1016/j.jmig.2021.04.020

PubMed Abstract | Crossref Full Text | Google Scholar

69. Uccella, S, Cromi, A, Casarin, J, Bogani, G, Pinelli, C, Serati, M, et al. Laparoscopy for ureteral endometriosis: surgical details, long-term follow-up, and fertility outcomes. Fertil Steril. (2014) 102:160–6.e2. doi: 10.1016/j.fertnstert.2014.03.055

PubMed Abstract | Crossref Full Text | Google Scholar

70. Giannini, A, Pisaneschi, S, Malacarne, E, Cela, V, Melfi, F, Perutelli, A, et al. Robotic approach to ureteral endometriosis: surgical features and perioperative outcomes. Front Surg. (2018) 5:51. doi: 10.3389/fsurg.2018.00051

PubMed Abstract | Crossref Full Text | Google Scholar

71. Frick, AC, Barakat, EE, Stein, RJ, Mora, M, and Falcone, T. Robotic-assisted laparoscopic management of ureteral endometriosis. JSLS: J Society of Laparoendoscopic Surgeons. (2011) 15:396–9. doi: 10.4293/108680811X13125733356314

PubMed Abstract | Crossref Full Text | Google Scholar

72. Hung, ZC, Hsu, TH, Jiang, LY, Chao, WT, Wang, PH, Chen, WJ, et al. Robot-assisted laparoscopic ureteral reconstruction for ureter endometriosis: case series and literature review. J Chinese Med Assoc: JCMA. (2020) 83:288–94. doi: 10.1097/JCMA.0000000000000249

PubMed Abstract | Crossref Full Text | Google Scholar

73. Possover, M, Baekelandt, J, Flaskamp, C, Li, D, and Chiantera, V. Laparoscopic neurolysis of the sacral plexus and the sciatic nerve for extensive endometriosis of the pelvic wall. Minimally Invasive Neurosurg: MIN. (2007) 50:33–6. doi: 10.1055/s-2007-970075

PubMed Abstract | Crossref Full Text | Google Scholar

74. Denton, RO, and Sherrill, JD. Sciatic syndrome due to endometriosis of sciatic nerve. South Med J. (1955) 48:1027–31. doi: 10.1097/00007611-195510000-00004

Crossref Full Text | Google Scholar

75. Lemos, N, Souza, C, Marques, RM, Kamergorodsky, G, Schor, E, and Girão, MJ. Laparoscopic anatomy of the autonomic nerves of the pelvis and the concept of nerve-sparing surgery by direct visualization of autonomic nerve bundles. Fertil Steril. (2015) 104:e11–2. doi: 10.1016/j.fertnstert.2015.07.1138

PubMed Abstract | Crossref Full Text | Google Scholar

76. Roman, H, Dehan, L, Merlot, B, Berby, B, Forestier, D, Seyer-Hansen, M, et al. Postoperative outcomes after surgery for deep endometriosis of the sacral plexus and sciatic nerve: a 52-patient consecutive series. J Minim Invasive Gynecol. (2021) 28:1375–83. doi: 10.1016/j.jmig.2020.10.018

PubMed Abstract | Crossref Full Text | Google Scholar

77. Clarizia, R, Manzone, M, Roviglione, G, Bruni, F, Ceccarello, M, Mautone, D, et al. Laparoscopic nerve Detrapment and Neurolysis of somatic pelvic nerves in deep endometriosis: prospective study of 433 patients. J Minim Invasive Gynecol. (2022) 29:S34. doi: 10.1016/j.jmig.2022.09.111

Crossref Full Text | Google Scholar

78. Possover, M, Schneider, T, and Henle, KP. Laparoscopic therapy for endometriosis and vascular entrapment of sacral plexus. Fertil Steril. (2011) 95:756–8. doi: 10.1016/j.fertnstert.2010.08.048

PubMed Abstract | Crossref Full Text | Google Scholar

79. Vilos, GA, Vilos, AW, and Haebe, JJ. Laparoscopic findings, management, histopathology, and outcome of 25 women with cyclic leg pain. J Am Assoc Gynecol Laparosc. (2002) 9:145–51. doi: 10.1016/S1074-3804(05)60122-3

PubMed Abstract | Crossref Full Text | Google Scholar

80. Possover, M . Five-year follow-up after laparoscopic large nerve resection for deep infiltrating sciatic nerve endometriosis. J Minim Invasive Gynecol. (2017) 24:822–6. doi: 10.1016/j.jmig.2017.02.027

PubMed Abstract | Crossref Full Text | Google Scholar

81. Roman, H, Crestani, A, and Merlot, B. Excision of deep endometriosis nodules of the sciatic nerve using robotic assistance, with video. J Visc Surg. (2022) 159:74–6. doi: 10.1016/j.jviscsurg.2021.11.007

PubMed Abstract | Crossref Full Text | Google Scholar

82. Roman, H, Seyer-Hansen, M, Dennis, T, and Merlot, B. Excision of deep endometriosis nodules of the sciatic nerve in 10 steps. J Minim Invasive Gynecol. (2021) 28:1685–6. doi: 10.1016/j.jmig.2021.05.019

PubMed Abstract | Crossref Full Text | Google Scholar

83. Kanno, K, Aiko, K, Yanai, S, Sawada, M, Sakate, S, and Andou, M. Clinical use of indocyanine green during nerve-sparing surgery for deep endometriosis. Fertil Steril. (2021) 116:269–71. doi: 10.1016/j.fertnstert.2021.03.014

PubMed Abstract | Crossref Full Text | Google Scholar

84. Gurusamy, KS, Aggarwal, R, Palanivelu, L, and Davidson, BR. Virtual reality training for surgical trainees in laparoscopic surgery. Cochrane Database of Syst Rev: Rev. (2009):Cd006575. doi: 10.1002/14651858.CD006575.pub2

Crossref Full Text | Google Scholar

85. Wottawa, CR, Genovese, B, Nowroozi, BN, Hart, SD, Bisley, JW, Grundfest, WS, et al. Evaluating tactile feedback in robotic surgery for potential clinical application using an animal model. Surg Endosc. (2016) 30:3198–209. doi: 10.1007/s00464-015-4602-2

PubMed Abstract | Crossref Full Text | Google Scholar

86. Pavone, M, Goglia, M, Campolo, F, Scambia, G, and Ianieri, MM. En-block butterfly excision of posterior compartment deep endometriosis: the first experience with the new surgical robot Hugo™ RAS. Facts Views Vis Obgyn. (2023) 15:359–62. doi: 10.52054/FVVO.14.5.104

PubMed Abstract | Crossref Full Text | Google Scholar

87. Olsen, RG, Hartwell, D, Dalsgaard, T, Madsen, ME, Bjerrum, F, Konge, L, et al. First experience with the Hugo™ robot-assisted surgery system for endometriosis: a descriptive study. Acta Obstet Gynecol Scand. (2024) 103:368–77. doi: 10.1111/aogs.14727

PubMed Abstract | Crossref Full Text | Google Scholar

88. Pavone, M, Seeliger, B, Alesi, MV, Goglia, M, Marescaux, J, Scambia, G, et al. Initial experience of robotically assisted endometriosis surgery with a novel robotic system: first case series in a tertiary care center. Updates Surg. (2024) 76:271–7. doi: 10.1007/s13304-023-01724-z

PubMed Abstract | Crossref Full Text | Google Scholar

89. Berlanda, N, Frattaruolo, MP, Aimi, G, Farella, M, Barbara, G, Buggio, L, et al. 'Money for nothing'. The role of robotic-assisted laparoscopy for the treatment of endometriosis. Reprod Biomed Online. (2017) 35:435–44. doi: 10.1016/j.rbmo.2017.05.010

PubMed Abstract | Crossref Full Text | Google Scholar

90. Byrn, JC, Hrabe, JE, and Charlton, ME. An initial experience with 85 consecutive robotic-assisted rectal dissections: improved operating times and lower costs with experience. Surg Endosc. (2014) 28:3101–7. doi: 10.1007/s00464-014-3591-x

PubMed Abstract | Crossref Full Text | Google Scholar

91. Turco, LC, Tortorella, L, Tuscano, A, Palumbo, MA, Fagotti, A, Uccella, S, et al. Surgery-related complications and long-term functional morbidity after segmental Colo-rectal resection for deep infiltrating endometriosis (ENDO-RESECT morb). Arch Gynecol Obstet. (2020) 302:983–93. doi: 10.1007/s00404-020-05694-0

PubMed Abstract | Crossref Full Text | Google Scholar

92. Kavallaris, A, Chalvatzas, N, Kelling, K, Bohlmann, MK, Diedrich, K, and Hornemann, A. Total laparoscopic hysterectomy without uterine manipulator: description of a new technique and its outcome. Arch Gynecol Obstet. (2011) 283:1053–7. doi: 10.1007/s00404-010-1494-1

PubMed Abstract | Crossref Full Text | Google Scholar

93. Ceccaroni, M, Clarizia, R, Bruni, F, D'Urso, E, Gagliardi, ML, Roviglione, G, et al. Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: the Negrar method. A single-center, prospective, clinical trial. Surg Endosc. (2012) 26:2029–45. doi: 10.1007/s00464-012-2153-3

PubMed Abstract | Crossref Full Text | Google Scholar

94. Asimakopoulos, AD, Pereira Fraga, CT, Annino, F, Pasqualetti, P, Calado, AA, and Mugnier, C. Randomized comparison between laparoscopic and robot-assisted nerve-sparing radical prostatectomy. J Sex Med. (2011) 8:1503–12. doi: 10.1111/j.1743-6109.2011.02215.x

PubMed Abstract | Crossref Full Text | Google Scholar

Keywords: endometriosis, robotic surgery, laparoscopy, diaphragm, urinary tract, Colon, rectum

Citation: Ferrari FA, Youssef Y, Naem A, Ferrari F, Odicino F, Krentel H and Moawad G (2024) Robotic surgery for deep-infiltrating endometriosis: is it time to take a step forward? Front. Med. 11:1387036. doi: 10.3389/fmed.2024.1387036

Received: 16 February 2024; Accepted: 26 February 2024;
Published: 05 March 2024.

Edited by:

Rafał Watrowski, Helios Hospital Müllheim, Germany

Reviewed by:

Matteo Pavone, Agostino Gemelli University Polyclinic (IRCCS), Italy
Manuel Maria Ianieri, Agostino Gemelli University Polyclinic (IRCCS), Italy

Copyright © 2024 Ferrari, Youssef, Naem, Ferrari, Odicino, Krentel and Moawad. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Antoine Naem, YW50b2luZS5uYWVtQGdtYWlsLmNvbQ==

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