{"paper_id":"6a659863-eaec-4ceb-8569-52ae38620404","body_text":"Vol.:(0123456789)1 3\nJournal of Robotic Surgery (2023) 17:2743–2747 \nhttps://doi.org/10.1007/s11701-023-01704-w\nRESEARCH\nWhat is the role of robotic surgery in ovarian cystectomy with fertility \npreservation?\nJu Hye Lee1 · So Yun Park2 · Kyungah Jeong1 · Ha Yeoung Yun1 · Hye Won Chung1\nReceived: 11 June 2023 / Accepted: 19 August 2023 / Published online: 10 September 2023 \n© The Author(s) 2023\nAbstract\nTo investigate the role of robotic single-site (RSS) ovarian cystectomy in fertility preservation, which was compared with \nsingle-port laparoscopic (SPL) surgery based on AMH changes. We retrospectively analyzed medical records of total 156 \npatients who underwent SPL (n  = 72) or RSS (n  = 84) surgery with the da  Vinci® Si or Xi system. The pre/post-operative \nAMH levels and total diameter of ovarian cysts were measured. In addition to the surgical method, AMH changes were \ncompared according to the laterality, multiplicity, and pathology of ovarian cysts. A comparison of the characteristics of the \nSPL group and RSS group, revealed that there were no significant differences in the average age, the diameter of the ovar -\nian cyst, and the number of locule. There were also no statistical differences between the pre-operative and post-operative \nAMH levels and the average surgical time including the docking time in robotic surgery. A comparison based on the surgi-\ncal methods, revealed that the decrease in post-operative AMH was lower in the RSS group (24.2 ± 35.9%) than in the SPL \ngroup (34.9 ± 29.1%) significantly (p = 0.044). In patients with endometriosis, the decrease in AMH was greater, than that \nin patients without endometriosis. A longer operation time, larger ovarian cysts and multi-locular cysts were associated with \nlower AMH level in both the SPL and RSS groups (Pearson correlation coefficient: – 0.320, p = 0.0001, – 0.218, p = 0.007,  \n– 0.236, p = 0.003, respectively). RSS ovarian cystectomy could be a promising new therapeutic option for fertility preserva-\ntion in complex cases to avoid an additional side port.\nKeywords Robotic single-site surgery · Single-port laparoscopic surgery · Anti-Müllerian hormone · Endometriosis\nIntroduction\nOvarian tumors are common in reproductive-aged women \nwho visit the gynecologic clinic. In the United States, it has \nbeen estimated that as many as 10% of women will undergo \nsurgical removal of an adnexal mass during their lifetime [1]. \nParticularly, endometriosis is a common gynecological dis-\nease that occurs in 5–10% of reproductive-aged women. Its \nincidence tends to increase gradually with early menarche, \ndelayed pregnancy, and decreased childbirth. Ovarian endo-\nmetriomas are found in 20% of patients with endometriosis. \nAlthough the progestin, dienogest is widely used as a treat-\nment for endometriosis, ovarian cystectomy seems to be the \nfavored modality of most gynecologists, given that complete \nexcision is associated with reduced disease recurrence [2 ].\nVarious studies have reported an increased risk of ovarian \ndamage and decreased ovarian reserve after ovarian cystec-\ntomy. To preserve ovarian function, suturing for hemostasis \nafter ovarian cystectomy is superior to electro-cauterization \nwith thermal energy [3–5].\nRecently, minimally invasive surgery is becoming \nincreasingly popular in the gynecological field owing to a \nshort hospitalization period, rapid recovery, and cosmetic \nbenefits [ 6]. Most young reproductive-aged women want \na fast recovery and less scarring. For this reason, mini-\nmally invasive surgery with a single incision is increasingly \npreferred. In accordance with this trend, single-port lapa-\nroscopic (SPL) surgery is being developed as a treatment \nJu Hye Lee and So Yun Park contributed equally to the manuscript.\n * Kyungah Jeong \n ogjeong@ewha.ac.kr\n1 Department of Obstetrics and Gynecology, College \nof Medicine, Ewha Womans University Mokdong Hospital, \nEwha Womans University, 1071, AnYangCheon-Ro, \nYangCheon-Gu, Seoul 07985, Korea\n2 Department of Obstetrics and Gynecology, Ewha Womans \nUniversity Seoul Hospital, College of Medicine, Ewha \nWomans University, Seoul, South Korea\n\n2744 Journal of Robotic Surgery (2023) 17:2743–2747\n1 3\noption. However, SPL surgery has some limitations due to \nthe use of semi-rigid and non-articulating instruments [7, 8].\nWith the adoption of the da Vinci® system (Intuitive \nSurgical Inc., Sunnyvale, CA, USA), it has become possible \novercome the shortcomings of laparoscopic surgery. Robotic \nsurgery reduces hospital stays and the amount of bleeding \nduring surgery by allowing surgeons to more easily conduct \ncomplicated procedures with enhanced visualization and \nwristed instruments [9].\nAnti-Müllerian hormone (AMH) is a dimeric glycopro-\ntein member of the transforming growth factor β-family. [10] \nIt is produced by granulosa cells of small, growing follicles \nin the ovary. It is also well known for its role in sexual dif-\nferentiation. Serum AMH level is strongly correlated with \nthe number of growing follicles; thus, AMH has attracted \nincreasing attention as a golden marker of ovarian reserve \n[11, 12]. Accumulating evidence suggests that AMH is the \nbest currently available measure of ovarian reserve.\nTherefore, we aimed to investigate the role of \nrobotic single-site (RSS) ovarian cystectomy in fertility \npreservation, which was compared with SPL surgery based \non AMH changes.\nMaterials and methods\nThis study was conducted as a retrospective chart review \non 156 patients who were planned for ovarian cystectomy \nvia RSS (n = 84) or SPL (n = 72) surgery at Ewha Womans \nUniversity Mokdong and Seoul Hospital from March 2017 \nto March 2023. All included patients underwent ovarian \nsurgery due to benign gynecologic diseases, which were \ndiagnosed based on the final pathology. Their ages ranged \nfrom 16 to 43 years. A total of 72 patients underwent lapa-\nroscopic surgery, and 84 patients underwent RSS ovarian \ncystectomy with the da Vinci Si or Xi system. All opera-\ntions were performed through the umbilicus with a Glove \nPort (NELIS, Seoul, Republic of Korea).\nSerum samples for AMH measurement were collected \nfrom each patient preoperatively and postoperatively. The \ntime of postoperative AMH measurement was determined \nin months from the time of operation to AMH measure-\nment after the operation. The serum AMH level was meas-\nured by electrochemiluminescence immunoassay using \nthe Elecsys AMH Plus reagent (Roche Diagnostics, Man-\nnheim, Germany).\nThe size of the ovarian cyst was determined based on \nthe sum of the average diameters measured by transvaginal \nor transrectal sonography before surgery. In addition to the \nsurgical method, AMH changes were compared accord -\ning to the laterality, multiplicity, and pathology of ovarian \ncysts. Pearson’s correlation was determined between the \npercentage of AMH reduction and total operation time, \ndiameter of the ovarian cyst, or number of locule. To eval-\nuate the ovarian reserve after surgery, the change between \npre-operative and post-operative serum AMH levels was \nmeasured.\nStatistical analysis was performed using SPSS ver -\nsion 22 (IBM, Seoul, Republic of Korea). All values with \np < 0.05 were considered as statistically significant. This \nstudy was approved by the Institutional Review Board of \nEwha Womans University Mokdong Hospital (IRB No. \n2020-04-029).\nResults\nAll 84 patients in the RSS group underwent ovarian cys -\ntectomy through the umbilicus successfully with only one \nscar. On the other hand, 45 (62.5%) of 72 patients in the SPL \ngroup needed one or two additional ports because the SPL \napproach has some limitations such as the range of motion \nwith rigid instruments. Additionally, in the RSS group, \nendometriosis, adhesion, and bilaterality accounted for 69%, \n78.6%, and 38.1% of patients, respectively compared with \nthose in the SPL group, 59.7%, 69.4%, and 30.6%, respec-\ntively (Fig.  1). There were additional complex cases in the \nRSS group compared with the SPL group.\nThe clinical characteristics, pre/post-operative AMH \nlevels, number of locule, total diameter of the ovarian \ncyst, and mean operation time are summarized in Table  1. \nA comparison of the characteristics of the SPL group \nand RSS group, revealed that there were no significant \ndifferences in the average age (29.0 ± 5.6 in the SPL group \nvs 28.2 ± 4.5 in the RSS group), the diameter of the ovarian \ncyst (7.10 ± 3.07 cm in the SPL group vs 7.98 ± 3.70 cm in \nthe RSS group), and the number of locules (1.8 ± 1.3 in the \nSPL group vs 2.1 ± 1.5 in the RSS group). There were also \nno statistical differences between the pre-operative and post-\noperative AMH levels (preoperative AMH 3.59 ± 1.95 ng/\nmL in the SPL group vs 3.45 ± 1.94 ng/mL in the RSS \ngroup, Post-operative AMH 2.53 ± 2.07 ng/mL in the SPL \ngroup vs 2.49  ± 1.58 ng/mL in the RSS group) and the \naverage surgical time (95.4 ± 33.2 min in the SPL group vs \n89.0 ± 26.7 min in the RSS group) including the docking \ntime in robotic surgery.\nAfter surgery, patients with endometriosis received hormone \nsuppression therapy with a GnRH agonist or dienogest, and the \nmeasured AMH level ranged from 20 to 30% to 50% lower on \naverage. A comparison of the number of patients who received \nhormone suppression therapy at the time of post-operative AMH \nmeasurement between the two groups, demonstrated that the \nnumber of patients in the SPL group (46 of 72 patients; 63.9%) \nwas relatively smaller than that of patients in the RSS group (62 \nout of 84 patients; 73.8%). The time of post-operative AMH \nmeasurement was an average of 5.5 months in the SPL group \n\n2745Journal of Robotic Surgery (2023) 17:2743–2747 \n1 3\nand 4.1 months in the RSS group after surgery, which showed \nno significant difference.\nAMH levels before and after surgery were compared \nbetween the SPL and RSS groups. Data on the percentage \nof AMH reduction after surgery are shown in Table  2. A \ncomparison based on the surgical methods, revealed that \nthe decrease in post-operative AMH was lower in the RSS \ngroup (24.2 ± 35.9%) than in the SPL group (34.9 ± 29.1%), \nshowing a statistically significant difference (p  = 0.044). \nIn patients with endometriosis, the decrease in AMH was \ngreater (35.9 ± 31.7%), than that in patients without endo-\nmetriosis (17.8 ± 33.1%), which also showed a statistically \nsignificant difference (p = 0.001). In addition, AMH reduc-\ntion was significant in the bilateral group compared with \nthe unilateral group (– 42.7 ± 30.7% in the bilateral group \nvs – 21.7 ± 32.4% in the unilateral group, p  = 0.0001). The \ndecrease in AMH was significant in the group with pel-\nvic adhesion compared with the group without adhesion \n(– 35.6 ± 30.7% in the adhesion group vs – 10.9 ± 33.9% in \nthe non-adhesion group, p = 0.0001).\nThe correlations between the percentage of AMH reduc-\ntion and various factors were analyzed using Pearson’s correla-\ntion coefficient. The correlation coefficient between the total \noperation time and percentage of AMH reduction indicated a \nsignificant negative correlation at – 0.320 (p = 0.0001), and the \ncorrelation coefficients indicated the significant negative corre-\nlation of the diameter of the ovarian cyst and number of locule \nwith the percentage of AMH reduction at – 0.214 (p = 0.007) \nand – 0.236 (p = 0.003), respectively (Table 3). In other words, \na longer operation time, larger ovarian cysts and multi-locular \ncysts were associated with lower AMH level in both the SPL \nand RSS groups.\nDiscussion\nLimited studies have compared for AMH levels after ovar -\nian cystectomy using a robotic system and a laparoscopic \ntechnique. In this study, a comparison between SPL surgery \nand RSS surgery demonstrated that, unlike the SPL tech-\nnique, the RSS system was feasible without additional ports, \nhowever, there were additional complex cases in the RSS \ngroup than in the SPL group due to the disadvantages of SPL \nsurgery such as collisions and clashing of instruments and a \nlimited range of motion [13, 14].\nFig. 1  Characteristics of RSS \nand SPL ovarian cystectomy. \nRSS Robotic single-site; SPL \nSingle-port laparoscopic\nTable 1  Clinical characteristics of patients\nSPL single-port laparoscopic; RSS robotic single-site; AMH anti- \nMüllerian hormone\na Values are presented as mean ± standard deviation\nSPL (n = 72) RSS (n = 84) p-value\nAge (years) 29.0 ± 5.6 28.2 ± 4.5 NS\nTotal diameter of ovarian cyst \n(cm)\n7.10 ± 3.07 7.98 ± 3.70 NS\nNumber of locule 1.8 ± 1.3 2.1 ± 1.5 NS\nDuration from operation to \npost-operative AMH test \n(month)\n5.5 ± 4.1 4.1 ± 7.3 NS\nPre-operative AMH (ng/mL) 3.59 ± 1.95 3.45 ± 1.94 NS\nPost-operative AMH (ng/mL) 2.53 ± 2.07 2.49 ± 1.58 NS\nMean operation time (min) 95.4 ± 33.2 89.0 ± 26.7 NS\n\n2746 Journal of Robotic Surgery (2023) 17:2743–2747\n1 3\nIt is well known that endometriomas can result in a \ngreater reduction in AMH level after surgery compared with \nother benign ovarian cysts such as teratomas of the ova-\nries due to adhesion. In this study, AMH tended to decrease \nfurther when accompanied by endometriosis. In addition, \ngreater AMH reduction in the presence of bilateral ovarian \ncysts and adhesion suggests that the more complex and dif-\nficult the surgery, the more the ovarian parenchyma can be \ndestroyed, and a meticulous surgery should be performed.\nA longer surgery time, a larger ovarian cyst size, and a \ngreater number of locule were negatively correlated with \nAMH changes. Therefore, in terms of fertility preservation, \nthe RSS system rather than SPL surgery should be used for \novarian cystectomy in more complex cases, such as endome-\ntriosis, or larger, multilocular or bilateral cysts with adhesion.\nSince the initial approval of robotic surgery for gynecologic \noperation in 2005, its use has been widely adopted, and its appli-\ncation has been expanded. However, the role of robotic surgery \nin case of benign ovarian tumors including endometriosis \nremains controversial. Operative times are consistently longer in \nrobotic surgery with no differences in quality of life and fertility \noutcomes. Berlanda et al. published an article titled “Money for \nnothing” on the role of robotic assisted laparoscopy in the treat-\nment of endometriosis [15]. Soto et al. reported a multicenter, \nrandomized, controlled trial comparing laparoscopy with robotic \nsurgery for endometriosis in 2017. They concluded that there \nwere no differences in perioperative outcomes between robotic \nand conventional laparoscopy [16].\nHowever, with the development of robotic systems, RSS \nsurgery has been upgraded with the da  Vinci® Xi system. In \naddition, with the development and release of the 4th genera-\ntion da  Vinci® single-port (SP) system specialized in single-\nsite surgery, robotic surgery has progressed tremendously. All \ninstruments in the da  Vinci® SP system have two joints, allowing \nmore delicate movements and the use of strong and diversified \ninstruments rather than conventional unsteady ones, making \nthem considerably more useful. Even if the surgery is complex, \nthe new da  Vinci® SP surgical system might be more feasible \nand safer, than RSS surgery with Si or Xi system. [17]\nOvarian surgery can reduce the ovarian reserve, espe-\ncially in cases of excessive coagulation for bleeding control. \nSuturing for hemostasis after ovarian cystectomy is supe-\nrior to thermal energy in preserving ovarian function [18]. \nTherefore, it is desirable to preserve ovarian function by \navoiding excessive manipulation using energy for hemostasis \nand suturing rapidly and accurately using a robotic system \nfor easy manipulation. Lee et al. suggested that ovarian func-\ntion may be better preserved with robotic ovarian cystectomy \ncompared with the laparoscopic approach for bilateral ovar-\nian endometriomas [19].\nIn the new da  Vinci® SP system, the scissors, which were \nnot available in the Si or Xi single-site system, were included \nto avoid tissue destruction due to electro-cauterization by \nallowing cold cut and fast suturing as much as possible. In \nthe future, RSS surgery using the da  Vinci® SP system could \nbe expected to have a better effect on fertility preservation \ncompared with that of SPL surgery.\nOur study has some limitations. First, since it is a retro-\nspective comparison study, more complex surgeries might \nbe selected for the RSS system. Second, the number of \npatients in the SPL group is slightly lower than that in the \nRSS group. However, there was no significant difference in \ncharacteristics between the two groups.\nAlthough there were additional complex cases and a \nhigher number of hormone suppression therapy patients at \nthe time of post-operative AMH measurement in the RSS \ngroup, the decrease in AMH after ovarian cystectomy was \nlower in the RSS group than in the SPL group. Therefore, \nthe advantages of robotic system for ovarian cystectomy \nmight be supposed in terms of fertility preservation.\nTable 2  Percentage of AMH \nreduction after ovarian \ncystectomy\nAMH anti-Müllerian hormone; SPL single-port laparoscopic; RSS robotic single-site\na Values are presented as mean ± standard deviation\nType of surgery (%) SPL (n = 72) RSS (n = 84) p-value\n – 34.9 ± 29.1  – 24.2 ± 35.9 0.044\nPathology (%) Endometriosis (n = 98) Non-endometriosis (n = 58) p-value\n – 35.9 ± 31.7  – 17.8 ± 33.1 0.001\nLaterality (%) Bilateral (n = 55) Unilateral (n = 101) p-value\n – 42.7 ± 30.7  – 21.7 ± 32.4 0.0001\nAdhesion (%) Adhesion (n = 115) Non-adhesion (n = 41) p-value\n – 35.6 ± 30.7  – 10.9 ± 33.9 0.0001\nTable 3  Correlation with serum AMH changes\nAMH anti-Müllerian hormone\nTotal (n = 156) Pearson’s Correlation \nCoefficient\np-value\nTotal operation time (min)  – 0.320 0.0001\nDiameter of the ovarian cyst (cm)  – 0.214 0.007\nNumber of locule  – 0.236 0.003\n\n2747Journal of Robotic Surgery (2023) 17:2743–2747 \n1 3\nIn conclusion, RSS ovarian cystectomy could be a prom-\nising new therapeutic option for fertility preservation in \ncomplex cases to avoid an additional side port. Following \nthe development of a robotic surgery system that could over-\ncome the limitations of laparoscopic surgery for women \nwho need fertility preservation, the application of a robotic \nsurgery system in ovarian cystectomy especially in cases \nof endometriosis should be considered. Further large-scale \nprospective cohort studies should be performed to validate \nthe long-term effects of robotic surgery on fertility pres-\nervation in benign ovarian cystectomy, including cases of \nendometriosis, which may be favorable.\nAuthor contributions All authors contributed to the study conception. \nJHL: data collection and management, investigation and manuscript \nwriting. SYP: data collection and management. KJ: conceptualization, \ndata management, data analysis and manuscript writing. HYY: data \ncollection. HWC: senior author, supervising consultant. All authors \nread and approved the final manuscript.\nFunding The authors declare that no funds, grants, or other support \nwere received during the preparation of this manuscript.\nData availability All data supporting the findings of this study are \navailable from corresponding author on reasonable request.\nDeclarations \nConflict of interest The authors have no relevant financial or non-fi-\nnancial interests to disclose.\nOpen Access This article is licensed under a Creative Commons Attri-\nbution 4.0 International License, which permits use, sharing, adapta-\ntion, distribution and reproduction in any medium or format, as long \nas you give appropriate credit to the original author(s) and the source, \nprovide a link to the Creative Commons licence, and indicate if changes \nwere made. The images or other third party material in this article are \nincluded in the article’s Creative Commons licence, unless indicated \notherwise in a credit line to the material. If material is not included in \nthe article’s Creative Commons licence and your intended use is not \npermitted by statutory regulation or exceeds the permitted use, you will \nneed to obtain permission directly from the copyright holder. To view a \ncopy of this licence, visit http://creativecommons.org/licenses/by/4.0/.\nReferences\n 1. Hilger WS, Magrina JF, Magtibay PM (2006) Laparoscopic man-\nagement of the adnexal mass. Clin Obstet Gynecol 49(3):535–548\n 2. Kostrzewa M, Wilczyński JR, Głowacka E, Żyła M, Szyłło K, Sta-\nchowiak G (2019) One-year follow-up of ovarian reserve by three \nmethods in women after laparoscopic cystectomy for endometrioma \nand benign ovarian cysts. Int J Gynaecol Obstet 146(3):350–356\n 3. Tsolakidis D, Pados G, Vavilis D, Athanatos D, Tsalikis T, Gianna-\nkou A et al (2010) The impact on ovarian reserve after laparoscopic \novarian cystectomy versus three-stage management in patients \nwith endometriomas: a prospective randomized study. 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Eur J Obstet Gynecol Reprod \nBiol 249:9–13\nPublisher's Note Springer Nature remains neutral with regard to \njurisdictional claims in published maps and institutional affiliations.","source_license":"CC0","license_restricted":false}