- Email: [email protected]
Laparoscopic surgery in gynaecological oncology
EJSO 32 (2006) 853e858
www.ejso.com
Laparoscopic surgery in gynaecological oncology D. Querleu a,*, E. Leblanc b, G. Ferron a, F. Narducci b a
De´partement de Chirurgie, Institut Claudius Regaud, 20 rue du Pont Saint Pierre, 31052 Toulouse, France b Department of Gynaecologic Oncology, Centre Oscar Lambret Cancer Center, Lille, France Accepted 23 March 2006 Available online 12 July 2006
Abstract Aims: The use of laparoscopic staging and/or surgery in the field of gynaecological oncology was pioneered in the late 1980s and the first reports were published in the early 1990s. The issue has been initially most controversial, and is still debated, with some justification considering the possible adverse consequences of surgical mismanagement of gynaecologic malignancy. Methods: The current literature has been reviewed and updated, concentrating on long-term, and/or comparative studies. Large observational studies have also been included. Recent papers concerning new developments have been selected. Findings: A number of papers have confirmed the absence of significant adverse effects on survival after laparoscopic diagnosis or surgery in gynaecological cancers. New developments cover virtually all the basic techniques in cancer surgery, including major exenterative surgery. The use of extraperitoneal technique for aortic dissections is emerging as a new tool. New indications, such as radical vaginal trachelectomy, radical parametrectomy, pelvic sentinel node identification, interval debulking surgery of adnexal malignancies, or the use of pretherapeutic surgical staging of uterine cancers, have been developed in direct relation with the use of laparoscopic techniques. Conclusions: Current available data and worldwide interest clearly demonstrate that laparoscopic techniques must now be part of the armamentarium of the gynaecologic oncologist. Postoperative morbidity and recurrence risk do not seem to be affected. Cost-efficiency of laparoscopic procedures is based on the reduction of hospital stay and recovery time, although operating room time is increased in some procedures. Combined training in gynaecologic oncology and in laparoscopic and/or vaginal surgery is more than ever mandatory to avoid the risk of inadequate staging or management of pelvic malignancies. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Laparoscopic surgery; Gynaecological oncology; Lymphadenectomy; Radical hysterectomy; Radical trachelectomy
Laparoscopic surgery in gynaecologic oncology was initially developed in France and in the United States by Daniel Dargent, Denis Querleu, Eric Leblanc, and Joel M. Childers.1 Long-term follow-up of patients and/or careful assessment of complications and drawbacks are now available, while new techniques are still under evaluation. The current literature has been reviewed, and personal data added for this paper. Laparoscopic surgical staging Laparoscopic transperitoneal node dissection The technique of transperitoneal pelvic lymph node dissection is routinely performed in most gynaecologic
* Corresponding author. Tel.: þ33 561 42 41 50; fax: þ33 561 42 41 17. E-mail address: [email protected] (D. Querleu). 0748-7983/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.ejso.2006.03.043
oncology centers as a staging procedure or as a part of surgical management of cervical and endometrial cancers. Several experimental randomized studies by independent investigators have provided evidence that the node count of laparoscopic dissections is not inferior to open dissections.2 The complication rate is extremely low in experienced hands. We have performed 694 transperitoneal lymph node dissections without a single laparotomy for complication. Although less easy, with more limitations, and a longer learning curve, transperitoneal laparoscopic aortic dissection is no longer an investigational procedure. Overall, a conversion rate of 18.5% and a complication rate of 12.4% are observed in our series of transperitoneal laparoscopic lymphadenectomies.3 Other large series from Germany and USA reported similar findings.4,5 Obesity is not a contra-indication and is not associated with a reduction in the number of retrieved nodes. Feasibility is high in patients with a BMI under 35. On the other hand,
854
D. Querleu et al. / EJSO 32 (2006) 853e858
a satisfactory laparoscopic pelvic and low aortic dissection for endometrial cancer is completed in only 44% of patients with a BMI index greater than 35. However, considering the reduction of complication rate and hospital stay provided by the laparoscopic approach, the technique deserves to be attempted in morbidly obese patients.4,6 Sentinel node identification Removal of a single targeted node from a node-bearing area is logically accomplished through minimal incisions. In addition, identification of minute lymphatic channels located deep in the pelvis requires some magnification, as provided by the laparoscope. The first attempts at sentinel node detection involved blue dye injection only. Further development of combined isotopic and blue dye mapping improved the detection rate up to 90%.7 With the development of laparoscopic probes, the concurrent use of radio-labeled colloid injections became possible, improving the detection rate.8 Sentinel nodes may be found in unusual areas such as common iliac or para-aortic sites. The sentinel node concept does not apply to obviously diseased nodes in which lymphatic flow is blocked, making uptake of markers impossible. In early cervical cancers, the finding of a positive sentinel node is considered in our center as in others as a contraindication for upfront surgery, an indication for immediate aortic dissection, and an argument to propose definitive chemoradiation therapy. Further pelvic dissection in such a circumstance is not advised, as it could increase the risk of radiation induced complication. On the other hand, the finding of negative sentinel nodes does not allow to limit pelvic node dissection. In our experience, micrometastasis was found in a non-sentinel node in a sentinel node negative patient,8 in accordance to findings by other groups at laparotomy9 or laparoscopy.10 In endometrial carcinomas, the completion of lymph node dissection is controversial. Pelvic sentinel node sampling could in the future be used as a mid-term between no dissection and full dissection. The finding of a positive pelvic sentinel node is an indication for aortic node dissection or sampling. It is not clear whether intraoperative direct subserosal injection of blue dye is superior to cervical injection for sentinel node identification in endometrial cancers, and intracervical injection is usually preferred,11 although hysteroscopic injection of isotopic tracer is feasible and may be superior.12 Paracervical (parametrial) lymphadenectomy The high short and long-term urinary dysfunction or complication rate of radical hysterectomy has motivated the evolution towards a reduction in radicality. Early cervical carcinomas are presently managed by modified radical hysterectomy, with no apparent increase in the rate of lateropelvic recurrence. However, the well documented finding
of pathologically or biologically positive parametrial nodes suggests a risk of late development of micrometastasis.13 Nerve-sparing dissection of the distal part of the cardinal ligament is supposed to prevent late lateropelvic recurrences without further impairing urinary function. In other terms, the combination of a modified radical hysterectomy with a parametrial lymph node dissection combines the radicality of parametrial resection with the low morbidity of a modified radical hysterectomy. The use of laparoscopic magnification is logically associated with a safe dissection and preservation of the vascular and nerve content of the distal part of the cardinal ligament.14 Laparoscopic extraperitoneal node dissection The common iliac and aortic extension of extraperitoneal dissections15,16 is a novel technique that combines surgical comfort and benefit for the patient in terms of de novo peritoneal adhesions, which is crucial in patients candidate for extended field irradiation.17 The main complication is the formation of giant lymphocysts that were observed at the beginning of our experience. Lymphocyst formation can be prevented if the peritoneum of the paracolic gutter is incised at the end of the procedure, in order to allow intraperitoneal drainage of the extraperitoneal dissection area. In advanced stage cervical cancer patients, the finding of negative common iliac and aortic nodes is a safe indication that aortic fields can be omitted. Our policy is to extend the dissection up to the renal vessels, using a left extraperitoneal approach, with a 27% positivity rate in a series of 111 patients. In our group, 3-year survival is as high as 80% using chemoradiation with pelvic fields in advanced cervical cancers. The finding of positive nodes is an indication of high risk of distant metastasis and death.16 Laparoscopic omentectomy and peritoneal staging of early adnexal carcinomas Careful examination, with the advantage of magnification, of the peritoneal surface and multiple random or oriented biopsies may be accomplished laparoscopically. Omentectomy is performed using electrosurgery, clips, or ultrasound hemostasis techniques. The omentum can be packed in a bag then retrieved through a vaginal or small abdominal incision. Appendectomy, which is part of surgical staging in mucinous adnexal tumors, is routinely performed through the laparoscope. Peritoneal staging is indicated, in conjunction with node dissection, in the reassessment of inadequately staged adnexal cancer patients. Using laparoscopic techniques, 18% of patients are upstaged and need adjuvant chemotherapy.18 Patients definitively classified as stage IA or IB after laparoscopic staging have an excellent prognosis.18 Laparoscopic peritoneal staging may also be proposed in the case of inadequately staged borderline ovarian tumors,
D. Querleu et al. / EJSO 32 (2006) 853e858
although the therapeutic implications of the finding of extraovarian disease are not clear.19,20 Laparoscopy in advanced ovarian carcinomas Neoadjuvant chemotherapy is increasingly used in advanced ovarian, tubal or peritoneal carcinomas, when primary surgery cannot reach optimal cytoreduction. The decision to abort an attempt at optimal cytoreductive surgery is based on the presence of extensive growth in the mesentery, lesser omentum, stomach and duodenum, or posterior hemidiaphragm. Disseminated disease can be detected and sampled for pathologic examination on CTscans, or surgically identified. Laparoscopy is preferable to exploratory laparotomy is this context, with a shorter recovery and quicker start of neoadjuvant chemotherapy. Decision laparoscopy may also precede interval debulking surgery with the same rationale, as interval procedures are worthwhile only if optimal cytoreduction is achieved. There are specific technical features for decision laparoscopy. Open laparoscopy using a supraumbilical or left upper quadrant approach allows evacuation of ascites and then introduction of the endoscope. Visual examination of the upper part of the abdomen and of the mesentery, where the majority of indications for neoadjuvant chemotherapy are found, is the main objective. Biopsies are taken. Washing of trocar openings with polyvidone iodine and if possible careful closure of the peritoneum at the end of the procedure are required. Portsite metastasis occurs in approximately 10% of laparoscopies in untreated peritoneal carcinomatosis, but is as chemosensitive as the peritoneal disease and never alters the treatment or outcome.21 Second-look procedures are less and less used. Laparoscopic second-look procedures are more difficult and less reliable than open second-look procedures, due to postoperative peritoneal adhesions. However, an obviously positive second-look laparoscopy provides definitive information. In addition, adhesiolysis may be used to ensure adequate distribution of intraperitoneal drugs when intraperitoneal chemotherapy is used as a closure therapy. Other indications for peritoneal staging Laparoscopic examination of the pelvic peritoneum is part of surgical staging procedures in advanced cervical cancers. Involvement of the anterior or posterior culde-sac is found in 11.5 and 6%, respectively, of patients.22 Laparoscopic preoperative examination of the peritoneal cavity and lymph node dissection is a tool to select, among candidates for pelvic exenteration for advanced or recurrent uterine cancer, the group of patients with no peritoneal carcinomatosis or positive aortic node. Only this group is likely to benefit from exploratory laparotomy after careful counselling and medical and psychological preparation.23,24
855
Laparoscopic or laparoscopically assisted surgical management of gynaecologic malignancies Radical hysterectomy Large series of 50e73 patients demonstrate the feasibility and safety of full laparoscopic radical hysterectomy in experienced hands.25e28 Ureterovaginal fistula formation and recurrence rate do not seem to be increased. The median operative time is 258 min in the hands of the pioneers of the method.27 The major benefits are less intraoperative blood loss and shorter hospital stay. However, after the initial description of laparoscopically assisted radical vaginal hysterectomy,29 larger series of 200 patients has been published, with reassuring results.30 In addition, radical vaginal hysterectomy combined with laparoscopic lymphadenectomy is still an alternative to full radical hysterectomy.31 In clinical practice, the three ‘‘minimally invasive’’ techniques for radical hysterectomy are not concurrent but complementary, and indication of each method is adapted to the individual patient. Parametrectomy Patients referred after the finding of cervical carcinoma on a simple hysterectomy specimen may be proposed additional surgery involving upper colpectomy and parametrectomy. Similar to radical hysterectomy, the procedure can be completed laparoscopically or vaginally (laparoscopically assisted).32,33 Radical trachelectomy Although full laparoscopic radical trachelectomy has been described,34 the most used technique worldwide is the vaginal radical trachelectomy pioneered by Dargent. Radical trachelectomy is a fertility sparing procedure adapted to selected patients, with node negative exocervical squamous cell carcinomas less than 2 cm in diameter. The procedure starts with a laparoscopic pelvic lymphadenectomy and is finished vaginally with a laterally extended removal of the cervix inspired from the Schauta operation, with the difference that the uterine isthmus and at least 5 mm of endocervical canal are preserved. A permanent cerclage is placed and an uterovaginal anastomosis is performed. Recent independent reports confirmed the oncological safety and obstetrical results of the procedure.35 In the Quebec experience, the planned procedure was successfully completed in 72 cases and was abandoned in 10 cases (12%) because of either positive nodes discovered at the time of surgery (4), positive endocervical margins (5) or extensive tubal adhesions (1). The actuarial recurrence-free survival is 95%. Patients with adenocarcinoma or lymph vascular space invasion were included after informed consent. In another large series, 18 patients out of 80 were
856
D. Querleu et al. / EJSO 32 (2006) 853e858
pregnant. Twenty-two pregnancies resulted in 12 live births after Cesarean section.36 Simple hysterectomy Full laparoscopic hysterectomy or laparoscopically assisted vaginal hysterectomy (LAVH), alone or in conjunction with laparoscopic lymphadenectomy, is used in the management of endometrial cancer. This is and probably will remain the main indication for laparoscopic surgery and is the topic of a small scale randomized study37 and numerous recent papers38e41 that consistently confirmed previous findings in favour of laparoscopic or laparoscopic assisted surgery in hospital stay, blood loss without identified adverse influence on complication and recurrence rates. Increased operating time compared to laparotomy is largely dependent on the learning curve but remains a concern. Proper selection of patients, excluding deep IC adenocarcinomas for fear of intraoperative rupture and patients in whom laparoscopic and/or vaginal surgery is likely to be difficult or dangerous for anatomical reasons, is mandatory. On the other hand, elderly patients presenting with endometrial cancer can be safely managed laparoscopically.42 Management of adnexal disease Laparoscopic diagnosis of the adnexal mass is beyond the scope of this review. Careful preoperative workup including ultrasound and Ca 125, laparoscopic examination of the adnexa by an experienced surgeon are the key to diagnostic and therapeutic efficacy. The full management of an ovarian or tubal invasion cancer using laparoscopic techniques is not standard. In our experience, it has been used only in a few selected cases of early and small volume (less than 4 cm) ovarian or tubal cancer. A French retrospective multicenter study did not evidence difference in outcome after laparoscopic management of ovarian cancers, although staging was suboptimal in a significant number of laparoscopically managed cases.43 More recently, the Iena team published a series of 13 patients with ovarian carcinoma, without adverse effect on outcome.44 In addition, one recent paper mentions the use of hand-assisted laparoscopy in the surgical management of ovarian cancer.45
Laparoscopically assisted exenteration The latest development of laparoscopic surgery is the demonstration that full laparoscopic pelvic exenteration is technically feasible.48,49 General surgeons and urologists master the techniques of laparoscopic rectal resection followed by colostomy and/or end to end anastomosis and cystectomy, respectively. Laparoscopic Bricker procedure or hand-assisted Miami pouch is also feasible. In a similar way, we are currently developing the concept of laparoscopically assisted vaginal exenteration for patient with recurrences involving the lower half of the vagina, urethra or low rectum. In four patients, we have completed the exenterative procedure vaginally and reconstructive steps using laparoscopy or hand-assisted laparoscopy. The benefit for the patient, considering that cosmetic considerations are not relevant in this group of patients, is not yet clear. The main remaining problem is vaginal reconstruction. In our series, an omental flap harvested at laparoscopy has been used, although the routine technique in our center is the vertical rectus abdominis flap.50 Associated techniques51 General surgery procedures associated with gynaecologic malignancies, such as colostomy or splenectomy for isolated metastasis can be performed or assisted by laparoscopy. Laparoscopy may help the radiation therapist or medical oncologist through the placement of pelvic displacement prosthesis, localization of interstitial brachytherapy implants, placement of intraperitoneal port-a-cath. Ovarian transposition is typically indicated in young female patients with early squamous cell carcinoma of the cervix or other malignancies who have planned brachytherapy or definitive pelvic radiation. Laparoscopic ligation of the hypogastric artery has been described as an alternative to embolization in severe hemorrhage related to uterine cancers. We have managed laparoscopically lymphocysts by intraperitoneal marsupialization, and vaginal eviscerations by laparoscopic omentoplasty combined with vaginal closure. New developments may be found using photodynamic detection of implants in follow-up laparoscopies of ovarian cancer patients in apparent complete remission. Intraperitoneal chemohyperthermia has been shown to be feasible in an experimental setting.52
Surgical management of borderline ovarian tumours Borderline ovarian tumors are surgically managed. The indication of laparoscopic surgery, including management of the primary tumor, conservative or radical management of the uterus and contralateral adnexa, and peritoneal staging, is gaining acceptance. Provided that the standards of surgical oncology are met, and that no large mass is present, long-term results are similar after laparoscopic surgery compared to laparotomy.46,47
Oncological hazards A lot of research work, with conflicting results, addressed the issue of tumor growth and abdominal wall grafts after CO2 laparoscopic procedure.51 Tumor growth is consistently greater after laparotomy than after laparoscopy. Pneumoperitoneum, not carbon dioxide, may create the conditions of seeding when a large number of tumor
D. Querleu et al. / EJSO 32 (2006) 853e858
cells are present. Use of low pressure, avoidance of exsufflation of gas through trocar opening, instillation of polyvidone iodine, use of bags to retrieve operative specimens and careful closure of the trocar openings may prevent abdominal wall metastases. In clinical practice, trocar site metastasis is uncommon in uterine cancer patients (less than 1%), more common in advanced ovarian cancer patients. In our series, six umbilical or trocar site metastases out of 915 patients were observed after an average follow-up of 70 months (unpublished data). However, abdominal wall metastases are frequently associated with peritoneal carcinomatosis, with the same chemosensitivity, and have never been the only cause of lethality. Interestingly, laparoscopic port scars unrelated to oncological procedures may be, as is the natural umbilicus, preferential sites of extension of extensive intraperitoneal disease. Increased positive peritoneal cytology in endometrial cancer patients is not a consequence of laparoscopy, but of the use of uterine cannula.53 It could be prevented, if cannulation is used, by occlusion of the tubes using bipolar cautery at the beginning of the operation. The learning curve is a concern. It has been extensively studied in our group for lymph node dissection.54,55 The learning curve for pelvic lymph node dissection reaches a plateau after not more than seven cases under supervision, while 15 para-aortic dissections are required. Quality control is mandatory. In a combined series of centers with a wide range of level of expertise, photographic records were examined by independent observers, and surgical sites inspected at immediate laparotomy. A few remaining nodes were observed in 15% of patients, mainly in the lateral common iliac area, although no positive missing node was identified.56 Conclusion Laparoscopy has gained acceptance as a tool in the armamentarium of the gynaecologic oncologist. Laparoscopic programs are burgeoning worldwide in cancer centers and gynaecologic oncology services. However, only a few centers routinely use the whole range of available techniques, as a consequence of additional operating room costs, inadequate equipment, lack of training, lack of definitive evidence-based demonstration, and/or theoretical concerns supported by experimental data and papers mentioning surgical complications or oncological drawbacks. Evidence is growing that a number of these concerns are not justified, although continuing effort to carefully evaluate laparoscopic surgery in gynaecological cancer is warranted. References 1. Childers M. The virtues and pitfalls of minimally invasive surgery for gynaecologic malignancies: an update. Curr Opin Obstet Gynecol 1999;11:51–9.
857
2. Lanvin D, Elhage A, Henry B, Leblanc E, Querleu D, Delobelle-Deroide A. Accuracy and safety of laparoscopic lymphadenectomy: an experimental prospective randomized study. Gynecol Oncol 1997;67:83–7. 3. Cartron G. Complications des lymphade´nectomies coelioscopiques. Medicine Thesis, Toulouse, 2004. 4. Kohler C, Klemm P, Schau A, et al. Introduction of transperitoneal lymphadenectomy in a gynecologic oncology center: analysis of 650 laparoscopic pelvic and/or paraaortic transperitoneal lymphadenectomies. Gynecol Oncol 2004;95:52–61. 5. Abu-Rustum NR, Chi DS, Sonoda Y, et al. Transperitoneal laparoscopic pelvic and para-aortic lymph node dissection using the argon-beam coagulator and monopolar instruments: an 8-year study and description of technique. Gynecol Oncol 2003;89:504–13. 6. Scribner DR, Walker JL, Johnson GA, McMeekin DS, Gold MA, Mannel RS. Laparoscopic pelvic and paraaortic lymph node dissection in the obese. Gynecol Oncol 2002;84:426–30. 7. Malur S, Krause N, Ko¨hler C, Schneider A. Sentinel lymph node detection in patients with cervical cancer. Gynecol Oncol 2001;80:254–7. 8. Lambaudie E, Collinet P, Narducci F, et al. Laparoscopic identification of sentinel lymph nodes in early stage cervical cancer. Prospective study using a combination of patent blue dye injection and technetium radiocolloid injection. Gynecol Oncol 2003;89:84–7. 9. Levenback C, Coleman RL, Burke TW, et al. Lymphatic mapping and sentinel node identification in patients with cervix cancer undergoing radical hysterectomy and pelvic lymphadenectomy. J Clin Oncol 2002;20:688–93. 10. Marchiole P, Buenerd A, Scoazec JY, Dargent D, Mathevet P. Sentinel lymph node biopsy is not accurate in predicting lymph node status for patients with cervical carcinoma. Cancer 2004;100:2154–9. 11. Barranger E, Cortez A, Grahek D, Callard P, Uzan S, Darai E. Laparoscopic sentinel node procedure using a combination of patent blue and radiocolloid in women with endometrial cancer. Ann Surg Oncol 2004;11:344–9. 12. Maccauro M, Lucignani G, Aliberti G, et al. Sentinel lymph node detection following the hysteroscopic peritumoural injection of (99m)Tc-labelled albumin nanocolloid in endometrial cancer. Eur J Nucl Med Mol Imaging 2005;32:569–74. 13. Van Trappen PO, Gyselman VG, Lowe DG, et al. Molecular quantification and mapping of lymph-node micrometastasis in cervical cancer. Cancer 2001;357:15–20. 14. Querleu D, Narducci F, Poulard V, et al. Modified radical vaginal hysterectomy with or without laparoscopic nerve-sparing dissection: a comparative study. Gynecol Oncol 2002;85:154–8. 15. Dargent D, Ansquer Y, Mathevet P. Technical development and results of left extraperitoneal laparoscopic paraaortic lymphadenectomy for cervical cancer. Gynecol Oncol 2000;77:87–92. 16. Sonoda Y, Leblanc E, Querleu D, et al. Prospective evaluation of surgical staging of advanced cervical cancer via a laparoscopic extraperitoneal approach. Gynecol Oncol 2003;91:326–31. 17. Occelli B, Narducci F, Lanvin D, et al. De novo adhesions with extraperitoneal endosurgical para-aortic lymphadenectomy versus transperitoneal laparoscopic para-aortic lymphadenectomy: a randomized experimental study. Am J Obstet Gynecol 2000;183:529–33. 18. Leblanc E, Querleu D, Narducci F, Occelli B, Papageorgiou T, Sonoda Y. Laparoscopic restaging of early stage invasive adnexal tumors: a 10-year experience. Gynecol Oncol 2004;94:624–9. 19. Querleu D, Papageorgiou T, Lambaudie E, Sonoda Y, Narducci F, Leblanc E. Laparoscopic restaging of borderline ovarian tumours: results of 30 cases initially presumed as stage IA borderline ovarian tumours. BJOG 2003;110:201–4. 20. Camatte S, Morice P, Thoury A, et al. Impact of surgical staging in patients with macroscopic ‘‘stage I’’ ovarian borderline tumours: analysis of a continuous series of 101 cases. Eur J Cancer 2004;40: 1842–9. 21. van Dam PA, DeCloedt J, Tjalma WA, Buytaert P, Becquart D, Vergote IB. Trocar implantation metastasis after laparoscopy in
858
22.
23.
24. 25.
26.
27.
28.
29. 30.
31.
32.
33.
34.
35.
36.
37.
38.
D. Querleu et al. / EJSO 32 (2006) 853e858 patients with advanced ovarian cancer: can the risk be reduced? Am J Obstet Gynecol 1999;181:536–41. Hertel H, Ko¨hler C, Elhawary T, Michels W, Possover M, Schneider A. Laparoscopic staging compared with imaging techniques in the staging of advanced cervical cancer. Gynecol Oncol 2002;87: 46–51. Plante M, Roy M. Operative laparoscopy prior to a pelvic exenteration in patients with recurrent cervical cancer. Gynecol Oncol 1998;69: 94–9. Ko¨hler C, Tozzi R, Possover M, Schneider A. Explorative laparoscopy prior to exenterative surgery. Gynecol Oncol 2002;86:311–5. Spirtos NM, Eisenkop SM, Schlaerth JB, Ballon SC. Laparoscopic radical hysterectomy (type III) with aortic and pelvic lymphadenectomy in patients with stage I cervical cancer. Surgical morbidity and intermediate follow-up. Am J Obstet Gynecol 2002;187:340–8. Park CT, Lim KT, Chung HW, et al. Clinical evaluation of laparoscopic-assisted radical vaginal hysterectomy with pelvic and/ or paraaortic lymphadenectomy. J Am Assoc Gynecol Laparosc 2002;9:49–53. Pomel C, Atallah D, Le Bouedec G, et al. Laparoscopic radical hysterectomy for invasive cervical cancer: 8-year experience of a pilot study. Gynecol Oncol 2003;91:534–9. Steed H, Rosen B, Murphy J, Laframboise S, De Petrillo D, Covens A. A comparison of laparoscopic-assisted radical vaginal hysterectomy and radical abdominal hysterectomy in the treatment of cervical cancer. Gynecol Oncol 2004;93:588–93. Querleu D. Laparoscopically assisted radical vaginal hysterectomy. Gynecol Oncol 1993;51:248–54. Hertel H, Kohler C, Michels W, Possover M, Tozzi R, Schneider A. Laparoscopic-assisted radical vaginal hysterectomy (LARVH): prospective evaluation of 200 patients with cervical cancer. Gynecol Oncol 2003;90:505–11. Roy M, Plante M, Renaud MC, Tetu B. Vaginal radical hysterectomy versus abdominal radical hysterectomy in the treatment of early-stage cervical cancer. Gynecol Oncol 1996;62:336–9. Lee YS, Lee TH, Koo TB, Cho YL, Park IS. Laparoscopic-assisted radical parametrectomy including pelvic and/or paraaortic lymphadenectomy in women after prior hysterectomy e three cases. Gynecol Oncol 2003;91:619–22. Kohler C, Tozzi R, Klemm P, Schneider A. ‘‘Schauta sine utero’’: technique and results of laparoscopic-vaginal radical parametrectomy. Gynecol Oncol 2003;91:359–68. Lee CL, Huang KG, Wang CJ, Yen CF, Lai CH. Laparoscopic radical trachelectomy for stage IB1 cervical cancer. J Am Assoc Gynecol Laparosc 2003;10:111–5. Plante M, Renaud MC, Francois H, Roy M. Vaginal radical trachelectomy: an oncologically safe fertility-preserving surgery. An updated series of 72 cases and review of the literature. Gynecol Oncol 2004; 94:614–23. Bernardini M, Barrett J, Seaward G, Covens A. Pregnancy outcomes in patients after radical trachelectomy. Am J Obstet Gynecol 2003; 189:1378–82. Malur S, Possover M, Michels W, Schneider A. Laparoscopic-assisted vaginal versus abdominal surgery in patients with endometrial cancer e a prospective randomized trial. Gynecol Oncol 2001;80:239–44. Holub Z, Jabor A, Bartos P, Eim J, Urbanek S, Pivovarnikova R. Laparoscopic surgery for endometrial cancer: long-term results of a multicentric study. Eur J Gynaecol Oncol 2002;23:305–10.
39. Eltabbakh GH. Analysis of survival after laparoscopy in women with endometrial carcinoma. Cancer 2002;95:1894–901. 40. Obermair A, Manolitsas TP, Leung Y, Hammond IG, McCartney AJ. Total laparoscopic hysterectomy for endometrial cancer: patterns of recurrence and survival. Gynecol Oncol 2004;92:789–93. 41. Homesley HD, Boike G, Spiegel GW. Feasibility of laparoscopic management of presumed stage I endometrial carcinoma and assessment of accuracy of myoinvasion estimates by frozen section: a gynecologic oncology group study. Int J Gynecol Cancer 2004;14:341–7. 42. Scribner Jr DR, Walker JL, Johnson GA, McMeekin SD, Gold MA, Mannel RS. Surgical management of early-stage endometrial cancer in the elderly: is laparoscopy feasible? Gynecol Oncol 2001;83: 563–8. 43. Lecuru F, Desfeux P, Camatte S, et al. Stage I ovarian cancer: comparison of laparoscopy and laparotomy on staging and survival. Eur J Gynaecol Oncol 2004;25:571–6. 44. Tozzi R, Ko¨hler C, Ferrara A, Schneider A. Laparoscopic treatment of early ovarian cancer: surgical and survival outcomes. Gynecol Oncol 2004;93:199–203. 45. Krivak TC, Elkas JC, Rose GS, et al. The utility of hand-assisted laparoscopy in ovarian cancer. Gynecol Oncol 2005;96:72–6. 46. Camatte S, Morice P, Atallah D, et al. Clinical outcome after laparoscopic pure management of borderline ovarian tumors: results of a series of 34 patients. Ann Oncol 2004;15:605–9. 47. Maneo A, Vignali M, Chiari S, Colombo A, Mangioni C, Landoni F. Are borderline tumors of the ovary safely treated by laparoscopy? Gynecol Oncol 2004;94:387–92. 48. Pomel C, Rouzier R, Pocard M, et al. Laparoscopic total pelvic exenteration for cervical cancer relapse. Gynecol Oncol 2003;91:616–8. 49. Pomel C, Castaigne D. Laparoscopic hand-assisted Miami Pouch following laparoscopic anterior pelvic exenteration. Gynecol Oncol 2004; 93:543–5. 50. Ferron G, Querleu D, Martel P, Letourneur B, Soulie M. Laparoscopically-assisted vaginal pelvic exenteration. Gynecol Oncol 2006;100: 551–5. 51. Querleu D, Leblanc E. Laparoscopic surgery for gynaecological oncology. Curr Opin Obstet Gynecol 2003;15:309–14. 52. Ferron G, Gesson-Paute A, Classe JM, Querleu D. Feasibility of laparoscopic peritonectomy followed by intra-peritoneal chemohyperthermia: an experimental study. Gynecol Oncol 2005;99: 358–61. 53. Vergote I, De Smet I, Amant F. High incidence of positive peritoneal cytology in low risk endometrial cancer treated by laparoscopically assisted vaginal hysterectomy. [letter]. Gynecol Oncol 2002;84: 537–9. 54. Querleu D, Lanvin D, Elhage A, Henry-Buisson B, Leblanc E. An objective experimental assessment of the learning curve for laparoscopic surgery: the example of pelvic and para-aortic lymph node dissection. Eur J Obstet Gynecol Reprod Biol 1998;81:55–8. 55. Occelli B, Narducci F, Lanvin D, Leblanc E, Querleu D. Learning curves for transperitoneal laparoscopic and extraperitoneal endoscopic paraaortic lymphadenectomy. J Am Assoc Gynecol Laparosc 2000;7: 51–3. 56. Schlaerth JB, Spirtos NM, Carson LF, Boike G, Adamec T, Stonebraker B. Laparoscopic retroperitoneal lymphadenectomy followed by immediate laparotomy in women with cervical cancer: a Gynecologic Oncology Group study. Gynecol Oncol 2002;85: 81–8.
www.ejso.com
Laparoscopic surgery in gynaecological oncology D. Querleu a,*, E. Leblanc b, G. Ferron a, F. Narducci b a
De´partement de Chirurgie, Institut Claudius Regaud, 20 rue du Pont Saint Pierre, 31052 Toulouse, France b Department of Gynaecologic Oncology, Centre Oscar Lambret Cancer Center, Lille, France Accepted 23 March 2006 Available online 12 July 2006
Abstract Aims: The use of laparoscopic staging and/or surgery in the field of gynaecological oncology was pioneered in the late 1980s and the first reports were published in the early 1990s. The issue has been initially most controversial, and is still debated, with some justification considering the possible adverse consequences of surgical mismanagement of gynaecologic malignancy. Methods: The current literature has been reviewed and updated, concentrating on long-term, and/or comparative studies. Large observational studies have also been included. Recent papers concerning new developments have been selected. Findings: A number of papers have confirmed the absence of significant adverse effects on survival after laparoscopic diagnosis or surgery in gynaecological cancers. New developments cover virtually all the basic techniques in cancer surgery, including major exenterative surgery. The use of extraperitoneal technique for aortic dissections is emerging as a new tool. New indications, such as radical vaginal trachelectomy, radical parametrectomy, pelvic sentinel node identification, interval debulking surgery of adnexal malignancies, or the use of pretherapeutic surgical staging of uterine cancers, have been developed in direct relation with the use of laparoscopic techniques. Conclusions: Current available data and worldwide interest clearly demonstrate that laparoscopic techniques must now be part of the armamentarium of the gynaecologic oncologist. Postoperative morbidity and recurrence risk do not seem to be affected. Cost-efficiency of laparoscopic procedures is based on the reduction of hospital stay and recovery time, although operating room time is increased in some procedures. Combined training in gynaecologic oncology and in laparoscopic and/or vaginal surgery is more than ever mandatory to avoid the risk of inadequate staging or management of pelvic malignancies. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Laparoscopic surgery; Gynaecological oncology; Lymphadenectomy; Radical hysterectomy; Radical trachelectomy
Laparoscopic surgery in gynaecologic oncology was initially developed in France and in the United States by Daniel Dargent, Denis Querleu, Eric Leblanc, and Joel M. Childers.1 Long-term follow-up of patients and/or careful assessment of complications and drawbacks are now available, while new techniques are still under evaluation. The current literature has been reviewed, and personal data added for this paper. Laparoscopic surgical staging Laparoscopic transperitoneal node dissection The technique of transperitoneal pelvic lymph node dissection is routinely performed in most gynaecologic
* Corresponding author. Tel.: þ33 561 42 41 50; fax: þ33 561 42 41 17. E-mail address: [email protected] (D. Querleu). 0748-7983/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.ejso.2006.03.043
oncology centers as a staging procedure or as a part of surgical management of cervical and endometrial cancers. Several experimental randomized studies by independent investigators have provided evidence that the node count of laparoscopic dissections is not inferior to open dissections.2 The complication rate is extremely low in experienced hands. We have performed 694 transperitoneal lymph node dissections without a single laparotomy for complication. Although less easy, with more limitations, and a longer learning curve, transperitoneal laparoscopic aortic dissection is no longer an investigational procedure. Overall, a conversion rate of 18.5% and a complication rate of 12.4% are observed in our series of transperitoneal laparoscopic lymphadenectomies.3 Other large series from Germany and USA reported similar findings.4,5 Obesity is not a contra-indication and is not associated with a reduction in the number of retrieved nodes. Feasibility is high in patients with a BMI under 35. On the other hand,
854
D. Querleu et al. / EJSO 32 (2006) 853e858
a satisfactory laparoscopic pelvic and low aortic dissection for endometrial cancer is completed in only 44% of patients with a BMI index greater than 35. However, considering the reduction of complication rate and hospital stay provided by the laparoscopic approach, the technique deserves to be attempted in morbidly obese patients.4,6 Sentinel node identification Removal of a single targeted node from a node-bearing area is logically accomplished through minimal incisions. In addition, identification of minute lymphatic channels located deep in the pelvis requires some magnification, as provided by the laparoscope. The first attempts at sentinel node detection involved blue dye injection only. Further development of combined isotopic and blue dye mapping improved the detection rate up to 90%.7 With the development of laparoscopic probes, the concurrent use of radio-labeled colloid injections became possible, improving the detection rate.8 Sentinel nodes may be found in unusual areas such as common iliac or para-aortic sites. The sentinel node concept does not apply to obviously diseased nodes in which lymphatic flow is blocked, making uptake of markers impossible. In early cervical cancers, the finding of a positive sentinel node is considered in our center as in others as a contraindication for upfront surgery, an indication for immediate aortic dissection, and an argument to propose definitive chemoradiation therapy. Further pelvic dissection in such a circumstance is not advised, as it could increase the risk of radiation induced complication. On the other hand, the finding of negative sentinel nodes does not allow to limit pelvic node dissection. In our experience, micrometastasis was found in a non-sentinel node in a sentinel node negative patient,8 in accordance to findings by other groups at laparotomy9 or laparoscopy.10 In endometrial carcinomas, the completion of lymph node dissection is controversial. Pelvic sentinel node sampling could in the future be used as a mid-term between no dissection and full dissection. The finding of a positive pelvic sentinel node is an indication for aortic node dissection or sampling. It is not clear whether intraoperative direct subserosal injection of blue dye is superior to cervical injection for sentinel node identification in endometrial cancers, and intracervical injection is usually preferred,11 although hysteroscopic injection of isotopic tracer is feasible and may be superior.12 Paracervical (parametrial) lymphadenectomy The high short and long-term urinary dysfunction or complication rate of radical hysterectomy has motivated the evolution towards a reduction in radicality. Early cervical carcinomas are presently managed by modified radical hysterectomy, with no apparent increase in the rate of lateropelvic recurrence. However, the well documented finding
of pathologically or biologically positive parametrial nodes suggests a risk of late development of micrometastasis.13 Nerve-sparing dissection of the distal part of the cardinal ligament is supposed to prevent late lateropelvic recurrences without further impairing urinary function. In other terms, the combination of a modified radical hysterectomy with a parametrial lymph node dissection combines the radicality of parametrial resection with the low morbidity of a modified radical hysterectomy. The use of laparoscopic magnification is logically associated with a safe dissection and preservation of the vascular and nerve content of the distal part of the cardinal ligament.14 Laparoscopic extraperitoneal node dissection The common iliac and aortic extension of extraperitoneal dissections15,16 is a novel technique that combines surgical comfort and benefit for the patient in terms of de novo peritoneal adhesions, which is crucial in patients candidate for extended field irradiation.17 The main complication is the formation of giant lymphocysts that were observed at the beginning of our experience. Lymphocyst formation can be prevented if the peritoneum of the paracolic gutter is incised at the end of the procedure, in order to allow intraperitoneal drainage of the extraperitoneal dissection area. In advanced stage cervical cancer patients, the finding of negative common iliac and aortic nodes is a safe indication that aortic fields can be omitted. Our policy is to extend the dissection up to the renal vessels, using a left extraperitoneal approach, with a 27% positivity rate in a series of 111 patients. In our group, 3-year survival is as high as 80% using chemoradiation with pelvic fields in advanced cervical cancers. The finding of positive nodes is an indication of high risk of distant metastasis and death.16 Laparoscopic omentectomy and peritoneal staging of early adnexal carcinomas Careful examination, with the advantage of magnification, of the peritoneal surface and multiple random or oriented biopsies may be accomplished laparoscopically. Omentectomy is performed using electrosurgery, clips, or ultrasound hemostasis techniques. The omentum can be packed in a bag then retrieved through a vaginal or small abdominal incision. Appendectomy, which is part of surgical staging in mucinous adnexal tumors, is routinely performed through the laparoscope. Peritoneal staging is indicated, in conjunction with node dissection, in the reassessment of inadequately staged adnexal cancer patients. Using laparoscopic techniques, 18% of patients are upstaged and need adjuvant chemotherapy.18 Patients definitively classified as stage IA or IB after laparoscopic staging have an excellent prognosis.18 Laparoscopic peritoneal staging may also be proposed in the case of inadequately staged borderline ovarian tumors,
D. Querleu et al. / EJSO 32 (2006) 853e858
although the therapeutic implications of the finding of extraovarian disease are not clear.19,20 Laparoscopy in advanced ovarian carcinomas Neoadjuvant chemotherapy is increasingly used in advanced ovarian, tubal or peritoneal carcinomas, when primary surgery cannot reach optimal cytoreduction. The decision to abort an attempt at optimal cytoreductive surgery is based on the presence of extensive growth in the mesentery, lesser omentum, stomach and duodenum, or posterior hemidiaphragm. Disseminated disease can be detected and sampled for pathologic examination on CTscans, or surgically identified. Laparoscopy is preferable to exploratory laparotomy is this context, with a shorter recovery and quicker start of neoadjuvant chemotherapy. Decision laparoscopy may also precede interval debulking surgery with the same rationale, as interval procedures are worthwhile only if optimal cytoreduction is achieved. There are specific technical features for decision laparoscopy. Open laparoscopy using a supraumbilical or left upper quadrant approach allows evacuation of ascites and then introduction of the endoscope. Visual examination of the upper part of the abdomen and of the mesentery, where the majority of indications for neoadjuvant chemotherapy are found, is the main objective. Biopsies are taken. Washing of trocar openings with polyvidone iodine and if possible careful closure of the peritoneum at the end of the procedure are required. Portsite metastasis occurs in approximately 10% of laparoscopies in untreated peritoneal carcinomatosis, but is as chemosensitive as the peritoneal disease and never alters the treatment or outcome.21 Second-look procedures are less and less used. Laparoscopic second-look procedures are more difficult and less reliable than open second-look procedures, due to postoperative peritoneal adhesions. However, an obviously positive second-look laparoscopy provides definitive information. In addition, adhesiolysis may be used to ensure adequate distribution of intraperitoneal drugs when intraperitoneal chemotherapy is used as a closure therapy. Other indications for peritoneal staging Laparoscopic examination of the pelvic peritoneum is part of surgical staging procedures in advanced cervical cancers. Involvement of the anterior or posterior culde-sac is found in 11.5 and 6%, respectively, of patients.22 Laparoscopic preoperative examination of the peritoneal cavity and lymph node dissection is a tool to select, among candidates for pelvic exenteration for advanced or recurrent uterine cancer, the group of patients with no peritoneal carcinomatosis or positive aortic node. Only this group is likely to benefit from exploratory laparotomy after careful counselling and medical and psychological preparation.23,24
855
Laparoscopic or laparoscopically assisted surgical management of gynaecologic malignancies Radical hysterectomy Large series of 50e73 patients demonstrate the feasibility and safety of full laparoscopic radical hysterectomy in experienced hands.25e28 Ureterovaginal fistula formation and recurrence rate do not seem to be increased. The median operative time is 258 min in the hands of the pioneers of the method.27 The major benefits are less intraoperative blood loss and shorter hospital stay. However, after the initial description of laparoscopically assisted radical vaginal hysterectomy,29 larger series of 200 patients has been published, with reassuring results.30 In addition, radical vaginal hysterectomy combined with laparoscopic lymphadenectomy is still an alternative to full radical hysterectomy.31 In clinical practice, the three ‘‘minimally invasive’’ techniques for radical hysterectomy are not concurrent but complementary, and indication of each method is adapted to the individual patient. Parametrectomy Patients referred after the finding of cervical carcinoma on a simple hysterectomy specimen may be proposed additional surgery involving upper colpectomy and parametrectomy. Similar to radical hysterectomy, the procedure can be completed laparoscopically or vaginally (laparoscopically assisted).32,33 Radical trachelectomy Although full laparoscopic radical trachelectomy has been described,34 the most used technique worldwide is the vaginal radical trachelectomy pioneered by Dargent. Radical trachelectomy is a fertility sparing procedure adapted to selected patients, with node negative exocervical squamous cell carcinomas less than 2 cm in diameter. The procedure starts with a laparoscopic pelvic lymphadenectomy and is finished vaginally with a laterally extended removal of the cervix inspired from the Schauta operation, with the difference that the uterine isthmus and at least 5 mm of endocervical canal are preserved. A permanent cerclage is placed and an uterovaginal anastomosis is performed. Recent independent reports confirmed the oncological safety and obstetrical results of the procedure.35 In the Quebec experience, the planned procedure was successfully completed in 72 cases and was abandoned in 10 cases (12%) because of either positive nodes discovered at the time of surgery (4), positive endocervical margins (5) or extensive tubal adhesions (1). The actuarial recurrence-free survival is 95%. Patients with adenocarcinoma or lymph vascular space invasion were included after informed consent. In another large series, 18 patients out of 80 were
856
D. Querleu et al. / EJSO 32 (2006) 853e858
pregnant. Twenty-two pregnancies resulted in 12 live births after Cesarean section.36 Simple hysterectomy Full laparoscopic hysterectomy or laparoscopically assisted vaginal hysterectomy (LAVH), alone or in conjunction with laparoscopic lymphadenectomy, is used in the management of endometrial cancer. This is and probably will remain the main indication for laparoscopic surgery and is the topic of a small scale randomized study37 and numerous recent papers38e41 that consistently confirmed previous findings in favour of laparoscopic or laparoscopic assisted surgery in hospital stay, blood loss without identified adverse influence on complication and recurrence rates. Increased operating time compared to laparotomy is largely dependent on the learning curve but remains a concern. Proper selection of patients, excluding deep IC adenocarcinomas for fear of intraoperative rupture and patients in whom laparoscopic and/or vaginal surgery is likely to be difficult or dangerous for anatomical reasons, is mandatory. On the other hand, elderly patients presenting with endometrial cancer can be safely managed laparoscopically.42 Management of adnexal disease Laparoscopic diagnosis of the adnexal mass is beyond the scope of this review. Careful preoperative workup including ultrasound and Ca 125, laparoscopic examination of the adnexa by an experienced surgeon are the key to diagnostic and therapeutic efficacy. The full management of an ovarian or tubal invasion cancer using laparoscopic techniques is not standard. In our experience, it has been used only in a few selected cases of early and small volume (less than 4 cm) ovarian or tubal cancer. A French retrospective multicenter study did not evidence difference in outcome after laparoscopic management of ovarian cancers, although staging was suboptimal in a significant number of laparoscopically managed cases.43 More recently, the Iena team published a series of 13 patients with ovarian carcinoma, without adverse effect on outcome.44 In addition, one recent paper mentions the use of hand-assisted laparoscopy in the surgical management of ovarian cancer.45
Laparoscopically assisted exenteration The latest development of laparoscopic surgery is the demonstration that full laparoscopic pelvic exenteration is technically feasible.48,49 General surgeons and urologists master the techniques of laparoscopic rectal resection followed by colostomy and/or end to end anastomosis and cystectomy, respectively. Laparoscopic Bricker procedure or hand-assisted Miami pouch is also feasible. In a similar way, we are currently developing the concept of laparoscopically assisted vaginal exenteration for patient with recurrences involving the lower half of the vagina, urethra or low rectum. In four patients, we have completed the exenterative procedure vaginally and reconstructive steps using laparoscopy or hand-assisted laparoscopy. The benefit for the patient, considering that cosmetic considerations are not relevant in this group of patients, is not yet clear. The main remaining problem is vaginal reconstruction. In our series, an omental flap harvested at laparoscopy has been used, although the routine technique in our center is the vertical rectus abdominis flap.50 Associated techniques51 General surgery procedures associated with gynaecologic malignancies, such as colostomy or splenectomy for isolated metastasis can be performed or assisted by laparoscopy. Laparoscopy may help the radiation therapist or medical oncologist through the placement of pelvic displacement prosthesis, localization of interstitial brachytherapy implants, placement of intraperitoneal port-a-cath. Ovarian transposition is typically indicated in young female patients with early squamous cell carcinoma of the cervix or other malignancies who have planned brachytherapy or definitive pelvic radiation. Laparoscopic ligation of the hypogastric artery has been described as an alternative to embolization in severe hemorrhage related to uterine cancers. We have managed laparoscopically lymphocysts by intraperitoneal marsupialization, and vaginal eviscerations by laparoscopic omentoplasty combined with vaginal closure. New developments may be found using photodynamic detection of implants in follow-up laparoscopies of ovarian cancer patients in apparent complete remission. Intraperitoneal chemohyperthermia has been shown to be feasible in an experimental setting.52
Surgical management of borderline ovarian tumours Borderline ovarian tumors are surgically managed. The indication of laparoscopic surgery, including management of the primary tumor, conservative or radical management of the uterus and contralateral adnexa, and peritoneal staging, is gaining acceptance. Provided that the standards of surgical oncology are met, and that no large mass is present, long-term results are similar after laparoscopic surgery compared to laparotomy.46,47
Oncological hazards A lot of research work, with conflicting results, addressed the issue of tumor growth and abdominal wall grafts after CO2 laparoscopic procedure.51 Tumor growth is consistently greater after laparotomy than after laparoscopy. Pneumoperitoneum, not carbon dioxide, may create the conditions of seeding when a large number of tumor
D. Querleu et al. / EJSO 32 (2006) 853e858
cells are present. Use of low pressure, avoidance of exsufflation of gas through trocar opening, instillation of polyvidone iodine, use of bags to retrieve operative specimens and careful closure of the trocar openings may prevent abdominal wall metastases. In clinical practice, trocar site metastasis is uncommon in uterine cancer patients (less than 1%), more common in advanced ovarian cancer patients. In our series, six umbilical or trocar site metastases out of 915 patients were observed after an average follow-up of 70 months (unpublished data). However, abdominal wall metastases are frequently associated with peritoneal carcinomatosis, with the same chemosensitivity, and have never been the only cause of lethality. Interestingly, laparoscopic port scars unrelated to oncological procedures may be, as is the natural umbilicus, preferential sites of extension of extensive intraperitoneal disease. Increased positive peritoneal cytology in endometrial cancer patients is not a consequence of laparoscopy, but of the use of uterine cannula.53 It could be prevented, if cannulation is used, by occlusion of the tubes using bipolar cautery at the beginning of the operation. The learning curve is a concern. It has been extensively studied in our group for lymph node dissection.54,55 The learning curve for pelvic lymph node dissection reaches a plateau after not more than seven cases under supervision, while 15 para-aortic dissections are required. Quality control is mandatory. In a combined series of centers with a wide range of level of expertise, photographic records were examined by independent observers, and surgical sites inspected at immediate laparotomy. A few remaining nodes were observed in 15% of patients, mainly in the lateral common iliac area, although no positive missing node was identified.56 Conclusion Laparoscopy has gained acceptance as a tool in the armamentarium of the gynaecologic oncologist. Laparoscopic programs are burgeoning worldwide in cancer centers and gynaecologic oncology services. However, only a few centers routinely use the whole range of available techniques, as a consequence of additional operating room costs, inadequate equipment, lack of training, lack of definitive evidence-based demonstration, and/or theoretical concerns supported by experimental data and papers mentioning surgical complications or oncological drawbacks. Evidence is growing that a number of these concerns are not justified, although continuing effort to carefully evaluate laparoscopic surgery in gynaecological cancer is warranted. References 1. Childers M. The virtues and pitfalls of minimally invasive surgery for gynaecologic malignancies: an update. Curr Opin Obstet Gynecol 1999;11:51–9.
857
2. Lanvin D, Elhage A, Henry B, Leblanc E, Querleu D, Delobelle-Deroide A. Accuracy and safety of laparoscopic lymphadenectomy: an experimental prospective randomized study. Gynecol Oncol 1997;67:83–7. 3. Cartron G. Complications des lymphade´nectomies coelioscopiques. Medicine Thesis, Toulouse, 2004. 4. Kohler C, Klemm P, Schau A, et al. Introduction of transperitoneal lymphadenectomy in a gynecologic oncology center: analysis of 650 laparoscopic pelvic and/or paraaortic transperitoneal lymphadenectomies. Gynecol Oncol 2004;95:52–61. 5. Abu-Rustum NR, Chi DS, Sonoda Y, et al. Transperitoneal laparoscopic pelvic and para-aortic lymph node dissection using the argon-beam coagulator and monopolar instruments: an 8-year study and description of technique. Gynecol Oncol 2003;89:504–13. 6. Scribner DR, Walker JL, Johnson GA, McMeekin DS, Gold MA, Mannel RS. Laparoscopic pelvic and paraaortic lymph node dissection in the obese. Gynecol Oncol 2002;84:426–30. 7. Malur S, Krause N, Ko¨hler C, Schneider A. Sentinel lymph node detection in patients with cervical cancer. Gynecol Oncol 2001;80:254–7. 8. Lambaudie E, Collinet P, Narducci F, et al. Laparoscopic identification of sentinel lymph nodes in early stage cervical cancer. Prospective study using a combination of patent blue dye injection and technetium radiocolloid injection. Gynecol Oncol 2003;89:84–7. 9. Levenback C, Coleman RL, Burke TW, et al. Lymphatic mapping and sentinel node identification in patients with cervix cancer undergoing radical hysterectomy and pelvic lymphadenectomy. J Clin Oncol 2002;20:688–93. 10. Marchiole P, Buenerd A, Scoazec JY, Dargent D, Mathevet P. Sentinel lymph node biopsy is not accurate in predicting lymph node status for patients with cervical carcinoma. Cancer 2004;100:2154–9. 11. Barranger E, Cortez A, Grahek D, Callard P, Uzan S, Darai E. Laparoscopic sentinel node procedure using a combination of patent blue and radiocolloid in women with endometrial cancer. Ann Surg Oncol 2004;11:344–9. 12. Maccauro M, Lucignani G, Aliberti G, et al. Sentinel lymph node detection following the hysteroscopic peritumoural injection of (99m)Tc-labelled albumin nanocolloid in endometrial cancer. Eur J Nucl Med Mol Imaging 2005;32:569–74. 13. Van Trappen PO, Gyselman VG, Lowe DG, et al. Molecular quantification and mapping of lymph-node micrometastasis in cervical cancer. Cancer 2001;357:15–20. 14. Querleu D, Narducci F, Poulard V, et al. Modified radical vaginal hysterectomy with or without laparoscopic nerve-sparing dissection: a comparative study. Gynecol Oncol 2002;85:154–8. 15. Dargent D, Ansquer Y, Mathevet P. Technical development and results of left extraperitoneal laparoscopic paraaortic lymphadenectomy for cervical cancer. Gynecol Oncol 2000;77:87–92. 16. Sonoda Y, Leblanc E, Querleu D, et al. Prospective evaluation of surgical staging of advanced cervical cancer via a laparoscopic extraperitoneal approach. Gynecol Oncol 2003;91:326–31. 17. Occelli B, Narducci F, Lanvin D, et al. De novo adhesions with extraperitoneal endosurgical para-aortic lymphadenectomy versus transperitoneal laparoscopic para-aortic lymphadenectomy: a randomized experimental study. Am J Obstet Gynecol 2000;183:529–33. 18. Leblanc E, Querleu D, Narducci F, Occelli B, Papageorgiou T, Sonoda Y. Laparoscopic restaging of early stage invasive adnexal tumors: a 10-year experience. Gynecol Oncol 2004;94:624–9. 19. Querleu D, Papageorgiou T, Lambaudie E, Sonoda Y, Narducci F, Leblanc E. Laparoscopic restaging of borderline ovarian tumours: results of 30 cases initially presumed as stage IA borderline ovarian tumours. BJOG 2003;110:201–4. 20. Camatte S, Morice P, Thoury A, et al. Impact of surgical staging in patients with macroscopic ‘‘stage I’’ ovarian borderline tumours: analysis of a continuous series of 101 cases. Eur J Cancer 2004;40: 1842–9. 21. van Dam PA, DeCloedt J, Tjalma WA, Buytaert P, Becquart D, Vergote IB. Trocar implantation metastasis after laparoscopy in
858
22.
23.
24. 25.
26.
27.
28.
29. 30.
31.
32.
33.
34.
35.
36.
37.
38.
D. Querleu et al. / EJSO 32 (2006) 853e858 patients with advanced ovarian cancer: can the risk be reduced? Am J Obstet Gynecol 1999;181:536–41. Hertel H, Ko¨hler C, Elhawary T, Michels W, Possover M, Schneider A. Laparoscopic staging compared with imaging techniques in the staging of advanced cervical cancer. Gynecol Oncol 2002;87: 46–51. Plante M, Roy M. Operative laparoscopy prior to a pelvic exenteration in patients with recurrent cervical cancer. Gynecol Oncol 1998;69: 94–9. Ko¨hler C, Tozzi R, Possover M, Schneider A. Explorative laparoscopy prior to exenterative surgery. Gynecol Oncol 2002;86:311–5. Spirtos NM, Eisenkop SM, Schlaerth JB, Ballon SC. Laparoscopic radical hysterectomy (type III) with aortic and pelvic lymphadenectomy in patients with stage I cervical cancer. Surgical morbidity and intermediate follow-up. Am J Obstet Gynecol 2002;187:340–8. Park CT, Lim KT, Chung HW, et al. Clinical evaluation of laparoscopic-assisted radical vaginal hysterectomy with pelvic and/ or paraaortic lymphadenectomy. J Am Assoc Gynecol Laparosc 2002;9:49–53. Pomel C, Atallah D, Le Bouedec G, et al. Laparoscopic radical hysterectomy for invasive cervical cancer: 8-year experience of a pilot study. Gynecol Oncol 2003;91:534–9. Steed H, Rosen B, Murphy J, Laframboise S, De Petrillo D, Covens A. A comparison of laparoscopic-assisted radical vaginal hysterectomy and radical abdominal hysterectomy in the treatment of cervical cancer. Gynecol Oncol 2004;93:588–93. Querleu D. Laparoscopically assisted radical vaginal hysterectomy. Gynecol Oncol 1993;51:248–54. Hertel H, Kohler C, Michels W, Possover M, Tozzi R, Schneider A. Laparoscopic-assisted radical vaginal hysterectomy (LARVH): prospective evaluation of 200 patients with cervical cancer. Gynecol Oncol 2003;90:505–11. Roy M, Plante M, Renaud MC, Tetu B. Vaginal radical hysterectomy versus abdominal radical hysterectomy in the treatment of early-stage cervical cancer. Gynecol Oncol 1996;62:336–9. Lee YS, Lee TH, Koo TB, Cho YL, Park IS. Laparoscopic-assisted radical parametrectomy including pelvic and/or paraaortic lymphadenectomy in women after prior hysterectomy e three cases. Gynecol Oncol 2003;91:619–22. Kohler C, Tozzi R, Klemm P, Schneider A. ‘‘Schauta sine utero’’: technique and results of laparoscopic-vaginal radical parametrectomy. Gynecol Oncol 2003;91:359–68. Lee CL, Huang KG, Wang CJ, Yen CF, Lai CH. Laparoscopic radical trachelectomy for stage IB1 cervical cancer. J Am Assoc Gynecol Laparosc 2003;10:111–5. Plante M, Renaud MC, Francois H, Roy M. Vaginal radical trachelectomy: an oncologically safe fertility-preserving surgery. An updated series of 72 cases and review of the literature. Gynecol Oncol 2004; 94:614–23. Bernardini M, Barrett J, Seaward G, Covens A. Pregnancy outcomes in patients after radical trachelectomy. Am J Obstet Gynecol 2003; 189:1378–82. Malur S, Possover M, Michels W, Schneider A. Laparoscopic-assisted vaginal versus abdominal surgery in patients with endometrial cancer e a prospective randomized trial. Gynecol Oncol 2001;80:239–44. Holub Z, Jabor A, Bartos P, Eim J, Urbanek S, Pivovarnikova R. Laparoscopic surgery for endometrial cancer: long-term results of a multicentric study. Eur J Gynaecol Oncol 2002;23:305–10.
39. Eltabbakh GH. Analysis of survival after laparoscopy in women with endometrial carcinoma. Cancer 2002;95:1894–901. 40. Obermair A, Manolitsas TP, Leung Y, Hammond IG, McCartney AJ. Total laparoscopic hysterectomy for endometrial cancer: patterns of recurrence and survival. Gynecol Oncol 2004;92:789–93. 41. Homesley HD, Boike G, Spiegel GW. Feasibility of laparoscopic management of presumed stage I endometrial carcinoma and assessment of accuracy of myoinvasion estimates by frozen section: a gynecologic oncology group study. Int J Gynecol Cancer 2004;14:341–7. 42. Scribner Jr DR, Walker JL, Johnson GA, McMeekin SD, Gold MA, Mannel RS. Surgical management of early-stage endometrial cancer in the elderly: is laparoscopy feasible? Gynecol Oncol 2001;83: 563–8. 43. Lecuru F, Desfeux P, Camatte S, et al. Stage I ovarian cancer: comparison of laparoscopy and laparotomy on staging and survival. Eur J Gynaecol Oncol 2004;25:571–6. 44. Tozzi R, Ko¨hler C, Ferrara A, Schneider A. Laparoscopic treatment of early ovarian cancer: surgical and survival outcomes. Gynecol Oncol 2004;93:199–203. 45. Krivak TC, Elkas JC, Rose GS, et al. The utility of hand-assisted laparoscopy in ovarian cancer. Gynecol Oncol 2005;96:72–6. 46. Camatte S, Morice P, Atallah D, et al. Clinical outcome after laparoscopic pure management of borderline ovarian tumors: results of a series of 34 patients. Ann Oncol 2004;15:605–9. 47. Maneo A, Vignali M, Chiari S, Colombo A, Mangioni C, Landoni F. Are borderline tumors of the ovary safely treated by laparoscopy? Gynecol Oncol 2004;94:387–92. 48. Pomel C, Rouzier R, Pocard M, et al. Laparoscopic total pelvic exenteration for cervical cancer relapse. Gynecol Oncol 2003;91:616–8. 49. Pomel C, Castaigne D. Laparoscopic hand-assisted Miami Pouch following laparoscopic anterior pelvic exenteration. Gynecol Oncol 2004; 93:543–5. 50. Ferron G, Querleu D, Martel P, Letourneur B, Soulie M. Laparoscopically-assisted vaginal pelvic exenteration. Gynecol Oncol 2006;100: 551–5. 51. Querleu D, Leblanc E. Laparoscopic surgery for gynaecological oncology. Curr Opin Obstet Gynecol 2003;15:309–14. 52. Ferron G, Gesson-Paute A, Classe JM, Querleu D. Feasibility of laparoscopic peritonectomy followed by intra-peritoneal chemohyperthermia: an experimental study. Gynecol Oncol 2005;99: 358–61. 53. Vergote I, De Smet I, Amant F. High incidence of positive peritoneal cytology in low risk endometrial cancer treated by laparoscopically assisted vaginal hysterectomy. [letter]. Gynecol Oncol 2002;84: 537–9. 54. Querleu D, Lanvin D, Elhage A, Henry-Buisson B, Leblanc E. An objective experimental assessment of the learning curve for laparoscopic surgery: the example of pelvic and para-aortic lymph node dissection. Eur J Obstet Gynecol Reprod Biol 1998;81:55–8. 55. Occelli B, Narducci F, Lanvin D, Leblanc E, Querleu D. Learning curves for transperitoneal laparoscopic and extraperitoneal endoscopic paraaortic lymphadenectomy. J Am Assoc Gynecol Laparosc 2000;7: 51–3. 56. Schlaerth JB, Spirtos NM, Carson LF, Boike G, Adamec T, Stonebraker B. Laparoscopic retroperitoneal lymphadenectomy followed by immediate laparotomy in women with cervical cancer: a Gynecologic Oncology Group study. Gynecol Oncol 2002;85: 81–8.