Feasibility of laparoscopic extraperitoneal surgical staging for locally advanced cervical carcinoma in a gynecologic oncology fellowship training program

Journal of Minimally Invasive Gynecology (2006) 13, 391–397

Feasibility of laparoscopic extraperitoneal surgical staging for locally advanced cervical carcinoma in a gynecologic oncology fellowship training program M. Patrick Lowe, MD, Afshin Bahador, MD, Laila I. Muderspach, MD, Alexander Burnett, MD, Luis Santos, MD, Angela Caffrey, MD, Lynda D. Roman, MD, and C. Paul Morrow, MD From the Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, University of Southern California Keck School of Medicine, Los Angeles, California (all authors). KEYWORDS: Laparoscopic extraperitoneal surgical staging; Cervical cancer; Minimally invasive surgery; Gynecologic oncology fellowship training

Abstract STUDY OBJECTIVE: Feasibility of laparoscopic extraperitoneal surgical staging for locally advanced cervical carcinoma in a gynecologic oncology fellowship training program. DESIGN: Retrospective analysis (II-2) of all patients who underwent laparoscopic extraperitoneal surgical staging at Women and Children’s Hospital for locally advanced cervical cancer between June 2002 and June 2005. SETTING: Gynecologic oncology fellowship training program at a University-County Hospital PATIENTS: Thirty-two patients with clinical stage IIB-IVA cervical carcinoma were identified. INTERVENTIONS: Laparoscopic extraperitoneal surgical staging for clinical stage IIB-IVA cervical cancer. MEASUREMENTS AND MAIN RESULTS: A total of 32 cases of laparoscopic extraperitoneal surgical staging for locally advanced cervical cancer performed by fellows-in-training were identified. Fellows were first assistant surgeon in 10 cases, and operating surgeon in 22 cases. Each fellow was mentored an average of 5 cases as first assistant surgeon. As operating surgeon, all 22 fellow cases (100%) were successfully performed without conversion to laparotomy. Fellow mean operative time was 163 minutes. Fellow mean aortic nodal count was 14. Fellow mean blood loss was 42 mL. The mean hospital stay was 1.6 days. Overall, 2 patients (6.2%) experienced a complication from the procedure. Over one half (53%) of the patients reported a prior abdominal surgery. No lymphedema has been reported in patients who underwent laparoscopic extraperitoneal surgical staging with a median follow-up of 10 months. Surgical comorbidities such as hypertension, diabetes, and obesity were common in the study group. A steep surgical learning curve for the fellows was demonstrated by comparing mean operative times to academic year. Aortic nodal metastasis was detected in 25% of cases, and 14% were occult. CONCLUSIONS: It is feasible to teach laparoscopic extraperitoneal surgical staging to fellows-intraining. Our data suggest that by the end of training, fellows can become proficient with the procedure and are capable of surgical outcomes and complication rates comparable to reported literature. © 2006 AAGL. All rights reserved.

1553-4650/$ -see front matter © 2006 AAGL. All rights reserved. doi:10.1016/j.jmig.2006.04.007

392

Journal of Minimally Invasive Gynecology, Vol 13, No 5, September/October 2006

Locally advanced cervical carcinoma is known to metastasize through the lymphatic system to the pelvic lymph nodes and subsequently to the aortic region. The incidence of aortic nodal metastasis for locally advanced cervical carcinoma has been previously reported in the literature.1,2 Surgical staging of locally advanced carcinoma of the cervix is a controversial procedure that has been described in the literature by numerous authors. This technique has evolved in the last 30 years from open laparotomy to retroperitoneal laparotomy to a transperitoneal or extraperitoneal laparoscopic (minimally invasive) approach. Data demonstrate that a laparoscopic approach for nodal staging is associated with fewer operative complications, fewer delays in initiating radiation therapy because of operative complications and shorter hospital stays and recently has been described to provide a survival advantage in patients with paraaortic nodal metastasis when greater than 5 nodes were removed.3–21 With regard to nonsurgical staging techniques such as computed tomography (CT), magnetic resonance imaging, and positron emission tomography, several published reports detail the inaccuracy in the detection of occult aortic nodal metastasis.22–27 The most recent advance in this technique is laparoscopic extraperitoneal surgical staging (LEPSS), a novel minimally invasive technique that allows for the detection of occult aortic metastasis with few operative complications and rapid postoperative recovery. Vasilev and McGonigle15 initially reported laparoscopic extraperitoneal surgical staging in 1995. This reported experience with an animal model was soon followed with a small human trial reporting the efficacy of laparoscopic extraperitoneal surgical staging in cervical carcinoma patients.16 Over the past few years, several prospective and retrospective studies have been published detailing the procedure, its modifications, and its usefulness in various gynecologic cancers.15–21 The bulk of this literature has evolved through the work of Dargent and Querleu17–19 who have helped pioneer the use of laparoscopic procedures in gynecologic oncology. These accumulating data have demonstrated the safety, efficacy, and feasibility of laparoscopic extraperitoneal surgical staging when in the hands of an experienced surgeon. However, there is very little data reporting on the experience of gynecologic oncology fellowsin-training with minimally invasive procedures, and to our knowledge, no report in the literature details the experience of gynecologic oncology fellows-in-training with laparoscopic extraperitoneal surgical staging for locally advanced cervical carcinoma. Fellows at the University of Southern California (USC) are exposed to and perform a number of laparoscopic and Corresponding author: M. Patrick Lowe, MD, The West Clinic, P.C. 100 North Humphreys Boulevard, Memphis TN 38120 or Division of Gynecologic Oncology, Women’s and Children’s Hospital, University of Southern California Keck School of Medicine, Room 1L4, 1240 N Mission Road, Los Angeles, CA 90033. E-mail: [email protected] or [email protected]. Submitted November 16, 2005. Accepted for publication April 13, 2006.

laparoscopic-assisted procedures. The aim of this article is to report our experience with the introduction of LEPSS into our fellowship training program. The results of our analysis demonstrate that it is feasible to teach laparoscopic extraperitoneal surgical staging to fellows-in-training. Our data suggest that by the end of training, fellows can become proficient with the procedure and are capable of surgical outcomes and complication rates comparable to reported literature.

Materials and methods After receiving approval from the Institutional Review Board, a retrospective analysis of all patients who underwent laparoscopic extraperitoneal surgical staging at Women’s and Children’s Hospital for locally advanced cervical cancer between June 2002 and June 2005 was performed. Patients with clinical stage IIB-IVA cervical carcinoma according to International Federation of Gynecology and Obstetrics (FIGO) staging were eligible for the procedure. Laparoscopic extraperitoneal surgical staging was offered to patients with locally advanced cervical cancer for whom no radiologic evidence (CT scan) of bulky (⬎1.5 cm) aortic nodal metastasis was detected, who were medically fit for surgery, and who did not require emergency radiation therapy for excessive vaginal bleeding/anemia. A total of 32 patients were identified for review. Records were reviewed for patient age, clinical stage, surgical comorbidities, tumor histologic condition, nodal count, operative time, body mass index, preoperative CT scan aortic node status, operative and postoperative complications, estimated blood loss, rate of conversion to laparotomy, and hospital stay. The timeframe for this analysis coincides with first academic year (2002) at USC that fellows-in-training assisted or performed most of these cases. Only 1 fellow and 1 faculty was present per case. The operating surgeon was defined as the individual who performed at least 80% of the procedure. The procedure can be broken into 5 parts: diagnostic laparoscopy to rule out intraperitoneal disease, the insertion of the retroperitoneal trocars, the development of the retroperitoneal space, the right aortic nodal dissection, and the left aortic nodal dissection. In each case, the operating surgeon performed at least 80% of the procedure. The role of the first assistant was to primarily operate the video scope and at times to perform a limited (20%) surgical role in the procedure. The role of first assistant enabled that fellow to learn to identify the anatomy and develop the surgical planes safely. Interactive mentoring was emphasized during each case in which the fellow was first assistant. This analysis reports the experience of the first 2 fellows at USC trained to perform laparoscopic extraperitoneal surgical staging. In this report, the fellow initially participated as first assistant surgeon for a prescribed number of cases with an attending surgeon (primarily C.P. Morrow). When the fellow’s skills were deemed proficient by the attending sur-

Lowe et al

Laparoscopic extraperitoneal surgical staging in fellowship training

geon, the fellow operated as primary surgeon with an attending as first assistant. The decision to allow the fellow to operate as primary surgeon was observational in nature and was based primarily on the surgical ability of the fellow from both a laparoscopic and traditional laparotomy standpoint, demonstration of a thorough understanding of the relevant anatomy, precision and skill as first assistant surgeon, and confirmation of excellent hand-eye coordination with laparoscopic instrumentation. Our surgical technique is adopted and slightly modified from Querleu and Dargent as reported recently by Burnett et al.20 Our nodal dissection begins at the mid-portion of the common iliac arteries and extends to the inferior mesenteric artery bilaterally. However in some cases, suspicious or enlarged aortic lymph nodes (grossly or radiologic) were sent during operation for frozen section analysis. If negative, the upper limit of the nodal dissection would terminate at the level of the inferior mesenteric artery. If positive, the nodal dissection would continue cephalad until all suspicious/enlarged nodes were resected or frozen section analysis of additional higher nodes was negative. We use a left-sided laparoscopic approach for most of our cases (90%).17 At the conclusion of each procedure, marsupialization of the retroperitoneum is performed to prevent lymphocyst formation. All fascial incision equal/greater than 1 cm are closed with delayed absorbable suture. The Versa Step bladeless expandable laparoscopic trocar system (United States Surgical Corporation, Norwalk, CT) for laparoscopic procedures was employed. The Versa-Step bladeless expandable trocar system utilizes a standard Veres needle enveloped by a sheath through which a 5-, 11-, or 12-mm trocar is then placed. The Versa Step combines the advantages of radial dilation of the fascia with the Versaseal universal seal. This universal seal maintains pneumoperitoneum while facilitating easy exchange of instruments ranging from 5 mm to 12 mm. For retroperitoneal procedures, we feel that this system allows for controlled insertion of the laparoscopic port into the retropneumoperitoneum safely and with minimal effort. All patients were seen and examined by a fellow and faculty member and presented at our weekly tumor board conference. In addition, each patient underwent preoperative CT scanning of the abdomen and pelvis to assess nodal status. Nodal status was recorded and documented for each patient by a board-certified radiologist at our tumor board conference. All pathologic specimens were reviewed by 1 of 2 board-certified gynecologic pathologists at our institution.

Results A review of the USC database between June 2002 and June 2005 identified 32 patients who underwent LEPSS for locally advanced cervical cancer. Thirty-one of 32 (97%) procedures were successfully performed without conversion to laparotomy. The patient demographics are shown in Ta-

Table 1

393

Patient demographics Demographics: Patients: n ⫽ 32 Mean Age 49.7 (15-76) Mean BMI 27.1 (17-39) Clinical Stage: IIB 16 (50%) IIIA 2 (6.2%) IIIB 11 (34%) IVA 1 (3.1%) Referred (Cut-Through) 2 (6.2%) Histology: Squamous 24 (75%) Adenocarcinoma 5 (16)% Other 3 (9.3%) Co-Morbidity: Hypertension 9 (30%) Diabetes Mellitus 6 (19%) Prior Abdominal Surgery 17 (53%) BMI ⬎ 30 11 (34%) (range 30-39)

ble 1. The mean age was 49. The mean body mass index was 27.1. The range for body mass index was 17 to 39. Surgical comorbidities such as hypertension (30%), diabetes (19%), and obesity (34%) were common in the study group. More than one half (53%) of the patients reported a prior abdominal surgery, most commonly a cesarean section or appendectomy. There were no operative or postoperative complications attributed to hypertension, diabetes, obesity, or prior abdominal surgery in our analysis. Our experience suggests that such surgical comorbidities should not be considered as a contraindication to performing LEPSS in these patients. According to FIGO staging, one half (50%) of the patients were stage IIB, one third (34%) were stage IIIB, and the remainder were stage IIIA (6.2%), stage IVA (3.1%), and unstaged (6.2%). Three fourths (75%) of the tumors were squamous in origin. The remainder were adenocarcinoma (16%), clear cell (3.1%), adenosquamous (3.1%), and small-cell neuroendocrine (3.1%). Operative outcomes for the fellows are listed are listed in Table 2. A total of 32 cases of laparoscopic extraperitoneal surgical staging for locally advanced cervical cancer performed by fellows-in-training were identified. Fellows were first assistant surgeon in 10 cases, and operating surgeon in 22 cases. Each fellow was mentored for a total of 5 cases as first assistant surgeon. As operating surgeon, all 22 fellow cases (100%) were successfully performed without conversion to laparotomy. Faculty mean operative time was 195 minutes as operating surgeon, while fellow mean operative time was 163 minutes as operating surgeon. The longer operative time of the faculty in this study reflects the additional time required to provide adequate mentoring to the fellow in the procedural and anatomical aspects of performing LEPSS. Fellow mean aortic nodal count was 14. Fellow mean blood loss was 42 mL. Estimated blood loss was calculated by visual inspection of the operative field, measured volumes, or sponge count by the surgeon and anesthesiologist. With the exception of a few cases, the esti-

394

Operative findings for fellows (n ⫽ 32)

Fellow operative findings Operating surgeon Assistant surgeon Mean no. Of cases (1st assistant surgeon) Fellow mean operative time Faculty mean operative time Fellow mean nodal count Conversion to laparotomy Conversion to transperitoneal approach Mean estimated blood loss Mean postoperative stay Overall aortic nodal metastasis Occult aortic nodal metastasis Fellow (operating) surgeon by academic year 2002-03 2003-04 2004-05 2002-05 (total) Fellow mean operative time (academic year) 2002-03 2003-04 2004-05 Overall (faculty ⫹fellow) operative time (academic year): 2002-03 2003-04 2004-05 2002-05

Mean Operative Time by Academic Year

250

22 cases 10 cases 05 cases 163 minutes (111-240) 195 minutes (155-240) 14 (5-36) None None

215

200 157 143

150 Minutes

100

42 mL (10-200) 1.6 days (1-6) 25%

50

14%

0 2 00 2

20 0 3

20 04

Academic Year

5 (56%) 6 (60%) 11 (85%) 22 (67%)

215 minutes (170-240) 157 minutes (131-180) 143 minutes (111-225)

210 minutes (170-240) 168 minutes (131-229) 150 minutes (111-225) p Value ⫽ .008

mated blood loss was calculated on visual inspection of the operative field alone. The mean hospital stay was 1.6 days. Twenty-five (25%) percent of the patients had positive aortic nodal metastasis detected on final pathologic study, of which 14% were occult. As the fellows demonstrated competence with the procedure, their number of cases as operating surgeon increased from 56% (5 of 9) in first academic year to 85% (11 of 13) in the third academic year. In addition, a steep surgical learning curve for the fellows was demonstrated by comparing mean operative times to academic year, as shown in Figure 1. Mean operative time for the fellows decreased from 215 minutes during the first academic year (2002–2003) to a mean operative of 143 minutes during the third academic year (2004 –2005). In comparison, in the largest series published to date the mean operative time was 157 minutes (Querleu et al as reported by Sonoda et al19). In Figure 2, a scatter plot of all operative times per academic year is shown. An analysis of the duration of surgery over time (2002–2005) was performed with simple linear regression, and a statistically significant decrease in the duration of surgery over time was observed, with a p value ⫽ .008 and r ⫽ value .35 (Table 2). Other variables analyzed revealed no statistically significant dif-

Figure 1

Mean fellow operative time by academic year.

ference in the number of nodes removed over time (Figure 3), no significant change in the length of stay over time, nor was there a correlation in the number of nodes removed and the duration of the surgery (Data not shown). Nine percent (9.3%) of the patients experienced a complication during the timeframe for the analysis. However, only 6.2% of the patients experienced a complication from the procedure (Table 3). In 1 patient the laparoscopic procedure was converted to laparotomy because of positive infrarenal nodes. This patient experienced a ureteral injury near the renal pelvis during the laparotomy portion of the procedure, and a ureteral anastomosis and stent placement was performed without complication. However, no complications were encountered during the laparoscopic portion of that patient’s procedure. This patient’s preoperative CT scan was negative for aortic nodal metastasis. The other patient complication was a postoperative lymphocyst requiring a drain placement (ultrasound guidance). As a result

Length of Operation by Year 300

Length of Operation (minutes)

Table 2

Journal of Minimally Invasive Gynecology, Vol 13, No 5, September/October 2006

200 157

100

0 2001.5

2002

2002.5

2003

Year

Figure 2

Length of operation by year.

2003.5

2004

200

Lowe et al

Laparoscopic extraperitoneal surgical staging in fellowship training Number of Nodes by Year

Table 3 Operative and postoperative complications (n ⫽ 32)

40

Lymphocyst formation Conversion to laparotomy Ureteral injury (after conversion laparotomy) Blood transfusion Retroperitoneal hematoma Bowel injury/obstruction Reoperation rate Lymphedema Total complication Adjusted rate Delay in radiation therapy

30 Number of Nodes

395

20

10

1(3.1%) 1(3.1%) 1(3.1%) 0(0.0%) 0(0.0%) 0(0.0%) 0(0.0%) 0(0.0%) 3(9.3%) 2(6.2%) 2(6.2%)

0 2002

2003

2004

Year

Figure 3

Number of nodes by year.

of operative complications, 6.2 % had a delay of 6 and 4 weeks before instituting definitive chemoradiation. No patient received a blood transfusion as a result of the procedure. There were no vascular injuries, postoperative hernias, bowel injuries, bowel obstruction, retroperitoneal abscess or hematomas, lymphedema detected, nor did any patient require reoperation for any circumstance. Of note, all patients in this series underwent marsupialization of the retroperitoneum at the conclusion of the procedure. There were no conversions from a retroperitoneal to a transperitoneal nodal dissection because of loss of retropneumoperitoneum from incidental peritoneal defects. This small but significant problem appears to have been eliminated by the use of vascular clips (n ⫽ 4) or the transperitoneal application of a laparoscopic grasper (n ⫽ 1) to seal peritoneal defects. This innovative technique developed in the latter half of our study corrects incidental peritoneal defects. These defects previously resulted in partial or complete loss of the operative retropneumoperitoneum. Defects are now repaired with the placement of laparoscopic vascular clip applicators (US Surgical Corporation [USSC] 5 or 10 mm) or laparoscopic Maryland graspers (USSC) that stabilize the retropneumoperitoneum. The technique has been successful in maintaining an operative pneumoperitoneum in the first 5 patients it was used. With regard to the detection of aortic nodal metastasis via nonsurgical staging techniques, all patients underwent preoperative CT scanning, and aortic nodal status was recorded for each patient. Twenty-eight (87%) of 32 patients had a CT scan negative for aortic nodal metastasis before operation. Four (13%) of 32 patients had a CT scan positive for aortic nodal metastasis before operation. Pathologic findings demonstrated that overall 8 (25%) of 32 patients had aortic nodal metastasis on final pathologic study. However, occult aortic nodal metastasis were detected in 4 (14%) of 28 patients whose preoperative CT scan was negative for aortic nodal metastasis (Table 4). Thus, if relying on nonsurgical staging techniques (CT scan) alone, 14% of patients with a negative preoperative CT scan would

have been undertreated by not receiving extended field radiation therapy. A sensitivity of 50% and a specificity of 100% for CT scanning detection of aortic nodal metastasis were observed (Table 4). This is comparable to the reported literature on the use of CT scans on locally advanced cervical cancer.9 –12 Use of magnetic resonance imaging or positron emission tomography scanning for nonsurgical staging is not routinely available in a timely, treatmentoriented fashion at our institution.

Discussion Since the early 1980s advances in laparoscopic surgery have been seen in almost every surgical specialty. In its infancy, laparoscopic surgical procedures were developed and pioneered by gynecologic surgeons and urologists. Since the birth of this era, laparoscopic surgical training has become a core requirement for residents training in obstetrics and gynecology. With the recent advances in laparoscopic surgical technology and advanced procedures, many obstetric and gynecology residents are beginning their practices with a full armamentarium of minimally invasive procedures available for their patients. In the field of gynecologic oncology, only a few advanced laparoscopic (minimally invasive) procedures are available for patient care. The published literature for advanced minimally invasive gynecologic oncology procedures has steadily grown over the last 10 years. This collection of studies has reported on various procedures such as laparoscopic assisted vaginal hysterectomy and nodal dissection, laparoscopic assisted

Table 4

Detection of occult aortic nodal metastasis

Aortic Nodal Status (Preoperative)

Positive

Negative

CT Scan Findings* Pathologic Metastasis

4/32 (13%) 4/4 (100%)

28/32 (87%) 4/28 (14%) (⫹ Occult Metastasis)

*Sensitivity, 50%; specificity, 100%.

396

Journal of Minimally Invasive Gynecology, Vol 13, No 5, September/October 2006

radical vaginal hysterectomy, total laparoscopic simple and radical hysterectomy, laparoscopic transperitoneal and retroperitoneal nodal staging, and laparoscopic assisted radical vaginal cervicectomy.7–21,27–32 However, the published literature for advanced laparoscopic procedures in gynecologic oncology fellowship training programs is virtually nonexistent. In a recent survey by Frumovitz et al,32 the vast majority of gynecologic oncology fellow respondents described their current fellowship training as limited with regard to minimally invasive procedures. However, the large majority (75%) of fellows rated their laparoscopic skill levels as good or very good, most likely the result of their residency training. In the same survey, Society of Gynecologic Oncologists respondents believed that laparoscopic instruction is an important part of fellowship training, but most of the same respondents (65%) use laparotomy for most surgeries. Both respondents agreed on a need for an increased emphasis (much or maximum) on fellowship training in laparoscopy.32 However, there are no guidelines or blueprints for implementation of such laparoscopic emphasis into gynecologic oncology fellowship training. The results of our fellows’ experience with laparoscopic extraperitoneal surgical staging within our fellowship program are exciting, but at the same time are precocious. However, it must be clarified that the mean of 5 cases reported for each fellow as first assistant does not infer that each fellow served as an assistant for 5 cases before operating as primary surgeon. There are 2 different surgicalanatomic approaches for the procedure: left-sided and rightsided. The right-sided approach is used less commonly. Thus the fellows in this study performed cases as primary surgeon from the left-sided approach before mentoring on the right-sided approach. The decision-making process to determine the fellow competence to operate as primary surgeon is discussed in the Methods section. The results of this study reflect the experience of the first 2 fellows at USC trained to perform laparoscopic extraperitoneal surgical staging. The operative time, estimated blood loss, nodal count, hospital stay, and complication rate reported in this article compare favorably with the reported literature for laparoscopic extraperitoneal surgical staging.15–21 The findings in this study are unique in that the data for the faculty and fellows were available for analysis. It is possible that if the fellows in this study had little or no advanced laparoscopic training before fellowship the results of this study could be impacted negatively. However, it is too early at our institution to comment, and longer follow-up data are required as additional fellows are trained in the procedure not only at USC but at other institutions. We recognize the fact that this analysis reflects only the experience of our first 2 fellows with LEPSS and plan to reanalyze our data as additional fellows are trained to perform the procedure. The emphasis on advanced laparoscopic surgery by the USC Division of Gynecologic Oncology has evolved since the inception of the procedures in the late 1990s. These

techniques were implemented at our institution by one of the co-authors (C. Paul Morrow) who received laparoscopic instruction while on sabbatical (with D. Dargent, Lyon, France, and M. Roy, Quebec City, Quebec). Advanced laparoscopic procedures learned in France were then introduced into our division and subsequently the fellowship. In the early developmental stages of our minimally invasive program, most of the faculty within the division had little or no formal advanced laparoscopic experience or training. The initial emphasis on laparoscopic training was with the faculty who quickly adapted and mastered several of these new procedures. Our initial experience with laparoscopic aortic nodal staging for locally advanced cervical cancer was via a transperitoneal approach. The transperitoneal approach is well documented in the literature as a safe and efficacious procedure.10 –14,31 Our experience with the transperitoneal approach, although successful, transitioned to an extraperitoneal approach. The advantage of an extraperitoneal approach is to avoid disruption of the peritoneum that could lead to bowel adhesion formation. In the presence of bulky nodal disease, we routinely perform open extraperitoneal nodal staging rather than use a laparoscopic approach. From our experience, it is critical that the faculty learns and masters the procedures before fellow instruction. Once these procedures are mastered, emphasis should then shift toward the fellows. The selection of fellows with a strong background in advanced laparoscopy can provide a solid foundation to build on during fellowship training. Some of our recent fellows received formal advanced laparoscopic training during residency with procedures such as; laparoscopic assisted vaginal hysterectomy, laparoscopic Burch colposuspension, laparoscopic sacrocolpopexy, laparoscopic pelvic lymph node sampling, laparoscopic paravaginal repair, intracorporeal knot tying, total laparoscopic hysterectomy, and laparoscopic supracervical hysterectomy with morcellation. The combination of experienced faculty, highly motivated fellows, and skilled laparoscopists (both at the faculty and fellow level) collectively and individually have contributed to our success.

Conclusion In summary, advanced laparoscopic procedures such as LEPSS should be encouraged and emphasized in fellowship training programs. The USC experience with advanced laparoscopy and that of other leaders within our specialty may serve as a model for other programs to institute advanced laparoscopy into their training programs. In the coming years, gynecologic oncologists will move toward and perform more diagnostic or therapeutic laparoscopic procedures for their patients. To advance the specialty and meet this demand, the next generation of gynecologic oncologists will need to obtain a solid foundation in advanced laparoscopy during fellowship training.

Lowe et al

Laparoscopic extraperitoneal surgical staging in fellowship training

References 1. Morrow CP, Curtin JP, Townsend DE. Synopsis of gynecologic oncology. 4th ed. New York: Churchill Livingston; 1993. 2. Nelson JH Jr, Boyce J, Macasaet M, Lu T, Bohorquez JF, Nicastri AD, et al. Incidence, significance, and follow-up of para-aortic lymph node metastasis in late invasive carcinoma of the cervix. Am J Obstet Gynecol. 1977;128:336 –340. 3. Berman ML, Lagasse LD, Watring WG, Ballon SC, Schlesinger RE, Moore JG, et al. The operative evaluation of patients with cervical carcinoma by an extraperitoneal approach. Obstet Gynecol. 1977;50: 658 – 664. 4. Goff BA, Muntz HG, Paley PJ, Tamimi HK, Koh WJ, Greer BE. Impact of surgical staging in women with locally advanced cervical cancer. Gynecol Oncol. 1999;74:436 – 442. 5. Heller PB, Maletano JH, Bundy BN, Barnhill DR, Okagaki T. Clinical-pathologic study of stage IIB, III, and IVA carcinoma of the cervix: extended diagnostic evaluation for paraaortic node metastasis. A GOG study group. Gynecol Oncol. 1990;38:425– 430. 6. Cosin JA, Fowler JM, Chen MD, Paley PJ, Carson LF, Twiggs LB. Pretreatment surgical staging of patients with cervical carcinoma: the case for lymph node debulking. Cancer. 1998;82:2241–2248. 7. Denschlag D, Gabriel B, Mueller-Lantzsch C, Tempfer C, Henne K, Gitsch G, et al. Evaluation of patients after extraperitoneal lymph node dissection for cervical cancer. Gynecol Oncol. 2005;658 – 664. 8. Downey GO, Potish RA, Adcock LL, Prem KA, Twiggs LB. Pretreatment surgical staging in cervical carcinoma: therapeutic efficacy of pelvic lymph node resection. Am J Obstet Gynecol. 1989;74:436 – 442. 9. Hasenburg A, Salama JK, Van TJ, Amosson C, Chiu JK, Kieback DG. Evaluation of patients after extraperitoneal lymph node dissection and subsequent radiotherapy for cervical cancer. Gynecol Oncol. 2002;64: 321–326. 10. Lai CH, Huang KG, Hong JH, Lee CL, Chou HH, Chang TC, et al. Randomized trial of surgical (extraperitoneal or laparoscopic) versus clinical staging in locally advanced cervical cancer. Gynecol Oncol. 2003;89:160 –167. 11. Chung HH, Lee S, Sim JS, Kim JY, Seo SS, Park SY, et al. Pretreatment laparoscopic surgical staging in locally advanced cervical cancer: preliminary results in Korea. Gynecol Oncol. 2005;97:468 – 475. 12. Marnitz S, Hohler C, Roth C, Fuller J, Hinkelbein W, Schneider A. Is there a benefit to pretreatment laparoscopic transperitoneal surgical staging in patients with advanced cervical cancer? Gynecol Oncol. 2005;99:536 –544. 13. Possover M, Krause N, Plaul K, Kuhne-Heid R, Schneider A. Laparoscopic para-aortic and pelvic lymphadenectomy: experience with 150 patients and review of the literature. Gynecol Oncol. 1998;71:19 – 28. 14. Vidaurreta J, Bermudez A, di Paola G, Sardi J. Laparoscopic staging in locally advanced cervical carcinoma: a new possible philosophy? Gynecol Oncol. 1999;75:366 –371. 15. Vasilev SA. Extraperitoneal laparoscopic para-aortic lymph node dissection: development of a technique. J Laparosc Endosc Surg. 1995; 5:85–90. 16. Vasilev SA, McGonigle KF. Extraperitoneal laparoscopic para-aortic lymph node dissection. Gynecol Oncol. 1996;61:315–320.

397

17. 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. 18. Querleu D, Dargent D, Ansquer Y, Leblanc E, Narducci F. Extraperitoneal endosurgical aortic and common iliac dissection in the staging of bulky or advanced cervical carcinomas. Cancer. 2000; 88:1883– 1991. 19. Sonoda Y, Leblanc E, Querleu D, Castelain B, Papageorgiou TH, Lambaudie E, et al. Prospective evaluation of surgical staging of advanced cervical cancer via a laparoscopic extraperitoneal approach. Gynecol Oncol. 2003;91:326 –331. 20. Burnett AF, O’Meara AT, Bahador A, Roman LD, Morrow CP. Extraperitoneal laparoscopic lymph node staging: The University of Southern California experience. Gynecol Oncol. 2004;95:189 –192. 21. Mehra G, Weekes ARL, Jacobs IJ, Visvanathan ??, Menon U, Jeyarajah AR. Laparoscopic extraperitoneal paraaortic lymphadenectomy: a study of its applications in gynecological malignancies. Gynecol Oncol. 2004;93:189 –193. 22. Subak LL, Hedvig H, Powell B, Azizi L, Stern JL. Cervical carcinoma: computed tomography and MRI for pre-operative staging. Obstet Gynecol. 1995;86:43–50. 23. Kim SH, Choi BI, Han JK, Kim HD, Lee HP, Kang SB, Lee JY, Han MO. Pre-operative staging of uterine cervical carcinoma: comparison of CT and MRI in 99 patients. J Comput Assist Tomography. 1993;4: 633– 640. 24. Scheidler J, Hricak H, Yu KK, Subak L, Segal MR. Radiological evaluation of lymph node metastases in patients with cervical cancer. A meta-analysis. JAMA. 1997;13:1096 –1101. 25. Yang WT, Lan W, Yu MY, Cheung TH, Metreweli C. Comparison of dynamic helical CT and dynamic MRI imaging in the evaluation of pelvic lymph nodes in cervical cancer. AJR. 2000;175:659 – 666. 26. Grigsby PW, Siegel BA, Dehadashti F. Lymph node staging by positron emission tomography in patients with carcinoma of the cervix. JCO. 2001;19:3745–3749. 27. Rose PG, Adler LP, Rodriguez M, Faulhaber PF, Adbul-Karim FW, Miraldi F. Positron emission tomography for evaluating para-aortic nodal metastasis in locally advanced cervical cancer before surgical staging: A surgico- pathologic study. JCO. 1999;17:41– 45. 28. 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 –348. 29. Abu-Rustum NR, Gemignani ML, Moore K, Sonoda Y, Venkatraman E, Brown C, et al. Total laparoscopic radical hysterectomy with pelvic lymphadenectomy using the argon-beam coagulator: pilot data and comparison to laparotomy. Gynecol Oncol. 2003;9:402– 409. 30. Dargent D, Martin X, Sacchetoni A, Mathevet P. Laparoscopic vaginal radical trachelectomy: a treatment to preserve the fertility of cervical carcinoma patients. Cancer. 2000;88:1877–1882. 31. Kohler C, Klemm P, Schau A, Possover M, Krause N, Tozzi R, 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. 32. Frumovitz M, Ramirez PT, Greer M, Gregurich MA, Wolf J, Bodurka DC, Levenback C. Laparoscopic training and practice in gynecologic oncology among Society of Gynecologic Oncologists members and fellows-in-training. Gynecol Oncol. 2004;94:746 –753.