Gynecologic Oncology 120 (2011) 362–367 Contents lists available at ScienceDirect Gynecologic Oncology j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y g y n o Twelve-year experience with laparoscopic radical hysterectomy and pelvic lymphadenectomy in cervical cancer Xiaojian Yan a, Guangyi Li b, Huiling Shang b,⁎, Gang Wang b, Yubin Han b, Tiecheng Lin b, Feiyun Zheng a a b Department of Obstetrics and Gynecology, The First Affiliated Hospital of Wenzhou Medical College, 325000 Wenzhou, China Department of Obstetrics and Gynecology, The First People's Hospital of Foshan, No. 81, North Lingnan Street, Chancheng District, Foshan, Guangdong, 528000, China a r t i c l e i n f o Article history: Received 30 August 2010 Available online 18 December 2010 Keywords: Cervical cancer Laparoscopy Radical hysterectomy a b s t r a c t Objectives. This study aims to evaluate the morbidity, oncological outcome, and prognostic factors of cervical cancer patients treated with laparoscopic radical hysterectomy and pelvic lymphadenectomy (LRH). Methods. Patients with cervical cancer undergoing LRH at the First People's Hospital of Foshan between August 1998 and March 2010 were enrolled in this study. The medical records were reviewed. Results. A total of 240 patients were identified. According to FIGO stage, the number of patients with stage Ia2, Ib1, Ib2, IIa, and IIb was 2, 163, 34, 35, and 6, respectively. The conversion rate was 1.25%. Intraoperative and postoperative complications occurred in 7.08% and 9.16% patients, respectively. Other medical problems included 74 cases (30%) of bladder dysfunction. Excluding the lost cases, the median follow-up of 221 cases was 35 months, and 5-year survival rate for Ia2, Ib1, Ib2, IIa was 100%, 82%, 66%, 60%, respectively. Univariate analysis showed factors impacting the survival rate were FIGO stage N Ib1, non-squamous histologic type, deep cervical stromal invasion, and lymph node metastasis (P = 0.027, 0.023, 0.007, 0.000). The Coxproportional hazards regression analysis indicated that only lymph node metastasis (OR = 3.827, P = 0.000) was independent of poor prognostic factor. The 5-year survival rates in Ib1 were 88% with negative lymph nodes and 59% with positive lymph nodes (P = 0.000). Conclusions. Our data demonstrate that LRH can be performed in stage Ia2–Ib1 or less advanced node negative cervical cancer patients without compromising survival. The feasibility of LRH for more advanced patients needs further investigations. © 2010 Elsevier Inc. All rights reserved. Introduction Acceptance of a new surgical technique in gynecologic oncology depends on several aspects, including technical feasibility, reasonable perioperative morbidity, adequacy of surgery, and better or at least same survival as the standard approach. Laparoscopic radical hysterectomy (LRH) has been reported since the early 1990s by Canis et al. [1] and Nezhat et al. [2]. Several teams throughout the world have recently reported promising results for early cervical cancer with this procedure, although the acceptance of LRH had been slow over the past 10 years [3]. LRH is technically feasible and associated with accepted intraoperative and postoperative complications. Its histopathologic outcome is also similar to that of radical abdominal hysterectomy (RAH) in terms of local radicality and lymph nodes yield. However, the currently existing recurrence and survival data are still immature to draw safe conclusions on its long-term oncological outcomes. It is particularly difficult to conceive a randomized trial for LRH. This is due to the limited number of ⁎ Corresponding author. Fax: +86 757 83812566. E-mail address: [email protected] (H. Shang). 0090-8258/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ygyno.2010.11.033 gynecologic oncologic departments where the procedure is available and to the relatively low frequency of recurrence, which implies a large sample size. In this paper, we present a comprehensive summary of 12 years of experience in LRH for cervical cancer. Materials and methods A retrospective review of LRH for 240 consecutive cervical cancers from August 1998 to March 2010 performed by the Gynecologic Division at the First People's Hospital of Foshan was conducted. The operations were performed by the team including 8 surgeons under the leading of Dr. Guangyi Li, who has extensive experience in gynecologic oncology and laparoscopic procedures. Informed consent was obtained from each patient after a thorough counseling therapeutic option, risks of the procedure, and possibility of conversion to laparotomy. The techniques described previously [4] had been modified in recent years. After induction of general anesthesia, patients were placed in lithotomic position. Traditionally, a simple uterine manipulator was inserted into the uterine cavity and with gauze attached to the uterine manipulator in the vagina. Recently, a new modified uterine manipulator with three different sizes of ring has been used to X. Yan et al. / Gynecologic Oncology 120 (2011) 362–367 maintain sufficient pneumoperitoneum, which allows a complete circumferential incision around the apex of the vaginal cuff before the specimen is removed. These ovaries were either resected or left in situ according to the stage and the patient's desire to preserve ovarian function. Systematic bilateral pelvic lymphadenectomy included dissection of common iliac nodes, external iliac nodes, internal iliac, obturator nodes, and deep inguinal lymph nodes. Lymph nodes were placed into a bag. LRH was performed by Piver-III standard transperitoneal route as described previously [4]. The specimen was removed, and the vagina was closed vaginally with drains, which were placed into vaginal cuff. Operative time was measured from the time of placement of the first trocar. Hospital stay was counted from the first postoperative day. Most patients received a voiding trial approximately 1 week after operation. Bladder dysfunction was defined by the criteria reported by Ramirez et al. [5] (more than 100 ml residual urine over 14 days). Patients failed the voiding trial had the catheter replaced for further bladder rest. Adjuvant therapy Among all the patients, 17 patients received neoadjuvant chemotherapy, radiotherapy, or concomitant CRT including 4 Ib2 patients, 7 IIa patients, 6 IIb patients. Neoadjuvant concomitant CRT with a platinum-based chemotherapy in combination with external beam radiotherapy to the pelvis (40–50 Gy) was given to IIb patients for down-staging. Adjuvant therapy after surgery was given to patients who had one or more risk factors such as lymph node metastases, bulky tumors, parametrial involvement, positive surgical margins, and deep cervical stromal invasion. Radiotherapy in these cases was administered as whole pelvis external beam radiation at a mean dose of 45 Gy (range, 40–50 Gy). Recently, chemotherapy based on cisplatin at a dose of 40 mg/m2 per week or 75 mg/m2 per 3 weeks was given postoperatively to patients with poor prognostic histological type or high-risk factors along with external beam pelvic irradiation. Follow-up Follow-up data were available for 221 patients. Univariate analysis of prognosis was performed using the log-rank test. The Life tables were used to calculate the overall survival rate. Survival curves were performed with the Kaplan–Meier method. The Cox-proportional hazards regression was employed to model the multivariate association of survival. The level of significance was P b 0.05. Results The patient's characteristics are shown in Table 1. There were 209 patients of squamous cell carcinoma (87.05%), 69.58% had grade 2 lesions. The mean number of resected pelvic lymph nodes was 23 (range, 8–58). Pelvic lymph node metastasis occurred in 58 patients (24.16%). Intraoperative data LRH was performed laparoscopically in 237 patients (98.75%). Bilateral salpingo-oophorectomy was performed in 156 patients (65%), whereas the remaining 84 patients (35%) had one or both adnexa preserved. Mean operative time was 264 min (range, 100–480 min). Median operative blood loss was 255 ml (range, 50–2000 ml). The transfusion rate was 8.33%. The median time to normal urine residual was 13 days (2–90 days), and the median length of hospital stay was 13 days (6–66 days). 363 Table 1 Patient characteristics of LRH (n = 240), among them 221 patients were followed up. Age (years) Weight (kg) FIGO stage Ia2 Ib1 Ib2 IIa1 IIa2 IIb Histology Squamous Adenocarcinoma Adenosquamous Adenoacanthoma Carcinomasarcoma Grade G1 G2 G3 Pelvic lymph nodes metastases n = 240 (total) n = 221 (followed up) 45 (24–74) 55 (35–80) 45 (24–74) 55 (35–80) 2 163 34 25 10 6 2 151 32 21 9 6 209 21 6 3 1 192 19 6 3 1 32 167 41 58 29 155 37 52 Intraoperative complications Intraoperative complications occurred in 17 patients (7.08%), including vascular injury (7), bladder injury (6), ureteral injury (3), and obturator nerve injury (1) (Table 2). All injuries were recognized intraoperatively and 3 (1.25%) patients required conversion to an open procedure. Postoperative data Among 22 patients (9.16%) who experienced postoperative medical or surgical problems, 4 patients had vesicovaginal fistula, 2 patients had ureterovaginal fistula, 6 patients had lymphocyst, 8 patients had lymphedema, and 2 patients had bowel obstruction (Table 2). Other medical problems included 74 cases (30.8%) of bladder dysfunction. Table 2 Intraoperative and postoperative complications of 240 patients. Complications Type of complication No. Treatment and outcome patient Intraoperative Vascular injury 7 complications 2 One was converted to laparotomy and successfully repaired Six were successfully treated laparoscopically One was converted to laparotomy and successfully repaired Five were successfully repaired laparoscopically One was converted to laparotomy Two were successfully treated by cystoscopic placement of double-J Successfully repaired laparoscopically with 3/0 Prolen Three closed by conservation treatment One successfully repaired vaginally Placed double-J ureteral stents 6 8 2 Observe Chinese medicine treatment Conservative management Bladder injury 6 Ureteral injury 3 Obturator nerve injury Postoperative Vesicovaginal complications fistula Ureterovaginal fistula Lymphocyst Lymphedema Bowel obstruction 1 4 364 X. Yan et al. / Gynecologic Oncology 120 (2011) 362–367 Fig. 1. Five-year survival after a median follow-up time of 35 months in 221 patients treated with LRH according to stage ≤ Ib1or stage N Ib1. Fig. 3. Five-year survival in stage Ib1 patients treated with LRH according to tumor diameter ≤ 2 cm (n = 74) or tumor diameter N 2 cm(n = 77). Oncological data regression analysis indicated that only lymph node metastasis OR = 3.827, P = 0.000) was independent of poor prognostic factors. There were 52 cases of patients with positive retroperitoneal nodes and 169 cases of patients with negative nodes. The 1-year, 3-year, 5-year overall survival rates in all stages were 93%, 89%, 84% with negative lymph nodes and 71%, 68%, 57% positive lymph nodes, P = 0.000. The 1-year, 3-year, 5-year survival rates were 90%, 87%, 82% in Ib1 (n = 151) and 80%, 76%, 66% in Ib2 (n = 32), P = 0.073. The 1-year, 3-year, 5-year survival rates in Ib1 were 96%, 92%, 88% with negative lymph nodes (n = 124) and 68%, 68%, 59% with positive lymph nodes (n = 27), P = 0.000. The 1-year, 3-year, 5-year survival rates in Ib1 were 92%, 89%, 89% with tumor diameter ≤ 2 cm (n = 74) and 88%, 86%, 76% with tumor diameter N2 cm(n = 77) (Fig. 3, P = 0.282). Among 240 cases, 19 cases were lost to follow-up, 25 cases were followed up to June 2007, and 196 cases were followed up to June 2010. The distribution of 221 cases according to FIGO stage was Ia2 n = 2, Ib1 n = 151, Ib2 n = 32, IIa n = 30, and IIb n = 6. The median follow-up was 35 months (range, 2–125 months). Eightyseven patients (39.4%) with one or more high-risk factors received postoperative adjuvant radiotherapy. Twenty-nine of these patients (33.3%) received concomitant CRT with a platinum-based chemotherapy. The other 134 (60.6%) received no future adjuvant therapy. Thirty-eight patients (17.19%) had recurrences or metastasis. Stage of recurrence was 24 at stage Ib1 (15.89%), 7 at stage Ib2 (21.88%), 7 at stage IIa (23.33%). No recurrence was found among the six patients at stage IIb within follow-up (median 27 months; range, 4–38 months). Sites of recurrence were pelvic or vaginal stump (13), abdominal cavity (3), lymph nodes (8), distant sites (8), and multiple sites (6). Among 38 patients with recurrence, 30 have died of their disease and 8 are alive with disease. Excluding the lost cases, the 5-year overall survival rate was 100% for Ia2, 79% for Ib (82% for Ib1, 66%for Ib2), 60% for IIa. Univariate analysis showed factors impacting the survival rate were FIGO stage N Ib1 (Fig. 1, P = 0.027), non-squamous histologic type (P = 0.023), deep cervical stromal invasion (P = 0.007), and lymph node metastasis (Fig. 2, P = 0.000). The Cox-proportional hazards Fig. 2. Five-year survival after a median follow-up time of 35 months in 221 patients treated with LRH according to lymph node involvement. Discussion Radical hysterectomy as described by Ernst Wertheim remains as the gold standard in the surgical management of operable cervical cancer. Introduction of laparoscopic pelvic lymphadenectomy (LPL) by Querleu et al. opened new perspectives for gynecologic oncology [6]. During the past 15 years, there has been an increasing interest in the possible role of laparoscopy in the treatment of cervical cancer, several teams worldwide have recently reported promising results [5,7–19] (Table 3). In most of these studies, patients enrolled were strictly selected from the stage Ib1 or less advanced or with node negative, which may explain the better prognosis. Although the feasibility of LRH has currently been proven in some stage Ib2–IIIb patients with an acceptable rate of complications, the follow-up time in those reported series is still too short to provide mature recurrence and survival data. In this study, six stage IIb patients received a neoadjuvant concomitant CRT and were alive at the last follow-up. Colombo et al. [18] have mentioned that TLRH after preoperative CRT is feasible for patients with locally advanced cervical cancer in 85% of the cases. TLRH compared with ARH was associated with favorable surgical outcome with comparable oncological results. However, effects of radiation on tissues could increase the difficulties of surgical dissection and the role of LRH after CRT for advanced cervical carcinoma remains controversial. Most of these studies have shown that LRH was a relatively timeconsuming procedure and the operative times ranged from 159 to 363 min [20], while Puntambekar et al. [10] reported an impressive 92 min (65–120 min), which was the shortest in the literature. Learning curve has been naturally confirmed in all series. Spirtos et al. [7,21] published 2 series of patients with cervical cancer treated with X. Yan et al. / Gynecologic Oncology 120 (2011) 362–367 Table 3 Studies of LRH including more than 18 patients each. Time Country Authors Number of case Palo Alto Women's Cancer Center 2003 France Institute Gustave Roussy Comprehensive Cancer Centre 2003 Australia King Edward Memorial Hospital for Women 2006 USA The University of Texas M.D. Anderson Cancer Center 2007 India The Galaxy Laparoscopy Institute, Pune 2007 China Southwest Hospital, Third Military Medical University Institute Spirtos et al. [7] Pomel et al. [8] Obermair et al. [9] Ramirez et al. [5] Puntambekar et al. [10] Xu et al. [11] 78 (26Ia2, 38Ib1, 14Ib2) 50 (5Ia1, 6Ia2, 39Ib1) 39 (13Ia, 24Ib, 1IIa, 1IVb) 18 (5Ia2, 13Ib1) 2007 Italy University of Insubria 2007 USA The University of Texas M. D. Anderson Cancer Center The Mount Sinai School of Medicine, Mount Sinai Medical Center San Gerardo Hospital, University of Miland Bicocca The First People's Hospital of Foshan Malzoni Medical Center, Avellino CRLC Val d'Aurelle Uccella et al. [12] Frumovitz et al. [13] Zakashansky et al. [14] 2002 USA 2007 USA 2009 Italy 2009 China 2009 Italy 2009 France 2009 Korea Kyungpook National University Hospital 248 (32Ia2, 216Ib1) 317 (82Ia2, 73Ib1, 52Ib2, 65IIa, 58IIb) 50 (7Ia2, 36Ib, 7IIa) 35 (2Ia1, 5Ia2, 28Ib1) 30 (1Ia1, 8Ia2, 17Ib1, 2 Ib2, 2IIa) Pellegrino et 101Ib1 al. [15] Yan et al. [16] 117 96Ib, 21IIa Malzoni et al. [17] Colombo et al. [18] Chong et al. [19] 77 (5Ia1, 24Ia2, 48Ib1) 46 (14Ib2, 4IIa, 28IIb) 100 (12Ia2, 56Ib1, 15Ib2, 15IIa, 2IIb) TLRH in 1996 and 2002, and the mean duration of their operation had been 253 min in the first group and 205 min in the second group of cases, respectively. Similarly, we observed that the operation time decreased significantly from 281 ± 70 min for the first 45 patients to 244 ± 61 min for the last 45 patients (P = 0.009) in our previous report [4]. However, our mean operation time of 240 patients was 264 min. Some surgeons were still in the “early phase” of the learning curves, which explained why we do not demonstrate a decrease in operation time. Our median blood loss was 255 ml, within a wellacceptable range for a procedure such as radical hysterectomy. Four existing comparative studies have confirmed a reduced blood loss during TLRH in comparison to RAH at a statistically significant level [20]. A major concern when evaluating surgical sampling is to evaluate lymph node status. The retrieval of a total number of 20 pelvic lymph nodes is considered to be the gold standard for an adequate complete lymphadenectomy [22]. In this study, the mean number of nodes obtained was 23. As we have previously mentioned, laparoscopic lymph node dissection was comparable to laparotomy in terms of node counts [4]. The rate of microscopic lymph node metastases was 24.16% for all patients and 17.88% for stage Ib1 in this study. It was consistent with 12–23% of lymph node metastases in stage I patients in the rest of the literature [23]. Our intraoperative complications rate was 7.08% with a conversion rate of 1.25%, which was consistent with some recent reports about LRH that the overall complication rate was between 2% and 13.2% with a conversion rate of 0% to 10.5% [7–19]. The main complications consist of vascular, bladder, ureteral, obturator nerve injuries. One case of obturator nerve transection occurred during pelvic lymphadenectomy, which can be repaired immediately using laparoscopic nerve epineural end to end with tension-free anastomosis technique. The patient had symptoms of adductor weakness with sensory trouble such as upper medial thigh anesthesia. A month later, the anesthesia disappeared and she was asymptomatic. Our strategies to prevent and treat other complications have been described previously [16]. To 365 prevent and eliminate complications, the gynecologist should be skilled in laparoscopic technique. Raatz et al. [24] suggested that a minimum of 50 LRH cases are needed to acquire adequate laparoscopic skills. Similar to laparotomy radical hysterectomy, postoperative complications were predominantly related to the urinary tract and affected 22 (9.16%) cases in our study, including ureterovaginal fistula, vesicovaginal fistula, lymphocyst, lymphedema, and bowel obstruction. In our previous report [4], the postoperative complication rate was 40% when bladder dysfunction was included. Functional disorders of the lower urinary tract were the most common long-term complications following radical hysterectomy for cervical cancer. The incidence of postoperative bladder dysfunction has been reported from 16.3% to 76% [25–28]. In this study, we found that 30.8% of patients had voiding bladder dysfunction, and the median time of resumption to normal bladder function was 13 days, which was similar to Ramirez et al.'s result (16 days, ranged from 13 to 29 days) [5]. Ralph et al. [29] revealed that the degree of postoperative voiding dysfunction was associated with the amount of resected vaginal, paravaginal, and parametrial tissues. Nerve-sparing concepts via a laprarotomy or laparoscopic approach have focused on the hypogastric nerve, the pelvic splanchnic nerve, and the distal part (vesical and uterovaginal branches) of the IHP during the dissection of the posterior leaf of the VUL, and have been proposed to reduce postoperative neurologic problems [30,31]. Park et al. [32] reported that their laparoscopic nerve-sparing technique was comparable with laparotomy in terms of early recovery of bladder function. Patients in their study were able to self-void at a mean of 10.3 days (range, 6–29 days) postoperatively. The rate returning to normal voiding function 14 and 21 days post-operatively was 92.0% and 95.2%, respectively. In this study, the median length of hospital stay was 13 days, which was longer than that in other series of LRH (ranged from 1 to 10.3 days). This is due to the fact that we were very conservative with the postoperative follow-up and wanted to ensure a minimum observation period equal to that of laparotomy. Currently, we usually discharge the patients on the day of bladder catheter removal. Oncological adequacy Oncological safety is the key to compare a new surgical technique with the currently gold standard in the management of a malignant disease. Recurrence of cervical cancer treated by LRH usually follows the same patterns as in patients treated with RAH. In a series of 221 cases of FIGO stage Ia2–IIb, with a median follow-up of 35 months, we observed a 17.19% recurrence rate, while it ranged from 12% to 25% for laparotomy [33,34]. The higher proportion of Ib2 and more advanced (30.77%) and positive node (23.53%) cervical cancer patients may explain our higher recurrence rate compared with those LRH studies in the literature (2.8–10%). Spirtos et al. [7] observed a 10.3% recurrence rate and 93.6% 5-year survival rate in 78 cases of stage Ia2–Ib (14 cases of Ib2) with a mean follow-up of 68.3 months. Obermair et al. [9] reported a 7.9% recurrence rate in a series of 39 cases after a median follow-up of 36.5 months. Pomel et al. [8] reported 50 cases of 6% recurrence rate and an estimated disease-free survival of 100% for stage Ia1 and 90.5% for stage Ia2 and Ib1. Puntambekar et al. [10] reported a 2.8% recurrence rate but no deaths in a series of 248 cases with stage Ia2–Ib1 after a median follow-up of 36 months. Pellegrino et al. [15] reported an 11% relapse rate and 95% survival rate in 101 cases of stage Ib1 with tumor size b3 cm after a median follow-up of 30 months. In Chong et al.' s series of 100 cases, after a median follow-up of 66.5 months, 10 patients had a recurrence, 9 of whom died. The 5-year overall survival rate was 96% in the first 50 patients and 90% in the second 366 X. Yan et al. / Gynecologic Oncology 120 (2011) 362–367 50 cases [19]. In this study, we reported an estimated 5-year survival rate of 100% for Ia, 79% for Ib (82% for Ib1, 66%for Ib2), 60% for IIa. Among 221 cases, 196 cases were followed-up to June 2010, while 25 cases were only followed-up to June 2007, which may affect the survival to some extent. As far as the survival rate of early stage of cervical cancer is concerned, lymph node is the only significant independent predictor for overall survival. The 5-year survival rate in Ib1 was 88% with negative lymph nodes and 59% with positive lymph nodes. This is consistent with other laparotomy studies on 5-year survival rate in patients of stage Ib–IIb, which reported a range from 87.3% to 94.7% with negative pelvic lymph nodes, whereas a range from 64% to 68.2% with positive pelvic lymph nodes [35]. Tumor size is recognized as a more important prognostic survival. However, in this study, no significant difference in 5-year survival rate was found in Ib1 patients when the tumor diameter N2 cm and ≤2 cm were compared (76% vs. 89%, P = 0.282). This needs to be warranted by further investigations. Patients with stage Ib2–IIa cervical cancer have rarely been reported in this setting. Chen et al. [36] reported the 5-year metastasis survival rate was 85.4%, which was almost identical to the data of Landoni et al. [33] following open surgery (83.9%). In Hertel et al.'s study, stage II and III patients were included and an overall 5-year survival rate of 83% was reported [37]. Sardi et al. [38] reported a better projected overall survival of 88% for Ib1 and 85% for Ib2. To our surprise, the current series demonstrates that the oncological outcome of LRH in patients of stage Ib2–IIa is worse than ever before. These results suggested that the oncological outcome of laparoscopic radical hysterectomy in advanced stage cases may differ from that of open surgery or concurrent chemoradiotherapy. We suggested that patients later than or equal to Ib2 stage and radiological positive nodes were not considered suitable for laparoscopy. And concomitant CRT may be the best choice for treatment. The US National Cancer Institute advised in 1999 that patients with stage Ib2 and advanced should be treated with CCRT. Laparoscopic radical hysterectomy is increasingly being performed by many gynecologists. The short-term follow-up in this study does not allow us to draw a definitive conclusion on the impact of laparoscopic technique on the outcome. 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