Objective
We sought to compare surgical and survival outcomes of laparoscopic radical hysterectomy (LRH) vs open radical hysterectomy (ORH) in elderly patients with early-stage cervical cancer.
Study Design
A retrospective analysis was performed on elderly patients (≥65 years) who underwent either LRH (n = 99) or ORH (n = 159) due to stage IA2-IIA2 cervical cancer.
Results
One patient (1%) in LRH group required conversion to laparotomy. Operating time ( P = .035), estimated blood loss ( P = .002), recovery of bowel movement ( P < .001), and postoperative hospital stay ( P < .001) were significantly shorter or lower in LRH group. Postoperative complications were significantly less frequent in LRH group ( P = .026). After the median follow-up time of 45 months, the 5-year disease-free survival (95% vs 93%, P = .350) and overall survival (96% vs 95%, P = .361) did not differ between LRH and ORH groups.
Conclusion
Elderly patients tolerated well both LRH and ORH. LRH was associated with better surgical outcomes compared to ORH without increasing intraoperative complications or decreasing survival.
Cervical cancer is the third most commonly diagnosed cancer and the fourth leading cause of cancer death in women worldwide. In South Korea, it is the sixth most common female cancer and the seventh leading cause of female cancer death.
The age of the peak incidence for cervical cancer is bimodal. The first age peak is between 30-39 years and the second is between 60-64 years. The world population is rapidly aging as life expectancies rise. The aging trend in South Korea is particularly striking as the elderly ≥65 years of age are predicted to account for 14% of Korea’s total population by 2018. In the United States, the number of elderly >65 years of age will be 19% of the population by 2030. Therefore, the incidence of elderly patients with cervical cancer will be increasing. And as the number of elderly patients with cancer increases, the optimal treatment for these patients becomes an important issue that must be solved.
Elderly patients with early-stage cervical cancer are less likely to undergo radical hysterectomy (RH), although the preferred standard management for early-stage cervical cancer is RH. Since 1988, only 2 retrospective studies dealing with the outcomes of RH for elderly patients with early-stage cervical cancer have been reported in the literature. Therefore, the outcomes after RH in elderly patients should be further evaluated. In addition, the outcomes of laparoscopic RH (LRH) in elderly patients with early-stage cervical cancer have never been reported in the medical literature, although LRH is now regarded as a reasonable alternative to open RH (ORH) because LRH is associated with less blood loss, earlier return of bowel movement, and a shorter hospital stay without increasing perioperative complications and without decreasing the survival rate of patients with early-stage cervical cancer. The purpose of this study is to compare the surgical and survival outcomes in elderly patients (≥65 years) with early-stage cervical cancer who underwent either LRH or ORH.
Materials and Methods
We performed a retrospective review of the medical records of elderly patients ≥65 years of age with International Federation of Obstetrics and Gynecology (FIGO) stage IA2-IIA2 cervical cancer who had undergone LRH or ORH at Asan Medical Center (AMC) Seoul, Korea, from 1999 through 2011; we received the approval of the Institutional Review Board of AMC to perform this study.
RH is recommended to all consecutive patients with early-stage cervical cancer (FIGO stage IA2-IIA) at AMC unless they refuse the procedure, have a poor performance status, or have uncontrolled severe medical disease. LRH was performed as described in our previous report. The surgical procedures and the extent of resection for ORH was the same as LRH except for the use of a generous midline abdominal incision from the pubic symphysis to the supraumbilical area. It is our policy to complete LRH or ORH if we encounter lymph node metastasis or parametrial invasion during surgery, although it is not yet clear whether the surgeon should complete RH or discontinue the procedure and administer concurrent chemoradiation therapy (CCRT). After surgery, patients with intermediate risk factors, eg, lymphovascular space invasion, large tumor, and deep cervical stromal invasion, were recommended to receive adjuvant radiation therapy in accordance with Gynecologic Oncology Group 92 criteria, and patients with ≥1 high risk factors, eg, resection margin involvement, parametrial invasion, or lymph node metastasis, were recommended to receive adjuvant CCRT. Some patients received adjuvant chemotherapy after discussing their options with their physician. After the completion of treatment, patients were followed up every 3 months for the first 2 years, every 6 months during the next 3 years, and yearly thereafter.
A postoperative complication was defined as any documented, adverse event occurring within 60 days after surgery. The Foley catheter was usually removed at 7 days after surgery. Bladder dysfunction was defined as voiding difficulty requiring reinsertion of a Foley catheter or clean intermittent catheterization. The return of bowel movement was defined as flatus passing and a return bowel sound. This was regarded as the return of bowel function. At this time point, meals were again served to the patients. Postoperative mortality was defined as death from any cause within 30 days after surgery. Following the use of the Kolmogorov-Smirnov test to determine whether the data showed a normal or nonnormal distribution, the mean or median values of the 2 groups were compared using the Student t test or the Mann-Whitney U test. Frequency distributions were compared using the χ 2 test or Fisher exact test. Disease-free survival (DFS) was defined as the time in months from the date of surgery to the date of relapse or censoring. Overall survival (OS) was defined as the time in months from the date of surgery to the date of death, last follow-up, or censoring. DFS and OS were estimated using the Kaplan–Meier method, and patient groups were compared using the log rank test and Cox proportional hazards model. All variables showing statistical significance by univariate analyses were included in a multivariate analysis involving the Cox proportional hazards model. P values < .05 in 2-sided tests were regarded as significant. All statistical analyses were performed using SPSS for Windows (version 11.0; IBM Corp, Armonk, NY).
Results
During the study period, 265 elderly patients (age ≥65 years) with a FIGO stage IA2-IIA2 cervical cancer were treated and followed up at AMC. Of these cases, 7 patients received CCRT (n = 5) or radiation therapy (n = 2) and 258 patients underwent RH. As a result, 99 and 159 elderly patients (age ≥65 years) underwent LRH or ORH, respectively. One patient (1%) in the LRH group required conversion to laparotomy due to rectal injury occurring during surgery. All patients underwent Piver-Rutledge type III hysterectomy with pelvic lymph node dissection. Paraaortic lymph node sampling was performed in 24 patients (24.2%) in the LRH group and in 107 patients (67.3%) in the ORH group ( P < .001).
Table 1 shows the characteristics of the study patients. There was no difference in age, body mass index, medical disease, previous abdominal surgery, preoperative squamous cell carcinoma antigen level, tumor histology, tumor grade, tumor size, lymphovascular space invasion, parametrial invasion, or lymph node metastasis between the LRH and the ORH group. However, more patients in LRH group had parity >2 ( P = .041) and deep cervical stromal invasion (>1/2) ( P = .039). More patients in ORH group had preoperative squamous cell carcinoma antigen level >3.2 ng/mL ( P = .002) and FIGO stage II disease ( P = .028). After surgery, 30 patients (30.4%) in the LRH group and 61 patients (38.4%) in the ORH group received adjuvant therapy ( P = .188). Seven (7.1%), 8 (8.1%), and 15 (15.2%) patients in the LRH group received chemotherapy, radiation therapy, and CCRT, respectively, as adjuvant therapy, and 20 (12.6%), 21 (13.2%), and 20 (12.6%) patients in the ORH group received chemotherapy, radiation therapy, and CCRT, respectively, as adjuvant therapy. There was no difference in the pattern of adjuvant therapy between the LRH and the ORH group patients ( P = .509). The adjuvant chemotherapy regimen was paclitaxel/cisplatin in 8 patients and paclitaxel/carboplatin in 13 patients. The chemotherapeutic regimen for CCRT was weekly cisplatin in 35 patients and paclitaxel/cisplatin or carboplatin in 6 patients.
| Characteristics | LRH (n = 99) | ORH (n = 159) | P value |
|---|---|---|---|
| Age, y | |||
| Mean (range) | 69.4 (65–78) | 70.0 (65–86) | .205 |
| 65-70, n (%) | 64 (64.6) | 97 (61) | .968 |
| 71-75, n (%) | 26 (26.3) | 52 (32.7) | |
| 76-80, n (%) | 9 (9.1) | 8 (5) | |
| >80, n (%) | 0 (0) | 2 (1.3) | |
| Body mass index, kg/m 2 | |||
| Mean (range) | 24.13 (17.8–29.4) | 24.69 (13.67–35.11) | .146 |
| <20, n (%) | 6 (6.1) | 15 (9.4) | .048 |
| 20-24.99, n (%) | 56 (56.6) | 77 (48.4) | |
| 25-29.99, n (%) | 37 (37.4) | 57 (35.8) | |
| ≥30, n (%) | 0 (0) | 10 (6.3) | |
| Parity, n (%) | |||
| ≤2 | 18 (18.2) | 47 (29.6) | .041 |
| >2 | 81 (81.8) | 112 (70.4) | |
| Medical disease, a n (%) | |||
| No | 56 (56.6) | 88 (55.3) | .848 |
| Yes | 43 (43.4) | 71 (44.7) | |
| Previous abdominal surgery, n (%) | |||
| No | 82 (82.8) | 132 (83) | .968 |
| Yes | 17 (17.2) | 27 (17) | |
| Preoperative SCC Ag level, ng/mL | |||
| Mean (range) | 1.56 (0–12.80) | 4.17 (0–123) | .309 b |
| ≤3.2, c n (%) | 93 (93.9) | 127 (79.9) | .002 |
| >3.2, c n (%) | 6 (6.1) | 32 (20.1) | |
| FIGO stage, n (%) | |||
| IA2 | 10 (10.1) | 5 (3.1) | .028 |
| IB1 | 74 (74.7) | 123 (77.4) | |
| IB2 | 8 (8.1) | 6 (3.8) | |
| IIA1 | 5 (5.1) | 18 (11.3) | |
| IIA2 | 2 (2) | 7 (4.4) | |
| Histology of tumor, n (%) | |||
| Squamous | 92 (92.9) | 145 (91.2) | .620 |
| Adenocarcinoma or adenosquamous | 7 (7.1) | 14 (8.8) | |
| Grade of tumor, n (%) | |||
| 1 | 9 (9.1) | 9 (5.7) | .251 |
| 2 | 49 (49.5) | 77 (48.4) | |
| 3 | 15 (15.2) | 16 (10.1) | |
| Not reported | 26 (26.3) | 57 (35.8) | |
| Tumor size, cm | |||
| Mean (range) | 2.5 (0.3–7) | 2.7 (0.3–11) | .170 b |
| ≤4, n (%) | 93 (93.9) | 144 (90.6) | .335 |
| >4, n (%) | 6 (6.1) | 15 (9.4) | |
| Depth of stromal invasion, n (%) | |||
| ≤1/2 | 35 (35.4) | 77 (48.4) | .039 |
| >1/2 | 64 (64.6) | 82 (51.6) | |
| Lymphovascular space invasion, n (%) | |||
| No | 85 (85.9) | 128 (80.5) | .270 |
| Yes | 14 (14.1) | 31 (19.5) | |
| Parametrial invasion, n (%) | |||
| No | 81 (81.8) | 129 (81.1) | .890 |
| Yes | 18 (18.2) | 30 (18.9) | |
| Lymph node metastasis, n (%) | |||
| No | 87 (87.9) | 139 (87.4) | .914 |
| Yes | 12 (12.1) | 20 (12.6) | |
| Adjuvant therapy, n (%) | |||
| No | 69 (69.7) | 98 (61.6) | .509 |
| Chemotherapy | 7 (7.1) | 14 (8.8) | |
| RT | 8 (8.1) | 21 (13.2) | |
| CCRT | 15 (15.2) | 26 (16.4) |
a Including diabetes mellitus, hypertension, arrhythmia, valvular heart disease, cerebrovascular accident, asthma, and hyperthyroidism;
Table 2 lists the surgical outcomes of the study patients. Preoperative and postoperative hemoglobin level, perioperative hemoglobin level change, transfusion requirement, and transfusion amount did not differ between the LRH and the ORH groups. However, operating time (253.8 vs 271.9 minutes, P = .035) was significantly shorter, estimated blood loss (375 mL vs 553 mL, P = .014) was significantly lower, and the time interval to return of bowel movement (2.3 vs 2.9 days, P = .005) and the length of the postoperative hospital stay (9.8 vs 20 days, P < .001) were significantly shorter in the LRH group. There was no difference in the number of total, pelvic, and paraaortic lymph nodes retrieved between LRH and ORH groups.
| Variable | LRH (n = 99) | ORH (n = 159) | P value |
|---|---|---|---|
| Operating time, min | 253.8 (145–423) | 271.9 (115–480) | .035 |
| Estimated blood loss, mL | 433.6 (130–1500) | 605.2 (120–2800) | < .001 a |
| Preoperative hemoglobin level, g/dL | 12.4 (8.6–14.4) | 12.2 (8.5–15) | .128 |
| Postoperative hemoglobin level, g/dL | 10.2 (7–13.8) | 10.3 (6–14.3) | .645 |
| Perioperative hemoglobin level, g/dL | 2.4 (–3.8 to 5.1) | 2.1 (–2.8 to 6.3) | .148 |
| Transfusion, n (%) | 39 (39.8) | 54 (34.6) | .404 |
| Transfusion amount, pt | 3.2 (1–16) | 3.4 (1–14) | .653 |
| Time interval to return of bowel movement, d | 2.2 (1–5) | 2.9 (1–8) | < .001 a |
| Postoperative hospital stay, d | 10.6 (4–33) | 16.8 (3–61) | < .001 a |
| No. of total lymph nodes retrieved, n | 30.5 (12–63) | 31.4 (3–61) | .504 |
| No. of pelvic lymph nodes retrieved, n | 29.8 (12–56) | 29.4 (1–12) | .730 |
| No. of paraaortic lymph nodes retrieved, n | 3.2 (1–10) | 3.0 (3–61) | .817 |
Table 3 shows the patients’ perioperative complications. Intraoperative complications occurred in 4 patients (4%) in the LRH group and in 3 patients (1.9%) in the ORH group ( P = .651). Postoperative complications occurred in 4 patients (4.2%) in LRH group and 20 patients (12.6%) in ORH group, respectively ( P = .026). Bladder dysfunction was documented in 17 LRH group patients (17.3%) and in 31 ORH group patients (19.5%), respectively ( P = .668). No one required reoperation due to postoperative complications, and there was no postoperative mortality.
| Variable | LRH (n = 99) | ORH (n = 159) | P value |
|---|---|---|---|
| Intraoperative complications | 4 (4) | 3 (1.9) | .300 |
| Vessel injury | 1 (1) | 2 (1.3) | .560 |
| Bowel injury | 1 (1) a | 0 (0) | 1.000 |
| Bladder injury | 2 (2) | 0 (0) | .525 |
| Ureter injury | 0 (0) | 1 (0.6) | .384 |
| Postoperative complications | 4 (4) | 20 (12.6) | .026 |
| Wound dehiscence | 1 (1) | 6 (3.8) | .014 |
| Incisional hernia | 1 (1) | 3 (1.9) | .159 |
| Ileus | 1 (1) | 4 (2.5) | .073 |
| Pelvic abscess | 0 (0) | 3 (1.9) | .055 |
| Ureteral stricture | 1 (1) | 4 (2.5) | .073 |
| Urinary fistula | 0 (0) | 1 (0.6) | .384 |
| Deep vein thrombosis | 1 (1) | 3 (1.9) | .159 |
| Pulmonary thromboembolism | 0 (0) | 1 (0.6) | .384 |
| Lumbosacral radiculopathy | 1 (1) | 0 (0) | 1.000 |
| Bladder dysfunction | 17 (17.3) | 31 (19.5) | .668 |
After the mean and median follow-up times of 54 and 45 months (range, 3-152 months), respectively, 3 patients (3%) in the LRH group and 9 patients (5.7%) in the ORH group had recurrence ( P = .381), and 2 patients (2%) in the LRH group and 7 patients (4.4%) in the ORH group died of their disease ( P = .489). The 5-year DFS was 95% for the LRH group and 93% for the ORH group ( P = .350), and the 5-year OS was 96% for the LRH group and 95% for the ORH group ( P = .361) ( Figure ). There was no difference in the follow-up time between the LRH and the ORH groups (mean, 49 vs 57 months; median, 44 vs 48 months; P = .100). On univariate analysis, FIGO stage II, large tumor size, lymphovascular space invasion, parametrial invasion, lymph node metastasis, and requirement of adjuvant therapy were associated with a significantly lower DFS ( Table 4 ). After adjusting for prognostic factors that were significant for DFS (FIGO stage II, large tumor size, lymphovascular space invasion, parametrial invasion, lymph node metastasis, and requirement of adjuvant therapy) in univariate analysis, the risk of recurrence was not different between LRH and ORH groups (odds ratio [OR], 1.69; 95% confidence interval [CI], 0.39–7.19; P = .476) ( Table 4 ). Large tumor size was the only significant factor for DFS in multivariate analysis (OR, 5.39; 95% CI, 1.19–24.52; P = .029) ( Table 4 ).
| Variables | Univariate analysis | Multivariate analysis | ||
|---|---|---|---|---|
| OR (95% CI) | P value | OR (95% CI) | P value | |
| Age (as a continuous variable) | 0.98 (0.83–1.16) | .825 | — | — |
| Parity (≤2 vs >2) | 0.69 (0.21–2.29) | .542 | — | — |
| Body mass index (≤24.5 vs >24.5 kg/m 2 ) a | 0.57 (0.17–1.89) | .358 | — | — |
| Medical disease | 0.64 (0.19–2.13) | .470 | — | — |
| Preoperative SCC Ag (≤3.2 vs >3.2 ng/mL) a | 0.72 (0.82–9.04) | .103 | — | — |
| FIGO stage (stage I vs II) | 6.03 (1.91–19.03) | .002 | 2.44 (0.59–9.96) | .214 |
| Histology (squamous vs adenocarcinoma or adenosquamous) | 0.96 (0.12–7.40) | .965 | — | — |
| Tumor size (≤4 vs >4 cm) | 12.45 (3.87–40.02) | < .001 | 5.39 (1.19–24.52) | .029 |
| Depth of stromal invasion (≤1/2 vs >1/2) | 2.74 (0.74–10.17) | .131 | — | — |
| Lymphovascular space invasion | 5.58 (1.79–17.35) | .003 | 3.30 (0.66–16.54) | .146 |
| Parametrial invasion | 10.92 (3.27–36.46) | < .001 | 3.73 (0.76–18.35) | .106 |
| Lymph node metastasis | 5.08 (1.61–16.01) | .006 | 1.11 (0.22–5.67) | .902 |
| Adjuvant therapy (not required vs required) | 4.20 (1.26–14.03) | .020 | 0.69 (0.13–3.56) | .659 |
| Surgery group (LRH vs ORH) | 1.87 (0.51–6.90) | .350 | 1.69 (0.39–7.19) | .476 |
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