ORIGINAL ARTICLE
Oncologic Outcomes of Single-incision Laparoscopic Surgery Compared With Conventional Laparoscopy for Colon Cancer Jung-A Yun, MD, Seong Hyeon Yun, MD, PhD, Yoon Ah Park, MD, Jung Wook Huh, MD, PhD, Yong Beom Cho, MD, PhD, Hee Cheol Kim, MD, PhD, and Woo Yong Lee, MD, PhD
Objective: The aim of this study is to document perioperative results and mid-term oncologic outcomes of single-incision laparoscopic (SIL) colectomy compared to conventional laparoscopic (CL) colectomy. Background: SIL surgery is an advance in minimally invasive operative techniques and is widely accepted for various types of surgery. Methods: We prospectively collected data from 767 patients who underwent radical colectomy (250 SIL colectomy and 517 CL colectomy) between 2010 and 2011 due to primary colon cancer and retrospectively analyzed these patients with propensity score matching. Results: Before matching, patients with CL surgery had a significantly higher percentage of comorbidities (49.2% vs 57.8%, P ¼ 0.024). Tumor location significantly differed between 2 groups: SIL surgery was performed more frequently in patients with right colon cancer. After propensity score matching, each group included 239 patients, and there was no difference between the SIL and CL surgery groups. Estimated blood loss was more in the patients with SIL colectomy, but the rate itself of intraoperative complications was not statistically different (P ¼ 0.662). The median follow-up period was 37 months. There were 20 recurrences in the SIL surgery group (8.4%), including 3 locoregional recurrences and 18 (7.5%) in the CL surgery group. Diseasefree survival at 48 months did not differ significantly between the SIL and CL surgery groups (89.8% vs 89.9%, P ¼ 0.548). Conclusions: SIL colectomy for colon cancer shows probably higher, but an acceptable complication rate and can provide resection and oncologic outcomes equal to those of CL colectomy. Keywords: colon cancer, oncologic outcome, single-incision laparoscopy
(Ann Surg 2016;263:973–978)
T
he standard treatment modality for colon cancer is radical surgery, which results in removal of the primary tumor and regional lymphatic tissue, ensuring adequate resection margins. Traditionally, colon cancer treatment required open surgery with a long skin incision and an extended hospitalization period. The laparoscopic approach, which caused less trauma to patients, emerged in the early 1990s.1 The first laparoscopic colectomy was reported in 1991 by Jacobs et al.2 Laparoscopic colectomy currently is accepted as the standard operative technique for colon cancer. Furthermore, laparoscopic colectomy has distinct advantages including shorter hospital stays, a reduction in postoperative pain, and more rapid recovery with comparable perioperative morbidity.3– 7 Several prospective randomized trials comparing a laparoscopic procedure with open colectomy have reported equivalent or even better oncologic outcomes.7,8 From the Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea. Disclosure: The authors have no conflicts of interest or financial ties to disclose. Reprints: Seong Hyeon Yun, MD, PhD, Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81, Irwon-ro, Gangnam-gu, Seoul 135-710, Korea. E-mail: [email protected]. Copyright ß 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0003-4932/14/26105-0821 DOI: 10.1097/SLA.0000000000001226
Annals of Surgery Volume 263, Number 5, May 2016
Single-incision laparoscopic (SIL) surgery is an advance in minimally invasive operative techniques and is widely accepted not only in colorectal surgery but also in urologic, gynecologic, and biliary surgery.9– 12 In some studies, SIL surgery showed equivalent operative and perioperative outcomes compared with conventional multiport laparoscopic surgery.13,14 Because SIL colectomy has only been performed recently, there is no follow-up data that addresses long-term oncologic outcomes. We have already reported equivalent oncologic outcomes of SIL right colectomy compared with CL right colectomy.14 However, the study contained a small number of patients and had a relatively short-term follow-up period of about 20 months. SIL colectomy is now considered a feasible operation in Samsung Medical Center, especially for patients with early colon cancer, and consists of about half of all laparoscopic procedures. The number of patients is steeply increasing, occupying approximately 30% among total operations performed in our institution. Concern about recurrences after SIL surgery is also increasing. Therefore, the major aim of this study is to document perioperative results and mid-term oncologic outcomes of SIL colectomy compared to CL colectomy. In addition, we analyzed the prognostic factors affecting disease-free and overall survivals in patients with colon cancer.
MATERIALS AND METHODS Patient Selection and Data Collection We retrospectively analyzed data from 811 patients who underwent laparoscopic colectomy due to nonhereditary primary colon cancer at Samsung Medical Center (Sungkyunkwan University School of Medicine) in Korea between 2010 and 2011. We included 767 patients but excluded 44 patients with metastatic disease. All operations were performed by 1 of 5 board-certified colorectal surgeons, and perioperative management including discharge criteria was similar for the SIL and CL surgery groups. All patients underwent elective surgery, received bowel preparation [2 bottles of 250 ml of magnesium citrate (Magcorol)] the day before the operation and received prophylactic antibiotics before the skin incision. The patients who underwent operations were permitted to drink water on postoperative day 1 and eat a soft diet on postoperative day 2, on the basis of their tolerance levels. Patients were discharged after they advanced to a regular diet and their surgical wounds no longer impaired daily activities. The patients were usually discharged after postoperative days 5 to 7. The institutional review board at Samsung Medical Center approved this study. Comprehensive chart reviews were performed to obtain clinicopathologic information, and follow-up data were obtained from medical records and the National Bureau of Statistics. Any postoperative event lengthening hospitalization by 3 or more days beyond the average duration of hospital stay was considered to be a postoperative complication. www.annalsofsurgery.com | 973
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Surgery Volume 263, Number 5, May 2016
Yun et al
Surgical Techniques The oncologic principles of surgery are the same in SIL and CL colectomy. All procedures were performed according to the 2001 National Cancer Institute (NCI) guidelines.15 In SIL surgery, all procedures including specimen retrieval were performed through just 1 transumbilical handmade glove port with a commercially available wound retractor using 3 laparoscopic instruments (two 12-mm and one 5-mm diameter trocar). The handmade glove port provided a wider range of motion for the trocars. CL surgery was performed using a 4 or 5 multiport including a 12-mm trocar for the camera in the periumbilical area. The lithotomy position was used according to the preference of the surgeon. Specimen retrieval was performed by extension of the incision in the periumbilical or left lower quadrant trocar site. Depending on the surgeon, a discrepancy in strategy exists between the medial-to-lateral and inferolateral-to-medial approaches in right colectomy. However, inferolateral-to-medial approaches were preferred in SIL right colectomy because of the lack of surgical assistant trocars to provide counter-traction. If the right colon was fully mobilized, the traction suture for counter-traction was more helpful. For left colectomy and anterior resection, division of inferior mesenteric and left colic vessels was performed preferentially. The wound was closed mainly with interrupted suture using absorbable monofilament.
Matching SIL right colectomy for right colon cancer was mainly performed in the initial period, and the distribution of the location of the main tumor was significantly different between SIL and CL colectomies. To minimize the difference, 1:1 propensity score matching was performed by using bivariate logistic regression. Comorbidities
and tumor location were selected as covariates in the regression model. They were chosen because they significantly differed between SIL and CL colectomy in basic characteristics of the overall cohort and may have influenced the surgeons’ decision making with respect to the choice of SIL versus CL surgery.
Statistical Analysis In all patients, disease-free survival was defined as the interval between the date of surgery and the date of the first detection of recurrence or the date of the last known follow-up without evidence of recurrence. Overall survival time was censored at the time of the last visit for regular follow-ups. Statistical analyses between the 2 groups were performed using t, x2, or Fisher exact tests. Regression analysis was performed using the Cox proportional hazard regression model in both univariate and multivariate analyses. Survival rates were estimated using the Kaplan-Meier method and compared using the log-rank test. Statistical results were considered significant if P < 0.05. Statistical analysis was performed using SPSS version 18.0 software (SPSS Inc, Chicago, IL).
RESULTS Basic Characteristics Between SIL and CL Surgery Groups Before and After Matching The total cohort included 250 patients who underwent SIL colectomy and 517 who underwent CL colectomy. Patients with CL surgery had a significantly higher rate of comorbidities (49.2% vs 57.8%, P ¼ 0.024). Tumor location significantly differed between the 2 groups; SIL surgery was performed more frequently in patients with right colon cancer. Other clinical parameters were not
TABLE 1. Baseline Clinical Characteristics Total Cohort SIL Surgery (n ¼ 250) Age, median (range), yrs Sex, n (%) Female Male BMI, median (range), kg/m2 Comorbidities, n (%) Preoperative CEA, median (range), ng/mL ASA score, n (%) 1 2–4 Previous abdominal surgery, n (%) Tumor location Cecum Ascending colon Hepatic flexure colon Transverse colon Splenic flexure colon Descending colon Sigmoid colon Tumor size, median (range), cm Operation type Right colectomy Transverse colectomy Left colectomy Anterior resection Low anterior resection Subtotal colectomy
60 (21–88) 112 138 23.76 123 1.84
(44.8) (55.2) (16.97–32.37) (49.2) (0.5–180.59)
Matched Cohort
CL Surgery (n ¼ 517)
P
59 (26–86) 212 305 23.88 299 2.05
0.285 0.319
(41.0) (59.0) (15.32–36.33) (57.8) (0.5–188.11)
105 (42.0) 145 (58.0) 64 (25.6)
206 (39.8) 311 (60.2) 140 (27.1)
22 98 28 21 2 12 67 3.5
(8.8) (39.2) (11.2) (8.4) (0.8) (4.8) (26.8) (0.1–11.5)
17 86 34 21 6 32 321 4.0
(3.3) (16.6) (6.6) (4.1) (1.2) (6.2) (62.1) (0.1–12.0)
160 1 18 68 2 1
(64.0) (0.4) (7.2) (27.2) (0.8) (0.4)
150 4 30 311 22 0
(29.0) (0.8) (5.8) (60.2) (4.3) (0.0)
0.881 0.024 0.415 0.569 0.664
Oncologic Outcomes of Single-incision Laparoscopic Surgery Compared With Conventional Laparoscopy for Colon Cancer Jung-A Yun, MD, Seong Hyeon Yun, MD, PhD, Yoon Ah Park, MD, Jung Wook Huh, MD, PhD, Yong Beom Cho, MD, PhD, Hee Cheol Kim, MD, PhD, and Woo Yong Lee, MD, PhD
Objective: The aim of this study is to document perioperative results and mid-term oncologic outcomes of single-incision laparoscopic (SIL) colectomy compared to conventional laparoscopic (CL) colectomy. Background: SIL surgery is an advance in minimally invasive operative techniques and is widely accepted for various types of surgery. Methods: We prospectively collected data from 767 patients who underwent radical colectomy (250 SIL colectomy and 517 CL colectomy) between 2010 and 2011 due to primary colon cancer and retrospectively analyzed these patients with propensity score matching. Results: Before matching, patients with CL surgery had a significantly higher percentage of comorbidities (49.2% vs 57.8%, P ¼ 0.024). Tumor location significantly differed between 2 groups: SIL surgery was performed more frequently in patients with right colon cancer. After propensity score matching, each group included 239 patients, and there was no difference between the SIL and CL surgery groups. Estimated blood loss was more in the patients with SIL colectomy, but the rate itself of intraoperative complications was not statistically different (P ¼ 0.662). The median follow-up period was 37 months. There were 20 recurrences in the SIL surgery group (8.4%), including 3 locoregional recurrences and 18 (7.5%) in the CL surgery group. Diseasefree survival at 48 months did not differ significantly between the SIL and CL surgery groups (89.8% vs 89.9%, P ¼ 0.548). Conclusions: SIL colectomy for colon cancer shows probably higher, but an acceptable complication rate and can provide resection and oncologic outcomes equal to those of CL colectomy. Keywords: colon cancer, oncologic outcome, single-incision laparoscopy
(Ann Surg 2016;263:973–978)
T
he standard treatment modality for colon cancer is radical surgery, which results in removal of the primary tumor and regional lymphatic tissue, ensuring adequate resection margins. Traditionally, colon cancer treatment required open surgery with a long skin incision and an extended hospitalization period. The laparoscopic approach, which caused less trauma to patients, emerged in the early 1990s.1 The first laparoscopic colectomy was reported in 1991 by Jacobs et al.2 Laparoscopic colectomy currently is accepted as the standard operative technique for colon cancer. Furthermore, laparoscopic colectomy has distinct advantages including shorter hospital stays, a reduction in postoperative pain, and more rapid recovery with comparable perioperative morbidity.3– 7 Several prospective randomized trials comparing a laparoscopic procedure with open colectomy have reported equivalent or even better oncologic outcomes.7,8 From the Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea. Disclosure: The authors have no conflicts of interest or financial ties to disclose. Reprints: Seong Hyeon Yun, MD, PhD, Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81, Irwon-ro, Gangnam-gu, Seoul 135-710, Korea. E-mail: [email protected]. Copyright ß 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0003-4932/14/26105-0821 DOI: 10.1097/SLA.0000000000001226
Annals of Surgery Volume 263, Number 5, May 2016
Single-incision laparoscopic (SIL) surgery is an advance in minimally invasive operative techniques and is widely accepted not only in colorectal surgery but also in urologic, gynecologic, and biliary surgery.9– 12 In some studies, SIL surgery showed equivalent operative and perioperative outcomes compared with conventional multiport laparoscopic surgery.13,14 Because SIL colectomy has only been performed recently, there is no follow-up data that addresses long-term oncologic outcomes. We have already reported equivalent oncologic outcomes of SIL right colectomy compared with CL right colectomy.14 However, the study contained a small number of patients and had a relatively short-term follow-up period of about 20 months. SIL colectomy is now considered a feasible operation in Samsung Medical Center, especially for patients with early colon cancer, and consists of about half of all laparoscopic procedures. The number of patients is steeply increasing, occupying approximately 30% among total operations performed in our institution. Concern about recurrences after SIL surgery is also increasing. Therefore, the major aim of this study is to document perioperative results and mid-term oncologic outcomes of SIL colectomy compared to CL colectomy. In addition, we analyzed the prognostic factors affecting disease-free and overall survivals in patients with colon cancer.
MATERIALS AND METHODS Patient Selection and Data Collection We retrospectively analyzed data from 811 patients who underwent laparoscopic colectomy due to nonhereditary primary colon cancer at Samsung Medical Center (Sungkyunkwan University School of Medicine) in Korea between 2010 and 2011. We included 767 patients but excluded 44 patients with metastatic disease. All operations were performed by 1 of 5 board-certified colorectal surgeons, and perioperative management including discharge criteria was similar for the SIL and CL surgery groups. All patients underwent elective surgery, received bowel preparation [2 bottles of 250 ml of magnesium citrate (Magcorol)] the day before the operation and received prophylactic antibiotics before the skin incision. The patients who underwent operations were permitted to drink water on postoperative day 1 and eat a soft diet on postoperative day 2, on the basis of their tolerance levels. Patients were discharged after they advanced to a regular diet and their surgical wounds no longer impaired daily activities. The patients were usually discharged after postoperative days 5 to 7. The institutional review board at Samsung Medical Center approved this study. Comprehensive chart reviews were performed to obtain clinicopathologic information, and follow-up data were obtained from medical records and the National Bureau of Statistics. Any postoperative event lengthening hospitalization by 3 or more days beyond the average duration of hospital stay was considered to be a postoperative complication. www.annalsofsurgery.com | 973
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Surgery Volume 263, Number 5, May 2016
Yun et al
Surgical Techniques The oncologic principles of surgery are the same in SIL and CL colectomy. All procedures were performed according to the 2001 National Cancer Institute (NCI) guidelines.15 In SIL surgery, all procedures including specimen retrieval were performed through just 1 transumbilical handmade glove port with a commercially available wound retractor using 3 laparoscopic instruments (two 12-mm and one 5-mm diameter trocar). The handmade glove port provided a wider range of motion for the trocars. CL surgery was performed using a 4 or 5 multiport including a 12-mm trocar for the camera in the periumbilical area. The lithotomy position was used according to the preference of the surgeon. Specimen retrieval was performed by extension of the incision in the periumbilical or left lower quadrant trocar site. Depending on the surgeon, a discrepancy in strategy exists between the medial-to-lateral and inferolateral-to-medial approaches in right colectomy. However, inferolateral-to-medial approaches were preferred in SIL right colectomy because of the lack of surgical assistant trocars to provide counter-traction. If the right colon was fully mobilized, the traction suture for counter-traction was more helpful. For left colectomy and anterior resection, division of inferior mesenteric and left colic vessels was performed preferentially. The wound was closed mainly with interrupted suture using absorbable monofilament.
Matching SIL right colectomy for right colon cancer was mainly performed in the initial period, and the distribution of the location of the main tumor was significantly different between SIL and CL colectomies. To minimize the difference, 1:1 propensity score matching was performed by using bivariate logistic regression. Comorbidities
and tumor location were selected as covariates in the regression model. They were chosen because they significantly differed between SIL and CL colectomy in basic characteristics of the overall cohort and may have influenced the surgeons’ decision making with respect to the choice of SIL versus CL surgery.
Statistical Analysis In all patients, disease-free survival was defined as the interval between the date of surgery and the date of the first detection of recurrence or the date of the last known follow-up without evidence of recurrence. Overall survival time was censored at the time of the last visit for regular follow-ups. Statistical analyses between the 2 groups were performed using t, x2, or Fisher exact tests. Regression analysis was performed using the Cox proportional hazard regression model in both univariate and multivariate analyses. Survival rates were estimated using the Kaplan-Meier method and compared using the log-rank test. Statistical results were considered significant if P < 0.05. Statistical analysis was performed using SPSS version 18.0 software (SPSS Inc, Chicago, IL).
RESULTS Basic Characteristics Between SIL and CL Surgery Groups Before and After Matching The total cohort included 250 patients who underwent SIL colectomy and 517 who underwent CL colectomy. Patients with CL surgery had a significantly higher rate of comorbidities (49.2% vs 57.8%, P ¼ 0.024). Tumor location significantly differed between the 2 groups; SIL surgery was performed more frequently in patients with right colon cancer. Other clinical parameters were not
TABLE 1. Baseline Clinical Characteristics Total Cohort SIL Surgery (n ¼ 250) Age, median (range), yrs Sex, n (%) Female Male BMI, median (range), kg/m2 Comorbidities, n (%) Preoperative CEA, median (range), ng/mL ASA score, n (%) 1 2–4 Previous abdominal surgery, n (%) Tumor location Cecum Ascending colon Hepatic flexure colon Transverse colon Splenic flexure colon Descending colon Sigmoid colon Tumor size, median (range), cm Operation type Right colectomy Transverse colectomy Left colectomy Anterior resection Low anterior resection Subtotal colectomy
60 (21–88) 112 138 23.76 123 1.84
(44.8) (55.2) (16.97–32.37) (49.2) (0.5–180.59)
Matched Cohort
CL Surgery (n ¼ 517)
P
59 (26–86) 212 305 23.88 299 2.05
0.285 0.319
(41.0) (59.0) (15.32–36.33) (57.8) (0.5–188.11)
105 (42.0) 145 (58.0) 64 (25.6)
206 (39.8) 311 (60.2) 140 (27.1)
22 98 28 21 2 12 67 3.5
(8.8) (39.2) (11.2) (8.4) (0.8) (4.8) (26.8) (0.1–11.5)
17 86 34 21 6 32 321 4.0
(3.3) (16.6) (6.6) (4.1) (1.2) (6.2) (62.1) (0.1–12.0)
160 1 18 68 2 1
(64.0) (0.4) (7.2) (27.2) (0.8) (0.4)
150 4 30 311 22 0
(29.0) (0.8) (5.8) (60.2) (4.3) (0.0)
0.881 0.024 0.415 0.569 0.664
