Retrospective Study
Copyright ©The Author(s) 2018. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Jan 7, 2018; 24(1): 76-86
Published online Jan 7, 2018. doi: 10.3748/wjg.v24.i1.76
Short- and long-term outcomes following laparoscopic vs open surgery for pathological T4 colorectal cancer: 10 years of experience in a single center
Zi-Feng Yang, De-Qing Wu, Jun-Jiang Wang, Ze-Jian Lv, Yong Li
Zi-Feng Yang, De-Qing Wu, Jun-Jiang Wang, Ze-Jian Lv, Yong Li, Department of General Surgery, Guangdong General Hospital, Guangdong Academy of Medical Sciences, Guangzhou 510080, Guangdong Province, China
ORCID number: Zi-Feng Yang (0000-0001-9523-603X); De-Qing Wu (0000-0001-6972-3192); Jun-Jiang Wang (0000-0002-2682-2104); Ze-Jian Lv (0000-0003-1119-4544); Yong Li (0000-0002-2643-4697).
Author contributions: Yang ZF and Wu DQ contributed equally to this work and designed the research; Wang JJ and Lv ZJ acquired the data; Yang ZF and Wu DQ analyzed and interpreted the data; Lv ZJ drafted the manuscript; all authors made critical revisions related to important intellectual content of the manuscript, and have read and approved the final version to be published.
Supported by Natural Science Foundation of Guangdong Province, No. 2016A030310328 and No. 2016A030313762.
Institutional review board statement: This study was evaluated and approved by the ethics committee at our institution.
Informed consent statement: All study participants, or their legal guardian, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: All authors declare no conflict of interest.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Yong Li, MD, PhD, Professor, Chief Doctor, Department of General Surgery, Guangdong General Hospital, Guangdong Academy of Medical Sciences, No. 106, Zhongshan 2nd Road, Guangzhou 510080, Guangdong Province, China. s_09zfyang@163.com
Telephone: +86-20-83827812-60910 Fax: +86-20-83827812
Received: October 26, 2017
Peer-review started: October 27, 2017
First decision: November 8, 2017
Revised: November 17, 2017
Accepted: November 21, 2017
Article in press: November 21, 2017
Published online: January 7, 2018

Abstract
AIM

To evaluate the short-term and long-term outcomes following laparoscopic vs open surgery for pathological T4 (pT4) colorectal cancer.

METHODS

We retrospectively analyzed the short- and long-term outcomes of proven pT4 colorectal cancer patients who underwent complete resection by laparoscopic or open surgery from 2006 to 2015 at Guangdong General Hospital.

RESULTS

A total of 211 pT4 colorectal cancer patients were included in this analysis, including 101 cases in the laparoscopy (LAP) group and 110 cases in the open surgery (OPEN) group [including 15 (12.9%) cases of conversion to open surgery]. Clinical information (age, gender, body mass index, comorbidities, American Society of Anesthesiologists score, etc.) did not differ between the two groups. In terms of blood loss, postoperative complications and rate of recovery, the LAP group performed significantly more favorably (P < 0.05). With regard to pT4a/b and combined organ resection, there were significantly more cases in the OPEN group (P < 0.05). The 3- and 5-year overall survival rates were 74.9% and 60.5%, respectively, for the LAP group and 62.4% and 46.5%, respectively, for the OPEN group (P = 0.060). The 3- and 5-year disease-free survival rates were 68.0% and 57.3%, respectively, for the LAP group and 55.8% and 39.8%, respectively, for the OPEN group (P = 0.053). Multivariate analysis showed that IIIB/IIIC stage, lymph node status, and CA19-9 were significant predictors of overall survival. PT4a/b, IIIC stage, histological subtypes, CA19-9, and adjuvant chemotherapy were independent factors affecting disease-free survival.

CONCLUSION

Laparoscopy is safely used in the treatment of pT4 colorectal cancer while offering advantages of minimal invasiveness and faster recovery. Laparoscopy is able to achieve good oncologic outcomes similar to those of open surgery. We recommend that laparoscopy be carried out in experienced centers. It is still required to screen the appropriate cases for laparoscopic surgery, optimize the preoperative diagnosis process, and reduce the conversion rate. Multi-center, prospective, and large-sample studies are required to assess these issues.

Key Words: pT4 colorectal cancer, Laparoscopy, Open surgery

Core tip: Laparoscopy has been widely used in the treatment of colorectal cancer and has achieved a good radical effect in oncology. However, current clinical association guidelines do not recommend laparoscopic surgery for T4 colorectal cancer. This study retrospectively collected the data of pathological T4 (pT4) colorectal cancer patients at Guangdong General Hospital from 2006 to 2015, aiming to compare outcomes of laparoscopic vs open surgery. The conclusion is that laparoscopy is safely used in the treatment of pT4 colorectal cancer while offering advantages of faster recovery. Laparoscopy is able to achieve good oncologic outcomes similar to those of open surgery.



INTRODUCTION

Colorectal cancer is a common malignant tumor. It is the third most diagnosed cancer and the fourth leading cause of cancer-related deaths worldwide[1]. In China, the incidence and mortality of colorectal cancer are ranked among the top five of all cancers; thus, colorectal cancer is a very serious public health problem[2]. In promoting comprehensive, individualized, and precise treatments to date, surgical treatment is still the only way to cure colorectal cancer. Since 1991, when Jacobs first reported the technical feasibility of laparoscopic colectomy[3], a number of successful randomized controlled studies have been conducted around the world to compare laparoscopy and laparotomy, with encouraging results achieved. The laparoscopic treatment of colorectal cancer can not only achieve similar short- and long-term outcomes comparable to laparotomy, but its advantage of minimal invasiveness has gradually been recognized and promoted[4-7]. The American Joint Committee on Cancer (AJCC) classifies T4 colorectal cancers as those that invade into other organs and structures and/or perforate the visceral peritoneum; laparoscopic surgery in colorectal cancer at this stage is difficult as it is hard to reach and violates the “no touch” principle. Therefore, the AJCC and European Association of Endoscopic Surgery do not recommend laparoscopic treatment of pathological T4 (pT4) colorectal cancer[8]. This study retrospectively collected the data of pT4 colorectal cancer patients at Guangdong General Hospital from 2006 to 2015, aiming to compare the outcomes of laparoscopic vs open surgery.

MATERIALS AND METHODS
Patients

All pT4 colorectal cancer patients treated at Guangdong General Hospital from 2006 to 2015 were enrolled in this study. All patients were staged according to the AJCC 7th edition manual for colorectal cancer. The inclusion criteria included the following: (1) age of 18-75 years; (2) proven T4 pathology; and (3) radical surgery (D3 lymph node dissection). The exclusion criteria included the following: (1) low rectal cancer (peritoneal reflection as the boundary); (2) preoperative neoadjuvant treatment; (3) non-neoplastic deaths; and (4) palliative resection.

Surgical procedure

Preoperative computed tomography (CT) and magnetic resonance imaging were used to determine the preoperative clinical stage. The decision to proceed with laparoscopy or open surgery was made for all subjects on a patient-by-patient basis following multidisciplinary discussions and meetings. All cases entailed surgical resection according to the Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines[9], which have the following requirements: D3 lymph node dissection (Figure 1) to ensure the appropriate resection length, and ensuring that the integrity of the mesorectum and intraoperative operations follow the principle of “no touch” (sharp separation, blood vessels first, tumor isolation, etc.). According to tumor location, the method of resection included the following: total colectomy, right colectomy, extended right colectomy, transverse colectomy, left colectomy, sigmoid colectomy, mid/upper anterior resection, and combined organ resection. Laparoscopic incision should not exceed 6 cm. The conversion cases were analyzed in the open surgery (OPEN) group.

Figure 1
Figure 1 Flowchart for selection of the extent of lymph node dissection (from reference 9).
Observation indexes

The preoperative indexes included age, gender, body mass index (BMI; kg/m2), comorbidity, American Society of Anesthesiologists (ASA) score, tumor location, hemoglobin, and tumor markers (CA19-9 and CEA). The intraoperative indexes included surgical and pathological outcomes. Surgical outcomes included the conversion rate (conversion was defined as an open surgery performed during the laparoscopic procedure in order to ensure complete resection, reconstruction, or hemostasis and not just for the extraction of specimens), tumor size, resection length, operative time, blood loss, intraoperative complications, combined organ resection, postoperative complications and mortality. Pathological outcomes included the number of lymph nodes dissected, lymph node status, margin, pT stage, pN stage, pTNM stage, Dukes stage, histological subtype, and differentiation. The postoperative recovery indexes included time to flatus, diet, and ambulation and hospital stays.

Follow-up

All patients were postoperatively referred to the 7th AJCC/UICC TNM stage for adjuvant chemotherapy. All patients were followed through outpatient visits. According to the NCCN guidelines, patients were subjected to a 5-year surveillance program consisting of physical examinations and tumor marker (CEA and CA19-9) analysis every 3 mo up to 2 years. Every 6 mo, patients had complete colonoscopies at one and three years after surgery. Thoracic and abdominal CT scans were planned every year for five years of surveillance.

Statistical analysis

Statistical analyses were performed using SPSS 19.0. Quantitative data are reported as the mean ± SD or median. Categorical data were compared by χ2 tests or Fisher’s exact test. Survival curves [overall survival (OS) and disease-free survival (DFS)] were derived from Kaplan-Meier estimates, and the curves were compared by the log-rank test. Prognostic factors were identified by univariate analysis and further tested by multivariate analysis. The results are reported as a hazard ratio (HR) with 95%CI. A P-value < 0.05 was considered statistically significant.

RESULTS

During the period from 2006 to 2015, we collected a total of 211 pT4a/bN0-2M0 cases according to enrollment criteria from 2308 cases of colorectal cancer at the Department of General Surgery of Guangdong General Hospital. There were 101 cases in the laparoscopy (LAP) group and 111 cases in the OPEN group (Figure 2).

Figure 2
Figure 2 Study flowchart showing patient selection. GGH: Guangdong general hospital; pT4: Pathological proven T4.

There were no significant differences in age, gender, BMI, ASA score, tumor location, hemoglobin, CA19-9, or CEA between the two groups (P > 0.05) (Table 1).

Table 1 Clinical information of 211 colorectal cancer cases.
Clinical informationLAPOPENP value
n = 101n = 110
Age> 60 yr55580.270
≤ 60 yr4652
GenderMale67660.392
Female3444
BMI (kg/m2)< 2467730.348
≥ 243437
ComorbiditiesYes39421.000
No6268
ASA scoreI890.715
II6372
III3029
Tumor locationMid/upper Rectum33350.989
Left colon4347
Right colon2528
HBG (g/L)mean ± SD124.0 ± 27.1120.7 ± 22.90.263
CA19-9 (U/mL)< 2778750.163
≥ 272335
CEA (ng/mL)< 560640.666
≥ 54146
Postoperative adjuvant chemotherapyYes49460.332
No5264
RecurrenceYes22250.711
No7985

For surgical outcome, conversion to open surgery occurred in 15 (12.9%) patients, and all conversion cases were analyzed in the OPEN group. There was no significant difference between the two groups in terms of intraoperative complications and postoperative complications within 30 d (P > 0.05). Laparoscopic surgery was slightly slower than open surgery (210.8 ± 88.9 min vs 173.5 ± 72.7 min, P = 0.028); there was less blood loss (155.0 ± 75.9 mL vs 235.1 ± 120.5 mL, P = 0.033) in laparoscopic surgery, whereas open surgery showed better resection lengths (15.5 ± 7.3 cm vs 19.5 ± 10.4 cm, P = 0.046). In the case of combined organ resection, there were 21 (19.1%) patients in the OPEN group, including three cases of abdominal wall resection, five cases of small bowel (except duodenum) resection, three cases of duodenum resection, two cases of urinary organ resection, one case of stomach resection, four cases of gynecologic organ resection, and three cases of liver resection; in contrast, there were only five cases in the LAP group (P = 0.001). For postoperative complications within 30 d, there were 12 (12.9%) cases in the LAP group, and there was a higher incidence in the OPEN group (31.8%, P = 0.006) (Table 2).

Table 2 Surgical outcomes of 211 colorectal cancer cases.
Surgical outcomeLAPOPENP value
n = 101n = 110
Conversion to open (n/%)15 (12.9)NR/
Tumor size (cm)mean ± SD5.4 ± 1.95.2 ± 2.50.765
Resection length (cm)mean ± SD15.5 ± 7.319.5 ± 10.40.046
Operative time (min)mean ± SD210.8 ± 88.9173.5 ± 72.70.028
Blood loss (mL)mean ± SD155.0 ± 75.9235.1 ± 120.50.033
Intraoperative complications380.117
Combined organ resectionTotal (%)5 (5.0)21 (19.1)0.001
Abdominal wall23
Small bowel (except duodenum)15
Duodenum03
Urinary organs02
Stomach11
Gynecologic organs14
Liver03
Postoperative complications within 30 dTotal (%)12 (12.9)35 (31.8)0.006
Anastomotic Hemorrhage12
Urinary injury01
Intraabdominal bleeding12
Leakage14
Gastroplegia24
Infection615
(incision and abdomen)
Disruption of incision05
Obstruction12
Postoperative morbidity within 30 d010.667

Regarding pathologic outcomes, no significant differences in the number of lymph nodes dissected, lymph node status, margin, pN stage, pTNM stage, Dukes stage, histological subtype, differentiation, or HER2 status were detected when comparing the two groups (P > 0.05). There were 21 pT4b cases in the OPEN group but only five cases in the LAP group; a comparison between the two groups in the pT stage revealed a statistically significant difference (P = 0.021) (Table 3).

Table 3 Pathologic outcomes of 211 colorectal cancer cases.
Pathologic outcomeLAPOPENP value
n = 101n = 110
Number of lymph nodes dissected< 1225380.134
≥ 127672
Lymph node status+67741.000
-3436
MarginR1230.779
R099107
pT stageT4a96890.021
T4b521
pN stageN036350.841
N12832
N23743
pTNM stageIIB + IIC34350.282
IIIB3024
IIIC3751
DukesB34350.883
C6775
Histological subtypeAdenocarcinoma87941.000
Myxoadenocarcinoma1416
DifferentiationPoor20250.719
Median/high8185
HER2-/+86960.871
++1010
+++54

With regard to postoperative recovery indexes, the LAP group was significantly better than the OPEN group (P < 0.05) in time to flatus, diet, and ambulation. The median hospital stay was 7 (5-21) d for the LAP group and 15 (7-31) d for the OPEN group, which showed a statistically significant difference between the two groups (P = 0.004) (Table 4).

Table 4 Postoperative recovery outcomes of 211 colorectal cancer cases.
Recovery outcomeLAPOPENP value
n = 101n = 110
Time to flatus (d)Median (range)2 (1-9)4 (3-15)0.037
Time to diet (d)Median (range)3 (2-18)7 (5-27)0.003
Time to ambulation (d)Median (range)2 (1-5)5 (3-9)0.027
Hospital staysMedian (range)7 (5-21)15 (7-31)0.004

The mean overall follow-up time was 36 mo (range, 2-24 mo); there was no difference between the LAP and OPEN groups in terms of OS and DFS. The 3- and 5-year OS rates were 74.9% and 60.5%, respectively, for the LAP group and 62.4% and 46.5%, respectively, for the OPEN group (P = 0.60) (Figure 3). The 3- and 5-year DFS rates were 68.0% and 57.3%, respectively, for the LAP group and 55.8 and 39.8%, respectively, for the OPEN group (P = 0.053) (Figure 4). Disease recurrence over the entire follow-up period was observed in 21.8% (n = 22) of patients in the LAP group and 22.7% (n = 25) of patients in the OPEN group (P = 0.711) (Table 1), without significant differences between the LAP and OPEN groups (P = 0.711). In the multivariate regression analysis, TNM stage (IIIB, IIIC), lymph node status (pN+), and CA19-9 were significant predictors of OS. TNM stage (IIIC), histological subtype, CA19-9, and chemotherapy were predictive of DFS (Tables 5 and 6).

Figure 3
Figure 3 The overall survival curve shows that 3- and 5-year overall survival rates were 74. 9% and 60.5%, respectively, in the LAP group and 62.4% and 46.5%, respectively, in the OPEN group. There was no significant difference between the LAP and OPEN groups (P = 0.060).
Figure 4
Figure 4 The disease-free survival curve shows that the 3- and 5-year disease-free survival rates were 68. 0% and 57.3%, respectively, in the LAP group and 55.8% and 39.8%, respectively, in the OPEN group. There was no significant difference between the LAP and OPEN groups (P = 0.053).
Table 5 Univariate and multivariate analyses of 211 pathological T4 colorectal cancer patients for overall survival.
Univariate analysis
Multivariate analysis
VariableHR (95%CI)P valueHR (95%CI)P value
Age1.217 (0.784-1.888)0.381
Gender0.807 (0.508-1.281)0.363
Surgical method (LAP and OPEN)1.528 (0.982-2.377)0.060
Tumor location
Mid/upper rectumReference group-
Left colon1.303 (0.813-2.091)0.272
Right colon0.792 (0.409-1.533)0.489
Comorbidities1.603 (1.007-2.552)0.0472.519 (1.436-4.419)0.142
pT4a/b0.790 (0.692-1.236)0.445
N stage
N0Reference group-
N11.328 (0.701-2.517)0.384
N22.079 (1.170-3.697)0.013
TNM stage
IIB + IICReference group-Reference group-
IIIB1.229 (0.564-2.679)0.6041.324 (0.785-1.753)0.019
IIIC3.092 (1.617-5.913)0.0011.104 (0.333-3.662)0.001
Lymph node status0.560 (0.324-0.968)0.0380.307 (0.103-0.919)0.035
No. of lymph nodes resected0.593 (0.385-0.915)0.0180.432 (0.264-0.708)0.123
Histological subtype0.369 (0.212-0.640)0.0000.433 (0.218-0.859)0.247
Differentiation0.326 (0.204-0.519)0.0000.460 (0.273-0.775)0.087
CA19-91.868 (1.195-2.922)0.0061.662 (1.212-2.280)0.002
CEA1.089 (0.706-1.680)0.0130.608 (0.356-1.038)0.068
Chemotherapy1.611 (1.040-2.494)0.0332.225 (1.394-3.552)0.181
Table 6 Univariate and multivariate analyses of 211 pathological T4 colorectal cancer patients for disease-free survival.
Univariate analysis
Multivariate analysis
VariableHR (95%CI)P valueHR (95%CI)P value
Age1.621 (1.010-2.601)0.0451.892 (1.111-3.223)0.419
Gender1.328 (0.824-2.141)0.243
Surgical method (LAP and OPEN)1.503 (0.933-2.422)0.094
Tumor location
Mid/upper rectumReference group-
Left colon1.010 (0.601-10697)0.969
Right colon0.818 (0.411-1.629)0.568
Comorbidities1.787 (1.058-3.019)0.0302.261 (1.235-4.139)0.080
pT4a/b0.818 (0.618-1.725)0.0131.214 (0.784-1.974)0.001
N stage
N0Reference group-
N11.134 (0.594-2.167)0.703
N21.553 (0.861-2.801)0.144
TNM stage
IIB + IICReference group-Reference group-
IIIB1.034 (0.471-2.269)0.9330.884 (0.393-1.989)0.765
IIIC2.284 (1.202-4.337)0.0121.831 (0.935-3.584)0.018
Lymph node status0.710 (0.411-1.229)0.221
No. of lymph nodes resected0.661 (0.411-1.061)0.087
Histological subtype0.456 (0.243-0.854)0.0140.469 (0.225-0.974)0.042
Differentiation0.439 (0.266-0.725)0.0010.662 (0.374-1.170)0.156
CA19-92.458 (1.526-3.960)0.0003.372 (1.968-5.778)0.000
CEA1.268 (0.790-2.036)0.3260.608 (0.356-1.038)0.072
Chemotherapy2.157 (1.323-3.514)0.0023.817 (2.194-6.639)0.000
DISCUSSION

Since the first report of laparoscopic colorectal resection in 1991, some prospective clinical studies of laparoscopic resection for colorectal cancer have confirmed that laparoscopic techniques not only achieve minimally invasive and cosmetic effects but also achieve faster recovery and similar oncologic outcomes compared with open surgery[10-12]. However, due to the large tumor size of T4 colorectal cancer and more frequent invasion of peripheral tissues or nearby organs, laparoscopic complete resection is difficult and has high risks; the majority of clinical studies have fewer cases of T4 colorectal cancer[13,14], and some studies do not enroll any such cases[15,16]. Therefore, the evidence-based data that support the laparoscopic resection in T4 colorectal cancer are limited. Laparoscopic resection of T4 colorectal cancer is regarded a technique that demands precision, and its efficacy remains controversial. The relevant guidelines do not recommend laparoscopy in T4 colorectal cancer[8]. However, due to the maturity and progress of the laparoscopic platform, coupled with the popularity of and improvements in laparoscopic techniques, some surgeons in certain experienced centers have tried to use laparoscopic techniques in T4 colorectal cancer, achieving similar short- and long-term outcomes to open surgery[17-20].

This study decided whether laparoscopic or open surgery should be performed based on the results of preoperative imaging examination and the patient’s condition; the main referenced indicators included the following: tumor location, tumor size, and the scope of invaded organ[21]. We found a statistically significant difference in the postoperative pT stage between the two groups (P = 0.021), with 21 cases of pT4b in the OPEN group. An examination of postoperative surgical outcomes (Table 2) revealed 21 cases of combined organ resection in the OPEN group, with the most commonly invaded organs including the small intestine, gynecological organs, and duodenum; in contrast, the LAP group had only five cases, and the number of cases of combined organ resection was thus significantly different for the two groups (P = 0.001), which is consistent with the results of previous studies[22,23]. These data also demonstrate that T4b stage may be an important consideration for surgeons to select laparoscopic or open surgery because it is very difficult to achieve the goal of complete resection using the “no touch” principle; therefore, guidelines do not recommend laparoscopic resection in T4 colorectal cancer[8]. However, such considerations lead to selective bias in the study, which is one of the limitations in both this study and a retrospective study.

Because of the larger tumor, a wide scope of invasion, combined with resection of other organs, especially due to the lack of laparoscopic experience in some centers, may lead to a high conversion rate. Previous studies of laparoscopic surgery in colorectal cancer (stage II-III)[11,15,24] reported that the conversion rate was 25% in the CLASSIC trial (for colon cancer), 17% in the COLOR trial, and 21% in the COSTSG trial, whereas a retrospective study of pT4 colorectal cancer showed that the conversion rate was 5.6%-24.7%[17,19,22,25-29]; this study showed a conversion rate of 12.9%, which is consistent with reports in the literature. The conversion rates reported by some studies of pT4 colorectal cancer in South Korea and Singapore were 5.6%, 7.7% and 8.6%[22,29,30], which are significantly lower than those from the US and Europe[17,18,25,27] (Table 7). We explain these differences as follows: (1) Laparoscopic technology and experience may differ between Asian and Western countries; (2) the conversion standard used was different; (3) there was a lack of preoperative imaging assessments to select appropriate laparoscopic surgery cases in Western countries; and (4) European populations had a higher BMI. All these factors increase the difficulty of surgery[17-25]. Thus, surgeons should choose the appropriate pT4 colorectal cases to perform laparoscopic surgery in order to reduce the conversion rate and ensure operation safety. We recommend laparoscopic surgery as an option in experienced centers and for T4a cases with tumor sizes < 5 cm and when only a single organ has been invaded by T4 colorectal cancer.

Table 7 Studies about laparoscopic surgery for pathological T4 colorectal cancer.
Ref.n (LAP:OPEN)Study periodStudy designCountrySingle/Multi centerConversion rateLocationComplication rate (LAP:OPEN)Tumor stageCombined resection (LAP:OPEN)RI rate(LAP:OPEN)5 years DFS (LAP:OPEN)5 years OS (LAP:OPEN)
Park et al[22], 201693:182000-2010RSSouth KoreaSingle5.6%Colon14.1%:31.5%-9.9%:32.5%5.5%:4.5%81.8%:73.9%95.3%:86.5%
rectum
Shukla et al[20], 201561:222003-2011RSUnited StatesSingle21%Colon28%:36%II:3523%:41%0%:4%75%:65%82%:81%
III:48(3 yr)(3 yr)
Kang et al[29], 201652:572003-2013RSSouth KoreaSingle7.7%Colon13.5%:36.8%II:4113.5%:36.8%-53.6%:62.6%60.7%:61.9%
III:68
de’Angelis et al[18], 2016106:1062005-2014RPSMFranceMulti12.2%Colon29.1%:35.3%II:8514.2%:18.9%5.7%:6.6%58.6%:59.9%57.6%:50.2%
SwitzerlandIII:127
de’Angelis et al[17], 201652:522005-2015RPSMFranceMulti21.2%Rectum30.8%:48.1%II:4226.9%:30.8%19.2%:17.3%66.7%:64.1%55.4%:53.3%
SwitzerlandIII:33
SpainIV:29
Chan et al[30], 201693:592008-2014RSSingaporeSingle8.6%Colon--0%:3.4%0%:0.7%-75%:80%
Leon et al[27], 201768:792008-2015RSItalySingle19%Colon7.4%:16.5%II:69-11.8%:11.5%40.3%:38.9%44.6%:39.4%
III:78
Ahmad et al[25], 2015455:4062011-2012RSCanadaACSNS24.7%Colon---26.2%:24.3%--
QIP

In this study, the LAP group had longer operative time (210.8 ± 88.9 min vs 173.5 ± 72.7 min, P = 0.028), which may be related to the lack of experience and the difficulty of this surgery[19]. The resection length (19.5 ± 10.4 cm) obtained in the OPEN group was significantly better (P = 0.046). The literature shows that the incidence of postoperative complications associated with laparoscopic surgery was clearly lower than that associated with open surgery[31]. In this study, the rate of postoperative complication within 30 d in the LAP group was 12.9% (12/101), which was lower than 31.8% (35/110) in the OPEN group, and the most common complications in the OPEN group were infection (incision and abdomen) and disruption of incision, similar to a previous report in the literature[32]. Therefore, attention should be paid to intraoperative sterile principles and the suture of incision.

With regard to postoperative recovery outcomes, the LAP group had clear advantages in time to flatus (P = 0.037), diet (P = 0.003), and ambulation (P = 0.027) and hospital stays (P = 0.004) compared with the OPEN group (Table 4). Laparoscopy has the advantages of minimal invasion and fast recovery, which is in agreement with many earlier clinical studies[12,15,16].

In colorectal cancer surgery, lymph node dissection and R0 resection are important factors affecting long-term survival[33]. We performed D3 lymphadenectomy (parenteral lymph node -middle lymph node-central lymph node)[34] according to the guidelines recommended by the JSCCR. Previous studies have shown that laparoscopic treatment of colorectal cancer achieved an R0 resection rate between 80.8% and 98%[11,16,18]. In this study, the percentage of cases with the number of lymph nodes dissected greater than 12 was 75.2% (76/101) in the LAP group and 65.5% (72/110) in the OPEN group, and the difference was not significantly different (P = 0.134). Concurrently, the R0 resection rate in the LAP group was 98% (99/101), whereas in the OPEN group, it was 97.3% (107/110), which was not significantly different (P = 0.779). Thus, we believe that laparoscopic treatment in pT4 colorectal cancer can achieve similar oncological outcomes to open surgery. Finally, no differences in the 3- and 5-year OS rates (P = 0.060) and in 3- and 5-year DFS rates (P = 0.053) were observed when comparing the two groups, suggesting that laparoscopy may be a valid and effective tool to treat pT4 colorectal cancer without jeopardizing oncologic results, in accordance with the previously reported series. Multivariate analysis in our series detected IIIB/IIIC stage, lymph node status, and CA19-9 as independent predictors of OS, and pT4a/b, IIIC stage, CA19-9, and adjuvant chemotherapy as independent predictors of DFS.

In conclusion, laparoscopic surgery may be safe and acceptable in the treatment of pathologic T4 colorectal cancer patients with fast recovery outcomes and oncologic outcomes compared with open surgery. Thus, laparoscopy should not be regarded as an absolute contraindication in the management of pT4 colorectal cancer. Finally, as this study is only a retrospective study in a single center with a small sample size, the results need to be confirmed by prospective, multi-center and large sample clinical studies.

ARTICLE HIGHLIGHTS
Research background

Laparoscopy has been widely used in the treatment of colorectal cancer and it has achieved a good radical effect in oncology. However, for the current clinical guidelines, laparoscopic surgery is not recommended in T4 colorectal cancer.

Research motivation

Due to the characteristics of T4 colorectal cancer, laparoscopic complete resection is difficult for the resection of this kind of tumor. The current colorectal studies about laparoscopy have fewer cases of T4 colorectal cancer, and some studies do not enroll any such cases. We tried to collect and analyze the data about laparoscopy in T4 colorectal cancer in order to add evidence-based clinical evidence.

Research objectives

We aimed to analyze the short- and long-term outcomes of proven pathological T4 colorectal cancer patients who underwent complete resection by laparoscopic or open surgery.

Research methods

We collected and analyzed the data of pT4 colorectal cancer cases at Guangdong General Hospital from 2006 to 2015. All patients were staged according to the AJCC 7th edition manual for colorectal cancer. We compared the laparoscopy (LAP) group and open (OPEN) group in clinical information, surgical and pathological outcomes, postoperative recovery outcomes, and survival.

Research results

There were 101 cases in the LAP group and 110 cases in the OPEN group [including15 (12.9%) cases of conversion to open surgery]. Clinical information did not differ between the two groups. In terms of blood loss, postoperative complications, and rate of recovery, the LAP group performed significantly more favorably (P < 0.05). With regard to pT4a/b and combined organ resection, there were significantly more cases in the OPEN group (P < 0.05). The 3- and 5-year overall survival rates were 74.9% and 60.5%, respectively, for the LAP group and 62.4% and 46.5%, respectively, for the OPEN group (P = 0.060). The 3- and 5-year disease-free survival rates were 68.0% and 57.3%, respectively, for the LAP group and 55.8% and 39.8%, respectively, for the OPEN group (P = 0.053). Multivariate analysis showed that IIIB/IIIC stage, lymph node status, and CA19-9 were significant predictors of overall survival. PT4a/b, IIIC stage, histological subtype, CA19-9, and adjuvant chemotherapy were independent factors affecting disease-free survival.

Research conclusions

Laparoscopic surgery may be safe and acceptable in the treatment of pathologic T4 colorectal cancer patients with fast recovery outcomes and oncologic outcomes compared with open surgery. We recommend that it can be carried out in experienced centers. It is required to screen the appropriate cases for laparoscopic surgery, optimize the preoperative diagnosis process, and reduce the conversion rate.

Research perspectives

Although our study shows that laparoscopy is able to achieve good clinicopathological and oncologic outcomes similar to those of open surgery, this study is only a retrospective study in a single center with a small sample, and the results need to be confirmed by prospective, multi-center and large sample clinical studies.

Footnotes

Manuscript source: Unsolicited manuscript

Specialty type: Gastroenterology and hepatology

Country of origin: China

Peer-review report classification

Grade A (Excellent): 0

Grade B (Very good): B, B

Grade C (Good): 0

Grade D (Fair): 0

Grade E (Poor): E

P- Reviewer: Kim SM, Sterpetti AV, Yokoyama S S- Editor: Chen K L- Editor: Wang TQ E- Editor: Huang Y

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