Published online Apr 15, 2004. doi: 10.3748/wjg.v10.i8.1167
Revised: August 1, 2003
Accepted: August 25, 2003
Published online: April 15, 2004
AIM: To evaluate the feasibility of laparoscopic resection of rectal carcinoma and to compare the short-term outcome of laparoscopic procedure with conventional open surgery for rectal cancer.
METHODS: Thirty-eight patients with rectal cancer were included in a prospective non-randomized study. The patients were assigned to laparoscopic (n = 18) or open (n = 18) colorectal resection. Case selection, surgical technique, and clinical and pathological results were reviewed.
RESULTS: The operative time was longer in laparoscopic resection group (LAP) than in open resection group (189 ± 18 min vs 146 ± 22 min, P < 0.05). Intraoperative blood loss and postoperative complications were less in LAP resection group than in open resection group. An earlier return of bowel motility was observed after laparoscopic surgery. The overall postoperative morbidity was 5.6% in the LAP resection group and 27.8% in open resection group (P < 0.05). No anastomotic leakage was found in both groups. The pathologic examination showed that the length of the resected specimen, the mean number of harvested lymph nodes in laparoscopic resection group were comparable to those in open resection group.
CONCLUSION: Laparoscopic total mesorectal excision (TME) for rectal cancer is a feasible but technically demanding procedure. The present study demonstrates the safety of the procedure, while oncologic results are comparable to the open surgery, with a favorable short-term outcome.
- Citation: Wu WX, Sun YM, Hua YB, Shen LZ. Laparoscopic versus conventional open resection of rectal carcinoma: A clinical comparative study. World J Gastroenterol 2004; 10(8): 1167-1170
- URL: https://www.wjgnet.com/1007-9327/full/v10/i8/1167.htm
- DOI: https://dx.doi.org/10.3748/wjg.v10.i8.1167
Since the first series of successful laparoscopic colon resections reported in 1991[1,2], the laparoscopic techniques for colorectal diseases have been accepted widely[3]. Although generally accepted for the treatment of benign diseases of the colon and rectum, the role of laparoscopic technique in cancer surgery remains controversial. Early reports of trocar site and wound recurrences of malignancies after laparoscopic procedures led to concerns over possible increased recurrences and the risk of peritoneal seeding from the pneumoperitoneum[4-6]. The ability to adhere to oncologic principles during laparoscopic surgical resection and the implications for long-term survival were also questioned.
The technical approach can significantly affect the outcome in colorectal cancer patients. The key principles including en bloc resection with removal of corresponding lymphatics, no-touch technique[7], and total mesorectal excision (TME) are often recommended in open surgery for colorectal cancer[8]. These oncologic principles are as important in laparoscopic surgery as in open surgery.
We presented our preliminary collected data on laparoscopic surgery for rectal carcinoma versus open resection in our university hospital to assess the safety and feasibility of laparoscopic resection of rectum with total mesorectal excision technique.
Thirty-six patients (16 women, 20 men) undergoing anterior recto-sigmoidal and abdominoperineal resections for rectal carcinoma between April 2002 and May 2003 at the 1st Affiliated Hospital of Nanjing Medical University (Nanjing, Jiangsu, China) were entered into a database. Pre- and post-operative care was standardized for both laparoscopic and open resection groups. Preoperative assessment included physical examination, liver function and carcinoembryonic antigen (CEA) tests, liver ultrosonography, and colonoscopy with biopsy. Patients who had intestinal obstruction, emergency surgery, adjacent organ invasion diagnosed preoperatively, and history of colon surgery were excluded for laparoscopic operation.
In laparoscopic resection group eighteen patients (9 women and 9 men) undergoing laparoscopic operation for rectal carcinoma were reviewed. Inclusion in the laparoscopic or conventional treatment group was not randomized. All patients were operated on by 2 groups of surgeons, 1 group of surgeons who had experiences in advanced laparoscopic techniques used a laparoscopic approach, and the other group of surgeons performed conventional resections.
The patients were treated with mechanical and antibiotic bowel preparation preoperatively. Surgery was done under general anesthesia. All patients received antibiotics intravenously at the time of induction in the operating room.
Patients were placed in the modified lithotomy position to facilitate either transanal stapled anastomosis or peritoneal resection. All patients had an indwelling urinary catheter. For the laparoscopic resection group the pneumoperitoneum was established with an intra-abdominal pressure of 15 mmHg.
The laparoscope was sited at the umbilicus, 4 trocars were inserted. In brief, two 5-mm ports were placed in the right and left upper quadrants and a 10-mm trocar for the left iliac fossa. A further 12-mm trocar was inserted in the right iliac fossa for the endoscopic stapling device. Mobilization and dissection of sigmoid colon and rectum were achieved by using ultrasonic scissors. The following procedures were required: left colon mobilization (including the splenic flexure if necessary), identification of the left ureter, and intracorporeal ligation of the inferior mesenteric vessels with clips or stapling devices. Rectum and mesorectum were mobilized through the avascular plane between the intact mesorectum anteriorly and Waldeyer’s fascia posteriorly by sharp dissection and extended down to the level of the levator muscle. The ureters, hypogastric nerve, and pelvic parasympathetic plexus were protected. After intracorporeal transaction of the distal bowel with endolineal staplers, the bowel was drawn out through a left lower quadrant incision under wound protection and divided with appropriate proximal clearance. The proximal anvil was placed extra corporeally, and anastomosis was performed by double stapling technique.
For abdominoperineal resection, laparoscopic procedures were followed by perineal resection in the standard fashion. A terminal colostomy was created at the left lower abdomin port site. With the help of the perineal surgeon, the rectum and the whole mesorectum were fully mobilized and the specimen was retrieved through the perineum wound. The perineum wound was closed primarily with placement of a drain connected to a low-pressure suction, in the pelvic cavity.
In the conventional surgery group open procedures were performed according to the surgeon’s established technique, conforming to standard rules for rectal cancer.
Characteristics of the patients, operative variables, and short-term outcomes were analyzed. The patient information including age, gender, premorbid conditions, and previous surgery was reviewed. Operative variables, and short-term outcomes including time to resumption of oral intake, first day to flatus, and duration of hospitalization were analyzed as clinical parameters for study. Pathology reports were reviewed to obtain lymph node harvest data, length of specimen, distance from the closest margin, and margin status. Intra- or post-operative complications were reviewed, and all results were compared with those of conventional rectal resections in the open group.
Statistical analysis was performed with Student’s t-test and χ2 test. Results are expressed as mean ± SD. A P value less than 0.05 was considered statistically significant.
The patients’ characteristics in laparoscopic or open resection group are summarized in Table 1. The two groups were comparable in terms of age, sex, American Society of Anesthesia score (ASA score), pathologic stage and type of resection.
LAP resection group (n = 18) | Open resection group (n = 18) | Difference (P value) | |
Age (Years) | 52.4 ± 7.9 | 54.1 ± 6.8 | NS |
Male/Female | 9:09 | 10:08 | NS |
ASAP score | 2.4 ± 0.2 | 2.5 ± 0.3 | NS |
Operations | |||
LAR | 11 | 12 | NS |
APR | 7 | 6 | NS |
Duke’s stage | |||
A | 3 | 3 | NS |
B | 9 | 7 | NS |
C | 6 | 8 | NS |
The mean operating time was significantly longer in LAP resection group than in open resection group. The amount of operative blood loss was lower in LAP resection group than in conventional surgery group (Table 2). No patients needed conversion to open surgery in laparoscopic resection group. However, rectum injury was found in two cases with low anterior resection after colon-rectum anastomosis. This was managed by laparoscopic suture closure and pelvic drainage for one week without further sequela. In one patient with heavy smoking history, significantly increased PaCO2 was found after two hours’ pneumoperitoneum during the operation, and the patient recovered after deflation of pneumoperitoneum and hyperventilation for a short period of 20 min (Table 3).
LAP resection group (n = 18) | Open resection group (n = 18) | Difference (P value) | |
Operative time (min) | 189 ± 18 | 146 ± 22 | < 0.05 |
Estimated blood loss (mL) | 136 ± 21 | 357 ± 34 | < 0.01 |
Passing flatus (h) | 43 ± 5 | 78 ± 12 | < 0.05 |
Oral intake (h) | 58 ± 9 | 89 ± 13 | < 0.05 |
Hospital stay (d) | 7.8 ± 1.5 | 9.1 ± 3.3 | NS |
Complication | Number of patients | P value | |
LAP (n = 18) | Open (n = 18) | ||
Intraoperative | |||
Bleeding | 0 | 2 | NS |
Rectum injury | 2 | 1 | NS |
Increased PaCO2 | 1 | 0 | NS |
Postoperative | |||
Wound infection | 0 | 1 | NS |
Urinary retention | 1 | 2 | NS |
Prolonged ileum ( > 4 d) | 0 | 2 | NS |
Morbidity (%) | 5.6 | 27.8 | < 0.05 |
Post-operative complications were more frequent in the open resection group than in LAP resection group (5.6% vs 27.8%; P < 0.05).
The passage of flatus occurred earlier in laparoscopic resection group, and oral intake could be started earlier in the LAP resection group (P < 0.05). Mean postoperative stay was shorter in LAP resection group than in open resection group, but the difference was not significant.
To assess the adequacy of oncological resection, several parameters were examined from pathology reports. Evaluation of the resected specimens is summarized in Table 4. The mean number of lymph nodes removed in LAP or open resection group was 7.8 ± 1.7 (range, 4-13) and 8.2 ± 2.3 (range, 3-15), respectively. No significant difference was found between the 2 groups. The average lengths of removed specimens with the two surgical procedures were also comparable. Tumor distances from the closest margin were similar too for the two procedures, and were adequate from an oncological standpoint of view. Histological examination revealed that proximal and distal margins were free of tumor in all surgical specimens in both groups.
LAP resection group (n = 18) | Open resection group (n = 18) | Difference (P value) | |
Lymph nodes harvest | 7.8 ± 1.7 | 8.2 ± 2.3 | NS |
Specimen length (cm) | |||
LAR | 19.4 ± 3.2 | 21.2 ± 2.9 | NS |
APR | 27.3 ± 4.1 | 25.8 ± 3.0 | NS |
Distal resection margin (cm) | |||
LAR | 4.3 ± 1.1 | 4.6 ± 1.6 | NS |
Surgical margins | clear | clear |
Laparoscopic techniques for colonic resection were described in 1991[1,2], only 4 years after the introduction of laparoscopic cholecystectomy. Compared with conventional open surgery, laparoscopic surgery could offer a faster recovery, minimized postoperative ileums and pain, a shorter stay in hospital and a quicker return to normal activity[9,10]. However, the better appearance was secondary in importance compared with recurrence and survival. Port site metastasis and lack of long-term data in oncological outcome for patients with laparoscopic resection of colorectal cancer are controversial issues.
The main controversies have centered on the oncologic adequacy of laparoscopic resection in comparison with classic open surgery[11]. During laparoscopic resection, the colon and rectum can be mobilized by retraction of the bowel, using endoscopic graspers such as Bablocks, and the peritoneal attachments divided, using ultrasonic or electrocautery scissors. Our experiences show that the rectum can be excised with an intact mesorectal facial envelope all the way down to the level of the pelvic floor. The magnified views obtained deep in the pelvis at laparoscopy may facilitate accurate mesorectal dissection and vegetable nerve protection. Radical en bloc excision of the rectum and mesorectum, by low anterior resection or abdomino - perineal, has been the standard treatment for advanced rectal carcinoma[12,13].
Concerning with port-site recurrence, numerous experimental studies have been published since 1991. They have analyzed the possible role of pneumoperitoneum and carbon dioxide[14-20], the pathophysiology of minimally invasive techniques on tumor response and immunity[21,22]. In laparoscopic procedure, the tumor was removed through small incisions[23] in the abdominal wall or perineal, and this maneuver may theoretically lead to a risk of tumor contamination. To avoid port-site metastasis, Balli et al[24] described a routine to follow in colorectal cancer resection: fixation of trocars to the abdominal wall, high vascular ligation, isolation of specimens before extraction from the abdominal cavity, and intraperitoneal and trocar site irrigation with a tumoricidai solution. With improved incision protection techniques, the reported port-site recurrence rate dropped rapidly. Zmora[25] reported a pot-site recurrence rate of 1% in a review of 1737 patients undergone laparoscopic colorectal resection for malignancy. Ramos et al[26] reported abdominal wall metastases in only 3 of 208 patients with a minimum follow-up period of 1 year. All recurrences were in patients with Duke’s C-stage carcinoma, and 2 of the 3 were found to have diffuse peritoneal carcinomatosis at the initial surgery. The port-site metastasis has not been a significant issue in the presence of adequate training and laparoscopic skills[27,28].
Moreover, laparoscopic surgery for rectal carcinoma should concern about the safety of the procedure, especially in low anterior resections for lower rectal carcinoma. The anastomotic leak rate reported in a larger series of laparoscopic anterior resection was consistently less than 10%, which was comparable to that of conventional open anterior resection[29,30]. In our present study, no anastamotic leak was found in laparoscopic resection group. However, the risks existed, especially in anterior resections for lower rectal carcinoma. For prevention of leakage, colorectal anastomosis must be tension-free and has a good blood supply. It was our routine to check the anastomosis for leaks in every case for laparoscopic low anterior resection. The pelvis was irrigated and filled with saline and the anastomosis was immersed. Then the rectum was insufflated with air, using a bulb syringe, for observing air bubbles. Pelvic drains were placed during all low anterior, abdominal perineal resections. Some authors have recommended protective ileostomy, and it might be used for low anterior resection in patients with borderline vascular status, malnutrition or neoadjuvant radiotherapy.
The stage I tumors (Duke’s A) do not invade beyond the muscularis propria and have no lymph node metastasis. For this reason, stage I tumors have been considered to be the best indication for laparoscopic colectomy, with a very low rate of conversion to laparotomy (0-1%)[31], no port-site metastasis and no deaths were reported at long-term follow-up[32]. Adachi et al[33] found that the mean size of stage I tumors was 2.86 cm and that most tumors < 2 cm in size were free of both serosal invasion and lymph node metastasis. In such situations, because of the inability to palpate colonic tumors during laparoscopy, tumor localization must be precisely identified before resection is undertaken. On-table colonscopy at the time of surgery not only leads to prolonged operative time, but also makes further laparoscopic dissection impossible because of colonic distension. It is very helpful to use X-ray imaging at the time of preoperative colonoscopic examination to site small lesions accurately.
The rate of conversion to laparotomy ranged from 1.45% to 48% in literatures with a mean conversion rate of 15%[34,35]. Reasons for conversion to open surgery are difficulty to provide exposure or to identify anatomy because of the larger tumor size and relatively smaller pelvis. Abdominal obesity or presence of adhesions from previous surgery may compound this difficulty. The fixity of the tumor or invasion to adjacent organs at laparoscopy needed to convert to a formal laparotomy in order to complete the planned procedure[35,36]. The preoperative patient evaluation and surgeon’s experience are important predictive factors as confirmed in our study.
Laparoscopic colorectal surgery invariably takes longer time than a corresponding open procedure. Again, operating time is reduced with increased laparoscopic experience. Our study also confirmed the low rate of postoperative complications after minimally invasive procedures. Postoperative ileum, urinary retention, and wound infections occurred less frequently than that in the open resection group. These advantages have also been confirmed by many authors[37,38].
Repeated evidences have indicated that a laparoscopic approach in colorectal cancer has several advantages including a shorter hospital stay, less pain, a better appearance and decreased postoperative analgesia requirements. In fact, laparoscopic surgery has been found to be associated with significantly decreased intraoperative blood loss and postoperative complications as well[39,40]. Furthermore, theoretic advantages of less physiologic trauma and immunologic suppression have recently received more attention in the literatures[38,41]. A less intensive inflammatory response has also been demonstrated after laparoscopic surgery compared with conventional open surgery. The results of the present study showed that laparoscopic approaches to rectal carcinoma did not compromise early postoperative recovery.
Advanced rectal tumors accounted for 83.3% of the cases in our study. However, no long-term follow-up has been available at this time. Cammpault[42] reported a 5-year survival rate of 60.7% in colorectal cancer patients with laparoscopic resection, with no difference compared with the open resection (62.5%). Recently, Franklin et al reported the results of laparoscopic colectomy in 50 consecutive patients with stage III colorectal cancer, which was performed at a single hospital. The overall survival rates at 3 and 5 years were 54.5% and 38.5%, respectively, and the cancer-adjusted survival rates were 60.8% and 49%[43].
For low rectal lesions laparoscopy-assisted abdominoperineal resection (28.6% in our series) also allowed earlier postoperative recovery, with an equivalent tumor clearance, morbidity, mortality, disease-free interval, and duration of survival[10].
To date, all reported comparative nonrandomized studies and randomized studies have shown no difference in recurrence and survival rates with laparoscopic versus open colorectal resection, and a lower overall morbidity with laparoscopic procedure[10].
In conclusion, our results suggest that laparoscopic resection for rectal cancer can be performed safely and without compromising oncological principles. There are definitely perioperative
advantages with laparoscopic surgery.
Edited by Zhao M and Wang XL Proofread Xu FM
1. | Cooperman AM, Katz V, Zimmon D, Botero G. Laparoscopic colon resection: a case report. J Laparoendosc Surg. 1991;1:221-224. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 83] [Cited by in F6Publishing: 85] [Article Influence: 2.6] [Reference Citation Analysis (0)] |
2. | Saclarides TJ, Ko ST, Airan M, Dillon C, Franklin J. Laparoscopic removal of a large colonic lipoma. Report of a case. Dis Colon Rectum. 1991;34:1027-1029. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 45] [Cited by in F6Publishing: 47] [Article Influence: 1.4] [Reference Citation Analysis (0)] |
3. | Hartley JE, Monson JR. The role of laparoscopy in the multimodality treatment of colorectal cancer. Surg Clin North Am. 2002;82:1019-1033. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 14] [Cited by in F6Publishing: 15] [Article Influence: 0.7] [Reference Citation Analysis (0)] |
4. | Cirocco WC, Schwartzman A, Golub RW. Abdominal wall recurrence after laparoscopic colectomy for colon cancer. Surgery. 1994;116:842-846. [PubMed] [Cited in This Article: ] |
5. | Wexner SD, Cohen SM. Port site metastases after laparoscopic colorectal surgery for cure of malignancy. Br J Surg. 1995;82:295-298. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 386] [Cited by in F6Publishing: 371] [Article Influence: 12.8] [Reference Citation Analysis (0)] |
6. | Lacy AM, Delgado S, García-Valdecasas JC, Castells A, Piqué JM, Grande L, Fuster J, Targarona EM, Pera M, Visa J. Port site metastases and recurrence after laparoscopic colectomy. A randomized trial. Surg Endosc. 1998;12:1039-1042. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 141] [Cited by in F6Publishing: 150] [Article Influence: 5.8] [Reference Citation Analysis (0)] |
7. | Slanetz CA. Effect of no touch isolation on survival and recurrence in curative resections for colorectal cancer. Ann Surg Oncol. 1998;5:390-398. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 25] [Cited by in F6Publishing: 27] [Article Influence: 1.0] [Reference Citation Analysis (0)] |
8. | Heald RJ, Husband EM, Ryall RD. The mesorectum in rectal cancer surgery--the clue to pelvic recurrence? Br J Surg. 1982;69:613-616. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 1985] [Cited by in F6Publishing: 1863] [Article Influence: 44.4] [Reference Citation Analysis (1)] |
9. | Monson JR, Darzi A, Carey PD, Guillou PJ. Prospective evaluation of laparoscopic-assisted colectomy in an unselected group of patients. Lancet. 1992;340:831-833. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 202] [Cited by in F6Publishing: 167] [Article Influence: 5.2] [Reference Citation Analysis (0)] |
10. | Yamamoto S, Watanabe M, Hasegawa H, Kitajima M. Prospective evaluation of laparoscopic surgery for rectosigmoidal and rectal carcinoma. Dis Colon Rectum. 2002;45:1648-1654. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 55] [Cited by in F6Publishing: 57] [Article Influence: 2.6] [Reference Citation Analysis (0)] |
11. | Baker RP, White EE, Titu L, Duthie GS, Lee PW, Monson JR. Does laparoscopic abdominoperineal resection of the rectum compromise long-term survival? Dis Colon Rectum. 2002;45:1481-1485. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 36] [Cited by in F6Publishing: 38] [Article Influence: 1.7] [Reference Citation Analysis (0)] |
12. | Reis Neto JA, Quilici FA, Cordeiro F, Reis JA, Kagohara O, Simões Neto J. Laparoscopic total mesorectum excision. JSLS. 2002;6:163-167. [PubMed] [Cited in This Article: ] |
13. | Morino M, Parini U, Giraudo G, Salval M, Brachet Contul R, Garrone C. Laparoscopic total mesorectal excision: a consecutive series of 100 patients. Ann Surg. 2003;237:335-342. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 125] [Cited by in F6Publishing: 229] [Article Influence: 10.9] [Reference Citation Analysis (0)] |
14. | Scheidbach H, Schneider C, Konradt J, Bärlehner E, Köhler L, Wittekind Ch, Köckerling F. Laparoscopic abdominoperineal resection and anterior resection with curative intent for carcinoma of the rectum. Surg Endosc. 2002;16:7-13. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 120] [Cited by in F6Publishing: 128] [Article Influence: 5.8] [Reference Citation Analysis (0)] |
15. | Nelson H. Laparoscopic colectomy for colon cancer--a trial update. Swiss Surg. 2001;7:248-251. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 12] [Cited by in F6Publishing: 15] [Article Influence: 0.7] [Reference Citation Analysis (0)] |
16. | Lujan HJ, Plasencia G, Jacobs M, Viamonte M, Hartmann RF. Long-term survival after laparoscopic colon resection for cancer: complete five-year follow-up. Dis Colon Rectum. 2002;45:491-501. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 56] [Cited by in F6Publishing: 61] [Article Influence: 2.8] [Reference Citation Analysis (0)] |
17. | Wexner SD, Sands DR. What's new in colon and rectal surgery. J Am Coll Surg. 2003;196:95-103. [DOI] [Cited in This Article: ] [Cited by in Crossref: 8] [Cited by in F6Publishing: 8] [Article Influence: 0.4] [Reference Citation Analysis (0)] |
18. | Chung CC, Ha JP, Tsang WW, Li MK. Laparoscopic-assisted total mesorectal excision and colonic J pouch reconstruction in the treatment of rectal cancer. Surg Endosc. 2001;15:1098-1101. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 43] [Cited by in F6Publishing: 43] [Article Influence: 1.9] [Reference Citation Analysis (0)] |
19. | Ishida H, Murata N, Idezuki Y. Increased insufflation pressure enhances the development of liver metastasis in a mouse laparoscopy model. World J Surg. 2001;25:1537-1541. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 9] [Cited by in F6Publishing: 10] [Article Influence: 0.4] [Reference Citation Analysis (0)] |
20. | Tomita H, Marcello PW, Milsom JW, Gramlich TL, Fazio VW. CO2 pneumoperitoneum does not enhance tumor growth and metastasis: study of a rat cecal wall inoculation model. Dis Colon Rectum. 2001;44:1297-1301. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 16] [Cited by in F6Publishing: 20] [Article Influence: 0.9] [Reference Citation Analysis (0)] |
21. | Basu A, Wexner SD, Bergamaschi R. Validity of current experimental evidence on laparoscopic surgery for colorectal cancer. Surg Endosc. 2003;17:179. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 4] [Cited by in F6Publishing: 4] [Article Influence: 0.2] [Reference Citation Analysis (0)] |
22. | Mehigan BJ, Hartley JE, Drew PJ, Saleh A, Dore PC, Lee PW, Monson JR. Changes in T cell subsets, interleukin-6 and C-reactive protein after laparoscopic and open colorectal resection for malignancy. Surg Endosc. 2001;15:1289-1293. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 33] [Cited by in F6Publishing: 31] [Article Influence: 1.3] [Reference Citation Analysis (0)] |
23. | Hackert T, Uhl W, Büchler MW. Specimen retrieval in laparoscopic colon surgery. Dig Surg. 2002;19:502-506. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 29] [Cited by in F6Publishing: 31] [Article Influence: 1.5] [Reference Citation Analysis (0)] |
24. | Balli JE, Franklin ME, Almeida JA, Glass JL, Diaz JA, Reymond M. How to prevent port-site metastases in laparoscopic colorectal surgery. Surg Endosc. 2000;14:1034-1036. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 51] [Cited by in F6Publishing: 53] [Article Influence: 2.2] [Reference Citation Analysis (0)] |
25. | Zmora O, Gervaz P, Wexner SD. Trocar site recurrence in laparoscopic surgery for colorectal cancer. Surg Endosc. 2001;15:788-793. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 63] [Cited by in F6Publishing: 71] [Article Influence: 3.1] [Reference Citation Analysis (0)] |
26. | Ramos JM, Gupta S, Anthone GJ, Ortega AE, Simons AJ, Beart RW. Laparoscopy and colon cancer. Is the port site at risk? A preliminary report. Arch Surg. 1994;129:897-89; discussion 900. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 125] [Cited by in F6Publishing: 125] [Article Influence: 4.2] [Reference Citation Analysis (0)] |
27. | Hazebroek EJ. COLOR: a randomized clinical trial comparing laparoscopic and open resection for colon cancer. Surg Endosc. 2002;16:949-953. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 189] [Cited by in F6Publishing: 202] [Article Influence: 9.2] [Reference Citation Analysis (0)] |
28. | Lumley J, Stitz R, Stevenson A, Fielding G, Luck A. Laparoscopic colorectal surgery for cancer: intermediate to long-term outcomes. Dis Colon Rectum. 2002;45:867-72; discussion 872-5. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 70] [Cited by in F6Publishing: 72] [Article Influence: 3.3] [Reference Citation Analysis (0)] |
29. | Pera M, Delgado S, García-Valdecasas JC, Pera M, Castells A, Piqué JM, Bombuy E, Lacy AM. The management of leaking rectal anastomoses by minimally invasive techniques. Surg Endosc. 2002;16:603-606. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 28] [Cited by in F6Publishing: 29] [Article Influence: 1.3] [Reference Citation Analysis (0)] |
30. | Scheidbach H, Schneider C, Huegel O, Bärlehner E, Konradt K, Wittekind C, Köckerling F. Laparoscopic sigmoid resection for cancer: curative resection and preliminary medium-term results. Dis Colon Rectum. 2002;45:1641-1647. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 19] [Cited by in F6Publishing: 19] [Article Influence: 0.9] [Reference Citation Analysis (0)] |
31. | Kakisako K, Sato K, Adachi Y, Shiraishi N, Miyahara M, Kitano S. Laparoscopic colectomy for Dukes A colon cancer. Surg Laparosc Endosc Percutan Tech. 2000;10:66-70. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 8] [Cited by in F6Publishing: 8] [Article Influence: 0.3] [Reference Citation Analysis (0)] |
32. | Franklin ME, Rosenthal D, Abrego-Medina D, Dorman JP, Glass JL, Norem R, Diaz A. Prospective comparison of open vs. laparoscopic colon surgery for carcinoma. Five-year results. Dis Colon Rectum. 1996;39:S35-S46. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 304] [Cited by in F6Publishing: 305] [Article Influence: 10.9] [Reference Citation Analysis (0)] |
33. | Adachi Y, Sato K, Shiraishi N, Kakisako K, Tanimura H, Kitano S. Tumor size of colorectal cancer: indication for laparoscopic surgery. Surg Laparosc Endosc. 1998;8:269-272. [DOI] [Cited in This Article: ] |
34. | Yong L, Deane M, Monson JR, Darzi A. Systematic review of laparoscopic surgery for colorectal malignancy. Surg Endosc. 2001;15:1431-1439. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 28] [Cited by in F6Publishing: 31] [Article Influence: 1.3] [Reference Citation Analysis (0)] |
35. | Gervaz P, Pikarsky A, Utech M, Secic M, Efron J, Belin B, Jain A, Wexner S. Converted laparoscopic colorectal surgery. Surg Endosc. 2001;15:827-832. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 128] [Cited by in F6Publishing: 120] [Article Influence: 5.2] [Reference Citation Analysis (0)] |
36. | Baker RP, White EE, Titu L, Duthie GS, Lee PW, Monson JR. Does laparoscopic abdominoperineal resection of the rectum compromise long-term survival? Dis Colon Rectum. 2002;45:1481-1485. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 36] [Cited by in F6Publishing: 38] [Article Influence: 1.7] [Reference Citation Analysis (0)] |
37. | Weeks JC, Nelson H, Gelber S, Sargent D, Schroeder G. Short-term quality-of-life outcomes following laparoscopic-assisted colectomy vs open colectomy for colon cancer: a randomized trial. JAMA. 2002;287:321-328. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 547] [Cited by in F6Publishing: 518] [Article Influence: 23.5] [Reference Citation Analysis (0)] |
38. | Wu FP, Sietses C, von Blomberg BM, van Leeuwen PA, Meijer S, Cuesta MA. Systemic and peritoneal inflammatory response after laparoscopic or conventional colon resection in cancer patients: a prospective, randomized trial. Dis Colon Rectum. 2003;46:147-155. [DOI] [Cited in This Article: ] [Cited by in Crossref: 126] [Cited by in F6Publishing: 120] [Article Influence: 5.7] [Reference Citation Analysis (0)] |
39. | Hasegawa H, Kabeshima Y, Watanabe M, Yamamoto S, Kitajima M. Randomized controlled trial of laparoscopic versus open colectomy for advanced colorectal cancer. Surg Endosc. 2003;17:636-640. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 151] [Cited by in F6Publishing: 146] [Article Influence: 7.0] [Reference Citation Analysis (0)] |
40. | Lacy AM, Garcia-Valdecasas JC, Delgado S, Castells A, Taura P, Pique JM, Visa J. Laparoscopic colectomy versus open colec-tomy for treatment of non-metastatic colon cancer: a radomised trail. Lancet. 2002;29:2224-2229. [DOI] [Cited in This Article: ] [Cited by in Crossref: 1901] [Cited by in F6Publishing: 1785] [Article Influence: 81.1] [Reference Citation Analysis (0)] |
41. | Allendorf JD, Bessler M, Whelan RL, Trokel M, Laird DA, Terry MB, Treat MR. Better preservation of immune function after laparoscopic-assisted vs. open bowel resection in a murine model. Dis Colon Rectum. 1996;39:S67-S72. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 80] [Cited by in F6Publishing: 82] [Article Influence: 2.9] [Reference Citation Analysis (0)] |
42. | Champault GG, Barrat C, Raselli R, Elizalde A, Catheline JM. Laparoscopic versus open surgery for colorectal carcinoma: a prospective clinical trail involving 157 cases with a mean follow-up of 5 years. Surg Laparosc Endosc Percutan Tech. 2002;12:88-95. [DOI] [Cited in This Article: ] [Cited by in Crossref: 29] [Cited by in F6Publishing: 31] [Article Influence: 1.4] [Reference Citation Analysis (0)] |
43. | Franklin ME, Kazantsev GB, Abrego D, Diaz-E JA, Balli J, Glass JL. Laparoscopic surgery for stage III colon cancer: long-term follow-up. Surg Endosc. 2000;14:612-616. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 82] [Cited by in F6Publishing: 85] [Article Influence: 3.5] [Reference Citation Analysis (0)] |