Int J Clin Exp Med 2014;7(12):4635-4645 www.ijcem.com /ISSN:1940-5901/IJCEM0002677
Review Article Laparoscopic surgery for colorectal cancer in China: an overview Ketao Jin1*, Jun Wang2*, Huanrong Lan1*, Ruili Zhang1 Department of Gastrointestinal Surgery and Laboratory of Translational Oncology, Public Research Platform, Taizhou Hospital, Wenzhou Medical University, Linhai 317000, Zhejiang, P.R. China; 2Department of Gynecology and Obstetrics and Laboratory of Translational Oncology, Public Research Platform, Taizhou Hospital, Wenzhou Medical University, Linhai 317000, Zhejiang, P.R. China. *Equal contributors. 1
Received September 21, 2014; Accepted November 25, 2014; Epub December 15, 2014; Published December 30, 2014 Abstract: Since its introduction into China in 2001, laparoscopic techniques have been extensively used for the surgical management of colorectal cancer during the last two decades in China. Like all the pioneers of the technique, Chinese gastrointestinal surgeons claim that laparoscopic surgery for colorectal cancer led to faster recovery, shorter hospital stay and more rapid return to daily activities respect to open surgery while offering the same functional and oncological results. There has been booming interest in laparoscopic surgery for colorectal cancer since 2006 in China. The last decade has witnessed national growth in the application of laparoscopic surgery for colorectal cancer and yielded a significant amount of scientific data to support its clinical merits and advantages. However, few prospective randomized controlled trials have investigated the benefits of laparoscopic surgery for colorectal cancer in China. In this article, we make an overview of the current data and state of the art of laparoscopic surgery for colorectal cancer in China. Keywords: Colon cancer, rectal cancer, laparoscopic surgery, review
Introduction Colorectal cancer is one of the leading causes of mortality worldwide [1]. Traditionally, cancers of the colon were removed through large abdominal incisions. Since the advent of laparoscopic surgery, it has become clear that patients benefit from a minimally invasive approach in a variety of ways [2]. In 1991, laparoscopic-assisted colectomy was first reported [3, 4]. Due to the development of minimally invasive techniques, the majority of colorectal procedures can be performed using a laparoscopic approach, and the indications for laparoscopic surgery have gradually expanded [5, 6]. A number of available prospectively randomized trials and meta-analyses of laparoscopic surgery for colorectal cancer [7-12] reported that laparoscopic-assisted colorectal surgery exhibited improved post-operative results, including less pain, a smaller incision, a faster recovery of gastrointestinal function, a shorter post-operative hospital stay and similar longterm survival, compared with those of open
colorectal surgery [13, 14]. Therefore, laparoscopic-assisted surgery has been widely accepted as an alternative to conventional open surgery for colorectal cancer. Because of the potential advantages, such as less invasiveness and postoperative pain, earlier recovery, better cosmetic results, milder morbidity, earlier time to walking, flatus, and oral intake, and quicker recovery with a shorter hospital stay, laparoscopic surgery for colorectal cancer was introduced into clinical practice in China in 2001 [15], and was gradually implemented and is now commonplace in China. There has been booming interest in laparoscopic surgery for colorectal cancer since it was first described in 2001 [15]. The last decade has witnessed national growth in the application of laparoscopic surgery for colorectal cancer yielding a significant amount of scientific data to support its clinical merits and advantages. With the development of laparoscopic techniques and the invention of new surgical equipments, scarless surgery is becoming increasingly popu-
Laparoscopic surgery for colorectal cancer in China English. However, 70 relevant reports (44.3%) have been written in Chinese. It is compelled to unveil the current status of laparoscopic surgery for colorectal cancer in China to the wider surgical fraternity based on the scientific data both in English and in Chinese. Pronounced rise in a number of articles dedicated to laparoscopic surgery for colorectal cancer is observed from 2009 to 2014, this probably corresponds both to an increased research interest of surgical community and to a wider clinical application of this patient-friendly approach. Figure 1. Numbers of full papers related to laparoscopic surgery for colorectal cancer in China (PubMed/Medline database).
lar. In single-incision laparoscopic surgery (SILS), also termed single-port laparoscopic surgery, the surgeon operates through a single entry point with a single incision of only 25-30 mm. Another innovation is natural orifice specimen extraction (NOSE). For this procedure, the specimen is extracted from a natural orifice such as the vagina or anus; therefore, an additional incision in the abdominal wall is not needed. The final innovation is natural orifice transluminal endoscopic surgery (NOTES). NOTES is the only type of surgery that lacks scarring of the abdominal wall, thus, NOTES may represent the next step in the evolution of mini-invasive surgery. Robotic surgery is an emerging technology that provides 3-dimensional imaging, tremor filtration, and motion scaling. With these advantages, robotic rectal cancer resection may overcome the limitations of conventional laparoscopic surgery. This article made an overview of the current data and state of the art for laparoscopic surgery for colorectal cancer in China. Literature of laparoscopic surgery for colorectal cancer in China Current literature was reviewed by searching PubMed/Medline database (from January 2001 to July 2014). A hundred and fifty-eight full articles were found to be relevant to laparoscopic surgery for colorectal cancer (Figure 1). A total of 88 (55.7%) publications were in 4636
Operative data of laparoscopic surgery for colorectal cancer
One hundred and seventeen suitable papers, consisting of prospective and retrospective studies, were identified [16-131]. Key outcomes of major studies written in English are summarized in the Tables 1 and 2 [16, 17, 19, 21-25, 27, 30-32, 35-37, 39-43, 45, 46, 48, 49, 50-52, 54, 56, 57, 63, 65, 66, 68, 69-71, 73-75, 79, 82-84, 89, 90-92, 95, 97, 99, 104, 107-114, 116, 118, 121, 122, 125-130]. Twenty nine of these were performed prospectively [24, 25, 30, 35, 42, 51, 63, 65, 66, 68, 73, 79, 83, 84, 89, 91, 97, 99, 104, 109, 110, 116, 118, 121, 125, 127-130 ], in which nine studies were prospective randomized controlled trials [30, 35, 63, 65, 73, 83, 99, 116, 127]. Common outcome measures includes operative data (operative time, estimated blood loss and conversion rate), short-term outcomes (days to liquid diet, days to flatus, and total hospital stay), complications (anastomotic stenosis, anastomotic bleeding, and anastomotic leakage), postoperative mortality data, overall survival, disease-free survival and follow-up period. Surgical approaches Surgical approaches of laparoscopic surgery for colorectal cancer performed by Chinese gastrointestinal surgeons are listed in Table 1, which includes multiport laparoscopic surgery (MLS), single-incision laparoscopic surgery (SILS), natural orifice specimen extraction (NOSE), natural orifice transluminal endoscopic Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China Table 1. Survey over major reports of laparoscopic surgery for colorectal cancer in China: operative data (Articles in English) Ref. [16]
PS/RS RS
Patient (n) 197
Approaches NOSE/MLS
TME Yes
[17] [19] [21] [23] [24] [25] [27] [30]
RS RS RS RS PS PS RS PS
119 80 289 24 21 51 64 70
Yes Yes Yes Yes Yes Yes Yes Yes
[32] [39] [45] [48] [51] [52] [51] [63] [66] [68] [73] [75] [82] [83]
RS RS RS RS PS RS RS PS PS PS PS RS RS PS
87 67 177 381 189 34 889 30 125 814 71 254 113 169
MLS MLS MLS NOSE NOSE MLS MLS 35 in NOTES; 35 in MLS MLS MLS MLS MLS MLS NOTES MLS MLS MLS MLS MLS MLS MLS MLS
Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes
LN 17.0 ± 8.3 in NOSE; 18.9 ± 11.6 in MLS 22.3 ± 8.6 11.86 ± 1.95 NA NA 17.8 ± 4.6 NA 11.68 ± 5.69 12 (6-33) in NOTES; 12 (6-29) in MLS 14 ± 5 20.3 ± 8.3 15.2 ± 10.1 12.5 ± 4.2 NA 12.92 ± 2.2 12.27 ± 9.02 16 (2-33) NA 13 (8-18) 18.7 ± 12 12.0 ± 6.9 20.3 ± 6.9 7.05 ± 5.05
NeoA No NA No NA NA NA Yes No NA NA NA No NA NA NA NA NA Yes NA NA No No No
OT (min) 111.6 ± 25.4 in NOSE; 115.3 ± 23.0 in MLS 257.8 ± 67.6 201.7 ± 6.91 155 ± 29 110.0 132 ± 85 181.5 (95.0-310.0) 183 ± 55 105 (60-170) in NOTES; 100 (59-210) in MLS 160 ± 40 216.4 ± 68.3 133 ± 36 176.4 ± 28.3 150 (81–360) 151.6 ± 25.93 201.66 ± 81.81 111 (74-165) NA 180 (141-218) 198 ± 48 135.6 ± 40.0 210.0 (100-420) 138.08 ± 23.79
BL (ml) 70.2 ± 66.1 in NOSE; 126.3 ± 58.6 in MLS 100 (100-200) 97.25 ± 9.97 128 ± 24 69.1 mL 84 ± 15 204.7 (80.0-1000.0) 168 ± 106 30 (10-50) in NOTES; 30 (10-100) in MLS 28 ± 5 86.9 ± 37.6 94 ± 34 58.3 ± 13.9 100 (0-1,000) 200.2 ± 114.69 100 20 (5-400) NA 100 (50-200) 110.1 (0-1,000) 101.5 ± 70.8 50.0 (0-1200) NA
C n (%) NA 9 (7.6) 1 (1.3) NA NA NA NA NA NA NA NA 5 (2.82) NA NA 0 43 (4.84) 1 (3.3) NA NA NA 8 (3) NA NA
Abbreviations: Ref., reference; PS, prospective study; RS, retrospective study; MLS, multiport laparoscopic surgery; NOSE, natural orifice specimen extraction; NOTES, natural orifice transluminal endoscopic surgery; RH, right hemicolectomy; TME, total mesorectal excision; LH, left hemicolectomy; SC, sigmoid colectomy; LAR, low anterior resection; AR, Abdominoperineal resection; TC, total colectomy; LN, number of lymph node harvested; NeoA, neoadjuvant chemotherapy; OT, operation time. BL, estimated blood loss; C, conversion rate; NA, data not available.
4637
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China surgery (NOTES), and totally laparoscopic surgery (TLS) for colorectal cancer. In our center, we had adopted MLS, SILS, and TLS. Operative time and blood loss Operative time varies significantly between the studies reflecting to type of performed laparoscopic surgery for colorectal cancer and accumulated experience/technical skills (Table 1). The estimated blood loss varies significantly from centre to centre and comprises around 10-1000 ml (Table 1). Major blood loss and need to blood transfusion in particular increase a risk of postoperative morbidity and mortality. Conversion to open surgery The conversion rate reported in the literature is in a range of 0-7.6% (Table 1). However, with surgical experience the conversion rate reduces and currently has no conversion to open surgery in expert centers in China. The main reason to conversion was bleeding. It is not appropriate to consider conversion from laparoscopic surgery to open surgery for colorectal cancer as a failure because patient’s safety and oncologic integrity of the procedure should be of supreme importance. Mortality, morbidity and postoperative complications Postoperative mortality rates following laparoscopic surgery for colorectal cancer vary between 0 to 11.8% (Table 2). Anastomotic stenosis, anastomotic bleeding, anastomotic leakage are the most feared complications in laparoscopic surgery for colorectal cancer. From the operative data, anastomotic stenosis rate ranged between 0 and 1.3%, anastomotic bleeding rate ranged between 0 and 7.8%, and anastomotic leakage rate ranged between 0 and 9.0% (Table 2). Laparoscopic surgery for colorectal cancer is associated with significant reduction in hospital stay. Postoperative hospital stay comprises 9.0 days in average (Table 2). Outcomes There are 26 studies reported the survival data of laparoscopic surgery for colorectal cancer in China [17, 19, 27, 35, 45, 48-51, 57, 63, 66, 68, 70, 73, 75, 79, 82, 83, 90, 95, 97, 107, 109, 125, 126]. Sixteen studies reported the 4638
long-term overall survival of laparoscopic surgery for colorectal cancer [35, 45, 48, 50, 51, 57, 63, 66, 68, 73, 83, 95, 97, 107, 109, 125]. Ng KH, et al. reported the long-term survival of laparoscopic rectal cancer resection at a single institution with 579 cases over a 15-year period. They reported the overall 5- and 10-year survivals for rectal cancer were 70% and 45.5%, respectively and the cancer-specific 5and 10-year survival was 76% and 56%, respectively [107]. Robotic surgery for colorectal cancer Though laparoscopic surgery for colorectal cancer offers a number of patient benefits compared to open surgery, such as less invasiveness and pain, speedier recovery, better cosmetic results, milder morbidity, earlier time to walking, flatus, and oral intake, and quicker recovery with a shorter hospital stay, several limitations and disadvantages are associated with conventional laparoscopic surgery. An important reason for this is the steep learning curve of this technique. In addition, some other limitations that hinder the development of laparoscopic surgery include tremor, 2-dimensional vision, poor ergonomics, the need of a skilled assistant, and the limited degrees of freedom of the instruments. In an effort to minimize the difficulty of laparoscopy, a robotic surgery system was introduced in China in 2005 [114]. Robotic surgery is thought to be able to overcome these limitations by providing 3-dimensional vision, 7 degrees of freedom of the instruments, enhanced ergonomics, tremor filtration, and superior dexterity [42, 80]. These advantages of robotic surgery make it extremely suitable for pelvic dissection, especially for patients with a narrow pelvis and/or local advanced disease and especially important for complex procedures, such as the dissection of lymph nodes around major vessels because of its tremor filtration and superior dexterity. Robotic surgery has many advantages over laparoscopic surgery, but some limitations in the current robotic technology still exist. When compared to conventional laparoscopic surgery, robotic surgery is associated with longer operation time, higher cost, and lacks tactile sensation and tensile feedback for the surgeon. Meanwhile, the limited data of the current work in China are preliminary and retrospective studies from single clinical center with Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China Table 2. Survey over major reports of laparoscopic surgery for colorectal cancer in China: Outcomes (Article in English) Ref.
Patient (n)
[16]
[17]
F
De
197
2.7 ± 0.8 in NOSE; 3.4 ± 0.9 in MLS
119
[19] [21] [23]
IC (n, %)
PC (n, %)
MH
OI
IL
AS
AB
3.3 ± 0.6 in NOSE; 3.9 ± 1.1 in MLS
NA
NA
NA
NA
NA
2.7 ± 1.0
NA
NA
NA
80
2.34 ± 0.12
NA
289
NA
NA
NA
NA
NA
NA
NA
24
3.1
NA
NA
NA
NA
NA
[24]
21
NA
NA
NA
NA
NA
[25]
51
2.5 (1.5-4.0)
4.0 (2.0-8.0)
NA
NA
[27]
64
NA
NA
NA
[30]
70
NA
NA
[32]
87
NA
NA
[39]
67
46.9 ± 14.8
[45]
177
[48] [51]
4 (3.4) 1 (0.8) 1 (0.8)
AL
HS (d)
2 (3.1) in NOSE; 9.0 ± 1.9 in NOSE; 6 (4.5) in MLS 9.9 ± 2.0 in MLS
M n (%)
FP (m)
OSR (%)
DFSR (%)
NA
NA
NA
NA
2 (1.7)
11.4 ± 4.7
1 (0.8)
30 (3-60)
92.0% in 3 years
84.6% in 3 years
NA
9.7 ± 0.59
NA
17.5
NA
NA
NA
8.9 ± 2.1
NA
NA
NA
NA
NA
NA
9.2
NA
NA
NA
NA
NA
0
1 (4.7)
6.1 ± 2.7
NA
12
NA
NA
NA
NA
NA
1 (3.1)
NA
6 (11.8)
NA
NA
NA
NA
5 (8)
NA
NA
3 (5)
12 (6‑39)
NA
17
38.7 ± 2.7
37.3 ± 2.5
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
1 (1.1)
5.2 ± 1.8
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
1 (1.4)
10.4 ± 4.3
NA
NA
NA
NA
2.1 ± 0.7 (2-5)
NA
NA
NA
3 (1.69)
NA
NA
7 (3.95)
10.4 ± 2.7 (7-27)
NA
54 (15-104)
97.18% in 1 year; 83.73% in 3 years 70.37% in 5 years; 68.99% in 6 years
NA
381
2.5 ± 1.8
NA
NA
NA
NA
NA
NA
3 (0.8)
NA
NA
51 (13-87)
84.4% in 3 years; 68.4% in 5 years
NA
189
NA
NA
NA
NA
NA
NA
NA
NA
5 (2-63)
1 (0.5)
22.9
52.8 % in 5 years
68.9 % in 5 years
[52]
34
2 ± 0.49
NA
NA
NA
NA
NA
NA
NA
9 (7-66)
NA
NA
NA
NA
[51]
889
NA
NA
NA
NA
NA
NA
7 (7.8)
8 (9.0)
9.88 ± 5.93
NA
29
78.0% in 3 years; 69.0% in 5 years
NA
[63]
30
NA
NA
NA
NA
NA
NA
NA
0
7 (5-19)
NA
33 (2-55)
80.0% in 5 years
NA
[66]
125
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
38 (5-113)
71.3% for stage II; 51% for stage III
59.2% for stage II; 45.4% for stage III
[68]
814
NA
NA
NA
NA
32 (3.9)
NA
NA
15 (1.8)
NA
4 (0.5)
40.3
74.1% in 5 years
81.9% in 5 years
[73]
71
3 (1-10)
NA
NA
NA
NA
NA
NA
1 (1.4)
7.8 (4-20)
NA
104 (44-156)
100% in Stage I, 68.7% in stage II, and 74.5% in stage III in 5 years
NA
[75]
254
NA
NA
NA
NA
NA
NA
1 (0.4)
5 (2.0)
NA
NA
37.1 (8.2-62.5)
NA
NA
[82]
113
NA
NA
NA
NA
NA
NA
NA
8 (8.1)
9.0 (7-52)
1 (0.9)
76.0 ± 30.3
91.7% in stage I, 82.8% in stage II, 66.7% in stage III in 5 years
NA
[83]
169
NA
NA
NA
NA
NA
0
NA
4 (2.4)
NA
0
44 (1-72)
94.0% in 1 year; 82.6% in 2 years; 76.0% in 3 years
NA
1 (1.3) 1 (1.3) 1 (1.3) 1 (1.3) 2 (2.5)
Abbreviations: Ref., reference; LD, days to liquid diet; De, days to first defecation; F, days to first flatus; IC, intraoperative complications; PC, post‑operative complications; MH, massive hemorrhage > 500 ml; OI, Organ injury; IL, ileus; IA, intestinal adhesion; AS, anastomotic stenosis; AB, anastomotic bleeding; AL, anastomotic leakage; HS, hospital stay (day); M, postoperative mortality; FP (m), follow-up period (month); OSR, overall survival rate (%); DFSR, Disease-free survival rate (%); NA, data not available.
4639
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China small sample sizes. Multicenter, randomized, prospective trials are needed to compare the short-term and long-term outcomes of robotic surgery with those of conventional laparoscopic surgery. In conclusion, there is no compelling reason to bar our interested Chinese gastrointestinal surgeons from performing laparoscopic surgery for colorectal cancer provided that they have received adequate training from major centers. The techniques spread are growing in China, as confirmed by the elevating number of recently published papers on this subject. However, only nine prospective randomized controlled trials have investigated the benefits of laparoscopic surgery for colorectal cancer in China. More randomized controlled clinical trials directly comparing the laparoscopic surgery and open approaches in China would be preferable and are extremely needed. Acknowledgements This work was supported by National Natural Science Foundation of China (Grants No. 81374014 and No. 81472210), Zhejiang Provincial Medical and Healthy Science and Technology Projects (Grant No. 2013KYA228), Zhejiang Provincial Science and Technology Project (Grant No. 2013C33112), Science Research Fund of Taizhou (Grants No. A121KY08, A131KY13-3 and A131KY13-12), and Enze Medical Research Fund (Grants No. 12EZA1, 13EZA2 and 13EZB6).
[3] [4] [5]
[6]
[7]
[8]
[9]
[10]
Disclosure of conflict of interest None. Address correspondence to: Dr. Ruili Zhang, Department of Gastrointestinal Surgery and Laboratory of Translational Oncology, Public Research Platform, Taizhou Hospital, Wenzhou Medical University, 150 Ximen Road, Linhai 317000, Zhejiang, P.R. China. Tel: +86-576-85189199/+86-13806561091; Fax: +86-576-85189199; E-mail: jinketao2001@zju. edu.cn
References [1] [2]
Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013; 63: 1130. Barkun JS, Barkun AN, Sampalis JS, Fried G, Taylor B, Wexler MJ, Goresky CA, Meakins JL. Randomised controlled trial of laparoscopic
4640
[11]
[12]
[13]
[14]
versus mini cholecystectomy. The McGill Gallstone Treatment Group. Lancet 1992; 340: 1116-9. Cooperman AM, Katz V, Zimmon D, Botero G. Laparoscopic colon resection: a case report. J Laparoendosc Surg 1991; 1: 221-4. Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc 1991; 1: 144-50. Ku G, Tan IB, Yau T, Boku N, Laohavinij S, Cheng AL, Kang YK, de Lima Lopes G Jr. Management of colon cancer: resource-stratified guidelines from the Asian Oncology Summit 2012. Lancet Oncol 2012; 13: e470-81. Miyajima N, Fukunaga M, Hasegawa H, Tanaka J, Okuda J, Watanabe M; Japan Society of Laparoscopic Colorectal Surgery. Results of a multicenter study of 1,057 cases of rectal cancer treated by laparoscopic surgery. Surg Endosc 2009; 23: 113-8. Abraham NS, Young JM, Solomon MJ. Metaanalysis of short-term outcomes after laparoscopic resection for colorectal cancer. Br J Surg 2004; 91: 1111-24. Aziz O, Constantinides V, Tekkis PP, Athanasiou T, Purkayastha S, Paraskeva P, Darzi AW, Heriot AG. Laparoscopic versus open surgery for rectal cancer: a meta-analysis. Ann Surg Oncol 2006; 13: 413-24. Neudecker J, Klein F, Bittner R, Carus T, Stroux A, Schwenk W; LAPKON II Trialists. Short-term outcomes from a prospective randomized trial comparing laparoscopic and open surgery for colorectal cancer. Br J Surg 2009; 96: 145867. Levy BF, Tilney HS, Dowson HM, Rockall TA. A systematic review of postoperative analgesia following laparoscopic colorectal surgery. Colorectal Dis 2010; 12: 5-15. Colon Cancer Laparoscopic or Open Resection Study Group; Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, Haglind E, Påhlman L, Cuesta MA, Msika S, Morino M, Lacy A, Bonjer HJ. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 2009; 10: 44-52. Braga M, Frasson M, Zuliani W, Vignali A, Pecorelli N, Di Carlo V. Randomized clinical trial of laparoscopic versus open left colonic resection. Br J Surg 2010; 97: 1180-6. Biondi A, Grosso G, Mistretta A, Marventano S, Toscano C, Gruttadauria S, Basile F. Laparoscopic-assisted versus open surgery for colorectal cancer: short- and long-term outcomes comparison. J Laparoendosc Adv Surg Tech A 2013; 23: 1-7. Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically as-
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
sisted and open colectomy for colon cancer. N Engl J Med 2004; 350: 2050-9. 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: 1098-101. Xingmao Z, Haitao Z, Jianwei L, Huirong H, Junjie H, Zhixiang Z. Totally laparoscopic resection with natural orifice specimen extraction (NOSE) has more advantages comparing with laparoscopic-assisted resection for selected patients with sigmoid colon or rectal cancer. Int J Colorectal Dis 2014; 29: 1119-24. Zhao LY, Chi P, Ding WX, Huang SR, Zhang SF, Pan K, Hu YF, Liu H, Li GX. Laparoscopic vs open extended right hemicolectomy for colon cancer. World J Gastroenterol 2014; 20: 792632. Ju H, Huang X, Zhu Y, Feng H, Li D. [Comparison of short-term outcomes of hand-assisted laparoscopic, laparoscopic, and open surgery in the treatment of rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2014; 17: 574-7. Chinese. Chen K, Zhang Z, Zuo Y, Ren S. Comparison of the clinical outcomes of laparoscopic-assisted versus open surgery for colorectal cancer. Oncol Lett 2014; 7: 1213-1218. Qin C, Li Q, Fu K, Meng J, Ren X. [Experiences of scarless laparoscopic radical resection of rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2014; 17: 486-8. Chinese. Chen T, Fang J, Wang Z, Zheng Z, Huang J, Wei B, Wei H. Laparoscopic Surgery Decreases the Surgical Risks Associated With Hyperlipidemia in Rectal Cancer: Retrospective Analysis of 495 Patients. Surg Laparosc Endosc Percutan Tech 2014; [Epub ahead of print] Cong JC, Chen CS, Ma MX, Xia ZX, Liu DS, Zhang FY. Laparoscopic intersphincteric resection for low rectal cancer: comparison of stapled and manual coloanal anastomosis. Colorectal Dis 2014; 16: 353-8. Zhang X, Zhou H, Hou H, Hu J, Wang H, Zhou Z. Totally laparoscopic resection with natural orifice specimen extraction for carcinoma of sigmoid colon and rectum: a feasible and innovative technique. J Clin Gastroenterol 2014; 48: e57-61. Han FH, Hua LX, Zhao Z, Wu JH, Zhan WH. Transanal natural orifice specimen extraction for laparoscopic anterior resection in rectal cancer. World J Gastroenterol 2013; 19: 77517. Hu JJ, Liang JW, Wang Z, Zhang XM, Zhou HT, Hou HR, Zhou ZX. Short-term outcomes of laparoscopically assisted surgery for rectal cancer following neoadjuvant chemoradiotherapy: a
4641
[26]
[27]
[28]
[29]
[30]
[31]
[32]
[33]
[34]
[35]
[36]
[37]
single-center experience. J Surg Res 2014; 187: 438-44. Zhou HT, Zhou ZX, Liang JW, Wang Z, Zhang XM, Hu JJ. [Analysis of 21 cases treated by total laparoscopic rectosigmoid cancer surgery with transanal natural orifice specimen extraction]. Zhonghua Yi Xue Za Zhi 2013; 93: 20824. Chinese. Cai Y, Zhou Y, Li Z, Xiang J, Chen Z. Surgical outcome of laparoscopic colectomy for colorectal cancer in obese patients: A comparative study with open colectomy. Oncol Lett 2013; 6: 1057-1062. Wu GJ, Xiao G, Zhou XP, Zhao G, Jia WZ, Yu T, An Q, Yang H, Long HK, Huang MX. [Laparoscopic with extralevator abdominoperineal excision for low rectal carcinoma]. Zhonghua Yi Xue Za Zhi 2013; 93: 1921-3. Chinese. Liu Y, Lu XM, Niu YF, Tao KX, Wang GB. [Application of laparoscopic transanal coloanal anastomosis in sphincter-preserving surgery for low rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2013; 16: 727-9. Leung AL, Cheung HY, Fok BK, Chung CC, Li MK, Tang CN. Prospective randomized trial of hybrid NOTES colectomy versus conventional laparoscopic colectomy for left-sided colonic tumors. World J Surg 2013; 37: 2678-82. Zhu Z, Tan JW, Tan HM, Hu BS, Chen K, Ding XM, Leng JJ, Chen F. The preliminary experience in simultaneous treatment of rectal cancer and synchronous liver metastases with laparoscopy. Turk J Gastroenterol 2013; 24: 127-33. Yang Q, Xiu P, Qi X, Yi G, Xu L. Surgical margins and short-term results of laparoscopic total mesorectal excision for low rectal cancer. JSLS 2013; 17: 212-8. Zhao LY, Wang YN, Yu J, Deng HJ, Hu YF, Mou TY, Li GX. [The safety and long-term survival after laparoscopic surgery versus open surgery for colon cancer]. Zhonghua Wai Ke Za Zhi 2013; 51: 314-9. Zhou T, Zhang GJ, Liu ZL, Tian HP. [Laparoscopic versus open intersphincteric resection for low rectal cancer: a clinical comparative study]. Zhonghua Wei Chang Wai Ke Za Zhi 2013; 16: 565-9. Tung KL, Cheung HY, Ng LW, Chung CC, Li MK. Endo-laparoscopic approach versus conventional open surgery in the treatment of obstructing left-sided colon cancer: long-term follow-up of a randomized trial. Asian J Endosc Surg 2013; 6: 78-81. Wang Q, Wang C, Sun DH, Kharbuja P, Cao XY. Laparoscopic total mesorectal excision with natural orifice specimen extraction. World J Gastroenterol 2013; 19: 750-4. Xing-mao Z, Hui-rong H, Zi-nian W, Hong-ying W, Jun-jie H, Zheng W, Jian-wei L, Jian-jun B,
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48]
[49]
Hai-tao Z, Zhi-xiang Z. Age, is it an obstacle for older surgeons to learn laparoscopic approach for colorectal cancer? Med Oncol 2013; 30: 495. Xiao Y, Sun XY, Niu BZ, Zheng Y, Xiong GB, Xuan ZX, Zhang GN, Zhou JL, Wu B, Lin GL, Qiu HZ. [Acquiring laparoscopic skill for colorectal surgery: based on the experience of a colorectal surgeon]. Zhonghua Wai Ke Za Zhi 2012; 50: 1063-7. Gong J, Shi DB, Li XX, Cai SJ, Guan ZQ, Xu Y. Short-term outcomes of laparoscopic total mesorectal excision compared to open surgery. World J Gastroenterol 2012; 18: 7308-13. Wong TM, Day W, Kwok SY, Lau YY, Yip WC. Single incision laparoscopic right hemicolectomy: different approaches. Chin Med J (Engl) 2013; 126: 238-41. Chen G, Liu Z, Han P, Li JW, Cui BB. The learning curve for the laparoscopic approach for colorectal cancer: a single institution’s experience. J Laparoendosc Adv Surg Tech A 2013; 23: 17-21. Du XH, Shen D, Li R, Li SY, Ning N, Zhao YS, Zou ZY, Liu N. Robotic anterior resection of rectal cancer: technique and early outcome. Chin Med J (Engl) 2013; 126: 51-4. Hua-Feng P, Zhi-Wei J, Gang W, Xin-Xin L, FengTao L. A novel approach for the resection of low rectal cancer. Surg Laparosc Endosc Percutan Tech 2012; 22: 537-41. Zhou YH, Peng X, Deng JZ, Cheng LQ, Li ZC, Zhu JC, Guo XX. [Causes of anastomotic leakage after colorectal cancer laparoscopic-assisted surgery]. Zhonghua Yi Xue Za Zhi 2012; 92: 2553-5. Han DP, Lu AG, Feng H, Wang PX, Cao QF, Zong YP, Feng B, Zheng MH. Long-term results of laparoscopy-assisted radical right hemicolectomy with D3 lymphadenectomy: clinical analysis with 177 cases. Int J Colorectal Dis 2013; 28: 623-9. Chi P, Chen ZF, Lin HM, Lu XR, Huang Y. Laparoscopic extralevator abdominoperineal resection for rectal carcinoma with transabdominal levator transection. Ann Surg Oncol 2013; 20: 1560-6. Wang DG, Suo J, Zhang Y, Yu JH, Chen Y, He L, Sun X, Xia MJ. [Use of laparoscope complete mesocolic excision in the surgical treatment of right colon cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 971-3. Li Z, Ying X, Shen Y, Ye P, Pan W, Chen H. Laparoscopic versus open surgery for rectal cancer: a clinical comparative study. J Int Med Res 2012; 40: 1599-607. Wang L, Tan HM, Tan JW, Chu Y, Ding XM, Dong JH. Laparoscopic approach for simultaneous treatment of rectal cancer and synchronous
4642
[50]
[51]
[52]
[53]
[54]
[55]
[56]
[57]
[58]
[59]
[60]
liver metastases: indications and initial experience. Hepatogastroenterology 2013; 60: 21721. Hu MG, Ou-yang CG, Zhao GD, Xu DB, Liu R. Outcomes of open versus laparoscopic procedure for synchronous radical resection of liver metastatic colorectal cancer: a comparative study. Surg Laparosc Endosc Percutan Tech 2012; 22: 364-9. She WH, Poon JT, Fan JK, Lo OS, Law WL. Outcome of laparoscopic colectomy for cancer in elderly patients. Surg Endosc 2013; 27: 30812. Han Y, He YG, Zhang HB, Lv KZ, Zhang YJ, Lin MB, Yin L. Total laparoscopic sigmoid and rectal surgery in combination with transanal endoscopic microsurgery: a preliminary evaluation in China. Surg Endosc 2013; 27: 518-24. Li BG, Nie XY, He YZ, Xie HH, Yu GZ, Du HP, Kong FD, Gong DH, Lin WB, Wu MJ. [The standardized practice of laparoscopic-assisted radical right hemicolectomy in order to achieve complete mesocolic excision]. Zhonghua Wai Ke Za Zhi 2012; 50: 215-8. Cheung TP, Cheung HY, Ng LW, Chung CC, Li MK. Hybrid NOTES colectomy for right-sided colonic tumors. Asian J Endosc Surg 2012; 5: 46-9. Chi P, Chen ZF, Lin HM, Lu XR, Huang Y. [Laparoscopic cylindrical abdominoperineal resection with transabdominal approach for lower rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 589-93. Feng B, Sun J, Ling TL, Lu AG, Wang ML, Chen XY, Ma JJ, Li JW, Zang L, Han DP, Zheng MH. Laparoscopic complete mesocolic excision (CME) with medial access for right-hemi colon cancer: feasibility and technical strategies. Surg Endosc 2012; 26: 3669-75. Lu L, Zhou D, Jian X, Deng J, Yang P, Ding W. Laparoscopic colorectomy for colorectal cancer: retrospective analysis of 889 patients in a single center. Tohoku J Exp Med 2012; 227: 171-7. Jiang HY, Zhang XF, Wang XZ, Li J, Zhang C. [Short-term outcomes of radical resection of rectal carcinoma: hand-assisted laparoscopy versus traditional laparoscopic approach]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 517-9. Yan W, Amin BH, Zhu B, Zhang NW, Lian DB, Fan Q. [Transanal specimen extraction in laparoscopic colorectal resection]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 505-7. Han Y, He YG, Lin MB, Zhang HB, Lu XS, Lv KZ, Hua ZL, Zhang YJ, Yin L. [Total laparoscopic sigmoid and rectal surgery combined with transanal endoscopic microsurgery]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 499-501.
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China [61] Zhong B, Liu F, Yu J, Liang Y, Zhao L, Mou T, Hu Y, Li G. [Comparison of long-term oncological outcomes of laparoscopic and open resection of rectal cancer]. Nan Fang Yi Ke Da Xue Xue Bao 2012; 32: 664-8. [62] Ge L, Wang HJ, Zhao ZL, Yang XH, Zhao WM, Hati P, Liu L. [Evaluation of short-term efficacy and safety after laparoscopic resection for mid-low rectal cancer]. Zhonghua Yi Xue Za Zhi 2012; 92: 98-101. [63] Ng LW, Tung LM, Cheung HY, Wong JC, Chung CC, Li MK. Hand-assisted laparoscopic versus total laparoscopic right colectomy: a randomized controlled trial. Colorectal Dis 2012; 14: e612-7. [64] Fang JF, Wei HB, Chen TF, Huang Y, Wei B, Zheng ZH, Huang JL, Xu HZ. [Laparoscopy-assisted combined radical resection for synchronous rectal and gastric cancer in elderly patients: report of two cases]. Zhonghua Wei Chang Wai Ke Za Zhi 2012 ; 15: 149-51. [65] Wang G, Jiang ZW, Zhao K, Gao Y, Liu FT, Pan HF, Li JS. Fast track rehabilitation programme enhances functional recovery after laparoscopic colonic resection. Hepatogastroenterology 2012; 59: 2158-63. [66] Liu L, Cao Y, Zhang G, Zhang L, Wang P, Gong J. Long-term outcomes after laparoscopic total mesorectal excision for advanced rectal cancer. S Afr J Surg 2011; 49: 186-9. [67] Song W, Han FH, He YL, Peng JJ, Cai SR, Li HM. [Comparison of clinical outcomes between laparoscopic-assisted and hand-assisted laparoscopic operations in colorectal cancer]. Zhonghua Yi Xue Za Zhi 2011; 91: 2485-7. [68] Law WL, Poon JT, Fan JK, Lo OS. Survival following laparoscopic versus open resection for colorectal cancer. Int J Colorectal Dis 2012; 27: 1077-85. [69] Yang Z, Xu H, Zhang W, Xu Y, Xu Z. A retrospective analysis of ultralow anterior resection vs. abdomino-perineal resection for lower rectal cancer. Hepatogastroenterology 2012; 59: 1780-3. [70] Chen KY, Xiang GA, Wang HN, Xiao FL. Simultaneous laparoscopic excision for rectal carcinoma and synchronous hepatic metastasis. Chin Med J (Engl) 2011; 124: 2990-2. [71] Zong L, Chen P, Kitano S, Jiang G, Tan J, Reddy SS, Zhao W, Shi L, Qing XH, Shi GH, Xu DF, Wang L, Jiang J. Clinical experience and analysis of laparoscopic total mesorectal excision combined with improved Bacon for the treatment of lower rectal cancer. Hepatogastroenterology 2011; 58: 1538-44. [72] Liang JW, Zhang XM, Zhou ZX, Wang Z, Bi JJ. [Learning curve of laparoscopic-assisted surgery for rectal cancer]. Zhonghua Yi Xue Za Zhi 2011; 91: 1698-701.
4643
[73] Li JC, Leung KL, Ng SS, Liu SY, Lee JF, Hon SS. Laparoscopic-assisted versus open resection of right-sided colonic cancer--a prospective randomized controlled trial. Int J Colorectal Dis 2012; 27: 95-102. [74] Liu T, Zhang C, Yu P, Chen J, Zeng D, Gan L, Lv W, Liu L, Yan X. Laparoscopic radical correction combined with extensive lymphadenectomy and pelvic autonomic nerve preservation for mid-to-low rectal cancer. Clin Colorectal Cancer 2011; 10: 183-7. [75] Sun J, Jiang T, Qiu Z, Cen G, Cao J, Huang K, Pu Y, Liang H, Huang R, Chen S. Short-term and medium-term clinical outcomes of laparoscopic-assisted and open surgery for colorectal cancer: a single center retrospective case-control study. BMC Gastroenterol 2011; 11: 85. [76] Li SY, Chen G, Chen G, Zuo FY, Wei XJ, Yuan Q, DU JF. [Clinical study of laparoscopic sphincterpreserving proctectomy for low rectal cancer using transanal telescopic anastomosis]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 532-4. [77] Zhang H, Li M, Zhan TC, Yao YF, Peng YF, Gu J. [Comparison of short-term postoperative outcomes between hand-assisted laparoscopic and conventional sigmoidectomy]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 462-4. [78] Zhou ZX, Zheng XF, Song HY, Jiang FZ, Wang ZJ, Zuo ZG, Cai HJ, Ruan XJ. [Laparoscopic total mesorectal excision combined with intersphincteric resection for ultra-low rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 440-2. [79] Ng DC, Co CS, Cheung HY, Chung CC, Li MK. The outcome of laparoscopic colorectal resection in T4 cancer. Colorectal Dis 2011; 13: e349-52. [80] Bao Y, Jiang ZW, Xie LF, Liu FT, Li JS. [Roboticassisted laparoscopic colectomy for colon cancer: a report of 13 cases]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 327-9. [81] Luo CY, Ji XX, Zhang J, Zhou YQ, Guan C. [Clinical study of laparoscopic rectal surgery without abdominal scar]. Zhonghua Yi Xue Za Zhi 2011; 91: 686-8. [82] Li S, Chi P, Lin H, Lu X, Huang Y. Long-term outcomes of laparoscopic surgery versus open resection for middle and lower rectal cancer: an NTCLES study. Surg Endosc 2011; 25: 3175-82. [83] Liang X, Hou S, Liu H, Li Y, Jiang B, Bai W, Li G, Wang W, Feng Y, Guo J. Effectiveness and safety of laparoscopic resection versus open surgery in patients with rectal cancer: a randomized, controlled trial from China. J Laparoendosc Adv Surg Tech A 2011; 21: 381-5. [84] Chen WT, Chang SC, Chiang HC, Lo WY, Jeng LB, Wu C, Ke TW. Single-incision laparoscopic
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China
[85]
[86]
[87]
[88]
[89]
[90]
[91]
[92]
[93]
[94]
[95]
versus conventional laparoscopic right hemicolectomy: a comparison of short-term surgical results. Surg Endosc 2011; 25: 1887-92. Cui J, Zhang JL, Wang S, Sun ZQ, Jiang XL. [A preliminary study of stenting followed by laparoscopic surgery for obstructing left-sided colon cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 40-3. Qiu XF, Lin L, Yuan SB, Yan F, Ding ZJ, Bai LP, Ye ZJ, Lin WJ, Qi ZQ, Liu ZC. [Transumbilical singleport access laparoscopic surgery for colorectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 34-6. Qiu HZ, Xiao Y, Wu B, Lin GL, Wu X. [Laparoscopic-assisted anterior perineal plane for ultra-low anterior resection of the rectal cancer(APPEAR)]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 24-6. Guan GX, Liu X, Jiang WZ, Chen ZF, Lu HS. [Short-term efficacy of laparoscopic-assisted right hemicolectomy with D3 lymph node dissection in colon cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2010; 13: 917-20. Feng B, Zhu QL, Xia Y, Lu AG, Wang ML, Li JW, Hu WG, Zang L, Mao ZH, Dong F, Ma JJ, Zheng MH. Direct and indirect costs and long-term survival of laparoscopic anterior resection for rectal cancer. Med Sci Monit 2010; 16: PH97102. Zheng MH, Feng B, Hu CY, Lu AG, Wang ML, Li JW, Hu WG, Zang L, Mao ZH, Dong TT, Dong F, Cai W, Ma JJ, Zong YP, Li MK. Long-term outcome of laparoscopic total mesorectal excision for middle and low rectal cancer. Minim Invasive Ther Allied Technol 2010; 19: 329-39. Li J, Chen R, Xu YQ, Wang XC, Zheng S, Zhang SZ, Ding KF. Impact of a laparoscopic resection on the quality of life in rectal cancer patients: results of 135 patients. Surg Today 2010; 40: 917-22. Zhu QL, Feng B, Lu AG, Wang ML, Hu WG, Li JW, Mao ZH, Zheng MH. Laparoscopic low anterior resection for rectal carcinoma: complications and management in 132 consecutive patients. World J Gastroenterol 2010; 16: 4605-10. Wu QH, Zhang T, Zang L, Mao ZH, Li JW, Lu AG, Wang ML, Zheng MH. [Impact of previous abdominal operations on the outcome of laparoscopic colorectal cancer surgery: a non-randomized cohort study]. Zhonghua Wai Ke Za Zhi 2010; 48: 675-80. Yan J, Ying MG, Zhou D, Chen X, Chen LC, Ye WF, Zang WD. [A prospective randomized control trial of the approach for laparoscopic right hemi-colectomy:medial-to-lateral versus lateral-to-medial]. Zhonghua Wei Chang Wai Ke Za Zhi 2010; 13: 403-5. Li JC, Lee JF, Ng SS, Yiu RY, Hon SS, Leung WW, Leung KL. Conversion in laparoscopic-assisted
4644
colectomy for right colon cancer: risk factors and clinical outcomes. Int J Colorectal Dis 2010; 25: 983-8. [96] Qin H, Zhang XP, Zhou Y, Li HC, Li T. [Experience of laparoscopic total mesorectal excision for middle or low rectal cancer]. Zhonghua Zhong Liu Za Zhi 2010; 32: 156-7. [97] Cheung HY, Ng KH, Leung AL, Chung CC, Yau KK, Li MK. Laparoscopic sphincter-preserving total mesorectal excision: 10-year report. Colorectal Dis 2011; 13: 627-31. [98] Wang XF, Ruan Y, Li W, Zhou SJ, Peng JF, Cai XJ. [Minimally invasive surgery for colorectal cancer with liver metastasis]. Zhonghua Yi Xue Za Zhi 2009; 89: 2277-9. [99] Cheung HY, Chung CC, Tsang WW, Wong JC, Yau KK, Li MK. Endolaparoscopic approach vs conventional open surgery in the treatment of obstructing left-sided colon cancer: a randomized controlled trial. Arch Surg 2009; 144: 1127-32. [100] Yu J, Zhang C, Wang YN, Hu YF, Cheng X, Li GX. [Laparoscopic versus open total mesorectal excision for the middle-lower rectal cancer: a clinical comparative study]. Zhonghua Wei Chang Wai Ke Za Zhi 2009; 12: 573-6. [101] Wan X, Zhang Y, Zhang Y. [Anus-preserving laparoscopic rectal resection in 75 patients with lower rectal cancer]. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2009; 34: 902-4. [102] Wang ZD, Wu ZY, Li Y, Wu WL, Lin F. [Clinical efficacy comparison between laparoscopy and open radical resection for 191 advanced colorectal cancer patients]. Zhonghua Wei Chang Wai Ke Za Zhi 2009; 12: 368-70. [103] Chen KY, Xiang GA, Wang HN, Xiao FL. [Simultaneous laparoscopic excision for the treatment of rectal carcinoma and the synchronous hepatic metastasis]. Zhonghua Zhong Liu Za Zhi 2009; 31: 69-71. [104] Li JC, Hon SS, Ng SS, Lee JF, Yiu RY, Leung KL. The learning curve for laparoscopic colectomy: experience of a surgical fellow in an university colorectal unit. Surg Endosc 2009; 23: 16038. [105] Mao ZH, Jin J, Li JW, Deng YX, Wang ML, Lu AG, Hu WG, Zheng MH. [Safety study of laparoscopic surgery for colorectal cancer in elderly patients]. Zhonghua Wei Chang Wai Ke Za Zhi 2009; 12: 244-8. [106] Xiong H, Yu J, Zhang C, Wang YN, Hu YF, Li GX. [Application of laparoscopic surgery following neoadjuvant chemoradiotherapy for mid-low rectal cancer]. Nan Fang Yi Ke Da Xue Xue Bao 2009; 29: 754-6. [107] Ng KH, Ng DC, Cheung HY, Wong JC, Yau KK, Chung CC, Li MK. Laparoscopic resection for rectal cancers: lessons learned from 579 cases. Ann Surg 2009; 249: 82-6.
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China [108] Ding KF, Chen R, Zhang JL, Li J, Xu YQ, Lv L, Wang XC, Sun LF, Wang JW, Zheng S, Zhang SZ. Laparoscopic surgery for the curative treatment of rectal cancer: results of a Chinese three-center case-control study. Surg Endosc 2009; 23: 854-61. [109] Cheung HY, Chung CC, Wong JC, Yau KK, Li MK. Laparoscopic rectal cancer surgery with and without neoadjuvant chemo-irradiation: a comparative study. Surg Endosc 2009; 23: 14752. [110] Law WL, Fan JK, Poon JT, Choi H, Lo OS. Laparoscopic bowel resection in the setting of metastatic colorectal cancer. Ann Surg Oncol 2008; 15: 1424-8. [111] Ng SS, Lee JF, Yiu RY, Li JC, Leung WW, Leung KL. Emergency laparoscopic-assisted versus open right hemicolectomy for obstructing rightsided colonic carcinoma: a comparative study of short-term clinical outcomes. World J Surg 2008; 32: 454-8. [112] Zhang H, Hu S, Zhi X, Wang L, Zhang G, Wang K. Laparoscopic proctocolectomy with ileal pouch-anal anastomosis. Surg Laparosc Endosc Percutan Tech 2007; 17: 388-91. [113] Zhang H, Hu S, Zhang G, Wang K, Chen B, Li B, Frezza EE. Laparoscopic versus open proctocolectomy with ileal pouch-anal anastomosis. Minim Invasive Ther Allied Technol 2007; 16: 187-91. [114] Ng SS, Lee JF, Yiu RY, Li JC, Hon SS. Telerobotic-assisted laparoscopic abdominoperineal resection for low rectal cancer: report of the first case in Hong Kong and China with an updated literature review. World J Gastroenterol 2007; 13: 2514-8. [115] Pan YF, Zhang XH, Jia XJ, Qu JM, Xiang YQ, Yang K, Lin BR, Zheng XF, Zheng J. [Laparoscopic abdominoperineal resection for low rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2007; 10: 253-6. [116] Liang JT, Lai HS, Lee PH, Huang KC. Comparison of functional and surgical outcomes of laparoscopic-assisted colonic J-pouch versus straight reconstruction after total mesorectal excision for lower rectal cancer. Ann Surg Oncol 2007; 14: 1972-9. [117] Yan SL, Xu ZB, Chi P, Lin HM. [Comparing the influencing factors of anastomotic bleeding in rectal carcinoma resection between laparoscopic and open radical approaches]. Zhonghua Wei Chang Wai Ke Za Zhi 2007; 10: 157-9. Chinese. [118] Ng SS, Yiu RY, Li JC, Lee JF, Leung KL. Emergency laparoscopically assisted right hemicolectomy for obstructing right-sided colon carcinoma. J Laparoendosc Adv Surg Tech A 2006; 16: 350-4.
4645
[119] Mao ZH, Chen HZ, Li JW, Lu AG, Wang ML, Hu WG, Zheng MH. [Comparison of inflammatory response after laparoscopic and conventional surgery for colorectal carcinoma]. Zhonghua Wei Chang Wai Ke Za Zhi 2006; 9: 297-300. [120] Qian LY, Wu JH, Chen DJ, Li XR, Wei YS. [Comparative study on long-term results of laparoscopic and open radical resection for colorectal carcinoma]. Zhonghua Wei Chang Wai Ke Za Zhi 2006; 9: 294-6. [121] Ng SS, Li JC, Lee JF, Yiu RY, Leung KL. Laparoscopic total colectomy for colorectal cancers: a comparative study. Surg Endosc 2006; 20: 1193-6. [122] Feng B, Zheng MH, Mao ZH, Li JW, Lu AG, Wang ML, Hu WG, Dong F, Hu YY, Zang L, Li HW. Clinical advantages of laparoscopic colorectal cancer surgery in the elderly. Aging Clin Exp Res 2006; 18: 191-5. [123] Mou YP, Yang P, Yan JF, Chen QL, Yuan XM, Zhu LH, Xu XW. [Clinical evaluation of laparoscopic radical resection of colon cancer]. Zhonghua Wai Ke Za Zhi 2006; 44: 581-3. [124] Li GX, Yan HT, Yu J, Lei ST, Xue Q, Cheng X. [Learning curve of laparoscopic resection for rectal cancer]. Nan Fang Yi Ke Da Xue Xue Bao 2006; 26: 535-8. [125] Tsang WW, Chung CC, Kwok SY, Li MK. Laparoscopic sphincter-preserving total mesorectal excision with colonic J-pouch reconstruction: five-year results. Ann Surg 2006; 243: 353-8. [126] Zheng MH, Feng B, Lu AG, Li JW, Wang ML, Mao ZH, Hu YY, Dong F, Hu WG, Li DH, Zang L, Peng YF, Yu BM. Laparoscopic versus open right hemicolectomy with curative intent for colon carcinoma. World J Gastroenterol 2005; 11: 323-6. [127] Zhou ZG, Hu M, Li Y, Lei WZ, Yu YY, Cheng Z, Li L, Shu Y, Wang TC. Laparoscopic versus open total mesorectal excision with anal sphincter preservation for low rectal cancer. Surg Endosc 2004; 18: 1211-5. [128] 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: 1167-70. [129] Zhou ZG, Wang Z, Yu YY, Shu Y, Cheng Z, Li L, Lei WZ, Wang TC. Laparoscopic total mesorectal excision of low rectal cancer with preservation of anal sphincter: a report of 82 cases. World J Gastroenterol 2003; 9: 1477-81. [130] Tsang WW, Chung CC, Li MK. Prospective evaluation of laparoscopic total mesorectal excision with colonic J-pouch reconstruction for mid and low rectal cancers. Br J Surg 2003; 90: 867-71. [131] Tan M, Guo B, Wu Z, Chen G, Zheng Z, Zhao Z. [Laparoscopic colorectomy for colorectal cancer]. Zhonghua Wai Ke Za Zhi 2002; 40: 76972.
Int J Clin Exp Med 2014;7(12):4635-4645
Review Article Laparoscopic surgery for colorectal cancer in China: an overview Ketao Jin1*, Jun Wang2*, Huanrong Lan1*, Ruili Zhang1 Department of Gastrointestinal Surgery and Laboratory of Translational Oncology, Public Research Platform, Taizhou Hospital, Wenzhou Medical University, Linhai 317000, Zhejiang, P.R. China; 2Department of Gynecology and Obstetrics and Laboratory of Translational Oncology, Public Research Platform, Taizhou Hospital, Wenzhou Medical University, Linhai 317000, Zhejiang, P.R. China. *Equal contributors. 1
Received September 21, 2014; Accepted November 25, 2014; Epub December 15, 2014; Published December 30, 2014 Abstract: Since its introduction into China in 2001, laparoscopic techniques have been extensively used for the surgical management of colorectal cancer during the last two decades in China. Like all the pioneers of the technique, Chinese gastrointestinal surgeons claim that laparoscopic surgery for colorectal cancer led to faster recovery, shorter hospital stay and more rapid return to daily activities respect to open surgery while offering the same functional and oncological results. There has been booming interest in laparoscopic surgery for colorectal cancer since 2006 in China. The last decade has witnessed national growth in the application of laparoscopic surgery for colorectal cancer and yielded a significant amount of scientific data to support its clinical merits and advantages. However, few prospective randomized controlled trials have investigated the benefits of laparoscopic surgery for colorectal cancer in China. In this article, we make an overview of the current data and state of the art of laparoscopic surgery for colorectal cancer in China. Keywords: Colon cancer, rectal cancer, laparoscopic surgery, review
Introduction Colorectal cancer is one of the leading causes of mortality worldwide [1]. Traditionally, cancers of the colon were removed through large abdominal incisions. Since the advent of laparoscopic surgery, it has become clear that patients benefit from a minimally invasive approach in a variety of ways [2]. In 1991, laparoscopic-assisted colectomy was first reported [3, 4]. Due to the development of minimally invasive techniques, the majority of colorectal procedures can be performed using a laparoscopic approach, and the indications for laparoscopic surgery have gradually expanded [5, 6]. A number of available prospectively randomized trials and meta-analyses of laparoscopic surgery for colorectal cancer [7-12] reported that laparoscopic-assisted colorectal surgery exhibited improved post-operative results, including less pain, a smaller incision, a faster recovery of gastrointestinal function, a shorter post-operative hospital stay and similar longterm survival, compared with those of open
colorectal surgery [13, 14]. Therefore, laparoscopic-assisted surgery has been widely accepted as an alternative to conventional open surgery for colorectal cancer. Because of the potential advantages, such as less invasiveness and postoperative pain, earlier recovery, better cosmetic results, milder morbidity, earlier time to walking, flatus, and oral intake, and quicker recovery with a shorter hospital stay, laparoscopic surgery for colorectal cancer was introduced into clinical practice in China in 2001 [15], and was gradually implemented and is now commonplace in China. There has been booming interest in laparoscopic surgery for colorectal cancer since it was first described in 2001 [15]. The last decade has witnessed national growth in the application of laparoscopic surgery for colorectal cancer yielding a significant amount of scientific data to support its clinical merits and advantages. With the development of laparoscopic techniques and the invention of new surgical equipments, scarless surgery is becoming increasingly popu-
Laparoscopic surgery for colorectal cancer in China English. However, 70 relevant reports (44.3%) have been written in Chinese. It is compelled to unveil the current status of laparoscopic surgery for colorectal cancer in China to the wider surgical fraternity based on the scientific data both in English and in Chinese. Pronounced rise in a number of articles dedicated to laparoscopic surgery for colorectal cancer is observed from 2009 to 2014, this probably corresponds both to an increased research interest of surgical community and to a wider clinical application of this patient-friendly approach. Figure 1. Numbers of full papers related to laparoscopic surgery for colorectal cancer in China (PubMed/Medline database).
lar. In single-incision laparoscopic surgery (SILS), also termed single-port laparoscopic surgery, the surgeon operates through a single entry point with a single incision of only 25-30 mm. Another innovation is natural orifice specimen extraction (NOSE). For this procedure, the specimen is extracted from a natural orifice such as the vagina or anus; therefore, an additional incision in the abdominal wall is not needed. The final innovation is natural orifice transluminal endoscopic surgery (NOTES). NOTES is the only type of surgery that lacks scarring of the abdominal wall, thus, NOTES may represent the next step in the evolution of mini-invasive surgery. Robotic surgery is an emerging technology that provides 3-dimensional imaging, tremor filtration, and motion scaling. With these advantages, robotic rectal cancer resection may overcome the limitations of conventional laparoscopic surgery. This article made an overview of the current data and state of the art for laparoscopic surgery for colorectal cancer in China. Literature of laparoscopic surgery for colorectal cancer in China Current literature was reviewed by searching PubMed/Medline database (from January 2001 to July 2014). A hundred and fifty-eight full articles were found to be relevant to laparoscopic surgery for colorectal cancer (Figure 1). A total of 88 (55.7%) publications were in 4636
Operative data of laparoscopic surgery for colorectal cancer
One hundred and seventeen suitable papers, consisting of prospective and retrospective studies, were identified [16-131]. Key outcomes of major studies written in English are summarized in the Tables 1 and 2 [16, 17, 19, 21-25, 27, 30-32, 35-37, 39-43, 45, 46, 48, 49, 50-52, 54, 56, 57, 63, 65, 66, 68, 69-71, 73-75, 79, 82-84, 89, 90-92, 95, 97, 99, 104, 107-114, 116, 118, 121, 122, 125-130]. Twenty nine of these were performed prospectively [24, 25, 30, 35, 42, 51, 63, 65, 66, 68, 73, 79, 83, 84, 89, 91, 97, 99, 104, 109, 110, 116, 118, 121, 125, 127-130 ], in which nine studies were prospective randomized controlled trials [30, 35, 63, 65, 73, 83, 99, 116, 127]. Common outcome measures includes operative data (operative time, estimated blood loss and conversion rate), short-term outcomes (days to liquid diet, days to flatus, and total hospital stay), complications (anastomotic stenosis, anastomotic bleeding, and anastomotic leakage), postoperative mortality data, overall survival, disease-free survival and follow-up period. Surgical approaches Surgical approaches of laparoscopic surgery for colorectal cancer performed by Chinese gastrointestinal surgeons are listed in Table 1, which includes multiport laparoscopic surgery (MLS), single-incision laparoscopic surgery (SILS), natural orifice specimen extraction (NOSE), natural orifice transluminal endoscopic Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China Table 1. Survey over major reports of laparoscopic surgery for colorectal cancer in China: operative data (Articles in English) Ref. [16]
PS/RS RS
Patient (n) 197
Approaches NOSE/MLS
TME Yes
[17] [19] [21] [23] [24] [25] [27] [30]
RS RS RS RS PS PS RS PS
119 80 289 24 21 51 64 70
Yes Yes Yes Yes Yes Yes Yes Yes
[32] [39] [45] [48] [51] [52] [51] [63] [66] [68] [73] [75] [82] [83]
RS RS RS RS PS RS RS PS PS PS PS RS RS PS
87 67 177 381 189 34 889 30 125 814 71 254 113 169
MLS MLS MLS NOSE NOSE MLS MLS 35 in NOTES; 35 in MLS MLS MLS MLS MLS MLS NOTES MLS MLS MLS MLS MLS MLS MLS MLS
Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes
LN 17.0 ± 8.3 in NOSE; 18.9 ± 11.6 in MLS 22.3 ± 8.6 11.86 ± 1.95 NA NA 17.8 ± 4.6 NA 11.68 ± 5.69 12 (6-33) in NOTES; 12 (6-29) in MLS 14 ± 5 20.3 ± 8.3 15.2 ± 10.1 12.5 ± 4.2 NA 12.92 ± 2.2 12.27 ± 9.02 16 (2-33) NA 13 (8-18) 18.7 ± 12 12.0 ± 6.9 20.3 ± 6.9 7.05 ± 5.05
NeoA No NA No NA NA NA Yes No NA NA NA No NA NA NA NA NA Yes NA NA No No No
OT (min) 111.6 ± 25.4 in NOSE; 115.3 ± 23.0 in MLS 257.8 ± 67.6 201.7 ± 6.91 155 ± 29 110.0 132 ± 85 181.5 (95.0-310.0) 183 ± 55 105 (60-170) in NOTES; 100 (59-210) in MLS 160 ± 40 216.4 ± 68.3 133 ± 36 176.4 ± 28.3 150 (81–360) 151.6 ± 25.93 201.66 ± 81.81 111 (74-165) NA 180 (141-218) 198 ± 48 135.6 ± 40.0 210.0 (100-420) 138.08 ± 23.79
BL (ml) 70.2 ± 66.1 in NOSE; 126.3 ± 58.6 in MLS 100 (100-200) 97.25 ± 9.97 128 ± 24 69.1 mL 84 ± 15 204.7 (80.0-1000.0) 168 ± 106 30 (10-50) in NOTES; 30 (10-100) in MLS 28 ± 5 86.9 ± 37.6 94 ± 34 58.3 ± 13.9 100 (0-1,000) 200.2 ± 114.69 100 20 (5-400) NA 100 (50-200) 110.1 (0-1,000) 101.5 ± 70.8 50.0 (0-1200) NA
C n (%) NA 9 (7.6) 1 (1.3) NA NA NA NA NA NA NA NA 5 (2.82) NA NA 0 43 (4.84) 1 (3.3) NA NA NA 8 (3) NA NA
Abbreviations: Ref., reference; PS, prospective study; RS, retrospective study; MLS, multiport laparoscopic surgery; NOSE, natural orifice specimen extraction; NOTES, natural orifice transluminal endoscopic surgery; RH, right hemicolectomy; TME, total mesorectal excision; LH, left hemicolectomy; SC, sigmoid colectomy; LAR, low anterior resection; AR, Abdominoperineal resection; TC, total colectomy; LN, number of lymph node harvested; NeoA, neoadjuvant chemotherapy; OT, operation time. BL, estimated blood loss; C, conversion rate; NA, data not available.
4637
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China surgery (NOTES), and totally laparoscopic surgery (TLS) for colorectal cancer. In our center, we had adopted MLS, SILS, and TLS. Operative time and blood loss Operative time varies significantly between the studies reflecting to type of performed laparoscopic surgery for colorectal cancer and accumulated experience/technical skills (Table 1). The estimated blood loss varies significantly from centre to centre and comprises around 10-1000 ml (Table 1). Major blood loss and need to blood transfusion in particular increase a risk of postoperative morbidity and mortality. Conversion to open surgery The conversion rate reported in the literature is in a range of 0-7.6% (Table 1). However, with surgical experience the conversion rate reduces and currently has no conversion to open surgery in expert centers in China. The main reason to conversion was bleeding. It is not appropriate to consider conversion from laparoscopic surgery to open surgery for colorectal cancer as a failure because patient’s safety and oncologic integrity of the procedure should be of supreme importance. Mortality, morbidity and postoperative complications Postoperative mortality rates following laparoscopic surgery for colorectal cancer vary between 0 to 11.8% (Table 2). Anastomotic stenosis, anastomotic bleeding, anastomotic leakage are the most feared complications in laparoscopic surgery for colorectal cancer. From the operative data, anastomotic stenosis rate ranged between 0 and 1.3%, anastomotic bleeding rate ranged between 0 and 7.8%, and anastomotic leakage rate ranged between 0 and 9.0% (Table 2). Laparoscopic surgery for colorectal cancer is associated with significant reduction in hospital stay. Postoperative hospital stay comprises 9.0 days in average (Table 2). Outcomes There are 26 studies reported the survival data of laparoscopic surgery for colorectal cancer in China [17, 19, 27, 35, 45, 48-51, 57, 63, 66, 68, 70, 73, 75, 79, 82, 83, 90, 95, 97, 107, 109, 125, 126]. Sixteen studies reported the 4638
long-term overall survival of laparoscopic surgery for colorectal cancer [35, 45, 48, 50, 51, 57, 63, 66, 68, 73, 83, 95, 97, 107, 109, 125]. Ng KH, et al. reported the long-term survival of laparoscopic rectal cancer resection at a single institution with 579 cases over a 15-year period. They reported the overall 5- and 10-year survivals for rectal cancer were 70% and 45.5%, respectively and the cancer-specific 5and 10-year survival was 76% and 56%, respectively [107]. Robotic surgery for colorectal cancer Though laparoscopic surgery for colorectal cancer offers a number of patient benefits compared to open surgery, such as less invasiveness and pain, speedier recovery, better cosmetic results, milder morbidity, earlier time to walking, flatus, and oral intake, and quicker recovery with a shorter hospital stay, several limitations and disadvantages are associated with conventional laparoscopic surgery. An important reason for this is the steep learning curve of this technique. In addition, some other limitations that hinder the development of laparoscopic surgery include tremor, 2-dimensional vision, poor ergonomics, the need of a skilled assistant, and the limited degrees of freedom of the instruments. In an effort to minimize the difficulty of laparoscopy, a robotic surgery system was introduced in China in 2005 [114]. Robotic surgery is thought to be able to overcome these limitations by providing 3-dimensional vision, 7 degrees of freedom of the instruments, enhanced ergonomics, tremor filtration, and superior dexterity [42, 80]. These advantages of robotic surgery make it extremely suitable for pelvic dissection, especially for patients with a narrow pelvis and/or local advanced disease and especially important for complex procedures, such as the dissection of lymph nodes around major vessels because of its tremor filtration and superior dexterity. Robotic surgery has many advantages over laparoscopic surgery, but some limitations in the current robotic technology still exist. When compared to conventional laparoscopic surgery, robotic surgery is associated with longer operation time, higher cost, and lacks tactile sensation and tensile feedback for the surgeon. Meanwhile, the limited data of the current work in China are preliminary and retrospective studies from single clinical center with Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China Table 2. Survey over major reports of laparoscopic surgery for colorectal cancer in China: Outcomes (Article in English) Ref.
Patient (n)
[16]
[17]
F
De
197
2.7 ± 0.8 in NOSE; 3.4 ± 0.9 in MLS
119
[19] [21] [23]
IC (n, %)
PC (n, %)
MH
OI
IL
AS
AB
3.3 ± 0.6 in NOSE; 3.9 ± 1.1 in MLS
NA
NA
NA
NA
NA
2.7 ± 1.0
NA
NA
NA
80
2.34 ± 0.12
NA
289
NA
NA
NA
NA
NA
NA
NA
24
3.1
NA
NA
NA
NA
NA
[24]
21
NA
NA
NA
NA
NA
[25]
51
2.5 (1.5-4.0)
4.0 (2.0-8.0)
NA
NA
[27]
64
NA
NA
NA
[30]
70
NA
NA
[32]
87
NA
NA
[39]
67
46.9 ± 14.8
[45]
177
[48] [51]
4 (3.4) 1 (0.8) 1 (0.8)
AL
HS (d)
2 (3.1) in NOSE; 9.0 ± 1.9 in NOSE; 6 (4.5) in MLS 9.9 ± 2.0 in MLS
M n (%)
FP (m)
OSR (%)
DFSR (%)
NA
NA
NA
NA
2 (1.7)
11.4 ± 4.7
1 (0.8)
30 (3-60)
92.0% in 3 years
84.6% in 3 years
NA
9.7 ± 0.59
NA
17.5
NA
NA
NA
8.9 ± 2.1
NA
NA
NA
NA
NA
NA
9.2
NA
NA
NA
NA
NA
0
1 (4.7)
6.1 ± 2.7
NA
12
NA
NA
NA
NA
NA
1 (3.1)
NA
6 (11.8)
NA
NA
NA
NA
5 (8)
NA
NA
3 (5)
12 (6‑39)
NA
17
38.7 ± 2.7
37.3 ± 2.5
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
1 (1.1)
5.2 ± 1.8
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
1 (1.4)
10.4 ± 4.3
NA
NA
NA
NA
2.1 ± 0.7 (2-5)
NA
NA
NA
3 (1.69)
NA
NA
7 (3.95)
10.4 ± 2.7 (7-27)
NA
54 (15-104)
97.18% in 1 year; 83.73% in 3 years 70.37% in 5 years; 68.99% in 6 years
NA
381
2.5 ± 1.8
NA
NA
NA
NA
NA
NA
3 (0.8)
NA
NA
51 (13-87)
84.4% in 3 years; 68.4% in 5 years
NA
189
NA
NA
NA
NA
NA
NA
NA
NA
5 (2-63)
1 (0.5)
22.9
52.8 % in 5 years
68.9 % in 5 years
[52]
34
2 ± 0.49
NA
NA
NA
NA
NA
NA
NA
9 (7-66)
NA
NA
NA
NA
[51]
889
NA
NA
NA
NA
NA
NA
7 (7.8)
8 (9.0)
9.88 ± 5.93
NA
29
78.0% in 3 years; 69.0% in 5 years
NA
[63]
30
NA
NA
NA
NA
NA
NA
NA
0
7 (5-19)
NA
33 (2-55)
80.0% in 5 years
NA
[66]
125
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
38 (5-113)
71.3% for stage II; 51% for stage III
59.2% for stage II; 45.4% for stage III
[68]
814
NA
NA
NA
NA
32 (3.9)
NA
NA
15 (1.8)
NA
4 (0.5)
40.3
74.1% in 5 years
81.9% in 5 years
[73]
71
3 (1-10)
NA
NA
NA
NA
NA
NA
1 (1.4)
7.8 (4-20)
NA
104 (44-156)
100% in Stage I, 68.7% in stage II, and 74.5% in stage III in 5 years
NA
[75]
254
NA
NA
NA
NA
NA
NA
1 (0.4)
5 (2.0)
NA
NA
37.1 (8.2-62.5)
NA
NA
[82]
113
NA
NA
NA
NA
NA
NA
NA
8 (8.1)
9.0 (7-52)
1 (0.9)
76.0 ± 30.3
91.7% in stage I, 82.8% in stage II, 66.7% in stage III in 5 years
NA
[83]
169
NA
NA
NA
NA
NA
0
NA
4 (2.4)
NA
0
44 (1-72)
94.0% in 1 year; 82.6% in 2 years; 76.0% in 3 years
NA
1 (1.3) 1 (1.3) 1 (1.3) 1 (1.3) 2 (2.5)
Abbreviations: Ref., reference; LD, days to liquid diet; De, days to first defecation; F, days to first flatus; IC, intraoperative complications; PC, post‑operative complications; MH, massive hemorrhage > 500 ml; OI, Organ injury; IL, ileus; IA, intestinal adhesion; AS, anastomotic stenosis; AB, anastomotic bleeding; AL, anastomotic leakage; HS, hospital stay (day); M, postoperative mortality; FP (m), follow-up period (month); OSR, overall survival rate (%); DFSR, Disease-free survival rate (%); NA, data not available.
4639
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China small sample sizes. Multicenter, randomized, prospective trials are needed to compare the short-term and long-term outcomes of robotic surgery with those of conventional laparoscopic surgery. In conclusion, there is no compelling reason to bar our interested Chinese gastrointestinal surgeons from performing laparoscopic surgery for colorectal cancer provided that they have received adequate training from major centers. The techniques spread are growing in China, as confirmed by the elevating number of recently published papers on this subject. However, only nine prospective randomized controlled trials have investigated the benefits of laparoscopic surgery for colorectal cancer in China. More randomized controlled clinical trials directly comparing the laparoscopic surgery and open approaches in China would be preferable and are extremely needed. Acknowledgements This work was supported by National Natural Science Foundation of China (Grants No. 81374014 and No. 81472210), Zhejiang Provincial Medical and Healthy Science and Technology Projects (Grant No. 2013KYA228), Zhejiang Provincial Science and Technology Project (Grant No. 2013C33112), Science Research Fund of Taizhou (Grants No. A121KY08, A131KY13-3 and A131KY13-12), and Enze Medical Research Fund (Grants No. 12EZA1, 13EZA2 and 13EZB6).
[3] [4] [5]
[6]
[7]
[8]
[9]
[10]
Disclosure of conflict of interest None. Address correspondence to: Dr. Ruili Zhang, Department of Gastrointestinal Surgery and Laboratory of Translational Oncology, Public Research Platform, Taizhou Hospital, Wenzhou Medical University, 150 Ximen Road, Linhai 317000, Zhejiang, P.R. China. Tel: +86-576-85189199/+86-13806561091; Fax: +86-576-85189199; E-mail: jinketao2001@zju. edu.cn
References [1] [2]
Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013; 63: 1130. Barkun JS, Barkun AN, Sampalis JS, Fried G, Taylor B, Wexler MJ, Goresky CA, Meakins JL. Randomised controlled trial of laparoscopic
4640
[11]
[12]
[13]
[14]
versus mini cholecystectomy. The McGill Gallstone Treatment Group. Lancet 1992; 340: 1116-9. Cooperman AM, Katz V, Zimmon D, Botero G. Laparoscopic colon resection: a case report. J Laparoendosc Surg 1991; 1: 221-4. Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc 1991; 1: 144-50. Ku G, Tan IB, Yau T, Boku N, Laohavinij S, Cheng AL, Kang YK, de Lima Lopes G Jr. Management of colon cancer: resource-stratified guidelines from the Asian Oncology Summit 2012. Lancet Oncol 2012; 13: e470-81. Miyajima N, Fukunaga M, Hasegawa H, Tanaka J, Okuda J, Watanabe M; Japan Society of Laparoscopic Colorectal Surgery. Results of a multicenter study of 1,057 cases of rectal cancer treated by laparoscopic surgery. Surg Endosc 2009; 23: 113-8. Abraham NS, Young JM, Solomon MJ. Metaanalysis of short-term outcomes after laparoscopic resection for colorectal cancer. Br J Surg 2004; 91: 1111-24. Aziz O, Constantinides V, Tekkis PP, Athanasiou T, Purkayastha S, Paraskeva P, Darzi AW, Heriot AG. Laparoscopic versus open surgery for rectal cancer: a meta-analysis. Ann Surg Oncol 2006; 13: 413-24. Neudecker J, Klein F, Bittner R, Carus T, Stroux A, Schwenk W; LAPKON II Trialists. Short-term outcomes from a prospective randomized trial comparing laparoscopic and open surgery for colorectal cancer. Br J Surg 2009; 96: 145867. Levy BF, Tilney HS, Dowson HM, Rockall TA. A systematic review of postoperative analgesia following laparoscopic colorectal surgery. Colorectal Dis 2010; 12: 5-15. Colon Cancer Laparoscopic or Open Resection Study Group; Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, Haglind E, Påhlman L, Cuesta MA, Msika S, Morino M, Lacy A, Bonjer HJ. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 2009; 10: 44-52. Braga M, Frasson M, Zuliani W, Vignali A, Pecorelli N, Di Carlo V. Randomized clinical trial of laparoscopic versus open left colonic resection. Br J Surg 2010; 97: 1180-6. Biondi A, Grosso G, Mistretta A, Marventano S, Toscano C, Gruttadauria S, Basile F. Laparoscopic-assisted versus open surgery for colorectal cancer: short- and long-term outcomes comparison. J Laparoendosc Adv Surg Tech A 2013; 23: 1-7. Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically as-
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
sisted and open colectomy for colon cancer. N Engl J Med 2004; 350: 2050-9. 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: 1098-101. Xingmao Z, Haitao Z, Jianwei L, Huirong H, Junjie H, Zhixiang Z. Totally laparoscopic resection with natural orifice specimen extraction (NOSE) has more advantages comparing with laparoscopic-assisted resection for selected patients with sigmoid colon or rectal cancer. Int J Colorectal Dis 2014; 29: 1119-24. Zhao LY, Chi P, Ding WX, Huang SR, Zhang SF, Pan K, Hu YF, Liu H, Li GX. Laparoscopic vs open extended right hemicolectomy for colon cancer. World J Gastroenterol 2014; 20: 792632. Ju H, Huang X, Zhu Y, Feng H, Li D. [Comparison of short-term outcomes of hand-assisted laparoscopic, laparoscopic, and open surgery in the treatment of rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2014; 17: 574-7. Chinese. Chen K, Zhang Z, Zuo Y, Ren S. Comparison of the clinical outcomes of laparoscopic-assisted versus open surgery for colorectal cancer. Oncol Lett 2014; 7: 1213-1218. Qin C, Li Q, Fu K, Meng J, Ren X. [Experiences of scarless laparoscopic radical resection of rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2014; 17: 486-8. Chinese. Chen T, Fang J, Wang Z, Zheng Z, Huang J, Wei B, Wei H. Laparoscopic Surgery Decreases the Surgical Risks Associated With Hyperlipidemia in Rectal Cancer: Retrospective Analysis of 495 Patients. Surg Laparosc Endosc Percutan Tech 2014; [Epub ahead of print] Cong JC, Chen CS, Ma MX, Xia ZX, Liu DS, Zhang FY. Laparoscopic intersphincteric resection for low rectal cancer: comparison of stapled and manual coloanal anastomosis. Colorectal Dis 2014; 16: 353-8. Zhang X, Zhou H, Hou H, Hu J, Wang H, Zhou Z. Totally laparoscopic resection with natural orifice specimen extraction for carcinoma of sigmoid colon and rectum: a feasible and innovative technique. J Clin Gastroenterol 2014; 48: e57-61. Han FH, Hua LX, Zhao Z, Wu JH, Zhan WH. Transanal natural orifice specimen extraction for laparoscopic anterior resection in rectal cancer. World J Gastroenterol 2013; 19: 77517. Hu JJ, Liang JW, Wang Z, Zhang XM, Zhou HT, Hou HR, Zhou ZX. Short-term outcomes of laparoscopically assisted surgery for rectal cancer following neoadjuvant chemoradiotherapy: a
4641
[26]
[27]
[28]
[29]
[30]
[31]
[32]
[33]
[34]
[35]
[36]
[37]
single-center experience. J Surg Res 2014; 187: 438-44. Zhou HT, Zhou ZX, Liang JW, Wang Z, Zhang XM, Hu JJ. [Analysis of 21 cases treated by total laparoscopic rectosigmoid cancer surgery with transanal natural orifice specimen extraction]. Zhonghua Yi Xue Za Zhi 2013; 93: 20824. Chinese. Cai Y, Zhou Y, Li Z, Xiang J, Chen Z. Surgical outcome of laparoscopic colectomy for colorectal cancer in obese patients: A comparative study with open colectomy. Oncol Lett 2013; 6: 1057-1062. Wu GJ, Xiao G, Zhou XP, Zhao G, Jia WZ, Yu T, An Q, Yang H, Long HK, Huang MX. [Laparoscopic with extralevator abdominoperineal excision for low rectal carcinoma]. Zhonghua Yi Xue Za Zhi 2013; 93: 1921-3. Chinese. Liu Y, Lu XM, Niu YF, Tao KX, Wang GB. [Application of laparoscopic transanal coloanal anastomosis in sphincter-preserving surgery for low rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2013; 16: 727-9. Leung AL, Cheung HY, Fok BK, Chung CC, Li MK, Tang CN. Prospective randomized trial of hybrid NOTES colectomy versus conventional laparoscopic colectomy for left-sided colonic tumors. World J Surg 2013; 37: 2678-82. Zhu Z, Tan JW, Tan HM, Hu BS, Chen K, Ding XM, Leng JJ, Chen F. The preliminary experience in simultaneous treatment of rectal cancer and synchronous liver metastases with laparoscopy. Turk J Gastroenterol 2013; 24: 127-33. Yang Q, Xiu P, Qi X, Yi G, Xu L. Surgical margins and short-term results of laparoscopic total mesorectal excision for low rectal cancer. JSLS 2013; 17: 212-8. Zhao LY, Wang YN, Yu J, Deng HJ, Hu YF, Mou TY, Li GX. [The safety and long-term survival after laparoscopic surgery versus open surgery for colon cancer]. Zhonghua Wai Ke Za Zhi 2013; 51: 314-9. Zhou T, Zhang GJ, Liu ZL, Tian HP. [Laparoscopic versus open intersphincteric resection for low rectal cancer: a clinical comparative study]. Zhonghua Wei Chang Wai Ke Za Zhi 2013; 16: 565-9. Tung KL, Cheung HY, Ng LW, Chung CC, Li MK. Endo-laparoscopic approach versus conventional open surgery in the treatment of obstructing left-sided colon cancer: long-term follow-up of a randomized trial. Asian J Endosc Surg 2013; 6: 78-81. Wang Q, Wang C, Sun DH, Kharbuja P, Cao XY. Laparoscopic total mesorectal excision with natural orifice specimen extraction. World J Gastroenterol 2013; 19: 750-4. Xing-mao Z, Hui-rong H, Zi-nian W, Hong-ying W, Jun-jie H, Zheng W, Jian-wei L, Jian-jun B,
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48]
[49]
Hai-tao Z, Zhi-xiang Z. Age, is it an obstacle for older surgeons to learn laparoscopic approach for colorectal cancer? Med Oncol 2013; 30: 495. Xiao Y, Sun XY, Niu BZ, Zheng Y, Xiong GB, Xuan ZX, Zhang GN, Zhou JL, Wu B, Lin GL, Qiu HZ. [Acquiring laparoscopic skill for colorectal surgery: based on the experience of a colorectal surgeon]. Zhonghua Wai Ke Za Zhi 2012; 50: 1063-7. Gong J, Shi DB, Li XX, Cai SJ, Guan ZQ, Xu Y. Short-term outcomes of laparoscopic total mesorectal excision compared to open surgery. World J Gastroenterol 2012; 18: 7308-13. Wong TM, Day W, Kwok SY, Lau YY, Yip WC. Single incision laparoscopic right hemicolectomy: different approaches. Chin Med J (Engl) 2013; 126: 238-41. Chen G, Liu Z, Han P, Li JW, Cui BB. The learning curve for the laparoscopic approach for colorectal cancer: a single institution’s experience. J Laparoendosc Adv Surg Tech A 2013; 23: 17-21. Du XH, Shen D, Li R, Li SY, Ning N, Zhao YS, Zou ZY, Liu N. Robotic anterior resection of rectal cancer: technique and early outcome. Chin Med J (Engl) 2013; 126: 51-4. Hua-Feng P, Zhi-Wei J, Gang W, Xin-Xin L, FengTao L. A novel approach for the resection of low rectal cancer. Surg Laparosc Endosc Percutan Tech 2012; 22: 537-41. Zhou YH, Peng X, Deng JZ, Cheng LQ, Li ZC, Zhu JC, Guo XX. [Causes of anastomotic leakage after colorectal cancer laparoscopic-assisted surgery]. Zhonghua Yi Xue Za Zhi 2012; 92: 2553-5. Han DP, Lu AG, Feng H, Wang PX, Cao QF, Zong YP, Feng B, Zheng MH. Long-term results of laparoscopy-assisted radical right hemicolectomy with D3 lymphadenectomy: clinical analysis with 177 cases. Int J Colorectal Dis 2013; 28: 623-9. Chi P, Chen ZF, Lin HM, Lu XR, Huang Y. Laparoscopic extralevator abdominoperineal resection for rectal carcinoma with transabdominal levator transection. Ann Surg Oncol 2013; 20: 1560-6. Wang DG, Suo J, Zhang Y, Yu JH, Chen Y, He L, Sun X, Xia MJ. [Use of laparoscope complete mesocolic excision in the surgical treatment of right colon cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 971-3. Li Z, Ying X, Shen Y, Ye P, Pan W, Chen H. Laparoscopic versus open surgery for rectal cancer: a clinical comparative study. J Int Med Res 2012; 40: 1599-607. Wang L, Tan HM, Tan JW, Chu Y, Ding XM, Dong JH. Laparoscopic approach for simultaneous treatment of rectal cancer and synchronous
4642
[50]
[51]
[52]
[53]
[54]
[55]
[56]
[57]
[58]
[59]
[60]
liver metastases: indications and initial experience. Hepatogastroenterology 2013; 60: 21721. Hu MG, Ou-yang CG, Zhao GD, Xu DB, Liu R. Outcomes of open versus laparoscopic procedure for synchronous radical resection of liver metastatic colorectal cancer: a comparative study. Surg Laparosc Endosc Percutan Tech 2012; 22: 364-9. She WH, Poon JT, Fan JK, Lo OS, Law WL. Outcome of laparoscopic colectomy for cancer in elderly patients. Surg Endosc 2013; 27: 30812. Han Y, He YG, Zhang HB, Lv KZ, Zhang YJ, Lin MB, Yin L. Total laparoscopic sigmoid and rectal surgery in combination with transanal endoscopic microsurgery: a preliminary evaluation in China. Surg Endosc 2013; 27: 518-24. Li BG, Nie XY, He YZ, Xie HH, Yu GZ, Du HP, Kong FD, Gong DH, Lin WB, Wu MJ. [The standardized practice of laparoscopic-assisted radical right hemicolectomy in order to achieve complete mesocolic excision]. Zhonghua Wai Ke Za Zhi 2012; 50: 215-8. Cheung TP, Cheung HY, Ng LW, Chung CC, Li MK. Hybrid NOTES colectomy for right-sided colonic tumors. Asian J Endosc Surg 2012; 5: 46-9. Chi P, Chen ZF, Lin HM, Lu XR, Huang Y. [Laparoscopic cylindrical abdominoperineal resection with transabdominal approach for lower rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 589-93. Feng B, Sun J, Ling TL, Lu AG, Wang ML, Chen XY, Ma JJ, Li JW, Zang L, Han DP, Zheng MH. Laparoscopic complete mesocolic excision (CME) with medial access for right-hemi colon cancer: feasibility and technical strategies. Surg Endosc 2012; 26: 3669-75. Lu L, Zhou D, Jian X, Deng J, Yang P, Ding W. Laparoscopic colorectomy for colorectal cancer: retrospective analysis of 889 patients in a single center. Tohoku J Exp Med 2012; 227: 171-7. Jiang HY, Zhang XF, Wang XZ, Li J, Zhang C. [Short-term outcomes of radical resection of rectal carcinoma: hand-assisted laparoscopy versus traditional laparoscopic approach]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 517-9. Yan W, Amin BH, Zhu B, Zhang NW, Lian DB, Fan Q. [Transanal specimen extraction in laparoscopic colorectal resection]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 505-7. Han Y, He YG, Lin MB, Zhang HB, Lu XS, Lv KZ, Hua ZL, Zhang YJ, Yin L. [Total laparoscopic sigmoid and rectal surgery combined with transanal endoscopic microsurgery]. Zhonghua Wei Chang Wai Ke Za Zhi 2012; 15: 499-501.
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China [61] Zhong B, Liu F, Yu J, Liang Y, Zhao L, Mou T, Hu Y, Li G. [Comparison of long-term oncological outcomes of laparoscopic and open resection of rectal cancer]. Nan Fang Yi Ke Da Xue Xue Bao 2012; 32: 664-8. [62] Ge L, Wang HJ, Zhao ZL, Yang XH, Zhao WM, Hati P, Liu L. [Evaluation of short-term efficacy and safety after laparoscopic resection for mid-low rectal cancer]. Zhonghua Yi Xue Za Zhi 2012; 92: 98-101. [63] Ng LW, Tung LM, Cheung HY, Wong JC, Chung CC, Li MK. Hand-assisted laparoscopic versus total laparoscopic right colectomy: a randomized controlled trial. Colorectal Dis 2012; 14: e612-7. [64] Fang JF, Wei HB, Chen TF, Huang Y, Wei B, Zheng ZH, Huang JL, Xu HZ. [Laparoscopy-assisted combined radical resection for synchronous rectal and gastric cancer in elderly patients: report of two cases]. Zhonghua Wei Chang Wai Ke Za Zhi 2012 ; 15: 149-51. [65] Wang G, Jiang ZW, Zhao K, Gao Y, Liu FT, Pan HF, Li JS. Fast track rehabilitation programme enhances functional recovery after laparoscopic colonic resection. Hepatogastroenterology 2012; 59: 2158-63. [66] Liu L, Cao Y, Zhang G, Zhang L, Wang P, Gong J. Long-term outcomes after laparoscopic total mesorectal excision for advanced rectal cancer. S Afr J Surg 2011; 49: 186-9. [67] Song W, Han FH, He YL, Peng JJ, Cai SR, Li HM. [Comparison of clinical outcomes between laparoscopic-assisted and hand-assisted laparoscopic operations in colorectal cancer]. Zhonghua Yi Xue Za Zhi 2011; 91: 2485-7. [68] Law WL, Poon JT, Fan JK, Lo OS. Survival following laparoscopic versus open resection for colorectal cancer. Int J Colorectal Dis 2012; 27: 1077-85. [69] Yang Z, Xu H, Zhang W, Xu Y, Xu Z. A retrospective analysis of ultralow anterior resection vs. abdomino-perineal resection for lower rectal cancer. Hepatogastroenterology 2012; 59: 1780-3. [70] Chen KY, Xiang GA, Wang HN, Xiao FL. Simultaneous laparoscopic excision for rectal carcinoma and synchronous hepatic metastasis. Chin Med J (Engl) 2011; 124: 2990-2. [71] Zong L, Chen P, Kitano S, Jiang G, Tan J, Reddy SS, Zhao W, Shi L, Qing XH, Shi GH, Xu DF, Wang L, Jiang J. Clinical experience and analysis of laparoscopic total mesorectal excision combined with improved Bacon for the treatment of lower rectal cancer. Hepatogastroenterology 2011; 58: 1538-44. [72] Liang JW, Zhang XM, Zhou ZX, Wang Z, Bi JJ. [Learning curve of laparoscopic-assisted surgery for rectal cancer]. Zhonghua Yi Xue Za Zhi 2011; 91: 1698-701.
4643
[73] Li JC, Leung KL, Ng SS, Liu SY, Lee JF, Hon SS. Laparoscopic-assisted versus open resection of right-sided colonic cancer--a prospective randomized controlled trial. Int J Colorectal Dis 2012; 27: 95-102. [74] Liu T, Zhang C, Yu P, Chen J, Zeng D, Gan L, Lv W, Liu L, Yan X. Laparoscopic radical correction combined with extensive lymphadenectomy and pelvic autonomic nerve preservation for mid-to-low rectal cancer. Clin Colorectal Cancer 2011; 10: 183-7. [75] Sun J, Jiang T, Qiu Z, Cen G, Cao J, Huang K, Pu Y, Liang H, Huang R, Chen S. Short-term and medium-term clinical outcomes of laparoscopic-assisted and open surgery for colorectal cancer: a single center retrospective case-control study. BMC Gastroenterol 2011; 11: 85. [76] Li SY, Chen G, Chen G, Zuo FY, Wei XJ, Yuan Q, DU JF. [Clinical study of laparoscopic sphincterpreserving proctectomy for low rectal cancer using transanal telescopic anastomosis]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 532-4. [77] Zhang H, Li M, Zhan TC, Yao YF, Peng YF, Gu J. [Comparison of short-term postoperative outcomes between hand-assisted laparoscopic and conventional sigmoidectomy]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 462-4. [78] Zhou ZX, Zheng XF, Song HY, Jiang FZ, Wang ZJ, Zuo ZG, Cai HJ, Ruan XJ. [Laparoscopic total mesorectal excision combined with intersphincteric resection for ultra-low rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 440-2. [79] Ng DC, Co CS, Cheung HY, Chung CC, Li MK. The outcome of laparoscopic colorectal resection in T4 cancer. Colorectal Dis 2011; 13: e349-52. [80] Bao Y, Jiang ZW, Xie LF, Liu FT, Li JS. [Roboticassisted laparoscopic colectomy for colon cancer: a report of 13 cases]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 327-9. [81] Luo CY, Ji XX, Zhang J, Zhou YQ, Guan C. [Clinical study of laparoscopic rectal surgery without abdominal scar]. Zhonghua Yi Xue Za Zhi 2011; 91: 686-8. [82] Li S, Chi P, Lin H, Lu X, Huang Y. Long-term outcomes of laparoscopic surgery versus open resection for middle and lower rectal cancer: an NTCLES study. Surg Endosc 2011; 25: 3175-82. [83] Liang X, Hou S, Liu H, Li Y, Jiang B, Bai W, Li G, Wang W, Feng Y, Guo J. Effectiveness and safety of laparoscopic resection versus open surgery in patients with rectal cancer: a randomized, controlled trial from China. J Laparoendosc Adv Surg Tech A 2011; 21: 381-5. [84] Chen WT, Chang SC, Chiang HC, Lo WY, Jeng LB, Wu C, Ke TW. Single-incision laparoscopic
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China
[85]
[86]
[87]
[88]
[89]
[90]
[91]
[92]
[93]
[94]
[95]
versus conventional laparoscopic right hemicolectomy: a comparison of short-term surgical results. Surg Endosc 2011; 25: 1887-92. Cui J, Zhang JL, Wang S, Sun ZQ, Jiang XL. [A preliminary study of stenting followed by laparoscopic surgery for obstructing left-sided colon cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 40-3. Qiu XF, Lin L, Yuan SB, Yan F, Ding ZJ, Bai LP, Ye ZJ, Lin WJ, Qi ZQ, Liu ZC. [Transumbilical singleport access laparoscopic surgery for colorectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 34-6. Qiu HZ, Xiao Y, Wu B, Lin GL, Wu X. [Laparoscopic-assisted anterior perineal plane for ultra-low anterior resection of the rectal cancer(APPEAR)]. Zhonghua Wei Chang Wai Ke Za Zhi 2011; 14: 24-6. Guan GX, Liu X, Jiang WZ, Chen ZF, Lu HS. [Short-term efficacy of laparoscopic-assisted right hemicolectomy with D3 lymph node dissection in colon cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2010; 13: 917-20. Feng B, Zhu QL, Xia Y, Lu AG, Wang ML, Li JW, Hu WG, Zang L, Mao ZH, Dong F, Ma JJ, Zheng MH. Direct and indirect costs and long-term survival of laparoscopic anterior resection for rectal cancer. Med Sci Monit 2010; 16: PH97102. Zheng MH, Feng B, Hu CY, Lu AG, Wang ML, Li JW, Hu WG, Zang L, Mao ZH, Dong TT, Dong F, Cai W, Ma JJ, Zong YP, Li MK. Long-term outcome of laparoscopic total mesorectal excision for middle and low rectal cancer. Minim Invasive Ther Allied Technol 2010; 19: 329-39. Li J, Chen R, Xu YQ, Wang XC, Zheng S, Zhang SZ, Ding KF. Impact of a laparoscopic resection on the quality of life in rectal cancer patients: results of 135 patients. Surg Today 2010; 40: 917-22. Zhu QL, Feng B, Lu AG, Wang ML, Hu WG, Li JW, Mao ZH, Zheng MH. Laparoscopic low anterior resection for rectal carcinoma: complications and management in 132 consecutive patients. World J Gastroenterol 2010; 16: 4605-10. Wu QH, Zhang T, Zang L, Mao ZH, Li JW, Lu AG, Wang ML, Zheng MH. [Impact of previous abdominal operations on the outcome of laparoscopic colorectal cancer surgery: a non-randomized cohort study]. Zhonghua Wai Ke Za Zhi 2010; 48: 675-80. Yan J, Ying MG, Zhou D, Chen X, Chen LC, Ye WF, Zang WD. [A prospective randomized control trial of the approach for laparoscopic right hemi-colectomy:medial-to-lateral versus lateral-to-medial]. Zhonghua Wei Chang Wai Ke Za Zhi 2010; 13: 403-5. Li JC, Lee JF, Ng SS, Yiu RY, Hon SS, Leung WW, Leung KL. Conversion in laparoscopic-assisted
4644
colectomy for right colon cancer: risk factors and clinical outcomes. Int J Colorectal Dis 2010; 25: 983-8. [96] Qin H, Zhang XP, Zhou Y, Li HC, Li T. [Experience of laparoscopic total mesorectal excision for middle or low rectal cancer]. Zhonghua Zhong Liu Za Zhi 2010; 32: 156-7. [97] Cheung HY, Ng KH, Leung AL, Chung CC, Yau KK, Li MK. Laparoscopic sphincter-preserving total mesorectal excision: 10-year report. Colorectal Dis 2011; 13: 627-31. [98] Wang XF, Ruan Y, Li W, Zhou SJ, Peng JF, Cai XJ. [Minimally invasive surgery for colorectal cancer with liver metastasis]. Zhonghua Yi Xue Za Zhi 2009; 89: 2277-9. [99] Cheung HY, Chung CC, Tsang WW, Wong JC, Yau KK, Li MK. Endolaparoscopic approach vs conventional open surgery in the treatment of obstructing left-sided colon cancer: a randomized controlled trial. Arch Surg 2009; 144: 1127-32. [100] Yu J, Zhang C, Wang YN, Hu YF, Cheng X, Li GX. [Laparoscopic versus open total mesorectal excision for the middle-lower rectal cancer: a clinical comparative study]. Zhonghua Wei Chang Wai Ke Za Zhi 2009; 12: 573-6. [101] Wan X, Zhang Y, Zhang Y. [Anus-preserving laparoscopic rectal resection in 75 patients with lower rectal cancer]. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2009; 34: 902-4. [102] Wang ZD, Wu ZY, Li Y, Wu WL, Lin F. [Clinical efficacy comparison between laparoscopy and open radical resection for 191 advanced colorectal cancer patients]. Zhonghua Wei Chang Wai Ke Za Zhi 2009; 12: 368-70. [103] Chen KY, Xiang GA, Wang HN, Xiao FL. [Simultaneous laparoscopic excision for the treatment of rectal carcinoma and the synchronous hepatic metastasis]. Zhonghua Zhong Liu Za Zhi 2009; 31: 69-71. [104] Li JC, Hon SS, Ng SS, Lee JF, Yiu RY, Leung KL. The learning curve for laparoscopic colectomy: experience of a surgical fellow in an university colorectal unit. Surg Endosc 2009; 23: 16038. [105] Mao ZH, Jin J, Li JW, Deng YX, Wang ML, Lu AG, Hu WG, Zheng MH. [Safety study of laparoscopic surgery for colorectal cancer in elderly patients]. Zhonghua Wei Chang Wai Ke Za Zhi 2009; 12: 244-8. [106] Xiong H, Yu J, Zhang C, Wang YN, Hu YF, Li GX. [Application of laparoscopic surgery following neoadjuvant chemoradiotherapy for mid-low rectal cancer]. Nan Fang Yi Ke Da Xue Xue Bao 2009; 29: 754-6. [107] Ng KH, Ng DC, Cheung HY, Wong JC, Yau KK, Chung CC, Li MK. Laparoscopic resection for rectal cancers: lessons learned from 579 cases. Ann Surg 2009; 249: 82-6.
Int J Clin Exp Med 2014;7(12):4635-4645
Laparoscopic surgery for colorectal cancer in China [108] Ding KF, Chen R, Zhang JL, Li J, Xu YQ, Lv L, Wang XC, Sun LF, Wang JW, Zheng S, Zhang SZ. Laparoscopic surgery for the curative treatment of rectal cancer: results of a Chinese three-center case-control study. Surg Endosc 2009; 23: 854-61. [109] Cheung HY, Chung CC, Wong JC, Yau KK, Li MK. Laparoscopic rectal cancer surgery with and without neoadjuvant chemo-irradiation: a comparative study. Surg Endosc 2009; 23: 14752. [110] Law WL, Fan JK, Poon JT, Choi H, Lo OS. Laparoscopic bowel resection in the setting of metastatic colorectal cancer. Ann Surg Oncol 2008; 15: 1424-8. [111] Ng SS, Lee JF, Yiu RY, Li JC, Leung WW, Leung KL. Emergency laparoscopic-assisted versus open right hemicolectomy for obstructing rightsided colonic carcinoma: a comparative study of short-term clinical outcomes. World J Surg 2008; 32: 454-8. [112] Zhang H, Hu S, Zhi X, Wang L, Zhang G, Wang K. Laparoscopic proctocolectomy with ileal pouch-anal anastomosis. Surg Laparosc Endosc Percutan Tech 2007; 17: 388-91. [113] Zhang H, Hu S, Zhang G, Wang K, Chen B, Li B, Frezza EE. Laparoscopic versus open proctocolectomy with ileal pouch-anal anastomosis. Minim Invasive Ther Allied Technol 2007; 16: 187-91. [114] Ng SS, Lee JF, Yiu RY, Li JC, Hon SS. Telerobotic-assisted laparoscopic abdominoperineal resection for low rectal cancer: report of the first case in Hong Kong and China with an updated literature review. World J Gastroenterol 2007; 13: 2514-8. [115] Pan YF, Zhang XH, Jia XJ, Qu JM, Xiang YQ, Yang K, Lin BR, Zheng XF, Zheng J. [Laparoscopic abdominoperineal resection for low rectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi 2007; 10: 253-6. [116] Liang JT, Lai HS, Lee PH, Huang KC. Comparison of functional and surgical outcomes of laparoscopic-assisted colonic J-pouch versus straight reconstruction after total mesorectal excision for lower rectal cancer. Ann Surg Oncol 2007; 14: 1972-9. [117] Yan SL, Xu ZB, Chi P, Lin HM. [Comparing the influencing factors of anastomotic bleeding in rectal carcinoma resection between laparoscopic and open radical approaches]. Zhonghua Wei Chang Wai Ke Za Zhi 2007; 10: 157-9. Chinese. [118] Ng SS, Yiu RY, Li JC, Lee JF, Leung KL. Emergency laparoscopically assisted right hemicolectomy for obstructing right-sided colon carcinoma. J Laparoendosc Adv Surg Tech A 2006; 16: 350-4.
4645
[119] Mao ZH, Chen HZ, Li JW, Lu AG, Wang ML, Hu WG, Zheng MH. [Comparison of inflammatory response after laparoscopic and conventional surgery for colorectal carcinoma]. Zhonghua Wei Chang Wai Ke Za Zhi 2006; 9: 297-300. [120] Qian LY, Wu JH, Chen DJ, Li XR, Wei YS. [Comparative study on long-term results of laparoscopic and open radical resection for colorectal carcinoma]. Zhonghua Wei Chang Wai Ke Za Zhi 2006; 9: 294-6. [121] Ng SS, Li JC, Lee JF, Yiu RY, Leung KL. Laparoscopic total colectomy for colorectal cancers: a comparative study. Surg Endosc 2006; 20: 1193-6. [122] Feng B, Zheng MH, Mao ZH, Li JW, Lu AG, Wang ML, Hu WG, Dong F, Hu YY, Zang L, Li HW. Clinical advantages of laparoscopic colorectal cancer surgery in the elderly. Aging Clin Exp Res 2006; 18: 191-5. [123] Mou YP, Yang P, Yan JF, Chen QL, Yuan XM, Zhu LH, Xu XW. [Clinical evaluation of laparoscopic radical resection of colon cancer]. Zhonghua Wai Ke Za Zhi 2006; 44: 581-3. [124] Li GX, Yan HT, Yu J, Lei ST, Xue Q, Cheng X. [Learning curve of laparoscopic resection for rectal cancer]. Nan Fang Yi Ke Da Xue Xue Bao 2006; 26: 535-8. [125] Tsang WW, Chung CC, Kwok SY, Li MK. Laparoscopic sphincter-preserving total mesorectal excision with colonic J-pouch reconstruction: five-year results. Ann Surg 2006; 243: 353-8. [126] Zheng MH, Feng B, Lu AG, Li JW, Wang ML, Mao ZH, Hu YY, Dong F, Hu WG, Li DH, Zang L, Peng YF, Yu BM. Laparoscopic versus open right hemicolectomy with curative intent for colon carcinoma. World J Gastroenterol 2005; 11: 323-6. [127] Zhou ZG, Hu M, Li Y, Lei WZ, Yu YY, Cheng Z, Li L, Shu Y, Wang TC. Laparoscopic versus open total mesorectal excision with anal sphincter preservation for low rectal cancer. Surg Endosc 2004; 18: 1211-5. [128] 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: 1167-70. [129] Zhou ZG, Wang Z, Yu YY, Shu Y, Cheng Z, Li L, Lei WZ, Wang TC. Laparoscopic total mesorectal excision of low rectal cancer with preservation of anal sphincter: a report of 82 cases. World J Gastroenterol 2003; 9: 1477-81. [130] Tsang WW, Chung CC, Li MK. Prospective evaluation of laparoscopic total mesorectal excision with colonic J-pouch reconstruction for mid and low rectal cancers. Br J Surg 2003; 90: 867-71. [131] Tan M, Guo B, Wu Z, Chen G, Zheng Z, Zhao Z. [Laparoscopic colorectomy for colorectal cancer]. Zhonghua Wai Ke Za Zhi 2002; 40: 76972.
Int J Clin Exp Med 2014;7(12):4635-4645
