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International Journal of Clinical and Experimental Medicine logoLink to International Journal of Clinical and Experimental Medicine
. 2014 Dec 15;7(12):4635–4645.

Laparoscopic surgery for colorectal cancer in China: an overview

Ketao Jin 1,*, Jun Wang 2,*, Huanrong Lan 1,*, Ruili Zhang 1
PMCID: PMC4307407  PMID: 25663960

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 long-term 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 popular. 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 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.

Figure 1

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Numbers of full papers related to laparoscopic surgery for colorectal cancer in China (PubMed/Medline database).

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.

Table 1.

Survey over major reports of laparoscopic surgery for colorectal cancer in China: operative data (Articles in English)

Ref. PS/RS Patient (n) Approaches TME LN NeoA OT (min) BL (ml) C n (%)
[16] RS 197 NOSE/MLS Yes 17.0 ± 8.3 in NOSE; 18.9 ± 11.6 in MLS No 111.6 ± 25.4 in NOSE; 115.3 ± 23.0 in MLS 70.2 ± 66.1 in NOSE; 126.3 ± 58.6 in MLS NA
[17] RS 119 MLS Yes 22.3 ± 8.6 NA 257.8 ± 67.6 100 (100-200) 9 (7.6)
[19] RS 80 MLS Yes 11.86 ± 1.95 No 201.7 ± 6.91 97.25 ± 9.97 1 (1.3)
[21] RS 289 MLS Yes NA NA 155 ± 29 128 ± 24 NA
[23] RS 24 NOSE Yes NA NA 110.0 69.1 mL NA
[24] PS 21 NOSE Yes 17.8 ± 4.6 NA 132 ± 85 84 ± 15 NA
[25] PS 51 MLS Yes NA Yes 181.5 (95.0-310.0) 204.7 (80.0-1000.0) NA
[27] RS 64 MLS Yes 11.68 ± 5.69 No 183 ± 55 168 ± 106 NA
[30] PS 70 35 in NOTES; 35 in MLS Yes 12 (6-33) in NOTES; 12 (6-29) in MLS NA 105 (60-170) in NOTES; 100 (59-210) in MLS 30 (10-50) in NOTES; 30 (10-100) in MLS NA
[32] RS 87 MLS Yes 14 ± 5 NA 160 ± 40 28 ± 5 NA
[39] RS 67 MLS Yes 20.3 ± 8.3 NA 216.4 ± 68.3 86.9 ± 37.6 NA
[45] RS 177 MLS Yes 15.2 ± 10.1 No 133 ± 36 94 ± 34 5 (2.82)
[48] RS 381 MLS Yes 12.5 ± 4.2 NA 176.4 ± 28.3 58.3 ± 13.9 NA
[51] PS 189 MLS Yes NA NA 150 (81–360) 100 (0-1,000) NA
[52] RS 34 NOTES Yes 12.92 ± 2.2 NA 151.6 ± 25.93 200.2 ± 114.69 0
[51] RS 889 MLS Yes 12.27 ± 9.02 NA 201.66 ± 81.81 100 43 (4.84)
[63] PS 30 MLS Yes 16 (2-33) NA 111 (74-165) 20 (5-400) 1 (3.3)
[66] PS 125 MLS Yes NA Yes NA NA NA
[68] PS 814 MLS Yes 13 (8-18) NA 180 (141-218) 100 (50-200) NA
[73] PS 71 MLS Yes 18.7 ± 12 NA 198 ± 48 110.1 (0-1,000) NA
[75] RS 254 MLS Yes 12.0 ± 6.9 No 135.6 ± 40.0 101.5 ± 70.8 8 (3)
[82] RS 113 MLS Yes 20.3 ± 6.9 No 210.0 (100-420) 50.0 (0-1200) NA
[83] PS 169 MLS Yes 7.05 ± 5.05 No 138.08 ± 23.79 NA NA
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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.

Table 2.

Survey over major reports of laparoscopic surgery for colorectal cancer in China: Outcomes (Article in English)

Ref. Patient (n) F De IC (n, %) PC (n, %) HS (d) M n (%) FP (m) OSR (%) DFSR (%)
MH OI IL AS AB AL
[16] 197 2.7 ± 0.8 in NOSE; 3.4 ± 0.9 in MLS 3.3 ± 0.6 in NOSE; 3.9 ± 1.1 in MLS NA NA NA NA NA 2 (3.1) in NOSE; 6 (4.5) in MLS 9.0 ± 1.9 in NOSE; 9.9 ± 2.0 in MLS NA NA NA NA
[17] 119 2.7 ± 1.0 NA NA NA 4 (3.4) 1 (0.8) 1 (0.8) 2 (1.7) 11.4 ± 4.7 1 (0.8) 30 (3-60) 92.0% in 3 years 84.6% in 3 years
[19] 80 2.34 ± 0.12 NA 1 (1.3) 1 (1.3) 1 (1.3) 1 (1.3) 2 (2.5) NA 9.7 ± 0.59 NA 17.5 NA NA
[21] 289 NA NA NA NA NA NA NA NA 8.9 ± 2.1 NA NA NA NA
[23] 24 3.1 NA NA NA NA NA NA NA 9.2 NA NA NA NA
[24] 21 NA NA NA NA NA NA 0 1 (4.7) 6.1 ± 2.7 NA 12 NA NA
[25] 51 2.5 (1.5-4.0) 4.0 (2.0-8.0) NA NA NA NA NA 1 (3.1) NA 6 (11.8) NA NA NA
[27] 64 NA NA NA NA 5 (8) NA NA 3 (5) 12 (6-39) NA 17 38.7 ± 2.7 37.3 ± 2.5
[30] 70 NA NA NA NA NA NA NA NA NA NA NA NA NA
[32] 87 NA NA NA NA NA NA NA 1 (1.1) 5.2 ± 1.8 NA NA NA NA
[39] 67 46.9 ± 14.8 NA NA NA NA NA NA 1 (1.4) 10.4 ± 4.3 NA NA NA NA
[45] 177 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
[48] 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
[51] 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
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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.

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 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 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 5- and 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 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).

Disclosure of conflict of interest

None.

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