Surg Today DOI 10.1007/s00595-014-0925-1

ORIGINAL ARTICLE

Feasibility and safety of laparoscopic surgery for metachronous colorectal cancer Toshiya Nagasaki • Takashi Akiyoshi • Masashi Ueno • Yosuke Fukunaga • Satoshi Nagayama • Yoshiya Fujimoto Tsuyoshi Konishi • Masami Arai • Toshiharu Yamaguchi



Received: 24 November 2013 / Accepted: 1 April 2014 Ó Springer Japan 2014

Abstract Purpose This study assessed the feasibility and safety of laparoscopic surgery for metachronous colorectal cancer in patients who had previously undergone surgery for primary colorectal cancer. Methods Of the 52 patients who underwent curative resection for metachronous colorectal cancer from August 2004 to April 2013, 26 each underwent laparoscopic and open surgery. Their clinical characteristics and surgical and postoperative outcomes were compared. Results The percentage of patients who underwent previous open surgery was significantly higher in the open group than in the laparoscopic group (92.3 vs. 65.4 %). The body mass index was higher in the laparoscopic group than in the open group (23.8 vs. 21.1 kg/m2), and the amount of blood loss was significantly smaller in the laparoscopic than in the open group (30 vs. 195 ml); however, the mean operative time did not differ significantly. The time to first flatus (1 vs. 3 days) and first stool (2 vs. 3.5 days), as well as the length of postoperative hospital stay (10 vs. 16 days), was significantly shorter in the laparoscopic group than in the open group, although

T. Nagasaki  T. Akiyoshi (&)  M. Ueno  Y. Fukunaga  S. Nagayama  Y. Fujimoto  T. Konishi  T. Yamaguchi Department of Gastroenterological Surgery, Cancer Institute Hospital, Japanese Foundation for Cancer Research, 3-8-31 Ariake, Koto-ku, Tokyo 135-8550, Japan e-mail: [email protected] M. Arai Department of Clinical Genetic Oncology, Cancer Institute Hospital, Japanese Foundation for Cancer Research, 3-8-31 Ariake, Koto-ku, Tokyo 135-8550, Japan

the rates of postoperative complications did not differ (15.4 vs. 23.1 %). Conclusions Laparoscopic surgery for metachronous colorectal cancer shows short-term benefits compared with open surgery and should be considered as a treatment option in these patients. Keywords Laparoscopic surgery  Metachronous colorectal cancer  Previous abdominal surgery  Lynch syndrome  Hereditary nonpolyposis colorectal cancer

Introduction Metachronous colorectal cancer is defined as the occurrence of an additional primary colorectal cancer more than 6 months after the detection of the index primary colorectal cancer. The incidence of metachronous colorectal cancer has been found to range from 0.2 to 3.6 % [1–4]. Patients with colorectal cancer now have a better prognosis due to medical advances. However, the longer a patient survives after the removal of colorectal cancer, the more likely they are to develop metachronous colorectal cancer. Therefore, the number of patients who undergo repeated colorectal cancer resection may increase in the future. Progressive improvements in technology and the experience of surgeons have made possible the extension of indications for laparoscopic surgery to operations that previously required open surgery. Few studies, however, have assessed the safety and feasibility of laparoscopic surgery for metachronous colorectal cancer. This study therefore assessed the feasibility and safety of laparoscopic surgery in patients with metachronous colorectal cancer who have previously undergone surgery for colorectal cancer.

123

Surg Today

Methods Patients were included if they had undergone curative resection for metachronous colorectal cancer via a laparoscopic or open approach between August 2004 and April 2013. Metachronous cancer was defined as a second or third primary colorectal cancer occurring more than 6 months after the diagnosis of the previous cancer, without evidence of local recurrence or metastasis from the primary tumor [5, 6]. Patients undergoing palliative surgery or transanal excision were excluded, as were those with anal canal cancer or adenoma. Patients with Lynch syndrome, also called hereditary nonpolyposis colorectal cancer (HNPCC), were included. These patients were assessed using microsatellite instability (MSI) tests and immunohistochemistry for MLH1, MSH2, MSH6 and PMS2, with Lynch syndrome finally diagnosed on genetic testing for germline mutations in the mismatch repair genes. A retrospective review of our prospectively maintained database identified 52 patients with metachronous colorectal cancer who had undergone curative resection between August 2004 and April 2013. The clinical features of the patients, including gender, age at surgery, body mass index (BMI; kg/m2), American Society of Anesthesiologists (ASA) classification score, presence or absence of Lynch syndrome, interval between operations for previous and metachronous cancers, type of previous operation, number of previous operations, tumor location and Union for International Cancer Control (UICC) TNM stage, were fully reviewed. Operative and postoperative parameters were also investigated, including the type of surgical procedure, extent of lymph node dissection, number of lymph nodes harvested, tumor size, operative time, estimated blood loss, resection of previous anastomotic site, rate of anus-preserving surgery, rate of conversion to open surgery, time to first flatus and first stool, postoperative complications, rate of reoperation and length of postoperative hospital stay. The data were compared between the patients who underwent laparoscopic (n = 26) and open (n = 26) surgery for metachronous colorectal cancer. Laparoscopic surgery was introduced at our institution in July 2005. The initial contraindications for laparoscopic surgery included bulky tumors, tumors invading adjacent organs and tumors with synchronous liver metastasis. However, the indications for laparoscopic surgery were gradually extended, as our surgical teams gained greater experience; at present, there are no longer contraindications for laparoscopic surgery [7]. The presence of abdominal adhesion is not contraindication for laparoscopic surgery, although the expectation of severe adhesion affects the decision to perform laparoscopic or open surgery. The final decision to perform laparoscopic or open

123

surgery in each patient was made at the surgeon’s discretion. All laparoscopic surgical procedures were performed by board-certified colorectal surgeons. Open conversion was defined as the creation of a larger or different skin incision than originally planned at the beginning of the operation. All open surgical procedures were performed by colorectal surgeons who had experienced more than 200 open colorectal surgeries. The summarized data are presented as medians and ranges. Categorical variables were compared using the Chisquare test or Fisher’s exact test, as appropriate, and continuous variables were compared using the Mann–Whitney U test. All p values \0.05 were considered to be statistically significant.

Results The study population comprised 52 patients, including 33 males and 19 females, with metachronous colorectal cancer. Of these patients, 48 had previously undergone one operation for colorectal cancer, while four had undergone two previous resections each. Table 1 shows the clinical differences between the previous and metachronous colorectal cancers. The time of diagnosis of previous colorectal cancers was divided into three periods: 1960–1980, 1980–2000 and 2000-present. Fifty-seven percent of previous colorectal cancer resection procedures were performed at other institutions. The locations of the previous and metachronous tumors were similar. Of the 56 previous resections, 12 were performed laparoscopically. Table 1 Differences between previous operations for primary colorectal cancer and operations for metachronous colorectal cancers Previous cancers (n = 56)a

Metachronous cancers (n = 52)

1960–1980

3

0

1980–2000

22

0

2000

31

52

Right colon

23

24

Left colon

21

20

Rectum

11

5

1 24/56 (42.9 %)

3 52/52 (100 %)

Open surgery

44

26

Laparoscopic surgery

12

26

Period of operation

Location

Multiple Operation performed at our institution Type of operation

a

Four patients underwent two previous operations each for colorectal cancer

Surg Today Table 2 Clinical characteristics of the patients who underwent laparoscopic and open surgery n = 52

Laparoscopic (n = 26)

Open (n = 26)

p value

16

17

0.7734

Female Age at surgery, years (range)

10 69 (23–89)

9 72 (46–87)

0.6735

BMI, kg/m2 (range)

23.8 (16.5–27.2)

Table 3 Surgical outcomes (laparoscopic vs. open surgery)

21.1 (14.8–29.4)

0.0805

10

7

II

15

16

III

1

3

Diagnosis of Lynch 5 (19.2 %) syndrome Interval between operations 6 months to 1 year

1

6 (23.1 %)

2

1–5 years

7

6

5–10 years

9

10

]10 years

9

8

17

24

Laparoscopic surgery

9

2

0.7342

2 Tumor locationa Right colon

24

24

2

2

14

13

Left colon

10

12

Rectum

4

3

0

4

0

I

10

7

II

9

11

III

3

6

IV

0

2

5

8

0.4021

Left hemicolectomy

2

3

Ileocecal resection

2

2

Transverse colectomy

5

2

Sigmoidectomy

8

2

3

5

1

3

Abdominoperineal resection or Hartmann

1

1

D1

3

4

D2

8

13

D3

15

9

Number of lymph nodes harvested

16 (6–44)

13 (1–55)

0.4349

Tumor size, mm (range)

27.5 (10–80)

33.5 (8–130)

0.4039

Operation time, min (range)

227.5 (128–522)

224 (75–465)

0.5955

D number

0.9141

0.0385

Number of previous operations 1

Right hemicolectomy

Subtotal or total colectomy

0.4580

Type of previous operation Open surgery

p value

Anterior resection

ASA score I

Open (n = 26)

Operative proceduresa

Gender Male

Laparoscopic (n = 26)

1.0000

0.8346

Pathological stage 0.1020

BMI body mass index, ASA score American Society of Anesthesiologists classification score a

The laparoscopic surgery group included one patient with triple primary cancers. The open surgery group included two patients each with double primary cancers

The 52 patients included 26 subjects (50 %) who underwent laparoscopic surgery and 26 subjects (50 %) who underwent open surgery for metachronous colorectal cancer. Table 2 summarizes the clinical characteristics of these patients. There were no significant differences between the groups in gender distribution, age at surgery, ASA status, diagnosis of Lynch syndrome, interval

0.2425

Blood loss, ml (range)

30 (2–435)

195 (15–940)

0.0001

Resection at previous anastomotic site

4 (15.4 %)

8 (30.8 %)

0.3238

Anus-preserving operation

25 (96.2 %)

25 (96.2 %)

1.0000

Conversion to open surgery

2 (7.7 %)





a

One patient in the laparoscopy group underwent simultaneous anterior resection and right hemicolectomy

between previous and metachronous surgeries, number of previous operations, tumor location or pathological stage. The BMI values tended to be higher in the laparoscopic group than in the open group (p = 0.0805). The percentage of previous open surgeries was significantly higher in the open group than in the laparoscopic group. Table 3 summarizes the surgical outcomes. The operative procedure, extent of lymph node dissection, number of lymph nodes harvested (16 vs. 13), tumor size (27.5 vs. 33.5 mm) and operative time (228 vs. 224 min) did not differ significantly between the laparoscopic and open groups. The amount of estimated blood loss was significantly smaller in the laparoscopic group than in the open group (30 vs. 195 ml). The number of patients requiring resection at a previous anastomotic site was smaller in the laparoscopic group than in the open group (4 vs. 8), although the difference was not statistically significant. Two patients (7.7 %) in the laparoscopic group required conversion to open surgery due to severe adhesion; both had previously undergone two resections each for

123

Surg Today Table 4 Postoperative outcomes (laparoscopic vs. open surgery) Laparoscopic (n = 26)

Open (n = 26)

p value

Time to first flatus passage, days (range)

1 (1–4)

3 (1–5)

0.0017

Time to first stool, days (range)

2 (1–13)

3.5 (1–10)

0.0232

Postoperative complications

0.7265

4 (15.4 %)

6 (23.1 %)

Surgical site infection

0

3

Ileus

0

3

Enterocolitis

1

0

Anastomotic site bleeding

1

0

Anastomotic leakage

1

0

1

0

Reoperation

Small bowel perforation

1 (3.8 %)

0 (0 %)

1.0000

Postoperative hospital stay, days (range)

10 (7–48)

16 (6–37)

0.0075

Mortality

0 (0 %)

0 (0 %)



colorectal cancer. The final pathological findings showed that all patients in both groups underwent R0 resection. Table 4 summarizes the postoperative outcomes. The time to first flatus (1 vs. 3 days) and first stool (2 vs. 3.5 days) was significantly shorter in the laparoscopic group than in the open group. The rate of postoperative complications did not differ significantly between the two groups (15.4 vs. 23.1 %). One patient in the laparoscopic group underwent reoperation 2 days later due to an injury to the small intestine, and another patient in the laparoscopic group had minor anastomotic leakage, which was managed conservatively. There were no deaths in either group. The postoperative hospital stay was significantly shorter in the laparoscopic group than in the open group (10 vs. 16 days).

Discussion Laparoscopic surgery is an accepted treatment option for colorectal cancer and is becoming increasingly performed worldwide. Less is known, however, about the safety of laparoscopic surgery for metachronous colorectal cancer. To our knowledge, this study is the largest study to date to analyze the feasibility of laparoscopic surgery for metachronous colorectal cancer, by comparing outcomes in these patients with those observed in subjects who underwent open surgery. A recent study evaluated the perioperative outcomes of six patients who underwent laparoscopic surgery and five patients who underwent open surgery for metachronous colorectal cancer [8]. The operative time was significantly shorter in the laparoscopic group; however, none of the

123

other variables differed significantly. Since the total number of patients was small (11), this study may have been too underpowered to detect statistically significant differences [8]. In contrast, the present study, which involved 52 patients, showed that the amount of blood loss was significantly lower, the rate of gastrointestinal recovery significantly faster and the length of hospital stay significantly shorter in the laparoscopic group than in the open surgery group. The efficacy of laparoscopic surgery for colon cancer has already been demonstrated [9–11], with this study being the first to show that laparoscopic surgery also benefits patients undergoing resection for metachronous colorectal cancer. During the second or third operation for metachronous colorectal cancer, it is sometimes difficult to decide whether the range of bowel resection should include the previous anastomotic site. For example, if the root of the inferior mesenteric artery was divided during the previous operation, dividing the middle colic artery during surgery for transverse colon cancer would result in an insufficient blood supply to the left colon, indicating the need to resect a longer portion of the left colon, including the previous anastomotic site. Among our patients, four of 26 (15 %) in the laparoscopic group and eight of 26 (31 %) in the open group underwent colorectal resection that included the previous anastomotic site. Moreover, 23 patients (88 %) in the laparoscopic group and 22 patients (85 %) in the open group underwent more than D2 lymph node dissection, with the number of lymph nodes retrieved not differing significantly between these two groups. Taken together, these results suggest the feasibility of laparoscopic radical surgery for metachronous colorectal cancer. We found that two of the 26 (7.7 %) patients who underwent laparoscopic surgery required conversion to open surgery, a conversion rate similar to that previously reported in patients who underwent laparoscopic multivisceral resection for primary colorectal cancer (6.7 %) [7] but higher than that noted in our previous study, which showed a 1.0 % conversion rate [12, 13]. The higher conversion rate observed in this study may have been due to the relatively high percentage of difficult laparoscopic surgeries for metachronous colorectal cancer. Other reports of laparoscopic colorectal cancer surgery in patients with a history of previous abdominal surgery have reported conversion rates ranging from 14.5 to 26.1 % [3, 14–19]. Both of our patients who required conversion to open surgery and the patient who required reoperation had undergone two previous open surgeries for colorectal cancer. Adequate case selection and substantial experience with laparoscopic colorectal cancer surgery are indispensable for successful laparoscopic surgery for metachronous colorectal cancer. A subgroup analysis of the laparoscopic surgery group showed that none of the nine patients who

Surg Today

underwent previous laparoscopic colorectal cancer surgery required conversion to open surgery and none experienced postoperative complications. Moreover, the length of postoperative hospital stay was significantly shorter in these patients (9 vs. 12 days, p = 0.0299) than in the 17 patients in the laparoscopic group who underwent previous open colorectal cancer surgery. Laparoscopic colorectal surgery has been reported to result in fewer instances of adhesion, compared with open surgery, due to reduced tissue handling and/or exposure of the bowel to the environment [20]. Patients with metachronous colorectal cancer who have undergone previous colorectal cancer surgery with laparoscopy may therefore be good candidates for laparoscopy. This study is associated with several limitations, including the relatively small number of patients and potentially different backgrounds of the patients in the laparoscopic and open groups. Furthermore, there was insufficient long-term follow-up, especially in the laparoscopic group. However, our results showed that laparoscopic surgery for metachronous colorectal cancer is feasible and safe under proper case selection, with shortterm benefits, including significantly lower blood loss, a faster gastrointestinal recovery and shorter hospital stay compared with open surgery. Laparoscopic surgery should therefore be considered a treatment option in patients with metachronous colorectal cancer. Conflict of interest Toshiya Nagasaki and the coauthors have no conflicts of interest or financial ties to disclose in association with this study.

6. 7.

8.

9.

10.

11.

12.

13.

14.

15.

16.

References 1. Belizon A, Sardinha CT, Sher ME. Converted laparoscopic colectomy: what are the consequences? Surg Endosc. 2006;20: 947–51. 2. Cali RL, Pitsch RM, Thorson AG, Watson P, Tapia P, Blatchford GJ, et al. Cumulative incidence of metachronous colorectal cancer. Dis Colon Rectum. 1993;36:388–93. 3. Law WL, Lee YM, Chu KW. Previous abdominal operations do not affect the outcomes of laparoscopic colorectal surgery. Surg Endosc. 2005;19:326–30. 4. Lam AK-Y, Gopalan V, Carmichael R, Buettner PG, Leung M, Smith R. Metachronous carcinomas in colorectum and its clinicopathological significance. Int J Colorectal Dis. 2012;27: 1303–10. 5. Bouvier A-M, Latournerie M, Jooste V, Lepage C, Cottet V, Faivre J. The lifelong risk of metachronous colorectal cancer

17.

18.

19.

20.

justifies long-term colonoscopic follow-up. Eur J Cancer. 2008;44:522–7. Park IJ, Yu CS, Kim HC, Jung YH, Han KR, Kim JC. Metachronous colorectal cancer. Colorectal Dis. 2006;8:323–7. Nagasue Y, Akiyoshi T, Ueno M, Fukunaga Y, Nagayama S, Fujimoto Y, et al. Laparoscopic versus open multivisceral resection for primary colorectal cancer: comparison of perioperative outcomes. J Gastrointest Surg. 2013;17:1299–305. Park SY, Choi G-S, Jun SH, Park J-S, Kim HJ. Laparoscopic salvage surgery for recurrent and metachronous colorectal cancer: 15 years’ experience in a single center. Surg Endosc. 2011;25: 3551–8. Veldkamp R, Kuhry E, Hop WCJ, Kazemier G, Bonjer HJ, Haglind E, et al. Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol. 2005;6:477–84. Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AMH, et al. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365:1718–26. Lacy AM, Garcı´a-Valdecasas JC, Delgado S, Castells A, Taura´ P, Pique´ JM, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet. 2002;359:2224–9. Akiyoshi T, Kuroyanagi H, Oya M, Ueno M, Fujimoto Y, Konishi T, et al. Factors affecting difficulty of laparoscopic surgery for left-sided colon cancer. Surg Endosc. 2010;24: 2749–54. Akiyoshi T, Kuroyanagi H, Fujimoto Y, Konishi T, Ueno M, Oya M, et al. Short-term outcomes of laparoscopic colectomy for transverse colon cancer. J Gastrointest Surg. 2010;14:818–23. Hamel CT, Pikarsky AJ, Weiss E, Nogueras J, Wexner SD. Do prior abdominal operations alter the outcome of laparoscopically assisted right hemicolectomy? Surg Endosc. 2000;14:853–7. Franko J, O’Connell BG, Mehall JR, Harper SG, Nejman JH, Zebley DM, et al. The influence of prior abdominal operations on conversion and complication rates in laparoscopic colorectal surgery. JSLS. 2006;10:169–75. Gonza´lez IA, Malago´n AM, Ferna´ndez EMLT, Dura´n JA, Luis HD, Pallares AC. Impact of previous abdominal surgery on colorectal laparoscopy results: a comparative clinical study. Surg Laparosc Endosc Percutan Tech. 2006;16:8–11. Vignali A, Di Palo S, De Nardi P, Radaelli G, Orsenigo E, Staudacher C, et al. Impact of previous abdominal surgery on the outcome of laparoscopic colectomy: a case-matched control study. Tech Coloproctol. 2007;11:241–6. Offodile AC, Lee SW, Yoo J, Whelan RL, Moradi D, Baxter R, et al. Does prior abdominal surgery influence conversion rates and outcomes of laparoscopic right colectomy in patients with neoplasia? Dis Colon Rectum. 2008;51:1669–74. Barleben A, Gandhi D, Nguyen X-M, Che F, Nguyen NT, Mills S, et al. Is laparoscopic colon surgery appropriate in patients who have had previous abdominal surgery? Am Surg. 2009;75: 1015–9. Bhardwaj R, Parker MC. Impact of adhesions in colorectal surgery. Colorectal Dis. 2007;9(Suppl 2):45–53.

123

Feasibility and safety of laparoscopic surgery for metachronous colorectal cancer.

This study assessed the feasibility and safety of laparoscopic surgery for metachronous colorectal cancer in patients who had previously undergone sur...
179KB Sizes 0 Downloads 3 Views