Optimal Surgery for Mid-Transverse Colon Cancer: Laparoscopic Extended Right Hemicolectomy Versus Laparoscopic Transverse Colectomy

  • Takeru Matsuda
  • Yasuo Sumi
  • Kimihiro Yamashita
  • Hiroshi Hasegawa
  • Masashi Yamamoto
  • Yoshiko Matsuda
  • Shingo Kanaji
  • Taro Oshikiri
  • Tetsu Nakamura
  • Satoshi Suzuki
  • Yoshihiro Kakeji
Original Scientific Report

Abstract

Background

Although the feasibility and safety of laparoscopic surgery for transverse colon cancer have been shown by the recent studies, the optimal laparoscopic approach for mid-transverse colon cancer is controversial.

Methods

We retrospectively analyzed the data of patients with the mid-transverse colon cancer at our institutions between January 2007 and April 2017. Thirty-eight and 34 patients who received extended right hemicolectomy and transverse colectomy, respectively, were enrolled.

Results

There were no significant differences in operating time, blood loss, and hospital stay between the two groups. Postoperative complications developed in 10 of 34 patients (29.4%; wound infection: 2 cases, anastomotic leakage: 2 cases, bowel obstruction: 1 case, incisional hernia: 2 cases, others: 3 cases) for the transverse colectomy group and in 4 of 38 patients (10.5%; wound infection: 1 case, anastomotic leakage: 0 case, bowel obstruction: 2 cases, incisional hernia: 0 case, others: 1 case) for the extended right hemicolectomy group (P = 0.014). Although the median number of harvested #221 and #222 LNs was similar between the two groups (6 vs. 8, P = 0.710, and 3 vs. 2, P = 0.256, respectively), that of #223 was significantly larger in extended right hemicolectomy than in transverse colectomy (3 vs. 1, P = 0.038). The 5-year disease-free and overall survival rates were 92.4 and 90.3% for the extended right hemicolectomy group, and 95.7 and 79.6% for the transverse colectomy group (P = 0.593 and P = 0.638, respectively).

Conclusions

Laparoscopic extended right hemicolectomy and laparoscopic transverse colectomy offer similar oncological outcomes for mid-transverse colon cancer. Laparoscopic extended right hemicolectomy might be associated with fewer postoperative complications.

Introduction

Transverse colon cancer had been excluded from many large-scale trials because of technical difficulty or for some other oncological reasons such as poor survival rate [1, 2, 3, 4, 5]. However, in recent years, many investigators have reported that laparoscopic surgery for transverse colon cancer is feasible and safe [6, 7, 8]. Its oncological outcome also does not seem to be inferior to that of open surgery. Therefore, laparoscopic surgery is considered one of the optimal treatment procedures for transverse colon cancer.

Importantly, the surgical procedure for transverse colon cancer can vary according to the tumor’s location. Laparoscopic extended right and left hemicolectomies are generally proposed for hepatic and splenic flexure cancers, respectively. However, the optimal laparoscopic approach for mid-transverse colon cancer is controversial [9]. Either extended right hemicolectomy or transverse colectomy is performed mainly based on the surgeon’s preference, but not on evidence because published data comparing the short- or long-term outcomes between those different laparoscopic approaches for mid-transverse colon cancer are unfortunately lacking.

The aim of the present study was to compare the surgical and oncological outcomes of laparoscopic extended right hemicolectomy and transverse colectomy for mid-transverse colon cancer.

Material and methods

Patients

This study was approved by the ethics committee of the institutional review board. We retrospectively analyzed prospectively collected data of patients who underwent laparoscopic colectomy for mid-transverse colon cancer at our institutions between January 2007 and April 2017. The mid-transverse colon is defined as the middle one-third of the transverse colon in this study. Altogether, 38 and 34 patients who received extended right hemicolectomy and transverse colectomy, respectively, for cStage I–III disease were enrolled in this study. Patients with metastatic disease (stage IV), more than one carcinoma in the colon, concomitant surgery for other organ carcinoma, or emergent surgery for bowel obstruction and/or perforation were excluded. Tumors were classified according to the American Joint Committee on Cancer (AJCC) TNM system.

Surgical techniques

Extended right hemicolectomy and transverse colectomy were performed as described previously [10, 11, 12]. Briefly, the surgery was performed using five ports. Lymphadenectomy along the superior mesenteric vein was performed in a cranial-to-caudal or a caudal-to-cranial manner. In both groups, the intestine was pulled out through a small incision and transected using linear staplers. Functional end-to-end anastomosis was performed extracorporeally using linear staplers in all cases. Closure of the mesenteric defect was performed only when the surgeon preferred.

Extended right hemicolectomy was defined as right hemicolectomy with division of the middle colic vessels at origin. Right hemicolectomy with D3 lymphadenectomy and preservation of the root of the middle colic vessels, or with D2 lymphadenectomy and division of both the right and left branches of the middle colic vessels at their origins, according to the Japanese Society for Cancer of the Colon and Rectum Guidelines, were also included in the extended right hemicolectomy group in this study. Therefore, in this study, the extended right hemicolectomy group included 3 types of lymphadenectomy: D3 with central resection of the middle colic artery (26 cases), D3 without central resection of the middle colic artery (5 cases), and D2 without central resection of the middle colic artery (7 cases).

Transverse colectomy was defined as partial resection of the transverse colon with D2 or D3 lymphadenectomy.

The type of surgery performed was based on surgeon perspective. All surgeries were performed by or under the supervision of 1 of 3 surgeons who were qualified by the endoscopic surgical skill qualification system of the Japan Society for Endoscopic Surgery (JSES).

Follow-up

All patients were followed at outpatient clinic every 3 months in the first 2 years postoperatively and every 6 months thereafter. Tumor markers including CEA and CA19-9 were examined on each follow-up, and computed tomography of the chest and abdomen was performed every 6 months. Total colonoscopy was performed every 2 years.

Data analysis

Clinical data, including patient and tumor characteristics, operative results, and postoperative outcomes, were collected and analyzed retrospectively. Comparisons of continuous parameters were performed by Student’s t test or Mann–Whitney’s U test, according to data distribution. The Chi-square test and Fisher’s exact test were used to analyze categorical variables. The Kaplan–Meier method was used to estimate overall survival (OS) and disease-free survival (DFS), and the log-rank test was used to compare survival curves. A P value of <0.05 was considered to indicate statistical significance. All analyses were performed using IBM SPSS Advanced Statistics v20.0 (IBM SPSS Statistics, IBM Corporation, Armonk, NY).

Results

There were no differences between the two groups in patient and tumor characteristics (Table 1).
Table 1

Patient and tumor characteristics

 

Extended right hemicolectomy (n = 38)

Transverse colectomy (n = 34)

P

Age, median (range)

73 (41–93)

73 (44–84)

0.754

Sex, n (%)

  

0.180

 Male

22 (57.9)

14 (41.2)

 

 Female

16 (42.1)

20 (58.8)

 

BMI (kg/m2), median (range)

25 (16–36)

24 (15–33)

0.778

ASA score, n (%)

  

0.866

 I

4 (10.5)

3 (8.8)

 

 II

29 (76.3)

26 (76.5)

 

 III

5 (13.2)

5 (14.7)

 

cStagea, n (%)

  

0.490

 I

16 (42.1)

17 (50.0)

 

 II

12 (31.6)

10 (29.4)

 

 III

10 (26.3)

7 (20.6)

 

pTa, n (%)

  

0.060

 T1

6 (15.8)

12 (35.3)

 

 T2

7 (18.4)

5 (14.7)

 

 T3

20 (52.6)

15 (44.1)

 

 T4

5 (13.2)

2 (5.9)

 

pNa, n (%)

  

0.021

 N0

29 (76.3)

22 (69.0)

 

 N1

7 (18.4)

10 (24.1)

 

 N2

2 (5.3)

2 (5.9)

 

 N3

0 (0)

0 (0)

 

pStagea, n (%)

  

0.402

 0

2 (5.3)

0 (0)

 

 I

12 (31.6)

13 (38.2)

 

 II

15 (39.5)

9 (26.5)

 

 III

9 (23.7)

12 (35.3)

 

Histological type, n (%)

  

0.779

 Well

18 (47.4)

17 (50.0)

 

 Moderately

19 (50.0)

15 (44.1)

 

 Other

1 (2.6)

2 (5.9)

 

Lymphatic invasion, n (%)

  

0.994

 Absent

21 (55.3)

19 (55.9)

 

 Present

17 (44.7)

15 (44.1)

 

Vascular invasion, n (%)

  

0.199

 Absent

15 (39.5)

15 (44.1)

 

 Present

23 (60.5)

19 (55.9)

 

Adjuvant chemotherapy, n (%)

  

0.851

 Yes

9 (23.7)

10 (24.1)

 

 No

29 (76.3)

24 (75.9)

 

ASA American Society of Anesthesiology

aTumors were classified according to the American Joint Committee on Cancer (AJCC)/TNM system

All patients received R0 resection in this study. The operative data are shown in Table 2. Operating time, blood loss, time to first flatus, time to soft diet intake, and hospital stay were similar between the two groups. However, postoperative complications developed significantly more frequently in the transverse colectomy group than in the extended right hemicolectomy group. Anastomotic leakage developed in two cases in the transverse colectomy group, but in none in the extended right hemicolectomy group. Incisional hernia was observed only in the transverse colectomy group. Two patients in the extended right hemicolectomy group and one in the transverse colectomy group developed bowel obstruction. The median number of the harvested lymph nodes overall was significantly larger in extended right hemicolectomy than in transverse colectomy (26 vs. 12, P = 0.000). Although the median number of harvested #221 and #222 LNs was similar between the two groups (6 vs. 8, P = 0.710, and 3 vs. 2, P = 0.256, respectively), that of #223 was significantly larger in extended right hemicolectomy than in transverse colectomy (3 vs. 1, P = 0.038) (Fig. 1).
Table 2

Surgical outcomes

 

Extended right hemicolectomy (n = 38)

Transverse colectomy (n = 34)

P

Operative time*, min (range)

250 (169–386)

238 (152–360)

0.120

Estimated blood loss*, g (range)

23 (0–400)

20 (0–250)

0.172

Lymphadenectomy, n (%)

  

0.226

 D2

7 (18.4)

9 (26.5)

 

 D3

31 (91.6)

25 (73.5)

 

The number of harvested lymph nodes*, n (range)

   

 #221

6 (3–13)

8 (3–16)

0.710

 #222

3 (0–10)

2 (0–16)

0.256

 #223

3 (0–14)

1 (0–13)

0.038

 Total

26 (1–56)

12 (1–37)

0.000

Transfusion, n (%)

  

0.447

 Yes

3 (7.9)

2 (5.9)

 

 No

35 (92.1)

32 (94.1)

 

Conversion to open surgery, n (%)

  

0.379

 Yes

1 (2.6)

0 (0)

 

 No

37 (97.4)

34 (100)

 

Time to first flatus*, days (range)

2 (0–4)

2 (0–5)

0.885

Time to liquid diet intake*, days (range)

4 (3–10)

4 (3–121)

0.512

Postoperative hospital stay*, days (range)

13 (8–41)

13 (8–46)

0.812

Postoperative complications, n (%)

4 (10.5)

10 (29.4)

0.014

 Wound infection

1

2

0.623

 Anastomotic leakage

0

2

0.129

 Bowel obstruction

2

1

0.623

 Incisional hernia

0

2

0.129

 Duodenal ulcer

1

0

0.341

 Lymphorrhea

0

1

0.287

 Heart failure

0

1

0.287

 Clostridium difficile colitis

0

1

0.287

*The data are expressed as the median (range)

Fig. 1

Lymph node mapping for transverse colon cancer according to the Japanese Society of Colorectal Surgeons. The dotted lines indicate the extent of lymphadenectomy by D2 and D3

Five-year DFS rates were 92.4 and 95.7% in the extended right hemicolectomy and transverse colectomy groups, respectively, while the 5-year OS rates were 90.3 and 79.6%, respectively. These frequencies were not significantly different (DFS, P = 0.593, and OS, P = 0.638, respectively) (Fig. 2).
Fig. 2

Disease-free survival curves (a) and overall survival curves (b) for patients treated with laparoscopic extended right hemicolectomy or laparoscopic transverse colectomy

Discussion

Although either laparoscopic extended right hemicolectomy or laparoscopic transverse colectomy would be optimal for mid-transverse colon cancer, which of them is performed seems to depend on the surgeon’s perspective rather than on patient and tumor characteristics due to a lack of sufficient evidence. To the best of our knowledge, this is the first study to compare the short- and long-term outcomes between those two surgeries for the treatment of mid-transverse colon cancer. Although operative and oncological outcomes were similar for both groups, postoperative complications were significantly more frequent in transverse colectomy compared with extended right hemicolectomy.

Similar studies on splenic flexure colon cancer have been reported by several investigators so far [13, 14, 15]. Angelis et al. [13] compared the short- and long-term outcomes of laparoscopic extended right hemicolectomy versus laparoscopic left colectomy. They reported similar operative and perioperative outcomes except for longer operative time in extended right hemicolectomy than in left colectomy. On the other hand, Gravante et al. [14] reported contradictory results in terms of operative time. They compared extended right hemicolectomy with left hemicolectomy and reported longer operative time for left hemicolectomy. In the latter study, most surgery was performed by an open approach, which might be one of the reasons for the opposite results in operative time. Chong et al. [9] compared the outcomes of transverse colectomy with those of extended colectomy for transverse colon cancer that occurred from the hepatic to the splenic flexure. In their study, both extended right hemicolectomy and left hemicolectomy were included in the extended colectomy group. Furthermore, a quarter of the patients in the transverse colectomy group underwent open surgery, while approximately half of extended colectomy group underwent laparoscopic surgery. They reported no differences in operative time and postoperative complications between the two groups. In any of those studies, contrary to our results, postoperative complications including anastomotic leakage did not differ between the groups.

Importantly, the oncological outcomes did not differ between the groups in any of those studies [9, 13, 14, 15], suggesting that the extent of lymphadenectomy was sufficient regardless of the type of surgery performed in those studies for transverse colon cancer. Park et al. [16] reported that metastasis to LNs along the right colic artery occurred in approximately 10% of the patients with mid-transverse colon cancer, while there was no metastasis to LNs along the ileocolic artery in those patients. They recommended to take great care in deciding the extent of segmental transverse colon resection for those patients. In this study, there was no case with LN metastasis along either the right colic vessels or the ileocolic vessels in the extended right hemicolectomy group. Although there was one case with LN recurrence in the extended right hemicolectomy group, that case had pN1 disease (only one metastasis in the pericolic region) and LN recurrence developed in the para-aortic and supraclavicular regions at 16 months postoperatively. On the other hand, there was no LN recurrence in the transverse colectomy group despite lymphadenectomy not being performed along the right colic vessels. Based on the concept of complete mesocolic excision and central vascular ligation, extended right hemicolectomy seems more radical procedure than transverse colectomy for the mid-transverse colon cancer, because the mid-transverse colon originally belongs to the midgut and is supplied by the superior mesenteric artery. However, in our settings, both procedures provided similar oncological outcomes. Therefore, in terms of oncological aspects, lymphadenectomy along the ileocolic vessels seems unnecessary for mid-transverse colon cancer, although it might be necessary to consider lymphadenectomy along the right colic vessels for those patients with apparent LN involvement. Furthermore, there were no significant differences in OS or DFS between D2 and D3 lymphadenectomy groups (data not shown). Although the number of the patients with pN (+) disease was limited and there was no case with pN (+) at #223 in this study, D2 might be sufficient at least for the mid-transverse colon cancer patients with cN0.

The 5-year OS was worse than the 5-year DFS in each group. This can be explained by the fact that there were more patients who died of other disease than those who died of disease recurrence. In the extended right hemicolectomy group, 2 patients died of other disease, although 2 patients with recurrence were both alive. In the transverse colectomy group, only 1 patient died of liver metastasis, while 2 patients died of esophageal cancer or lung cancer.

Only cases that were treated with laparoscopic surgery were included in the present study, because laparoscopic surgery has become the most popular approach for colon cancer treatment in recent years. Most previous studies compared the outcomes between laparoscopic and open surgeries [17, 18, 19, 20, 21], but no study has focused on the type of laparoscopic surgery for mid-transverse colon cancer. Mobilization of the splenic and/or hepatic flexure is required to accomplish laparoscopic surgery for mid-transverse colon cancer. In particular, the laparoscopic splenic flexure procedure is considered technically challenging because of its anatomical complexity [22]. For laparoscopic extended right hemicolectomy, lymphadenectomy along the middle colic, right colic, and ileocolic vessels is necessary, although splenic flexure mobilization is not required. On the other hand, for laparoscopic transverse colectomy, both splenic mobilization and hepatic mobilization need to be performed, although lymphadenectomy along the right colic and ileocolic vessels is unnecessary. Therefore, our result that operative time did not differ between the two groups appears to make sense.

The possible reasons for more complications in the transverse colectomy group need to be addressed. The different surgeons might be one of the main reasons for the worse result in transverse colectomy. Although all surgeries were performed by or under the supervision of the expert surgeons, the type of surgery performed depended on the surgeon perspective in this study. Therefore, the surgeon’s preference or skills in this type of surgery might affect the outcomes. Another reason can be associated with the more complicated procedures including splenic flexure mobilization in laparoscopic transverse colectomy.

On the other hand, there is a concern about possible drawbacks in extended right hemicolectomy. The extended resection of the colon including the ileocecal valve might affect bowel movement, enteric bacteria, and nutrition status after a long-term period. Although such data are unavailable in this study, they should be evaluated in the future study.

The present study has some limitations. First, it was a retrospective study and patient selection bias cannot be excluded. To overcome this problem, a prospective randomized study is required. Second, the number of the patients included was small despite of the relatively long follow-up period because this study focused only on the mid-transverse colon cancer. A multicenter study will be necessary to collect sufficient number of patients.

In conclusion, both laparoscopic extended right hemicolectomy and laparoscopic transverse colectomy offer similar oncological outcomes for mid-transverse colon cancer. Laparoscopic extended right hemicolectomy might be associated with fewer postoperative complications than laparoscopic transverse colectomy. For a more definitive conclusion, prospective trials on a larger scale are required.

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Copyright information

© Société Internationale de Chirurgie 2018

Authors and Affiliations

  • Takeru Matsuda
    • 1
  • Yasuo Sumi
    • 2
  • Kimihiro Yamashita
    • 3
  • Hiroshi Hasegawa
    • 3
  • Masashi Yamamoto
    • 3
  • Yoshiko Matsuda
    • 3
  • Shingo Kanaji
    • 3
  • Taro Oshikiri
    • 3
  • Tetsu Nakamura
    • 3
  • Satoshi Suzuki
    • 3
  • Yoshihiro Kakeji
    • 3
  1. 1.Division of Minimally Invasive Surgery, Department of SurgeryKobe University Graduate School of MedicineKobeJapan
  2. 2.Division of International Clinical Cancer Research, Department of SurgeryKobe University Graduate School of MedicineKobeJapan
  3. 3.Division of Gastrointestinal Surgery, Department of SurgeryKobe University Graduate School of MedicineKobeJapan

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