Preservation of the left colic artery and superior rectal artery in laparoscopic surgery can reduce anastomotic leakage in sigmoid colon cancer.

BACKGROUND: The aim was to study the clinical significance in the preservation of the left colic artery (LCA) and superior rectal artery (SRA) for the laparoscopic resection of sigmoid colon cancer (SCC). PATIENTS AND METHODS: A total of 316 patients with SCC were divided into two groups. Group A received D3 resection with preservation of LCA and SRA, whereas Group B ligatured artery at the root of the inferior mesenteric artery. The operation time, number of resected lymph nodes, blood loss and anastomotic leakage rate were compared.
RESULTS: In Group A, the average operation time was 283.02 ± 51.48 min, the average blood loss was 111.81 ± 77.08 ml and the average lymph node dissection was 14.8 ± 7.7. There was no statistical significance in blood loss and number of resected lymph nodes between Group A and B (P > 0.05). Longer operating time were observed in Group A as compared to Group B (P < 0.05). The anastomotic leakage rate had statistical significance between these two groups (P < 0.05).
CONCLUSIONS: Preservation of LCA and SRA was safe and feasible for the laparoscopic surgery of SCC, which could reduce anastomotic leakage rate.

INTRODUCTION

In laparoscopic colorectal cancer surgery, blood supply is an important factor, which affects the healing of anastomosis. The blood supply of lower part of the left colon, sigmoid colon and upper rectum were mainly by the inferior mesenteric artery (IMA) and edge blood vessels from the superior mesenteric artery (SMA). From the anatomical point of view, truncated the IMA, the blood supply of lower part of sigmoid colon and rectal were mainly provided by the SMA.[1] Thus, the greater the impact of intestinal blood supply, higher the incidence of anastomotic leakage. Theoretically, blood supply of residual intestinal in patients retained the left colic artery (LCA) and superior rectal artery (SRA) was more abundant after surgery, and the probability of anastomotic leakage was lower. The retention of LCA and SRA can effectively ensure anastomotic blood supply and reduce the risk of anastomotic leakage.[2] However, the laparoscopic approach with LCA and SRA preservation in the sigmoid colon cancer resection has not been reported before. To explore the surgical effect of preserving LCA and SRA on the SCC, this study was performed with the procedure of LCA and SRA preservation and compared with the conventional surgical procedures.

PATIENTS AND METHODS

Patient selection

From January 2014 to November 2018, patients with sigmoid colon cancer (SCC) who underwent laparoscopic surgery in the Qilu Hospital of Shandong University were retrospective analysed. The inclusion criteria were as follows: (1) patients with complete clinical and pathological data, (2) post-operative pathological diagnosis of adenocarcinoma, (3) tumour did not invade the surrounding tissues or organs, (4) no distant metastasis and (5) no pre-operative radiotherapy. The exclusion criteria were as follows: (1) incomplete medical records, (2) post-operative pathological diagnosis could not be obtained, (3) intraoperative findings of invasion or distant metastasis of surrounding tissues and organs, (4) surgical records are not clear vascular retention, (5) pre-operative tumour local radiotherapy and (6) laparoscopic surgery transferred to laparotomy during surgery.

These patients were divided into the vessel preserving group (Group A) and conventional surgical group (Group B). Group A received radical resection with preservation of the LCA and SRA, whereas Group B received conventional surgery (high ligation of the IMA). The operation time, number of resected lymph nodes, blood loss and anastomotic healing status were compared between these two groups.

Surgical procedures

Patients were in lithotomy position. Five abdominal trocars were set. In the vessel preserving group (Group A), we put in the laparoscopy and run routine exploration, looking for IMA and other anatomical signs. Then, open the peritoneum from the right side of IMA, separate the sigmoid mesenteric along the gap between the fascia of the Toldt's fascia to the IMA [Figure 1a]. Resect the lymphatic adipose tissue along the IMA, revealing the vascular roots [Figure 1b]. Resect along the direction of the LCA to bare the LCA until the intersection region of inferior mesenteric vein (IMV) and cleaning lymphatic adipose tissue around vessels [Figure 1c]. Then, we cut off the branches of sigmoid colon blood vessels, completely retain the SRA and superior rectal vein [Figure 1d]. Resect along the root of IMA and IMV to the distal, cleaning the lymphatic adipose tissue around blood vessels [Figure 1e]. In the conventional surgical group (Group B), the IMA and IMV were dissected at the lower border of pancreas. Figure 1f showed the different resect location of IMA between Group A and Group B.

Figure 1

The dissection sequence was described as follows: (a) Open the peritoneum from the right side of IMA, separate the sigmoid mesenteric along the gap between the fascia of the Toldt's fascia to the inferior mesenteric artery; (b) resect the lymphatic adipose tissue along the IMA, revealing the vascular roots; (c) resect along the direction of the LCA to bare the LCA until the intersection region of IMV, cleaning lymphatic adipose tissue around vessels; (d) cut off the branches of sigmoid colon blood vessels, complete retain the SRA and SRV and (e) Resect along the root of IMA and IMV to the distal, cleaning the lymphatic adipose tissue around blood vessels; (f) the different resect location of IMA between Group A and Group B. (AA: Abdominal aorta, IMA: Inferior mesenteric artery, IMV: Inferior mesenteric vein, LCA: Left colic artery, SRA: Superior rectal artery, SRV: Superior rectal vein, SCA: Sigmoid colon artery)

Both two groups received sigmoid resection according to the principle of total mesorectal excision. The pre-sacral fascia was dissected downwards to at least 5 cm beyond the distal of tumour. The hypogastric nerves and pelvic autonomic nerve plexi were carefully preserved. Then, the proximal and distal segment of sigmoid colon was exteriorised and transected. Nail anvil was set in the proximal end of sigmoid colon. Finally, we reconstructed bowel continuity by end-to-end colorectal anastomosis. After reconstruction of the digestive tract, we checked the blood supply of anastomosis, sutured incisions stratified, then end the operation.

Evaluation of the surgical outcomes

Patient data were collected from the records of the medical records, post-operative pathology reports, major examinations and laboratory findings. The main evaluation indexes included (1) operation time, (2) lymph node dissection number, (3) intraoperative blood loss and (4) healing situation. Post-operative follow-up by phone or outpatient visits were followed up every 3–6 months to observe post-operative recovery within 1 year. Turbid drainage (bowel contents) and the presence of peritonitis were defined as anastomotic leakage after the surgery.

Ethics statement

The study was approved by the Ethics Committee of Qilu Hospital of Shandong University, Jinan, China. All patients included in this study were provided and signed written informed consent. All procedures performed in studies involving human participants were carried out in accordance with the ethical standards of the institutional research committee and the 1964 Helsinki Declaration and its later amendments or with comparable ethical standards.

RESULTS

A total of 316 patients with SCC were enrolled in this study. Patients of vessel preserving group (Group A, 127 cases) received curative colectomy with low dissection of IMA and preservation of the LCA and SRA. Patients of conventional surgical group (Group B, 189 cases) received conventional surgery with high dissection at the root of IMA. In Group A, there were 77 males and 50 females, with the average (±standard deviation [SD]) age was 52.0 ± 10.5 years. The average (± SD) body mass index of Group A was 21.4 ± 5.1 kg/m2 (range: 18.1–35.2). The average (± SD) diameter of tumour in Group A was 4.3 ± 1.2 cm. Fifty patients were diagnosed with poor differentiation (including Signet-ring cell and mucinous) tumour, whereas 77 patients were diagnosed with moderately and well differentiation tumour. Number of patients with different tumour classification were 60 (ulcer type), 26 (mass type) and 41 (infiltration type). Fifty-five patients were diagnosed with pT 1–2 stage, and 72 patients were 3–4 a stage. The number of patients with pathologic tumour–node–metastasis stage I, IIa, IIb, IIIa, IIIb and IIIc was 5, 20, 24, 17, 27 and 34, respectively. Patients and tumour characteristics of Group B were listed in Table 1. The clinical-pathologic factors had no statistical significance between Groups A and B (all P > 0.05).

Table 1

Patients and tumour characteristics of Group A and Group B

Variables	Group A (n=127)	Group B (n=189)	Value	P
Sex
Male/female	77/50	111/78	0.11	0.736#
Age, year (average±SD)	52.0±10.5	53.1±10.1	−0.93	0.357*
BMI (average±SD)	21.4±5.1	21.7±5.8	−0.47	0.637*
Diameter of tumour (cm, average±SD)	4.3±1.2	4.1±1.2	1.45	0.147*
Poor differentiation/moderately and well-differentiated tumours	50/77	72/117	0.05	0.820#
Tumour classification
Ulcer type	60	68	4.00	0.135#
Mass type	26	47
Infiltration type	41	74
pT
pT1-2/T3-4a	55/72	81/108	0.01	0.937#
pTNM
I	5	10	1.86	0.761#
Iia	20	37
Iib	24	38
IIIa	17	30
IIIb	27	32
IIIc	34	42

*t-test, #χ2 test. BMI: Body mass index, SD: Standard deviation, pTNM: Pathological tumour–node–metastasis

In Group A, the average operation time was 283.02 ± 51.48 min (range: 210–360). The average number of dissected lymph nodes was 24.8 ± 7.7 (range: 14–50). The average blood loss was 111.81 ± 77.08 ml (range: 20–300). As to the post-operative complications, anastomotic leakage occurred in two patients (2/127, 1.6%). Post-operative ileus was detected in four patients (4/127, 3.2%). Abdominal abscess was detected in five patients (5/127, 3.9%). There were no repeated patients or post-operative abdominal bleeding in Group A. There was no surgical mortality in both two groups. As the surgical procedure of vessel preserving was more complicated, the operation time of Group A was significantly higher than that of Group B (P = 0.002). However, as to post-operative complications, the anastomotic leakage rate of Group A (2/127, 1.6%) was significantly lower than that of Group B (13/189, 6.9%) (P = 0.032). Intraoperative and post-operative outcomes of Groups A and B were listed in Table 2.

Table 2

Intraoperative and post-operative outcomes of Group A and Group B

Variables	Group A (n=127)	Group B (n=189)	Value	P
Operation time, min (average±SD)	253.02±71.48	228.57±62.87	3.21	0.002*
Intraoperative blood loss, ml (average±SD)	111.81±77.08	107.14±86.53	0.49	0.624*
Intraoperative blood transfusion	7	6	1.05	0.305#
Distance from the distal cutting edge, cm (average±SD)	4.31±2.23	4.22±2.12	0.36	0.717*
Number of lymph nodes dissected (average±SD)	24.8±7.7	23.9±7.2	1.06	0.290*
Cutting length, cm (average±SD)	18.23±4.41	17.77±2.65	1.05	0.293*
Post-operative hospital days, day (average±SD)	7.4±2.1	8.7±1.9	−1.32	0.188*
Re-operated patients	0	2		0.518†
Post-operative ileus	4	7		1.000†
Abdominal abscess	5	6		0.761†
Cardiopulmonary complications	6	11	0.18	0.672#
Anastomotic leakage after surgery	2	13		0.032†
Post-operative abdominal bleeding	0	1		1.000†
Short-term post-operative mortality (%)	0	0		NA

*t-test, #χ2 test, †Fisher’s exact test

DISCUSSION

It has become a consensus that the blood supply of anastomosis is important to prevent anastomotic leakage. However, there has been a controversial between high versus low ligation of the IMA in the surgery for sigmoid colon cancer (SCC). The main difference was that whether the ligation was above or below the LCA.[3] Some anatomy studies showed that the marginal artery of Drummond was absent in 5% of colorectal cancer patients, which was called the Griffith's point.[4] These results implied that preservation of the LCA in SCC may improve the blood supply of proximal sigmoid colon.[5] Meanwhile, preservation of the SRA could ensure enough blood supply to the remnant distal sigmoid colon and the upper rectum. This was important for the SCC surgery, especially for colectomy of proximal SCC, in which the long distal bowel was retained.

Here, we described our laparoscopic D3 dissection technique for SCC with preservation of the LCA and SRA to maintain the blood supply of the remnant bowel. The key of this operation was to dissect the perivascular lymph nodes while retaining the integrity of SRA. Under laparoscopy, the visual field of surgeons was expanded, and the vessels could be fully exposed. Accurate anatomy through laparoscopic surgery preserved the upper rectal blood vessels during the radical resection of SCC, which could effectively guarantee blood supply of the anastomosis.

It has been estimated that the mean distance between the root of IMA and LCA was 4.0 cm. However, in some cases, the distance could be even longer, which made the dissection of lymph node at the root of IMA (D3) and recognition of the root of LCA difficult.[6] Recent advances in enhanced computed tomography have enabled the reconstruction of three-dimensional images of the IMA and LCA, which may make the recognition of the LCA easier.[7]

The lymph nodes were dissected according to the American Joint Committee on Cancer/Union of International Cancer Control guidelines. In these guidelines, lymph nodes around the root of the IMA were defined as D3 station.[8] In our study, dissection of D3 station lymph nodes around the IMA and LCA posed special surgical technical tips. In this study, patients of Group A dissected similar lymph nodes to those of Group B (24.8 ± 7.7 vs. 23.9 ± 7.2, P > 0.05). Liang and Lai[9] used the da Vinci robot surgery system to perform the distal rectal cancer (RC) surgery. They dissected lymph nodes around the root of IMA (D3) and preserved the LCA at the same time. An average of 26.1 ± 7.2 (range: 10–44) lymph nodes was reported.[10] Another study showed that D3 dissection around the root of the IMA and LCA and achieved an adequate number of harvested lymph nodes.[11]

It has become a consensus that patients who received LCA preserving surgery had better anastomotic blood supply. Guo et al.[12] measured the stump pressure of marginal artery after colon reconstruction in RC surgery with the LCA preserving. They found that the blood supply of anastomosis was positive linear correlated with stump pressure of marginal artery. They concluded that curative surgery with LCA preservation could improve the blood supply of anastomosis and reduce the anastomosis complications. In a recent meta-analysis, researchers favoured vascular preservation of the IMA and SRA to prevent anastomotic complications in patients with SCC and RC.[13] Patients with preserved vascular supply of remnant bowel had several post-operative advantages. In our study, Group A and Group B had comparable age, gender and surgical approach. Our results suggested that patients with preserved LCA and SRA (the Group A) had less anastomotic leakage (P = 0.035) and a significantly shorter hospital stay (P < 0.05). There was no significant difference in death rate between these two groups (P > 0.05). These results suggested that this technique provided better anastomotic blood supply without differences in node retrieval number. In our view, if we use the surgical technique of lymph nodes dissection at the root of IMA with preservation of the LCA and SRA simultaneously, the adequate number of lymph node harvested and sufficient blood supply of the remnant colon can be achieved.

CONCLUSIONS

Our results indicated that laparoscopic dissection of D3 lymph nodes with preservation of the LCA and SRA was safe and feasible for the treatment of sigmoid colon cancer. This surgical technique could reduce anastomotic leakage rate and should be recommended as a better treatment option for patients with sigmoid colon cancer.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.