Chao Zhang, Ang Li, Tao Luo, Yu Li, Fei Li, Jia Li

Abstract

Key words: Anatomy; Digital subtraction angiography; Elderly; Inferior mesenteric artery;Left-sided colorectum

INTRODUCTION

Colorectal cancer (CRC) largely affects elderly patients, and the incidence of CRC increases with age, peaking at 70 years[1,2]. Laparoscopic surgery has made it possible for elderly CRC patients to undergo surgical treatment and has become a standard procedure around the world. Handling of the inferior mesenteric artery (IMA) and vein is important in low anterior resection and abdominoperineal excision for radical resection of left-sided CRC. However, the branching pattern of the IMA varies among individuals, and the hemoperfusion region has become one of the important issues related to the anastomotic complication and the outcome of CRC resection in elderly patients. Thus, it is very important to identify these variations to ensure successful vessel ligation during surgery for left-sided CRC. Additionally, no evidence-based studies have focused on IMA perfusion and arterial communication between the superior mesenteric artery (SMA) and IMA in elderly patients. Understanding the characteristics of these vessels and applying appropriate techniques are mandatory for improving the quality of surgery and the outcomes in elderly CRC patients. To the best of our knowledge, this report is the first to address the angiographic anatomy of the left-side colorectum in elderly patients. In the present study, we aimed to demonstrate the characteristics, bifurcation, and distribution of the IMA and termination of the anastomotic perfusion of the left colon and rectum in elderly patients using digital subtraction angiography (DSA) that could facilitate safe CRC tumor resection in elderly population.

MATERIALS AND METHODS

Patient selection

Here, we present a retrospective study (Jan 2016-Dec 2018) of 837 patients who underwent abdominal angiographic examination. This study was approved by the hospital ethical committee, and all participants signed an informed consent form. The inclusion criteria were as follows: (1) Patients aged ≥ 65 years[2,3]; (2) Patients who underwent interventional therapy and selective IMA angiography; and (3) Patients with stable vital signs without arterial spasm or excessive contraction. Patients with a history of abdominal surgery or radiotherapy, vasculitis (such as Leriche syndrome and Takayasu disease), congenital vascular malformation, acute hemorrhage, or severe shock were excluded. A total of 154 patients were finally included to be observed.

Digital subtraction angiography protocol

DSA was performed under local anesthesia, usually using the right femoral approach.A 5-F cobra-shaped catheter (Cordis, NJ, United States) or the SIM1 catheter (Cook,IN, United States) was introduced into the femoral artery to catheterize the abdominal aorta and the catheter tip was towards the anterior (ventral) direction. Selective DSA was performed with the catheter tip in the proximal part of the IMA using nonionic Optiray contrast medium (ioversol, 350 mg I/mL; Covidien, Dublin, Ireland; 9 mL, 3 mL/s) with the anteroposterior oblique projection. All DSA procedures were performed by abdominal interventional radiologists with over 10 years of experience(Zhang C, Li A and Luo T).

Measurements and classification

The general and IMA-specific characteristics were analyzed. The branching pattern of the IMA was classified into four different categories according to the origin of the left colic artery (LCA). The length and diameter of the IMA trunk were also measured.Collateral arterial arches and the IMA hemoperfusion region were also recorded. All data were measured and analyzed using the Philips Medical Workshop System(Philips Medical Co., NY, United States).

Statistical analysis

Student'st-test and the chi-squared test were applied to evaluate differences in continuous variables and categorical variables for univariate analyses, respectively.All of the analyses were performed using the IBM SPSS Statistics 22 software, and differences were considered statistically significant atP＜ 0.05.

RESULTS

Overall characteristics of patients

Between January 2016 and December 2018, a total of 154 patients were retrospectively observed, including those with digestive system malignancy, like colorectal,hepatobiliary (primary or metastasis), and pancreatic cancer, who did not underwent open or laparoscopic abdominal surgery; and gastrointestinal hemorrhage without severe shock or arterial spasm or excessive contraction (Figure 1). Out of 154 patients,90 were male and 64 were female. The patients' age ranged between 65 and 92 years;the average age was 72.5 ± 5.5 years. Forty (26.0%) patients had a history of atherosclerosis, including 34 coronary heart disease; 11 ischemic cerebrovascular disease; and 4 arteriosclerotic obliteration of the lower limb (Table 1).

IMA characteristics and branching patterns

In this study, we observed that the length of the IMA trunk varied from 1.1 to 7.8 cm,with an average length of 3.7 ± 1.5 cm. The diameter of the IMA trunk was 3.4 ± 0.5 mm and varied between 2.1 and 4.8 mm (Table 1). Of all 154 patients, 25 had arteriosclerotic lesions in the IMA and its branches, including 10 with stenosis, 3 with occlusion, and 12 with atherosclerotic plaque in the arterial wall (Figure 2). We also evaluated the branches of the IMA, including the LCA, sigmoid artery (SA), and superior rectal artery (SRA). We classified the branching patterns of the LCA into four types: Type I, LCA arose independently from the IMA; type II, the LCA and SA arose from the IMA at the same point; type III, the LCA, SA, and SRA were branched from a common trunk from the IMA; and type IV, the LCA was lacking as described in a previous radiological study[4]. The patterns of the IMA are shown in Figure 3. The majority of patients were classified with either type I [n= 68 (44.2%)] or type II [n= 54(35.1%)]; 26 (16.9%) of them had the common bifurcation of the IMA (type III), and a small number of patients [n= 6 (3.9%)] lacked the LCA (type IV).

IMA perfusion region and collateral circulation

We also observed the arterial perfusion region of the IMA by angiography (Figure 4).In all cases, perfusion from the IMA to the distal region reached the middle of therectum, and arterial perfusion to the proximal region exceeded the splenic flexure and reached the transverse colon in 104 (67.5%) cases (Figure 4A). However, in 50 (32.5%)patients, perfusion terminated at the splenic flexure (Figure 4B) and supplied only the descending colon (Figure 4C and D). The interruption of hemoperfusion in the area of the splenic flexure of the colon through the connection of the left branch of the middle colonic artery and the ascending branch of the LCA is known as Griffiths' critical point, which demonstrates that the integrity of the marginal artery is impaired; this occurred in 74 (48.1%) of the elderly patients in our study.

Table 1 General characteristics and inferior mesenteric artery characteristics

The collateral circulation existed in the colonic perfusion region, including the marginal artery (Drummond's artery), the ascending branch of the LCA (aLCA) to supply the transverse colon, and the other thick, tortuous arterial arch (arc of Riolan),which may connect the mesenteric collateral channels, with a frequency of 100%,22.7%, and 1.9%, respectively (Figure 5). When the marginal artery or the aLCA was involved as a bypass during mesenteric occlusion, it became grossly enlarged. There were 2 cases of mesenteric artery trunk occlusion, including 1 in the SMA and 1 in the IMA. The arc of Riolan and Drummond's artery compensated in the case of SMA occlusion (Figure 5B), and the aLCA and Drummond's artery compensated for IMA occlusion (Figure 5C).

Figure 1 Flow chart summarizing patient enrollment.

To determine which clinical features or IMA characteristics would be associated with the hemoperfusion region of the IMA, univariate and multivariate regression analyses were performed. The results showed that the integrity of the marginal artery and compensation of the collateral circulation, such as the aLCA and the arc of Riolan,were independently associated with the hemoperfusion region of the IMA. The collateral circulation could increase the region of IMA perfusion; however, the presence of the impaired integrity of the marginal artery decreased the IMA perfusion region, only supplying areas lower than the splenic flexure. In addition, the type IV IMA pattern could be a negative factor for IMA hemoperfusion, with aPvalue equal to 0.05. Meanwhile, the univariate analysis also revealed that the presence of IMA atherosclerotic lesions or comorbidity of atherosclerosis could be negative factors for IMA hemoperfusion, with aPvalue less than 0.05 (Table 2).

DISCUSSION

Anastomotic healing is an important issue in CRC surgery and could be influenced by many factors, including the ligation level of the IMA, continuity of marginal vessels,presence of atherosclerotic lesions in the mesenteric artery, and exertion of mesenteric tension on the site of anastomosis in the operative process[5]. Anastomotic ischemia is believed to be one of the major reasons and risks for the development of anastomotic leakage[6,7]. Hence, it is very important to identify variations in the IMA to ensure adequate anastomotic perfusion during left-sided colorectal operations. On the other hand, atherosclerotic diseases may also affect visceral arteries in elderly patients, such as the IMA and its branches, but no related studies have focused on evaluating the conditions of the IMA in elderly patients.

Importantly, there are two methods to divide and ligate the IMA during surgery for left-sided CRC: Ligating the IMA proximal to the origin of the LCA (high ligation);and performing ligation distal to the origin of the LCA (low ligation)[8]. To date, the region of lymphadenectomy and the frequency of anastomotic leakage in the two techniques remain controversial[9]. In high ligation, the left colon becomes more mobile and more lymph nodes are dissected[10], whereas in low ligation, possible ischemia in the proximal colon is avoided[11]. However, some studies have reported that high ligation of the IMA does not increase the frequency of anastomotic leakage[12]. Hence, understanding the anatomy and applying appropriate techniques are of instructive significance for improving the quality of surgery and the outcomes.

Figure 2 Demonstration of lesions in the inferior mesenteric artery and branches of the inferior mesenteric artery on digital subtraction angiography. The arrows represent the lesion sites including stenosis and occlusion. A: Superior rectal artery stenosis with plaque; B: Superior rectal artery occlusion; C: Inferior mesenteric artery trunk occlusion. The distal blood supply came from left colic artery compensation for the superior mesenteric artery.

First, we evaluated the variations in IMA branching. In the majority of cases, the IMA was classified as type I or II (79.3%). These results are consistent with the previous results of 3D-CT angiography, which revealed frequencies of types I, II, III,and IV of 41% to 47%, 9% to 20%, 27% to 44%, and 5% to 6%, respectively[4,13]. As an anatomical variation, the low ligation procedure should theoretically correspond to the IMA pattern at different levels and the branches[14]. The LCA can easily be preserved in standard type I patients, with the ligation level below the LCA and above the SA. However, in type II patients, the vessels of the sigmoid colon are very likely to remain with retention of the LCA. Surgeons should pay more attention to hemostasis during dissection of the sigmoid colon. In type III patients, low ligation is relatively difficult, and for branch ligation, it is necessary to separate the IMA bifurcation carefully to clearly expose the LCA, SA, and even SRA. Patients suspected of having type IV variation should undergo an adequate preoperative imaging evaluation, such as by 3D-CT angiography, to determine the existence of the LCA.Excessive separation of the IMA to search for the LCA among the vessels of the left colon may cause entry of the wrong plane and lead to injury of the gonadal vessels or even the ureter.

Ensuring the best colonic perfusion remains a concern to surgeons[15,16]. The purpose of our study was to reveal the arterial characteristics of elderly patients and determine an anatomical basis for the surgical strategy in terms of the process of IMA ligation.Although multiple techniques have been used for evaluating the perfusion of the left colorectum, including angiography[17], laparoscopic ultrasonography[18], and ICG fluorescence-assisted navigation[19], only angiography can demonstrate the perfusion region of the whole colorectum, the flow direction, and the collateral arteries directly,without requiring extra time during the operation. Indeed, in our study, the hemoperfusion region of the IMA was observed. Interestingly, the range of IMA perfusion also varied, but in most cases (67.5%), the IMA could supply beyond the splenetic flexure to the transverse colon, even reaching the hepatic flexure in some cases. However, in 32.5% of cases, the hemoperfusion of the IMA split at or below the splenetic flexure. Based on the univariate and multivariate regression analyses in this study, the integrity of the marginal artery, collateral compensation, type IV IMA pattern, IMA atherosclerotic lesion, and history of atherosclerosis could be independently associated with hemoperfusion of the left-sided colorectum.

Generally, this phenomenon is interrupted when the LCA bifurcates at Griffith's point, which is located at the splenic flexure, where the left branch of the middle colic artery meets the aLCA. This area receives poor hemoperfusion, and it is susceptible to damage and ischemia in radical resection of left-sided CRC. A previous study has reported that if the marginal artery is deficient at Griffith's point, over-dissection and freeing of the proximal limb could result in anastomotic ischemia[20]. Our study also revealed that the hemoperfusion of the IMA only reached the descending colon, with an incomplete marginal artery at Griffith's point. For this reason, considerable care must be taken not to disrupt the bifurcation of the LCA that replaces the function of the marginal artery in this area[21]. Collateral compensation could be a protective factor against proximal limb hemoperfusion. Three different types of collateral vessels were discerned[22]: Drummond's artery, the aLCA, and the arc of Riolan. The marginal artery of the colon runs along the descending colon, with a prevalence of 100%.However, the other two run close to the center of the mesentery: The aLCA,representing the left arm of the SMA-IMA connection, is reported to be present in 63%to 100% of patients[23]. Nevertheless, in our study, the aLCA was present in only 24.7%of the 154 elderly patients because the aLCA was counted only when forming an arch with the Drummond's artery at the distal transverse colon. The arc of Riolan is supposedly a thick, tortuous, uniform vessel connecting the proximal segments of the middle colic artery and LCA, representing the central point of anastomosis[24]. It can be distinguished from a normal aLCA because while this vessel is not tortuous, it runs along the descending colon and is rarely visualized by angiography.

Figure 3 Patterns of inferior mesenteric artery bifurcation. A: Illustration of the bifurcation of the inferior mesenteric artery (IMA) [only one sigmoid artery (SA) was showed in the illustration of IMA branches]. Type I: The LCA arose independently from IMA; type II: The LCA and SA arose from the IMA at the same point; type III:The LCA, SA, and SRA were branched from a common trunk from the IMA; and type IV: LCA was lacking; B: Angiography of the bifurcation of the IMA. IMA: Inferior mesenteric artery; SRA: Superior rectal artery; LCA: Left colic artery; SA: Sigmoid artery.

However, IMA lesions, history of arteriosclerosis, and IMA pattern (absence of the LCA) were still identified as being associated with the hemoperfusion of the left colon based on univariate regression analysis. A previous study[25]reported that the existence of plaque increased with age, and the prevalence of plaque in the IMA was approximately 7% in all age groups; in our study, this value was 16.2% in elderly patients. Furthermore, more lesions emerged at bifurcations, such as at the opening of the IMA and SRA. Similar to the carotid and lower limb arteries, bifurcations facilitate turbulence and plaque formation, inducing stenosis or occlusion[26,27]. On angiography in our study, the lesions could be a risk factor for poor hemoperfusion of the left-side colon. Similarly, in one case report, an abnormally dilated ex-collateral artery induced colic ischemia with an imbalance in the blood flow after sigmoid colectomy[28]. When the colic ischemia is chronic, the ischemic colitis occurs. Ischemic colitis is most commonly caused by insulting to the small vessels supplying the colon, including atherosclerosis and complication of vascular and bowel surgeries. The risk factors for ischemic colitis included age greater than 60, diabetes, hypertension, atherosclerosis,and other factors[29]. Regarding the prevalence of ischemic colitis for the anatomic considerations, the left part of the colon seems to be more affected by ischemic colitis in 75%-80% of cases because of the incomplete vascular anastomosis at Griffith's point as above mentioned, which could just demonstrate the correlation between such changes and the vessel characteristics[30,31].

The present study had some inherent limitations. Angiography could show only the anteroposterior plane of the region, and no Dyna-CT reconstruction was performed because it is difficult for elderly patients to cooperate with holding abdominal respiration. Alternatively, 3D-CT angiography could also provide helpful information, including length, branching, pattern, and the surrounding position of the IMA, to determine the optimal ligation level of the IMA in laparoscopic radical resection of left-sided CRC, which can precisely estimate the difficulties of the surgery and make the individual surgical strategy[4,13]. Moreover, because this study was not a randomized controlled study of left-sided CRC, it is difficult to determine the advantages and reveal the significance of presurgical angiography of the IMA, such as shortened operative time and reduced blood loss; additionally, anastomotic hemoperfusion after colectomy was not presented.

Figure 4 Demonstration of the colonic hemoperfusion region by angiography of the inferior mesenteric artery. The arrows represent the inferior mesenteric artery (IMA) perfusion to the proximal region of the colon. A: IMA perfusion exceeded the splenic flexure and reached the transverse colon; B: IMA perfusion onlyachieved the splenic flexure and stopped; C: IMA perfusion reached only the descending colon with the left colic artery; D: IMA perfusion reached only the descending colon without the left colic artery.

In conclusion, the IMA and its branches are prone to arteriosclerosis, as are the carotid and coronary arteries, in the elderly population. We concluded that IMA perfusion may be interrupted at the splenic flexure, the risk for which is increased with an incomplete marginal artery, the lack of other collateral arteries, and other factors. The applicability and precision of preoperative angiography for identification of the IMA branching pattern and perfusion region could mitigate the difficulties of the surgery and lead to individualized surgical strategies for elderly CRC patients.

Table 2 Univariate and multivariate analyses of inferior mesenteric artery hemoperfusion region with clinical features

ARTICLE HIGHLIGHTS

Research motivation

We demonstrated the characteristics, bifurcation, and distribution of the IMA and termination of the anastomotic perfusion of the left colon and rectum in elderly patients.

Research objectives

To retrospectively analyze the clinical and IMA angiographic characteristics of 154 patients over 65 years using digital subtraction angiography.

Research methods

We enrolled 154 patients (＞ 65 years old) who underwent digital subtraction angiography of the IMA. The clinical characteristics, bifurcation, and distribution of the IMA and termination of the anastomotic perfusion of the left colon and rectum were examined. Perfusion regions were crossreferenced with clinical and anatomical features.

Research results

Of 154 patients, 25 (16.2%) had IMA lesions. The left colic artery arose independently from the IMA in 44.2% of patients, shared a trunk with the sigmoid artery in 35.1%, shared an opening with the sigmoid and superior rectal arteries in 16.9%, and was absent in 5.1%. The IMA perfusion region stopped at the splenic flexure in 50 (32.5%) patients. Collateral circulation other than the marginal artery, including the ascending left colic artery and the arc of Riolan, appeared in 38 patients. The inferior mesenteric artery perfusion region was independently associated with the IMA atherosclerotic lesion, branching pattern, collateral circulation, and marginal artery integrity.

Research conclusions

The IMA and its branches are prone to arteriosclerosis in the elderly population. IMA perfusion may be interrupted at the splenic flexure, the risk for which is increased with an incomplete marginal artery, the lack of other collateral arteries, and the comorbidity of atherosclerosis.

Research perspectives

The applicability and precision of preoperative angiography for the IMA branching and perfusion patterns could facilitate geriatric laparoscopic surgery, especially for the elderly leftsided colorectal cancer patients who are suspected with poor IMA perfusion.