Anatomical variations in right colon vascularization:
Its implication in complete mesocolic excision with D3
lymphadenectomy. A cross-sectional study.
Juan Pablo Campana1, Catalina Poggi1, Lorena Savluk2, José Viñas1,
Esteban González Salazar1, Ricardo Mentz1, Gustavo Rossi1,
Sergey Efetov3,4, Kirill Puzakov4, Albina Zubayraeva4, Carlos Alberto Vaccaro1
1 Colorectal Surgery Section, General Surgery Department, Hospital Italiano de Buenos Aires, Argentina.
2 Imaging Diagnostic Service, Hospital Italiano de Buenos Aires, Argentina.
3 Surgical Department N2, University Clinical Hospital N4
4 I.M. Sechenov First Moscow State Medical University
ABSTRACT
Background: Complete mesocolic excision with D3 lymphadenectomy (CME-D3) improves the outcomes of patients operated on for colon cancer. Proper recognition of vascular anatomy is essential to avoid complications.
Aim: Primary outcome was to determine the prevalence of anatomical variations of the superior mesenteric artery (SMA) and its branches in relation to the superior mesenteric vein (SMV). Secondary outcome was to evaluate the association between these anatomical variations and sex and ethnicity of the patients.
Design: Cross-sectional study.
Material and methods: Two hundred twenty-five patients with right colon cancer diagnosed between January 2017 and December 2020 were included. Two independent radiologists described the vascular anatomy of computed tomography angiography scans. The population was divided into 2 groups and subdivided into 6 groups (1a–c, 2a–c), according to the relationship of the SMA and its branches with the SMV.
Results: The ileocolic artery was constant, crossing the SMV on its posterior aspect in 58.7% of the cases. The right colic artery, present in 39.6% of the patients, crossed the SMV on its anterior aspect in 95.5% of the cases. The most frequent subgroup variant was 2a followed by 1a (36.4 and 24%, respectively). No association was found between anatomical variants and gender or ethnic origin.
Conclusions: The anatomical variations of the SMA and its branches are common, with no predominant pattern. There was no association between anatomical variations and gender or ethnic origin in our cohort. Preoperative evaluation of these variations by computed tomography angiography scan is useful to avoid vascular injuries during CME-D3.
Key words: complete mesocolic excision, D3 lymphadenectomy, vascular anatomy, right colon
The authors declare no conflicts of interest.
Correspondence: Juan Pablo Campana. juan.campana@hospitalitaliano.org.ar. Tte. Gral. Juan Domingo Perón 4190, CABA. CP C1199ABB. Ph: (+54 11) 4959–0200.
Juan Pablo Campana ORCID 0000-0002-0420-5906; Catalina Poggi ORCID 0000-0002-3430-8375
Lorena Savluk ORCID 0000-0002-9939-8260; José Viñas ORCID 0000-0001-8615-7436
Esteban González Salazar ORCID 0000-0003-3831-522X; Ricardo E. Mentz ORCID 0000-0002-6746-8869
Gustavo L. Rossi 0000-0002-4451-6709; Sergey Efetov 0000-0003-0283-2217
Kirill Puzakov ORCID 0000-0001-9017-8205; Albina Zubayraeva ORCID 0000-0001-8284-3922;
Carlos A. Vaccaro ORCID 0000-0002-1299-5864
INTRODUCTION
Extrapolated from oncologic surgery for rectal cancer, the concept of complete mesocolic excision (CME) with central vascular ligation and D3 lymphadenectomy in right hemicolectomy for colon cancer has recently re-emerged.1 Compared to standard mesocolic resection (conventional D2 right hemicolectomy), this surgical strategy presents a greater 5-year overall survival and a greater number of lymph nodes removed, although it could potentially be associated with a greater number of complications.2-5
In oncological resection of the right colon, D3 lymphadenectomy corresponds to the dissection of the central lymph node groups located on the anterior face of the superior mesenteric vein (SMV) from the level of the middle colic vein (MCV) to the ileocolic vein (IVC).6 To perform this dissection it is essential to know the vascular anatomy of the right colon, including its anatomical variations, to minimize the possibility of intraoperative vascular accidents. In particular, it is important to know the relationships of the arterial branches with the SMV and its branches, since lymphadenectomy may be more difficult when the ileocolic artery (ICA) crosses posterior to the SMV.7
Currently, there are few published studies that relate the vascular anatomy of the right colon to D3 dissection and that describe the most frequent relationships of the SMA and its branches with the SMV.8,9
The main objective of this study was to determine the prevalence of the different anatomical variations of the SMA and its branches and their relationships with the SMV studied by computed tomography (CT) in patients with undergoing right hemicolectomy for colon cancer in a closed cohort from Argentina.
Secondly, it was proposed to evaluate the association between the different anatomical variants with the sex and ethnicity of the patients.
MATERIAL AND METHODS
An observational cross-sectional study was carried out that included patients older than 18 years with cancer of the right colon who underwent surgery consecutively in a tertiary hospital in Argentina between January 2017 and December 2020.
Cancer of the right colon was defined as adenocarcinoma located in the cecum, ascending colon, hepatic flexure, and proximal transverse colon.
All patients underwent a CT to study the different anatomical variations of the SMA and its branches and their relationships with the SMV.
The excluded patients were those: 1) with previous major abdominal resections by laparotomy or laparoscopy, 2) whose preoperative CT was without intravenous contrast, and 3) in whom both radiologists did not agree on the definitive vascular diagnosis.
The ethnic origin was divided into 4 groups: European, Amerindian, African and Asian, according to the subcontinental origin of the ancestry components of the different individuals.10
The study was approved by the Ethics Committee for Institutional Research Protocols (CEPI) of the Hospital Italiano de Buenos Aires.
Tomographic protocol
The tube current was adjusted by automatic exposure control based on the patient's body constitution (300-550 mA/s). The tube power was 120 kVp and
the slice thickness was 0.5-1.0 mm. The non-ionic and iodinated contrast Omnipaque® (350 mg Iodine/ml injectable solution) was used. Contrast was administered at 3.0-3.5 ml at a dose of 1-2 ml/kg body weight. Studies were reported according to the following protocol: non-contrast phase; arterial phase (the scan starts automatically after maximum contrast enhancement in the aorta); venous phase (imaging delayed 40-50 seconds after bolus injection); late phase (10 minutes after bolus injection) for evaluation of the urinary tract.
To assess the vascular anatomy in detail, 3D volume rendering (3D reconstruction) was used as exemplified in Fig. 1.
Figure 1. Computed tomography angiography with 3D reconstruction. The ileocolic artery (AIC) can be seen crossing the superior mesenteric vein (VMS) on its anterior face aspect, and the right colic artery (ACD) crossing it on its posterior aspect. It corresponds to the type 1c variant.
Definitions
The middle colic artery (MCA), defined as the first branch of the SMA, goes to the transverse colon through the mesocolon. The ICA was defined as the last branch that emerges from the right side of the SMA and approaches the ileocecal valve. The right colic artery (RCA) was defined as that branch that arises from the SMA between the MCA and the ICA, in the direction of the ascending colon. This vessel can also originate from a common trunk with the MCA or ICA.
Based on the classification by Efetov et al.,11 we divided the population into two groups according to the
relationships between ICA and SMV: Type 1: ICA runs ventrally to the SMV. Type 2: ICA runs dorsally to the SMV.
Taking into account the relationships of the MCA and RCA with the SMV, six possible scenarios emerge, schematized in Fig. 2:
Type 1a: both ICA and MCA run ventrally to the SMV and RCA is absent.
Type 1b: ICA, RCA, and MCA run ventrally to the MSV. Type 1c: ICA and MCA run ventrally to the SMV, while RCA run dorsally.
Type 2a: ICA runs dorsally to the SMV, MCA runs ventrally, and RCA is absent.
Type 2b: ICA and RCA lie dorsally to the SMV and MCA lies ventrally. Type 2c: ICA runs dorsally to the SMV, while
RCA and MCA run ventrally.
Figure 2. Classification of anatomical variants. A) Type 1a. B) Type 1b. C) Type 1c. D) Type 2a. E) Type 2b. F) Type 2c. VMS: superior mesenteric vein. SMA: superior mesenteric artery. MCA: middle colic artery. ICA: ileocolic artery. RCA: right colic artery.
Procedure
All CTs were independently assessed by two radiologists who described the vascular anatomy as previously defined. To minimize the bias related to interobservational variation, a description of the vascular anatomy was performed according to standardized criteria.11
Sample calculation
A simple consecutive sampling method was carried out. The calculation of the sample size was made based on the Argentine population according to the 2022 census. Taking into account 70% of the population over 18 years of age (according to census data) and considering a margin of error of 6% with a 95% confidence level, the calculated sample size was 225 patients.
Statistic analysis
Categorical variables were reported as proportions and continuous variables as means with their respective standard deviations or medians with their interquartile ranges, according to distribution. The chi-square test or Fisher's exact test was used for categorical variables and Student's t-test for continuous variables. All the statistical tests were two-tailed and a value of p<0.05 was considered statistically significant. STATA®, version 13 software (StataCorp LLC, Texas, United States) was used for all analyses.
RESULTS
Of the 274 patients operated on, 49 were excluded, leaving a total of 225 patients for analysis (Fig. 3).
The sex of the population was predominantly female (60%) and the
mean age was 74±12 (range: 33-94) years. The most frequent tumor locations were the cecum (44%) and ascending colon (43.1%). The most prevalent ethnic group was European (97.8%). The rest of the demographic and clinical characteristics are presented in Table 1.
Figure 3. Flowchart.
ICA was present in all patients. In 58.7% of the patients (n=132) it ran dorsally to the SMV (Type 2). RCA was present in 39.6% of patients (n=89); it was a branch of the MCA in 47.2% of the cases, a direct branch of the SMA in 45.8% and a branch of the ICA in only 7%. The RCA run ventrally to the SMV in 95.5% of the patients (n=85).
The MCA was present in 98.7% of the patients (n=222); in all of them it emerged from the anterior aspect of the SMA. Only one patient presented, as an anatomical variation, a common trunk between the ICA and the MCA, in which case the RCA was absent.
Table 1. Demographic variables and clinical characteristics.
|
Variables |
Patients n = 225 |
|
|
Age, mean ± SD |
74 ± 12 |
|
|
Women % (n) |
60 (135) |
|
|
Ethnicity, % (n) European Amerindian African Asian |
97.8 (220) 0.4 (1) 0 1.8 (4) |
|
|
Weight, mean ± SD |
71 ± 17 |
|
|
Height, mean ± SD |
1.6 2 ± 0.1 |
|
|
BMI, mean ± SD |
27 ± 5 |
|
|
Location, % (n) Cecum Ascending colon Hepatic flexure Transverse colon |
44 (99) 43.1 (97) 8 (18) 4.9 (11) |
SD: standard deviation. BMI: body mass index.
The most frequent subgroup variant was type 2a followed by type 1a (36.4 and 24%, respectively). The prevalence of the different combinations of variations is presented in Table 2.
Table 2. Frequency of anatomical variations.
|
Anatomical variations |
Patients n = 225 |
|
|
ICA present, % (n) |
100 (225) |
|
|
RCA present, % (n) |
39.6 (89) |
|
|
MCA present, % (n) |
98.7 (222) |
|
|
Type 1, % (n) 1a 1b 1c |
41.3 (93) 24 (54) 17.3 (39) 0 |
|
|
Type 2, % (n) 2a 2b 2c |
58.7 (132) 36.4 (82) 1.8 (4) 20.4 (46) |
ICA: ileocolic artery; RCA: right colic artery; MCA: middle colic artery.
The course of the ICA along the anterior aspect of the SMV vs. the posterior aspect was not associated with the patient gender (women: 61.3 vs. 59.1%, respectively; p=0.74) or the ethnic origin (European: 98.9 vs. 97%, Amerindian: 0 vs. 0.8%, African: 0 vs. 0%, Asian: 1.1 vs. 2.3%, respectively; p=0.56) (Table 3).
There was also no association between the presence of RCA and gender (women: 56.2 vs. 62.5%; respectively; p=0.34) or ethnicity (European: 96.6 vs. 98.5%, Amerindian: 1.1 vs. 0%, African: 0 vs. 0%, Asian: 2.2 vs. 1.5%, respectively; p=0.42) (Table 4).
Table 3. Bivariate analysis according to the ileocolic artery.
|
Variables |
Type 1 (n = 93) |
Type 2 (n = 132) |
P value |
|
|
Age, mean ± SD |
73 ± 12 |
75 ± 12 |
0.38 |
|
|
Women, % (n) |
61.3 (57) |
59.1 (78) |
0.74 |
|
|
Ethnicity, % (n) European Amerindian African Asian |
98.9 (92) 0 0 1.1 (1) |
97 (128) 0.8 (1) 0 2.3 (3) |
0.56 |
|
|
Weight, mean ± SD |
71 ± 16 |
71 ± 17 |
0.98 |
|
|
Height, mean ± SD |
1.62 ± 0.1 |
1.61 ± 0.1 |
0.42 |
|
|
BMI, mean ± SD |
26 ± 4 |
27 ± 5 |
0.62 |
|
|
Location, % (n) Cecum Ascending colon Hepatic flexure Transverse colon |
39.8 (37) 46.2 (43) 9.7 (9) 4.3 (4) |
47 (62) 40.9 (54) 6.8 (9) 5.3 (7) |
0.64 |
SD: standard deviation. BMI: body mass index.
DISCUSSION
To the best of our knowledge and experience, this descriptive study represents the first to analyze the vascular anatomy of the right colon in a Latin American population using CT scan with IV contrast. In this population, the ICA is found more frequently on the posterior aspect of the SMV. The RCA was present in approximately half of the patients and in most cases it crossed the SMV on its anterior aspect. In the two cases in which the RCA passed through the posterior aspect of the SMV, the ICA did so in the same way. This coincides with the findings reported by Murono et al.12
The vascular variations of the SMA and its branches have been addressed in the literature from an anatomical point of view. Most of the studies are non-systematic reviews13 or descriptive cadaveric studies.6,14,15 However, none of them emphasize the anatomical relationships of the arterial branches supplying the colon with the SMV, which is the most important technical landmark when performing CME with central ligation and D3 lymphadenectomy.
Table 4. Bivariate analysis according to the right colic artery.
|
Variables |
RCA present (n = 89) |
RCA absent (n = 136) |
P value |
|
|
Age, mean ± SD |
75 ± 11 |
73 ± 12 |
0.22 |
|
|
Women, % (n) |
56.2 (50) |
62.5 (85) |
0.34 |
|
|
Ethnicity, % (n) European Amerindian African Asian |
96.6 (86) 1.1 (1) 0 2.2 (2) |
98.5 (134) 0 0 1.5 (2) |
0.42 |
|
|
Weight, mean ± SD |
72 ± 14 |
70 ± 19 |
0.6 |
|
|
Height, mean ± SD |
1.62 ± 0.1 |
1.61 ± 0.1 |
0.2 |
|
|
BMI, mean ± SD |
27 ± 4 |
27 ± 5 |
0.96 |
|
|
Location, % (n) Cecum Ascending colon Hepatic flexure Transverse colon |
42.7 (38) 47.2 (42) 6.7 (6) 3.4 (3) |
44.9 (61) 40.4 (55) 8.8 (12) 5.9 (8) |
0.68 |
RCA: right colic artery. SD: standard deviation. BMI: body mass index.
The ICA is a constant branch of the SMA. The literature disagrees regarding on which is the most frequent relationship between the ICA and the SMV. Consistent with the findings of some studies,14-16 in our population the ICA is found more frequently (58.7%) posterior to the SMV.
On the other hand, the RCA is much more variable. While most groups report that it is present in approximately 30% of cases17 and is located anterior to the SMV, in our population its presence slightly exceeded this number (36.9%), also crossing mostly by the anterior aspect of the SMV.
Regarding the MCA, in our series it was present in 98.7% of the patients, always emerging from the anterior aspect of the SMV, in accordance with other reports.13,17
The most frequent combinations of anatomical variations in our study were types 2a and 1a (36.4 and 24%, respectively). Likewise, in the Russian population type 2a predominated with 43.8% of cases. In contrast, in the Chinese population type 1a predominates with 30.8% and the position of the ICA with respect to the SMV is balanced,11 while in more than 60% of our patients the ICA crosses the SMV by its posterior aspect.
Our population is highly influenced by European migrations,18 which could explain our findings, which are more similar to those of the Russian population. In our series, European ancestry was higher than the rest of the subgroups (97.8%).
We found no association between the course of the ICA and the gender or ethnic origin of each individual. We also did not detect an association between the presence of the RCA and these same variables. Therefore, the anatomical differences published between the eastern and western population could not be confirmed in our study. However, we believe this could be because the sample size calculation was performed to assess prevalence and not subgroups differences. Future studies should expand the sample to determine differences between different ethnic groups.
The variability of the vascular anatomy of the right colon and that of the relationships between the branches of the SMA and SVM offer an additional difficulty for the surgeon. Currently, it is feasible to know the anatomy through preoperative studies, being the CT scan with IV contrast and 3D vascular reconstruction a highly specific and sensitive non-invasive study for its evaluation.19,20 The preoperative assessment of these studies should become a regular practice by the surgical team in order to know the vascular anatomy that will have to face during surgery and thus reduce the most important intraoperative morbidity related to D3 lymphadenectomy, such as SMV injury.21
This study has some limitations that deserve to be highlighted. First, the cross-sectional design carries the limitation of the interpretation of causality for association analyses. However, in our study the associations were only evaluated in variables unalterable over time, such as anatomical variations, gender and ethnic traits. Secondly, the sampling was of a simple consecutive type, which facilitates the incorporation of individuals into the study but has the drawback of being less representative of the general population. Third, the different anatomical variants were evaluated by CT scan and not confirmed during the surgical procedure, which may decrease the quality of the data collected. However, CT scan with 3D reconstruction has shown high sensitivity and specificity for the diagnosis of vascular anatomy in numerous publications.12,22 In addition, all CT scans were analyzed by two independent radiologists and only those studies in which both professionals agreed on the diagnosis of vascular anatomy were included.
CONCLUSION
The SMA and its branches have variable relationships with the SMV, without a predominant pattern.
There was no association between these variations and the gender or ethnic origin of the population analyzed.
Evaluation of these anatomic variants by CT angiography should be routinely incorporated into the preoperative planning of a right colectomy with CME and D3 lymphadenectomy, in order to avoid undesirable intraoperative complications.
REFERENCES