Muro No 2019

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Original article doi:10.1111/codi.

14886

Vascular anatomy of the splenic flexure, focusing on the


accessory middle colic artery and vein
K. Murono , H. Miyake, D. Hojo, H. Nozawa, K. Kawai, K. Hata, T. Tanaka, T. Nishikawa,
Y. Shuno, K. Sasaki, M. Kaneko, S. Emoto, H. Ishii, H. Sonoda and S. Ishihara
Department of Surgical Oncology, Faculty of Medicine, The University of Tokyo, Tokyo, Japan

Received 1 July 2019; accepted 8 October 2019; Accepted article online 25 October 2019

Abstract

Aim Recently, the accessory middle colic artery dorsal side of the pancreas in 15 (20.3%) of these 74
(AMCA) has been recognized as the vessel that supplies patients. Similarly, the destination of the IMV was
blood to the splenic flexure. However, the positional located on the dorsal side of the pancreas in 65 (31.7%)
relationship between the AMCA and inferior mesenteric of patients.
vein (IMV) has not been evaluated. Herein, we aimed
Conclusion The SFV was observed in most patients,
to evaluate the anatomy of the AMCA and the splenic
and the LCA or AMCA was the common accompany-
flexure vein (SFV).
ing artery. In some patients these vessels were located
Method Two hundred and five patients with colorectal on the dorsal side of the pancreas and not below it.
cancer who underwent enhanced CT preoperatively were Preoperative evaluation of this anatomy may be benefi-
enrolled in the present study. The locations of the cial for lymph node dissection during left-sided hemi-
AMCA and IMV were evaluated, focusing on the posi- colectomy.
tional relationship between the vessels and pancreas –
Keywords Vascular anatomy, splenic flexure, colon
below the pancreas or to the dorsal side of the pancreas.
cancer, accessory middle colic artery, splenic flexure vein
Results The AMCA was observed in 74 (36.1%)
What does this paper add to the literature?
patients whereas the SFV was found in 177 (86.3%)
It is important to have an image of the left colic artery
patients. The left colic artery (LCA) was the major (LCA), the accessory middle colic artery (AMCA), the
artery accompanying the SFV in 87 (42.4%) of patients. splenic flexure vein (SFV) and the pancreas preopera-
The AMCA accompanied the SFV in 65 (32.7%) tively. The LCA or AMCA was the major artery accom-
patients. In 15 (7.8%) patients, no artery accompanied panying the SFV. The AMCA was located behind the
the SFV. The origin of the AMCA was located on the pancreas in 20.3% of patients.

splenic flexure. In a previous report, the AMCA was


Introduction
observed in 36.4% of patients, and the incidence
Central ligation of the mesenteric artery is necessary to reached 85.3% in patients with a deficit in the LCA [7].
achieve complete mesocolic excision [1,2]. During Because lymphatic flow and lymph node metastases
laparoscopic surgery, CT angiography is useful for a along the AMCA are detected via indocyanine green
preoperative understanding of the vascular anatomy [3– (ICG) fluorescent imaging, lymph node dissection by
6]. The left colic artery (LCA) and middle colic artery ligating the AMCA centrally may contribute to a better
primarily supply blood to the splenic flexure. Recently, prognosis [8]. Lymphatic flow can be detected along
the accessory middle colic artery (AMCA) was found to with the drainage vein [8]. Therefore, it is important to
also supply blood to the splenic flexure. Typically, the understand the branching pattern of the AMCA as well
AMCA originates from the superior mesenteric artery as the anatomy of the drainage vein from the splenic
(SMA), running below the pancreas and toward the flexure (the splenic flexure vein, SFV) [9].
The SFV usually flows into the inferior mesenteric
Correspondence to: Koji Murono, Department of Surgical Oncology, Faculty of vein (IMV), and the destination of the IMV is some-
Medicine, the University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033,
Japan. times located on the dorsal side of the pancreas. There-
E-mail: [email protected] fore, the positional relationship between the destination

392 Colorectal Disease ª 2019 Association of Coloproctology of Great Britain and Ireland. 22, 392–398
K. Murono et al. Vascular anatomy of the splenic flexure

of the IMV and the pancreas must be identified. The 5 mm. Moreover, two patients who underwent surgery
anatomy of the IMV has been evaluated by Arimoto for abdominal aortic aneurysm and two who underwent
et al. [9]. However, the relationship between the artery, colectomy were excluded. A total of 205 patients [122
vein and pancreas has not been evaluated. men and 83 women with a median age of 67 (range
In the current study we aimed to evaluate the anat- 23–90) years] were finally enrolled. This study was
omy of the AMCA and SFV, with a particular focus on approved by the ethics committees of the University of
the branching pattern and positional relationship among Tokyo (no. 3252-(7)).
these vessels and the pancreas.

Protocol of CT scans
Method
Enhanced CT scanning was performed during the arte-
rial and venous phases. Arterial phase CT scans were
Patient selection
performed using the bolus tracking method and a
Of the 229 patients with colorectal cancer who under- method described previously [10]. CT scan images were
went preoperative CT scans from July 2017 to July reviewed using a picture archiving and communication
2018, the 205 who underwent an enhanced thin-slice system workstation (General Electric Medical Systems,
(slice thickness ≤ 1 mm) CT scan were enrolled in the Milwaukee, Wisconsin, USA). The anatomy was anal-
present study. Fifteen patients underwent nonenhanced ysed using both CT angiography and a two-dimensional
CT scan, and the slice thickness in five patients was (2D) axial view. In some typical cases, the artery, vein

(a) (b)

(c) (d)

Figure 1 Patterns of the accompanying


artery with the inferior mesenteric vein:
(a) the accessory middle colic artery, (b)
the left colic artery, (c) the Moskowitz
artery, (d) no artery.

Colorectal Disease ª 2019 Association of Coloproctology of Great Britain and Ireland. 22, 392–398 393
Vascular anatomy of the splenic flexure K. Murono et al.

and pancreas were reconstructed using 3D imaging for Table 1 Patient characteristics (n = 205 patients).
presentation of the branching pattern. The arteries were
Feature Value
reconstructed using the 3D volume rendering tech-
nique, and the veins and pancreas were reconstructed
Gender
by tracing them manually as a region of interest. Image
Male 122 (59.5%)
processing was performed using OsiriX MD (Pixmeo Female 83 (40.5%)
SARL, Switzerland). Age (years) 67 (23–90)
Body height (cm) 162.1  9.3
Body weight (kg) 61.8  14.0
Definitions of the AMCA and SFV
BMI (kg/m2) 23.3  4.1
Although the AMCA typically originates from the SMA, AMCA
we previously reported that the AMCA sometimes origi- Present 74 (36.1%)
nates from the coeliac artery, hepatic artery and jejunal Absent 131 (63.9%)
artery [7]. Therefore, the AMCA was defined as the Origin of AMCA
SMA 67 (32.7%)
artery running below the pancreas and toward the sple-
Splenic artery 5 (2.4%)
nic flexure.
Common hepatic artery 2 (1.0%)
The AMCA and LCA sometimes merge and supply No AMCA 131 (63.9%)
the splenic flexure (Fig. 1c). In such cases, we defined SFV
the connecting artery between the LCA and AMCA as Present 177 (86.3%)
the Moskowitz artery, which is the collateral artery that Absent 28 (13.7%)
runs more centrally than Riolan’s arch [11,12]. These Artery accompanying SFV
connecting arteries are often called meandering arteries AMCA 67 (32.7%)
[13,14]. LCA 87 (42.4%)
The names of the veins are usually defined according Moskowitz† 7 (3.4%)
to the accompanying arteries. It was difficult to define None 16 (7.8%)
No SFV 28 (13.7%)
the name of the vein from the splenic flexure because
Destination of IMV
the vein sometimes accompanied the LCA and some-
SMV 94 (45.9%)
times the AMCA. Therefore, the drainage vein from the Splenic vein 111 (54.1%)
splenic flexure running below the pancreas was defined LCA
as the SFV [9]. Present 196 (95.6%)
Absent 9 (4.4%)
LCA location
Evaluation of the anatomy of the AMCA and SFV
Ventral to IMV 140 (68.3%)
First, the presence and branching pattern of the AMCA Dorsal to IMV 56 (27.3%)
and SFV were evaluated. If the SFV was observed, the Location of the origin of AMCA
artery accompanying the SFV was evaluated. In the Below pancreas 59 (28.8%)
Dorsal to pancreas 15 (7.3%)
presence of the Moskowitz artery, it is challenging to
Location of the destination of SFV
identify which artery (LCA or AMCA) is the accompa-
Below pancreas 169 (82.4%)
nying artery. Therefore, the Moskowitz artery is defined Dorsal to pancreas 8 (3.9%)
as the accompanying artery in these cases. Location of the destination of IMV
Finally, the location of the origin of the AMCA and Below pancreas 140 (68.3%)
the destination of the SFV and IMV were evaluated Dorsal to pancreas 65 (31.7%)
with a focus on the positional relationship between Location of the origin of SMA
these vessels and the pancreas. Each vessel was classified Below pancreas 94 (46.3%)
according to location, as follows: below, dorsal to or Dorsal to pancreas 88 (42.4%)
above the pancreas. Above pancreas 23 (11.2%)

Values are given as: number (%), median (range) or average 


Statistical analysis SD.
AMCA, accessory middle colic artery; BMI, body mass index;
To evaluate the association between the clinical parame- IMV, inferior mesenteric artery; LCA, left colic artery; SFV,
ters and positional relationship between the vessels and drainage vein from splenic flexure.
pancreas, Fisher’s exact probability test was applied. All †Moskowitz artery: connection of LCA and AMCA.
analyses were performed using JMP14.0 software (SAS

394 Colorectal Disease ª 2019 Association of Coloproctology of Great Britain and Ireland. 22, 392–398
K. Murono et al. Vascular anatomy of the splenic flexure

Institute Inc., Cary, North Carolina, USA), and a P- destination of the SFV was located below the pancreas
value < 0.05 was considered statistically significant. in 169 of 177 patients. By contrast, the origin of the
AMCA was located on the dorsal side of the pancreas in
20.3% (15/74) of cases. When the origin of the AMCA
Results
was the splenic artery or common coeliac artery, the
AMCA was located on the dorsal side of the pancreas in
Bifurcation patterns of the AMCA and SFV
six (85.7%) of seven patients, which was significantly
The characteristics of the patients and the bifurcation higher than the rate in patients for whom the origin
patterns of the AMCA and SFV are shown in Table 1. was the SMA (P = 0.0003) (Table 2).
The AMCA was observed in 74 (36.1%) patients. In 67
of these 74 patients (90.5%) the AMCA originated from
AMCA SFV
the SMA, and this accounts for more than 90% of cases.
IMV
The AMCA originated from the splenic artery in five
patients and from the common hepatic artery in two
patients. The LCA was absent in 9 (4.4%) of the
patients. Among the nine patients without a LCA, the
AMCA was observed in seven (77.8%) (data not shown).
The SFV was present in 177 (86.3%) patients. In all
cases the destination of the SFV was the IMV. The rela-
LCA Descending branch
tionship between the SFV and the arteries was divided
IMA of LCA
into one of four types (Fig. 1): the SFV running along
the LCA, the AMCA, the Moskowitz artery and with-
out any artery. The LCA was the major artery accompa-
nying the SFV in 87 (42.4%) of patients. The AMCA
ran along with the SFV in 65 (31.7%) patients. When
the AMCA was present, the accompanying artery was
the AMCA or the Moskowitz artery. In 15 (7.3%)
patients, only the drainage vein was detected below the
pancreas from the splenic flexure, and no artery was
detected. Figure 2 Typical case of the Moskowitz artery (dotted line).
When the Moskowitz artery becomes atrophic or absent, the
AMCA would be the accompanying artery. When the central
Positional relationship between these vessels and the side of the AMCA becomes atrophic, the LCA would be the
pancreas accompanying artery. IMA, inferior mesenteric artery; IMV,
inferior mesenteric vein; LCA, left colic artery; AMCA, acces-
We evaluated the positional relationship between the sory middle colic artery; SVV, drainage vein from the splenic
AMCA, SFV, IMV and pancreas (Table 1). The flexure.

Table 2 Relation between the branching pattern and the location of AMCA and IMV.

Location of the origin of the AMCA

Below the pancreas Dorsal to the pancreas P-value

Origin of the AMCA SMA 57 (85.1%) 10 (14.9%) 0.0003


CHA/SA 1 (14.3%) 6 (85.7%)

Location of the destination of the IMV

Below the pancreas Dorsal to the pancreas P-value

Destination of the IMV SMV 67 (71.3%) 27 (28.7%) 0.40


Splenic vein 73 (65.8%) 38 (34.2%)

AMCA, accessory middle colic artery; CHA, common hepatic artery; IMV, inferior mesenteric vein; SA, splenic artery; SMA,
superior mesenteric artery; SMV, superior mesenteric vein.

Colorectal Disease ª 2019 Association of Coloproctology of Great Britain and Ireland. 22, 392–398 395
Vascular anatomy of the splenic flexure K. Murono et al.

The IMV was located on the dorsal side of the pan- IMV
SFV
creas in 65 (31.7%) of the patients (Table 1). The rate
was not associated with the destination of the IMV
(Table 2).

Discussion and conclusions


The AMCA was present in 74 (36.1%) of patients in
the present study, which is consistent with the result of
previous studies based on cadaveric dissection [15–17],
LCA
intra-operative findings [8], angiography results [18]
and CT scans [7,19]. Moreover, the AMCA originated IMA
from the SMA in more than 90% of the patients. This
result is also consistent with that of our previous study
[7]. The lymph nodes around the AMCA should be dis-
sected during the surgery for cancer of the splenic flex-
ure.
In patients without LCA, the AMCA was observed
in 7 (77.8%) of patients, which is significantly higher
than that observed for the other cases. The rate was also
consistent with our previous study. These data support
the idea that the LCA and AMCA complement each
Figure 3 Typical case without an accessory middle colic artery.
other’s blood supply to the splenic flexure and that the
During lymph node dissection for splenic flexure cancer, the
LCA becomes atrophic or is absent in cases where the inferior mesenteric vein (IMV) should be dissected above the
AMCA is present [7,17]. It is important to detect the arrow point to resect the full length of the left colic artery
AMCA in cases of double colonic cancer. When right (LCA) (SFV, drainage vein from splenic flexure).
hemicolectomy and sigmoidectomy are performed, the
AMCA is sometimes necessary to preserve the splenic
flexure. The presence of the AMCA is also important of the IMV at its destination, which is usually just
during right hemicolectomy after surgery for abdominal below the pancreas, may be required to achieve central
aortic aneurysm because the blood flow to the inferior ligation of the mesenteric vessels.
mesenteric artery is usually impaired. The origin of the AMCA and the destinations of the
The SFV was present in 177 (86.3%) of patients. IMV and SFV were on the dorsal side of the pancreas
When the AMCA was present, the SFV ran along with in 15 (20.2%), 65 (31.7%) and 8 (3.9%) of patients,
the AMCA in all patients. The LCA was the accompa- respectively. This result is consistent with that of previ-
nying artery in 87 (84.4%) of 103 patients without the ous studies [9]. In patients with gastric cancer, the posi-
AMCA. When the Moskowitz artery existed, this artery tional relationship between the splenic artery, vein and
accompanied the SFV, as shown in Fig. 1(c). When the pancreas was associated with pancreatic fistula after gas-
Moskowitz artery is atrophic or absent (as represented trectomy [20]. A concealed type of splenic artery
by dotted lines in Fig. 2), the AMCA would be the behind the pancreas was associated with longer surgical
accompanying artery. When the central side of the time, a higher volume of blood loss and higher postop-
AMCA becomes atrophic or absent, the LCA would be erative morbidity [21,22]. Moreover, it was also corre-
the accompanying artery. These data also support the lated with longer operative time and a higher volume of
complementary blood supply from the LCA and blood loss during laparoscopic distal pancreatectomy
AMCA. [23]. In these cases it may be associated with a higher
When the AMCA was absent, the LCA ran along risk of central ligation of the AMCA and IMV. In par-
with the SFV toward the splenic flexure in most cases ticular, an anatomical image must be obtained when the
(Fig. 1b). During lymph node dissection for splenic AMCA originates from the splenic or common hepatic
flexure cancer, the IMV should be dissected above the artery because the AMCA was located on the dorsal side
joint portion of the SFV into the IMV to resect the full of the pancreas in 85.7% of the patients.
length of the LCA (as represented by arrows in Fig. 3). The present study had some limitations. First, the
Moreover, lymphatic flow along the IMV has been anatomy was not confirmed intra-operatively. The pan-
observed using ICG imaging [8]. Therefore, dissection creas and the vessels may move in a head-down

396 Colorectal Disease ª 2019 Association of Coloproctology of Great Britain and Ireland. 22, 392–398
K. Murono et al. Vascular anatomy of the splenic flexure

position, which may affect the frequency of location of study of 536 patients and a review of the literature. Int J
the AMCA, SFV and IMV. Second, the incidence of Colorectal Dis 2016; 31: 1633–8.
lymph node metastases around the AMCA and IMV 5 Willard CD, Kjaestad E, Stimec BV, Edwin B, Ignjatovic
was not evaluated in the present study. Therefore, we D. Preoperative anatomical road mapping reduces variabil-
ity of operating time, estimated blood loss, and lymph
could not discuss the proper ligation level to achieve
node yield in right colectomy with extended D3 mesen-
adequate lymph node dissection. Whether central liga-
terectomy for cancer. Int J Colorectal Dis 2019; 34: 151–
tion of the AMCA and IMV is necessary even if these 60.
vessels are concealed at the dorsal side of the pancreas 6 Nesgaard JM, Stimec BV, Bakka AO, Edwin B, Ignjatovic
has not been fully elucidated. Moreover, when the SFV D. Navigating the mesentery: a comparative pre- and per-
does not have an accompanying artery we did not vali- operative visualization of the vascular anatomy. Colorectal
date whether central ligation of the IMV is required. Dis 2015; 17: 810–8.
In conclusion, the SFV was present in 177 (86.3%) 7 Miyake H, Murono K, Kawai K et al. Evaluation of the vas-
of the patients, and the LCA or AMCA was the com- cular anatomy of the left-sided colon focused on the acces-
mon accompanying artery. In some patients these ves- sory middle colic artery: a single-centre study of 734
sels were located on the dorsal side of the pancreas. patients. Colorectal Dis 2018; 20: 1041–6.
8 Watanabe J, Ota M, Suwa Y, Ishibe A, Masui H, Nagahori
Preoperative evaluation of this anatomy may contribute
K. Evaluation of lymph flow patterns in splenic flexural
to lymph node dissection during left-sided hemicolec-
colon cancers using laparoscopic real-time indocyanine green
tomy. fluorescence imaging. Int J Colorectal Dis 2017; 32: 201–7.
9 Arimoto A, Matsuda T, Hasegawa H et al. Evaluation of
Acknowledgement the venous drainage pattern of the splenic flexure by preop-
erative three-dimensional computed tomography. Asian J
This research is supported by Grants-in-Aid for Scien- Endosc Surg 2018; 12: 412–6.
tific Research (C: grant number 17K10620, C: grant 10 Murono K, Kawai K, Kazama S et al. Anatomy of the infe-
number 17K10621, C: grant number 17K10623 and rior mesenteric artery evaluated using 3-dimensional CT
C: grant number 18K07194) from the Japan Society angiography. Dis Colon Rectum 2015; 58: 214–9.
for the promotion of Science. This research is supported 11 Moskowitz M, Zimmerman H, Felson B. The meandering
mesenteric artery of the colon. Am J Roentgenol Radium
by the Project for Cancer Research and Therapeutic
Ther Nucl Med 1964; 92: 1088–99.
Evolution (P-CREATE), grant number:
12 Garcia-Granero A, Sanchez-Guillen L, Carreno O et al.
18cm0106502h0003 from the Japan Agency for Medi- Importance of the Moskowitz artery in the laparoscopic
cal Research and Development (AMED). medial approach to splenic flexure mobilization: a cadaveric
study. Tech Coloproctol 2017; 21: 567–72.
13 Gourley EJ, Gering SA. The meandering mesenteric artery:
Conflicts of interest
a historic review and surgical implications. Dis Colon Rec-
There are no conflicts of interest. tum 2005; 48: 996–1000.
14 Lange JF, Komen N, Akkerman G et al. Riolan’s arch:
confusing, misnomer, and obsolete. A literature survey of
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