DOI: 10.1002/jhbp.

901

SYST E M AT I C R E V I E W

Precision anatomy for safe approach to pancreatoduodenectomy

for both open and minimally invasive procedure: A systematic
review

Kohei Nakata1*  | Ryota Higuchi2*  | Naoki Ikenaga1  | Leon Sakuma3  | Daisuke Ban4  |

Yuichi Nagakawa5   | Takao Ohtsuka6  | Horacio J. Asbun7  | Ugo Boggi8  |
Chung-­Ngai Tang9  | Christopher L. Wolfgang10  | Hitoe Nishino5   | Itaru Endo11   |
Akihiko Tsuchida5  | Masafumi Nakamura1   | Study Group of Precision Anatomy for
Minimally Invasive Hepato-­Biliary-­Pancreatic surgery (PAM-­HBP Surgery)
1
Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
2
Department of Surgery, Institute of Gastroenterology, Tokyo Women's Medical University, Tokyo, Japan
3
Professor with Special Assistant, Kawasaki Medical School, Okayama, Japan
4
Department of Hepatobiliary and Pancreatic Surgery Division, National Cancer Center Hospital, Tokyo, Japan
5
Department of Gastrointestinal and Pediatric Surgery, Tokyo Medical University, Tokyo, Japan
6
First Department of Surgery, Kagoshima University School of Medicine, Kagoshima, Japan
7
Division of Hepatobiliary and Pancreas Surgery, Miami Cancer Institute, Miami, FL, USA
8
Division of General and Transplant Surgery, Pisa University Hospital, Pisa, Italy
9
Department of Surgery, Pamela Youde Nethersole Eastern Hospital, Hong Kong SAR, China
10
Department of Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA
11
Department of Gastroenterological Surgery, Yokohama City University Graduate School of Medicine, Yokohama, Japan

Correspondence
Masafumi Nakamura, Department of
Surgery and Oncology, Graduate School of
Medical Sciences, Kyushu University, 3-­1-­1
Maidashi, Fukuoka 812-­8582, Japan.
Email: mnaka@surg1.med.kyushu-u.ac.jp
Abstract
Background: Minimally invasive pancreatoduodenectomy (MIPD) has recently
gained popularity. Several international meetings focusing on the existing literature
on MIPD were held; however, the precise surgical anatomy of the pancreas for the
safe use of MIPD has not yet been fully discussed. The aim of this study was to carry
out a systematic review of available articles and to show the importance of identify-
ing the anatomical variation in pancreatoduodenectomy.
Methods: In this review, we described variations in surgical anatomy related to
MIPD. A systematic search of PubMed (MEDLINE) was conducted, and the refer-
ences were identified manually.
Results: The search strategy yielded 272 articles, with 77 retained for analysis. The
important anatomy to be considered during MIPD includes the aberrant right hepatic
artery, first jejunal vein, first jejunal artery, and dorsal pancreatic artery. Celiac artery
stenosis and a circumportal pancreas are also important to recognize.

*Co-­first authors.

© 2021 Japanese Society of Hepato-­Biliary-­Pancreatic Surgery

J Hepatobiliary Pancreat Sci. 2021;00:1–15.  |

wileyonlinelibrary.com/journal/jhbp     1
 |
2      NAKATA et al.

Conclusions: We conclude that only certain anatomical variations are associated di-
rectly with perioperative outcomes and that identification of these particular varia-
tions is important for safe performance of MIPD.

KEYWORDS
anatomical variation, minimally invasive pancreatoduodenectomy, pancreatic resection,
pancreatoduodenectomy, surgical anatomy

1  |   IN TRO D U C T ION references of included studies to identify further eligible ar-

Since laparoscopic pancreatectomy was first reported in
1992,1 it has gained popularity.2 Several systematic reviews
and cohort studies have shown that laparoscopic pancreatec-
tomy has better or comparable perioperative outcomes to
open pancreatectomy.3-­6 However, as a laparoscopic proce-
dure, it has not gained the same widespread acceptance as
other laparoscopic surgeries,2 likely owing to the difficulty
in performing the procedure7 as a result of the complexity of
the local anatomy and the fact that procedures are frequently
performed with concomitant pancreatitis.
Several international meetings regarding minimally inva-
sive pancreatic resection (MIPR) have been held over the past
decade. In 2016, the first international state-­of-­the-­art con-
ference on MIPR was held in São Paulo,8 with major themes
as follows: best-­level evidence of outcomes for MIPR; the
Cost/Value/Quality of Life assessment of MIPR; training
of MIPR, including education and credentialing; and devel-
opment of best approaches to analyze MIPR outcomes. In
2020, the Miami International Evidence-­based Guidelines on
MIPR were published based on the conference that was held
in Miami.9 However, the surgical anatomy of the pancreas for
safe MIPR has not yet been fully discussed.
Variations in the local anatomy of the pancreas and the
relationship between anatomical variation and perioperative
results of pancreatoduodenectomy (PD) have been described
in reports and case series. Therefore, the aim of this study
was to carry out a systematic review to identify the import-
ant anatomical variations to consider when performing a
pancreatoduodenectomy.
ticles. We applied no restrictions related to the study meth-
odology for vessel characterization: surgical, radiological, or
cadaveric. Both “MESH terms” and “Title/Abstract” were
used for searching relevant studies. The keywords used are
listed in the supplementary table (Supplemental Table 1).
2.2  |  Study eligibility criteria
We reviewed all studies that investigated the branching pat-
tern and morphometric data of the peripancreatic vessels that
are related to PD. The exclusion criteria were as follows: (1)
animal studies; (2) case reports, editorials, and letters to the
editor; (3) overlapping or duplicate reports; and (4) languages
other than English.
2.3  |  Primary outcomes and
study evaluation
Primary outcomes for the search were peripancreatic vascu-
lar branching patterns that may affect the surgical outcome
of PD. Secondary outcomes were anatomical relationships
between the venous and arterial branches, and morphometric
data of the blood vessels that could have an impact on PD.
Three reviewers (NK, HR, and IN) performed the evaluation
of the methodological quality and extraction of data from
the individual studies independently. Any disagreements
were resolved by discussion. All selected manuscripts were
evaluated in accordance with the Scottish Intercollegiate
Guidelines Network (SIGN) methodology.

2  | METHODS
2.1  |  Study selection and quality assessment
This systematic review was conducted based on the preferred
reporting items for systematic reviews and meta-­analyses
statement.10 We conducted an electronic literature search
to identify all published studies in PubMed databases, from
their inception to July 2020. Additionally, we screened the
3  |  RESULTS
The search strategy yielded a total of 272 articles includ-
ing titles and abstracts of the studies. After considering the
inclusion and exclusion criteria, a total of 41 articles were
selected. After the full texts of these articles were reviewed,
22 articles were selected from the search strategy. In addi-
tion with 55 reports from hand search, 77 articles were finally
NAKATA et al.
analyzed in the review. Based on the systematic review, the
most frequent pattern of vessels around the pancreas was
drawn (Figure 1).
3.1  |  Hepatic artery
3.1.1  |  Definition of the terms
One of the important anatomical variations in vessels is the
variations of the hepatic artery. There are several terms that
describe the variation of hepatic arteries: “aberrant,” “ac-
cessory,” “replacement,” “substitute,” and “anomalous.”11-
­18
However, the definitions of these terms were different in
each report and were not explained or defined in several re-
ports. Crocetti et al18 described right hepatic artery (RHA)
variations to be divided into “accessory” and “aberrant.”
They described “accessory” as an additional artery that pro-
vides hepatic vascularization, and the definition would be
acceptable and frequently used. They also defined “aber-
rant” as a branch of superior mesenteric artery (SMA) that
is the only blood supply to the liver; however, most of the
reports referred to this variation as “replaced.”11-­17 Shukla
et al17 defined a “replaced” artery to be one that did not arise
from the celiac axis, whereas in other reports the origin did
not matter. The term “anomalous” seems to be used with
a similar meaning to “aberrant,” further suggesting simi-
larity to either “accessory” or “replaced.” Considering the
frequency of use in the previous reports and the meaning
of the word itself, the variation of RHA should be divided
into “accessory” or “replaced” as follows: “replaced” RHA
is the one that is originating from arteries that are the only
blood supply to the liver, irrespective of the route of origin;
“accessory” RHA is an extra artery that provides hepatic
vascularization. Further, “aberrant” should include both “ac-
cessory” and “replaced.”
F I G U R E 1   Vessels around the
pancreas. GCT, gastro-­colic trunk; AIPDV,
anterior inferior pancreatoduodenal vein;
PIPDV, posterior inferior pancreatoduodenal
vein, IMV inferior mesenteric vein; ARCV,
GCT
accessory right colic vein, SPV splenic vein;
AIPDV
LGA, left gastric artery, CHA, common ARCV
hepatic artery, SpA, splenic artery, SMA, PIPDV
IPDA
superior mesenteric artery, IPDA, inferior
pancreatoduodenal artery
|
     3
3.1.2  |  Variation of hepatic artery
The common hepatic artery usually originates from the celiac
artery, which then gives rise to the gastroduodenal artery and
proper hepatic artery (PHA). The most common course of
(RHA) is posterior to the common bile duct. The incidence
of the anterior course of the RHA in the normal population
ranges from 1.4%–­10%.19-­21 Recently, Mori et al22 reported
of the 33 cases with congenital biliary dilatation (CBD), 10
cases (30.3%) showed anterior course of the RHA. The inci-
dence is significantly higher than that in cases without CBD.
Michel et al23 classified the patterns of celiac trunk into 10
patterns and Hiatt et al24 modified the classification into five
types (Figure 2a). Chen et al25 summarized the incidence of
anatomic variation of the hepatic artery in 10 studies which
come from various areas.23-­32 The distributions of the types
in Hiatt's classification24 are not substantially different be-
tween studies. There was no literature showing the racial dif-
ference in the arterial variations around peripancreatic head
by direct comparison. Globally, however, population-­based
reports have identified an incidence of type I HA (typical/
normal anatomy) of 67.1% in the United States (US), 74.0%
in Europe, and 69.4% in Asia (Japan) (Table 1). Regarding
the anatomy of the celiac trunk, the normal form, defined as
a trifurcated trunk with a left gastric artery (LGA), common
hepatic artery (CHA), and splenic artery (SpA), has been
reported in 91.4% of individuals of white European descent
(Caucasian), 89.3% of Japanese descent, 89.1% of Korean de-
scent, 70.0% of Indian descent, and 61.0% of Black descent.
Japanese and Korean populations presented significantly
more variations in the celiac trunk than in the Caucasian pop-
ulation, though this difference was not significant. Although
greater variations were identified among individuals of
Indian and Black descent, it is important to note that the
sample sizes to date have been small. Further investigation is
needed to confirm race-­specific differences in HA anatomy.33
LGA
SpA
CHA
SPV
IMV
J1A
J1V
SMA
 |
4      NAKATA et al.

(a) Type 1 Type 2 Type 3

a-LHA
LGA

SpA
CHA

SMA a-RHA

Type 4 Type 5

a-LHA

r-CHA

a-RHA

(b)

r-RHA

r-RHA

Dorsal type Intrapancreatic type

r-RHA
r-RHA

r-RHA
r-RHA
NAKATA et al.      5
|
F I G U R E 2   (a). Types of hepatic artery (Hiatt's classification). Type 1, Normal; Type 2, Aberrant (replaced or accessory) left hepatic artery
from left gastric artery; Type 3, Aberrant (replaced or accessory) RHA from SMA; Type 4, double replaced system; Type 5, common hepatic artery
from SMA. LGA, left gastric artery; CHA, common hepatic artery; SpA, splenic artery; SMA, superior mesenteric artery; a-­LHA, aberrant left
hepatic artery; a-­RHA, aberrant right hepatic artery. (b) Route of replaced right hepatic artery. Dorsal type: a route behind the head of the pancreas
and then posteriorly and laterally to the main portal vein before reaching the liver. Intrapancreatic type: a route behind the head of the pancreas
and then posteriorly and laterally to the main portal vein before reaching the liver. CT examination of intrapancreatic type. r-­RHA, replaced right
hepatic artery

3.1.3  |  Aberrant hepatic artery
Aberrant RHA is included in Hiatt's types 3 to 5. Of these
variations, type 5 (replaced CHA from SMA) was termed as
a hepatomesenteric trunk and can be included in the category
of “aberrant” RHA. Hiatt et al analyzed extrahepatic arterial
anatomy from 1000 donor liver cases and reported that the
frequency of aberrant RHA was 12.9%. Others also reported
that the frequency of aberrant RHA was 13.8%-­20.7% after
Hiatt's classification, and these results were similar to those
reported by Hiatt.12,18,34-­41 Although aberrant RHA classi-
fied by Hiatt's types originate from SMA, there are other rare
variations of aberrant RHA that originate from the aorta, left
gastric artery, celiac artery, and gastroduodenal artery.39
The main origin of aberrant RHA was SMA, celiac artery,
and aorta, and the frequency was reported to be 74.1%-­80.7%,
18.0%-­19.2%, and 7.9%, respectively.11,42 The most frequent
running pattern of aberrant RHA was the route behind the
head of the pancreas and then posteriorly and laterally to the
main portal vein before reaching the liver (Figure 2b) (85.7%-­
100%).11,35 Crocetti et al18 reported that 59% of aberrant RHA
followed a ventral course of the head of the pancreas, the
frequency was not so high considering the previous reports
and our experience.11,35 The intrapancreatic course would
affect the procedure of PD, with Ishigami et al reporting a
frequency of intrapancreatic course of 0.38%43 (Figure 2b).
3.1.4  |  Impact of aberrant RHA on
intraoperative and postoperative outcomes
significant difference between the two groups.12,35-­41 There
was no significant difference in R0 resection between the two
groups. Kim et al41 reported the influence of aberrant RHA
on MIPD (robotic PD) and showed that there was no signif-
icant difference in the postoperative outcomes between the
aberrant RHA and normal RHA groups. Considering these
findings, postoperative and oncological outcomes seemed
unaffected by this variation provided that aberrant RHA
was preoperatively identified and managed correctly. Okada
et al40 reported that R1 resection rates were higher in patients
with tumors situated within 10 mm from the root of replaced
RHA than in patients with tumors situated more than 10 mm
away. They concluded that replacement of RHA adjacent to
pancreatic carcinoma should be divided to obtain R0 resec-
tion in PD.
3.2  |  Superior mesenteric vein
(SMV) and branches
3.2.1  | SMV
The prevalence (or visualized) rate of the SMV was re-
ported to be 100%44,45 and mean diameter to be within
9.9-­11.3  mm.44,46 The prevalence of single trunks was
76.5%-­92.5%,46,47 two trunks was 23.5%,47 and two intes-
tinal branches joining the splenic vein was 7.5% without
trunks.46 The incidence of SMV inversion was reported to be
0.5%-­4.3%.45,46,48

A total of 2593 patients from 10 articles were analyzed
(Table 2a). The frequency of aberrant RHA was 16.7%. Four
reports described the rate of preoperative identification of
aberrant RHA as 83.7% (108 of 129 cases). The preserva-
tion rate of aberrant RHA was 84.0% (330 of 393 cases) and
accidental resection or ligation occurred in 16 cases (4.0%).
Of the 47 cases where the aberrant RHA was intentionally
resected, reasons were oncological necessity in 39 cases
(83.0%) and technical necessity in eight cases (17.0%).
For the analysis of perioperative outcomes, a total of 2402
patients from nine articles were analyzed (Table 2b). Crocetti
et al18 reported that operative time and blood loss were pro-
longed and higher in the aberrant RHA group than in the nor-
mal RHA group; however, the other eight reports showed no
3.2.2  |  First (and second) jejunal veins (JVs)
There are several similar terms such as "first jejunal vein”
(FJV),44,46,49 "jejunal vein trunk” (JVT),45 "first jejunal
trunk” (FJT),7,8,50,51 "first jejunal venous trunk” (FJVT),52
“jejunal veins”,53 “first (and second) jejunal branches of the
SMV,”54,55 and "proximal dorsal jejunal vein” (PDJV)56 for
the blood vessels in some similar areas. First, the JV was
defined as the first major branch of the SMV,49 while the
FJVT was defined as the first-­order trunk comprised several
JVs draining into the SMV from the proximal jejunum52
or confluence of the first and second jejunal veins.50 Most
of the reports use both the terms with similar meanings,
interchangeably.
 6     
| NAKATA et al.

The prevalence (or visualized) rate of FJV was reported to

69.4
11.2
be 97%-­100%44,45,50-­52 and the mean diameter to be within 4.5-­

5.3
1.9
3.4
8.6
%
7.9 mm.44,46,51,52,55,57 The FJV was dorsal to the SMA in 63.0%-­
87.2% of cases, on ventral side in 5.8%-­41.0% cases, and on

Total
815
132

101
62
both sides in 2.3%-­21.9% cases (Figure 3a).45-­47,49,50,52-­56 The

22
40
mean number of JVs crossing the origin of SMA to the origin
Suzuki

of the middle colic artery (MCA) was 1.1 ± 0.3, between the

Japan
110
24)

origins of the MCA and ileocolic artery (ICA) was 1.4 ± 0.5,

Asia (Japan)

25
15

36
8
6
and within 1 cm caudal to the origin of the ICA was 1.0 ± 0.0.57
The prevalence of the patterns of first and second jejunal
Chen

Japan
705
107
15)

veins branching separately was 12%-­16%, and those forming

47
14
34
65
a common trunk was 84%-­88%.50,52 Kobayashi et al52 focused
on the branching pattern of the trunk and reported that two
74.0
7.4
9.8
0.8
2.9
5.2
%

JVs were present in 30.1% of cases, three JVs in 30.1%, four

or more JVs in 27.7% (four JVs in 23.6%) of cases (Figure 3b).
1,298
Total

Ishikawa et al50 examined the drainage territory of the FJVT

129
172
14
51
91

and found that the prevalence of first to second jejunal artery

Koops 23)

region was 52%, first to third jejunal artery region was 38%,
Germany

first to fourth jejunal artery region was 8%, and first to fifth
478

jejunal artery region was 2%. It has also been reported that
18
72

17
11
8

approximately 5% of cases had FJV draining directly into the

splenoportal venous confluence.45,55
Iezzi

Italy
378
22)

32
49

19
46

Nakamura et al49 reported that "first jejunal vein-­oriented

0

mesenteric excision for PD" significantly reduced blood loss

Makisalo

as compared to classical PD (median blood loss 569  g vs

1,094 g). Nagakawa et al58 reported that operative time was
UK
21)

76
4
7
2
3
8

significantly reduced by the right SMA approach using the

Europe

PDJV pre-­isolation method in laparoscopic pancreatoduo-

Soin

366
UK

denectomy compared with the classical approach (mean total

20)

75
44

12
26
4

operative time 541.7 min vs 489.4 min.

67.1
11.3
13.0
4.3
1.4
2.8
%

3.2.3  |  Inferior pancreatoduodenal vein

1,340
Total

(IPDV) / anterior inferior pancreatoduodenal vein

226
260
85
27
55

(AIPDV) / posterior inferior pancreatoduodenal

vein (PIPDV)
Michels

110
19)
US

The prevalence (or visualized) rate and mean diameters

36
36
8
5
1
T A B L E 1   The difference of Hiatt's variation by race

of IPDV, AIPDV, and PIPDV were reported to be 59.0%,

36.0%-­75.0%, and 36.0%-­66.6%, and 1.6 mm, 1.4 mm, and
Gruttadauria

1.5  mm, respectively.46,51 The prevalence of outflow veins

of the IPDV was 79.0% for FJV, 21.0% for SMV50; that
Note: US; United States, UK; United Kingdom.
405

105

of AIPDV was 58.7% for FJV, 24.8% for SMV, 11.3% for
18)
US

81

52

52
6

gastro-­colic trunk (GCT), 3.7% for second JV, and 1.6% for
third JV46 ; and that of PIPDV was 60.9% for FJV, 22.3%
Varotti

for SMV, 7.6% for second JV, 1.6% for third JV, 1.6% for il-
17)
US
68
12
13
2
1
0

eocolic vein, 1.6% for GCT, and 2.1% for portal vein (PV).46
Hiatt

757

106
16)
US

US

97

23
15
2

3.2.4  |  GCT (gastro-­colic trunk)

Country
Author

Type 1
Type 2
Type 3
Type 4
Type 5

The prevalence (or visualized) rate of GCT was re-

other

ported to be 86.9%-­100%,44,51,59 the mean diameter within

NAKATA et al.
3.3-­4.2 mm,44,51,59 and the mean length 10.7 mm.59 The vari-
ous types of anatomical tributaries were 56.1%-­93.0% of the
gastro-­pancreato-­colic trunk, 17.8% of the GCT, 7.0%-­12.7%
of the gastro-­pancreatic trunk, and 0.9% of the pancreato-­
colic trunk.44,51,59 Miyazawa et al subclassified 93% of the
GCT depending on the number of inflowing colon veins into
the right gastroepiploic vein and anterior superior pancrea-
toduodenal vein as: 71% of type I (superior right colic vein
[SRCV]), 20% of type II (SRCV + right colic vein [RCV] or
middle colic vein [MCV]), and 2% of type III (SRCV + RCV
+MCV). Furthermore, 100% of SRCV, 14.3% of RCV, and
13.4% of MCV flowed into the GCT, and 85.7% of the RCV
and 86.6% of the MCV flowed into the SMV.60 The mean
vertical distance between the MCA and the GCT origins was
reported to be 10.0-­12.6 mm.57
3.2.5  |  Inferior mesenteric vein (IMV)
The prevalence (or visualized) rate of IMV was reported to be
90.2%-­97.0%,44,45,47 and the mean diameter to be 3.9  mm.45
The prevalence of area where the IMV passes was reported
to be of the ventral SMA in 18.6% of cases and the area from
the root of the SMA in 81.4%47 cases. As for the outflow
route of IMV, it has been reported that it joins the splenic
vein in 53.0%-­71.7% of cases, SMV in 18.9%-­31.6% of cases,
SPV-­Portal Vein (PV) confluence in 7.6%-­17.0% of cases,45-
­47,55,61
FJV in 0.6%-­4.0% of cases,45,46,55 ileal trunk in 0.3%
of cases,46,55 and the left trunk of two SMV trunks in 5.4% of
cases.47
3.2.6  |  Left gastric vein (LGV)
The prevalence (or visualized) rate of LGV was reported to
be 93.1%-­100%.47,62 The prevalence of outflow route of the
LGV was reported to be 39.0%-­65.0% to PV, 30.3%-­46.3%
to SPV, and 4.7%-­14.7% to SV-­PV confluence.46,47,62 LGV
resection was an independent risk factor for sinistral (left-­
sided) portal hypertension in patients with combined PV re-
section.63 If the LGV drains into the PV, then the LGV-­PV
route is an important drainage route when performing SPV
ligation. Therefore, the LGV should be preserved in these
cases, if oncologically acceptable.
3.2.7  |  Anterior superior pancreatoduodenal
vein (ASPDV), posterior superior
pancreatoduodenal vein (PSPDV)
The prevalence (or visualized) rate and mean diam-
eters of ASPDV and PSPDV were reported to be 50.0%-­
88.0% and 90.0%-­95.0%, and 1.6-­1.7  mm and 1.9-­2.6  mm,
|
     7
respectively.44,46,51 The prevalence of the outflow vessels of
ASPDV and PSDPV was 83.2% and 0% for the GCT, 10.2%
and 0% for the right gastroepiploic vein, 5.5% and 2.0% for
SMV, and 1.0% and 98% for PV,46 respectively.
3.3  |  Other arteries
3.3.1  |  Inferior pancreatoduodenal artery
(IPDA) / anterior inferior pancreatoduodenal
artery (AIPDA) / posterior inferior
pancreatoduodenal artery (PIPDA)
The prevalence (or visualized) rate and mean diameters
of IPDA were reported to be 53.8%-­ 100%42,46,64-­66 and
64
2.7  mm, respectively. The prevalence of the branching
pattern of IPDA was reported to be 55.6%-­83.3% of the
common trunk type with jejunal arteries,46,50,52,53,65-­68 9.3%-­
35.8% of IPDA independent type,50,52,53,66-­69 and 9.3%-­11.3%
of AIPDA-­and PIPDA-­independent types.66,68 Most of the
origins of IPDA were from SMA, but 1.0%-­5.6% of replaced
RHA,46,50,53 0.8%-­ 8.3% of MCA,46,65 0.6%-­ 3.3% of right
46,65
colic artery, and 0.5%-­1.7% of arc of Buhler, which is a
collateral circulation between the coeliac trunk and the supe-
rior mesenteric artery,46,65 were also reported. Inoue et al re-
ported that the IPDA origin was of dorsal aspect from 5 to 7
o'clock of SMA in 65.6% of cases, right aspect from 8 to 12
o'clock of SMA in 20.8% of cases, and left aspect from 0 to 4
o'clock of SMA in 13.7% of cases.53 Horiguchi et al reported
that the mean distance between the IPDA (or AIPDA) and
middle colic artery was 17.6-­18.6 mm.67 The prevalence (or
visualized) rate and mean diameters of AIPDA and PIPDA
were reported to be 60.0%-­73.1% and 72%-­86.4%,70,71 and
2.1 mm and 2.0 mm,70 respectively. The origins of AIPDA
and PIPDA were IPDA in 50.0% and 45.5% of cases, SMA in
22.2% and 36.4% of cases, J1A in 16.7% and 18.2% of cases,
and J2A in 11.1% and 0% of cases, respectively.70
3.3.2  |  Jejunal artery (JA)
The mean number of JAs arising along the left side of the SMA
was 3.7-­3.8.57,65 Of these, 1.86 JAs arose cranially to the MCA.57
3.3.3  |  Dorsal pancreatic artery (DPA)
The prevalence (or visualized) rate and mean diameters
of DPA were reported to be 65.4%-­96.3%,66,70,71 and 2.0-­
3.5  mm,70,72 respectively. The origin of DPA was splenic
artery in 38.5%-­ 46.1% of cases, hepatic artery (HA) in
15.4%-­25.7% of cases, celiac artery in 7.7%-­8.6% of cases,
JA or MCA in 5.7% of cases, CHA in 7.7% cases and right
 |
8      NAKATA et al.

T A B L E 2   (a) Analysis of frequency of aberrant RHA (b) Analysis of perioperative outcomes from nine articles that included a total of 2402
patients

Year Total number a-­RHA Non-­aRHA

21
2009 Stauffer 191 31 160
2009 Jah22 135 28 107
23
2011 Eschuis 758 143 615
2014 Kim24 289 40 249
25
2013 Sulpice 213 29 184
26
2014 Rammohann 225 43 182
2015 Okada27 180 25 155
28
2016 Kim 73 15 58
2018 Alexakis12 232 35 197
2019 Crocetti18 297 44 253
total 2,593 433 (16.7%) 2,160

Operative time Blood loss

Total non-­ non-­ non-­

Year number a-­RHA aRHA a-­RHA SD aRHA SD P a-­RHA SD aRHA SD P
22
2009 Jah 135 28 107 400 NA 400 NA NS 1,400 N.A. 1,200 N.A. NS
23
2011 Eschuis 758 143 615 299 91 300 86 NS 1,100 963 1,050 1,200 NS
25
2013 Sulpice 213 29 55 334.5 83 341 106 NS NA NA NA NA NA
2014 Kim24 289 37 212 479 85 439 128 NS 950 N.A. 650 N.A. NS
26
2014 Rammonnhann 225 43 182 480 45 420 44 NS 390 45 360 52 NS
2015 Okada27 180 25 155 420 74 417 86 NS 1,046 762 997 1,008 NS
2016 Kim28 73 15 58 443.7 50.1 463.6 105.2 NS 545.8 729 310.1 267.6 NS
12
2018 Alexakis 232 35 70 NA NA NA NA NA NA NA NA NA NA
2019 Crocetti18 297 44 253 451 58 317 27 <0.001 729 488 508 119 <0.001
Note: NA, not available; a-­RHA, aberrant right hepatic artery; SD, standard deviation, POPF, DGE,

gastroepiploic artery (RGEA) in 7.7% of cases.66,70,72 Jiang
et al reported that ligation of DPA prior to dissection of the
uncinate process improved resection time and blood loss in
laparoscopic PD.72
3.3.4  |  Transverse pancreatic arteries (TPA)
is known as celiac artery stenosis (CAS) and the inci-
dence of CAS is reported to be 7.3% (Figure  4).73 The
most common and important collateral arteries are pan-
creatoduodenal arcades (95% of cases) and dorsal pancre-
atic arteries (76% of cases).74 Therefore, the division of
these arcades could cause ischemia of the upper abdomi-
nal organs.

The prevalence (or visualized) rate of TPA was reported to be

76.9% in single and 15.0% in double artery. The prevalence
rate of origin of TPA was 26.9% for DPA, 19.2% for SMA,
7.7% for SpA, and 3.8% for RGEA.70
3.4  |  Celiac Stenosis
3.4.1  |  Frequency of celiac artery stenosis
The celiac artery arises directly from the aorta and mainly
supplies blood flow to the stomach, pancreas, spleen, and
liver. The obstruction or occlusion of the celiac artery
3.4.2  |  Management of celiac artery stenosis
The management of CAS is divided into the dissection of
the median arcuate ligament (MAL), preservation of col-
lateral arteries, reconstruction, and preoperative dilation.
The main cause of CAS is median arcuate ligament syn-
drome (MALS) and atherosclerosis; therefore, CAS should
be properly managed by addressing the root cause.75 If the
reason for CAS is diagnosed as MALS and blood supply
is decreased after the occlusion testing, division of MAL
is the first step in the management of CAS. MAL division
is not a complex procedure, and Gaujoux et al76 reported
NAKATA et al.      9
|

Diagnosis N Preservation Resection Intentional Accidental

26 24 7 5 2
NA 24 4 3 1
NA 130 13 8 5
NA NA NA NA NA
20 23 6 6 0
NA 34 9 7 2
25 19 6 6 0
NA 13 2 2 0
NA 30 5 2 3
37 33 11 8 3
108 (83.7%) 330 (84.0%) 63 (16.0%) 47 (12.0%) 16 (4.0%)

mortality complication Hemorrhage POPF DGE

non-­ non-­ non-­ non-­ non-­ R0

a-­RHA aRHA P a-­RHA aRHA P a-­RHA aRHA P a-­RHA aRHA P a-­RHA aRHA P ratio
0 2 NS NA NA NA NA NA NA 5 16 NS 4 15 NS NS
2 13 NS 80 303 NS 11 44 NS 18 87 NS 48 193 NS NA
3 3 NS 14 32 NS 4 9 NS 3 9 NS 10 24 NS NS
0 1 NS 9 88 0.04 1 16 NS 1 12 NS 4 16 NS NS
1 3 NS NA NA NS 1 4 NS 2 9 NS 23 98 NS NS
0 1 NS 1 20 NS 0 5 NS 1 9 NS 2 8 NS NA
0 2 NS 5 25 NS 1 5 NS 2 5 NS NA NA NA NS
2 4 NS 4 19 NS 0 2 NS 2 9 NS 1 1 NS NS
7 33 NS NA NA NA 2 12 NS 5 27 NS 5 37 NS NS

successful rates of 87% for MAL division (20 of 23 cases).
If the blood flow is not recovered after MAL division, re-
vascularization or preservation of the collateral arteries
should be considered. Although endovascular intervention
is not recommended as a sole management for MALS, it
remains an option for managing residual symptoms follow-
ing MAL division.77
When CAS is diagnosed as being secondary to atheroscle-
rosis, division of MAL will not provide benefit76 and revas-
cularization or preservation of collateral arteries should be
considered. In addition, preoperative endovascular stenting
or balloon angioplasty can be considered.78,79
type I, when the ventral bud of the pancreas fuses with the
body and ductal system of the pancreas posterior to the portal
vein; type II when type I is associated with pancreas divisum;
and type III, when the uncinate process alone is involved in
the encasement of the vessels and fusion. Each may be fur-
ther divided as follows: a) supra-­splenic; b) infra-­splenic;
and c) mixed depending on its relationship to the splenic
vein.81,82 In this anomaly, postoperative pancreatic fistula
in patients undergoing pancreatectomy has been reported to
increase.43,80,83 Therefore, a shift of the resection plan to the
left is proposed for PD.80,82,83

3.5  |  Circumportal pancreas (portal annular
pancreas)
Circumportal pancreas is an asymptomatic pancreatic anom-
aly with a prevalence from 1.1% to 3.4% of the general popu-
lation, in which the uncinate process of the pancreas encircles
the portal vein (Figure 5).80 It is proposed to be classified as
4  |  DISCUSSION
In this study, we present a systematic review of the surgi-
cal anatomy of the pancreas and its relationship with perio-
perative outcomes of PD. This is important as although the
indications for MIPDs have increased, few reports have fo-
cused on the relevant surgical anatomy. However, a clear
understanding of anatomical relationships is essential as
 |
10      NAKATA et al.

(a) The jejunal vein runs across the route in relation to the SMA

IPDV IPDV IPDV

GCT
GCT GCT GCT J1V
J1V J1V
IPDV
IPDV IPDV
IPDV FJT
J2V J2V
J2V
SMV SMA
SMV SMA
SMV SMA Both type
Dorsal FJV(FJT) (Dorsal plus ventral) Ventral J1V (J2V)

(b) The first jejunal trunk regarding the number of the jejunal vein

J1V

12.2 % 30.1 % 30.1 % 23.6 %

F I G U R E 3   (a) Course of the jejunal vein in relation to the SMA. The first jejunal vein was located dorsal to the SMA in 63.0%-­87.2% cases,
on ventral side in 5.8%-­41.0% cases, and on both sides in 2.3%-­21.9% cases. GCT; gastro-­colic trunk, IPDV; inferior pancreatoduodenal vein,
SMV; superior mesenteric vein, SMA; superior mesenteric artery, FJT; first jejunal trunk, FJV; first jejunal vein. (b) The number of jejunal veins
off the first jejunal trunk. Kobayashi et al reported the prevalence of one jejunal vein (JV) to be 12.2%, of two JVs to be 30.1%, of three JVs to be
30.1%, and of four or more JVs to be 27.7% (with a prevalence of four JVs of 23.6%)

most peripancreatic vessels are located deep to the pancreas
and, therefore, are not readily observable. In addition, tactile
feedback is not available during MIPD. To avoid potential
damage during PD, preoperative evaluation of these variation
with CT examination and sharing the information with surgi-
cal team would be helpful.
The most frequently reported anatomical variation related
to PD is an aberrant RHA, with a preoperative diagnostic
rate of 83.7%. This diagnostic rate seems low and could be
related to differences in the condition of contrast enhance-
ment, such as timing of contrast administration, and the res-
olution of CT between studies. If arterial variations of CT
were assessed using the early arterial phase and thin slices,
nearly all aberrant RHA could be identified preoperatively.
In addition, multiplanar reconstructions for detecting arterial
anatomy, as well as the use of standardized reporting tem-
plates, might be helpful for universal improvement of ana-
tomical diagnosis.84,85
The rate of accidental ligation or resection of an aber-
rant RHA is estimated at 4.0%. Eshuis et al36 reported that
accidental ligation or resection occurred mainly during bile
duct dissection. The most common course of an aberrant
RHA is posterior to the head of the pancreas, then passing
posteriorly and laterally to the main PV before reaching the
NAKATA et al.
F I G U R E 4   Blood flow under the (a)
celiac stenosis. (a) Contrast-­enhanced
multidetector CT shows celiac artery
stenosis due to the median arcuate ligament
compression (arrow). CT, computed
tomography. (b) Collateral blood flow
GDA
in the presence of celiac artery stenosis.
The arrow shows retrograde blood supply
to the upper abdominal organs through
pancreaticoduodenal arcades and the dorsal
pancreatic artery. GDA, gastroduodenal
artery; DPA, dorsal pancreatic artery
PV
F I G U R E 5   Circumportal pancreas.
The portal vein (thin arrow) was surrounded
by the pancreatic parenchyma. The Wirsung
duct (thick arrow) runs behind the PV. PV,
portal vein
liver; this course places the aberrant RHA at risk of injury
during the dissection of the hepatoduodenal ligament. To
prevent accidental injury, the aberrant RHA should be first
identified and dissected from the hepatoduodenal ligament
and pancreas, to the extent possible, toward the origin of
the aberrant RHA, which is the SMA in most cases. If HA
resection is performed, it may lead to liver ischemia, ab-
scess, and bile leak, or to the formation of a pseudoaneu-
rysm. If the damaged aberrant RHA is an accessory RHA,
reconstruction would not be needed. However, if the injured
artery is a replaced RHA, it should be reconstructed or re-
paired, with a repair being more commonly selected.12,36
Eshuis et al36 reported on 13 cases of intended sacrifice or
accidental damage of an aberrant RHA and they showed two
related complications: one is delayed massive hemorrhage
and intra-­abdominal abscess. Although all five cases of acci-
dental injury were repaired, it was not clear from this report
if repair was attempted in cases of intended sacrifice of the
aberrant RHA. Therefore, it is difficult to identify the fre-
quency of complications related to sacrifice of a replaced
RHA. Even if the injured replaced RHA was repaired, there
is a risk for obstruction, pseudoaneurysm, and bile leak-
age, which can lead to ischemic injury; therefore, a care-
ful postoperative follow-­up is warranted. In their report on
patients who underwent preoperative embolization and PD,
|
     11
(b)
Stenosis
DPA
combined with resection of the replaced RHA, Okada et al40
did not identify any incidence of ischemic complications.
Preoperative embolization stimulates the development of
collateral arteries within the liver, which can prevent isch-
emic liver damage. Therefore, reconstruction might not be
needed when surgery is planned with preoperative prepa-
ration. Considering the results of perioperative outcomes,
postoperative and oncological outcomes do not appear to be
influenced by the presence of anatomical HA variation, pro-
vided that the aberrant RHA is identified preoperatively and
appropriately managed.
We reviewed variation in the anatomy of PV systems, with
most reports regarding the JVs. We identified several ana-
tomical classifications that are used, these being dependent
on the vessels being focused on during the PD procedure.
Nakamura et al49 and Ishikawa et al50 classified the relation-
ships between the FJV and the SMA. This classification is
important when dissecting the mesoduodenum as the J1V is
embedded in the mesoduodenum. In addition, as Ishikawa
et al50 and Kobayashi et al52 pointed out, the name of the
“first jejunal vein” is confusing as the first-­order JV is usu-
ally composed of multiple JVs; therefore, the FJV should be
named the first jejunal trunk. Nagakawa et al58 defined PDJV
branching from the dorsal side of the SMV and drainage of
the IPDVs. The PDJV indicates the first or second jejunal
 |
12      NAKATA et al.
trunk, which is case-­dependent. This definition seems to be
reasonable from a surgical and anatomical point of view.
CAS is sometimes observed on CT examination; however,
it is usually underestimated because of the asymptomatic na-
ture due to the well-­developed collateral arteries. Bull et al86
reported two cases of hepatic ischemia immediately after di-
vision of the gastroduodenal arcade, with the blood flow to
the liver recovered by dissecting fibrotic tissue around the
celiac artery. Therefore, CAS should be carefully identified
before surgery for patients requiring PD. CAS should be
considered when the gastroduodenal artery (GDA) or DPA
is larger than usual on preoperative imaging. A temporary
occlusion test of the GDA should be performed to identify
the adequacy of blood supply to the upper abdominal organs
by digital or visual identification of pulsation of the CHA
and the PHA. Doppler ultrasonography of the CHA and the
PHA can also be useful to evaluate the blood supply. Of note,
postoperative acute MALS may occur even in the absence of
MALS evidence on preoperative CT and a negative occlusion
clamping test during surgery.87-­89 Sanchez et al87 hypothe-
sized that lymphadenectomy of the celiac region or prolonged
back bend patient position may lead to a temporary MALS,
with exacerbation of a non-­significant CAS. Presence of a
circumportal pancreas might not be included in the anatom-
ical study of the pancreatic venous system due to its overall
low prevalence.
In this study, we reviewed the variations in surgical
anatomy, its importance for the PD procedure itself, and its
relationship with perioperative outcomes. Though not all
variations have been associated with perioperative results,
identification of these variations is definitely important for
the safety of patients undergoing PD. In addition, though
identifying all vessels before surgery might be difficult, it
would be important to know the type of anatomical variation
of vessels around the pancreas. Dissemination of this knowl-
edge would improve surgeons’ awareness of safe PD pro-
cedures. Although few reports have focused on MIPD, the
procedure itself is the same as open PD. In addition, small
vessels are more likely to be identified on MIPD owing to
the magnification effect in minimally invasive surgery. We
hope that this review will play a role in enhancing the safety
of PD.
COLLABORATORS
Study group of Precision Anatomy for Minimally Invasive
Hepato-­Biliary-­Pancreatic surgery (PAM-­HBP surgery):
Mohammed Abu Hilal, Brian K.P. Goh, Jin He, Goro
Honda, Jin-­ Young Jang, Chang Moo Kang, Michael L.
Kendrick, David A. Kooby, Rong Liu, Yoshiharu Nakamura,
Chinnusamy Palanivelu, Shailesh V. Shrikhande, Kyoichi
Takaori, Shin-­ E Wang, Anusak Yiengpruksawan, Yoo-­
Seok Yoon, Giammauro Berardi, Shingo Kozono, Yusuke
Watanabe, Giovanni Maria Garbarino, Yoshiya Ishikawa,
Aya Maekawa, Yoshiki Murase, Giuseppe Zimmitti,
Masakazu Yamamoto.
ACKNOWLEDGMENTS
This review was performed in preparation for the
“Precision Anatomy for Minimally Invasive Hepato-­
Biliary-­Pancreatic Surgery: Expert Consensus Meeting,”
which will be held during the 32nd annual meeting of the
Japanese Society of Hepato-­Biliary-­Pancreatic Surgery in
Tokyo in February 2021. Details on the design of this pro-
ject were decided by Masafumi Nakamura, Takao Ohtsuka,
Yuichi Nagakawa, Daisuke Ban, Kohei Nakata, Hitoe
Nishino, Akihiko Tsuchida, and Itaru Endo. Hitoe Nishino
contributed to the progress of this project as the secre-
tariat. The literature was searched and reviewed by Ryota
Higuchi, Naoki Ikenaga, and Kohei Nakata. The draft of
the manuscript was critiqued by Masafumi Nakamura,
Kohei Nakata, Takao Ohtsuka, Yuichi Nagakawa, Daisuke
Ban, Horacio J. Asbun, Ugo Boggi, Chung-­Ngai Tang, and
Christopher L. Wolfgang. All authors approved the final
manuscript.
CONFLICT OF INTEREST
None declared.
ORCID
Yuichi Nagakawa  https://orcid.org/0000-0003-1169-8160
Hitoe Nishino  https://orcid.org/0000-0003-3785-7502
Itaru Endo  https://orcid.org/0000-0001-5520-8114
Masafumi Nakamura  https://orcid.
org/0000-0002-6196-8643
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SUPPORTING INFORMATION
Additional supporting information may be found online in
the Supporting Information section.
How to cite this article: Nakata K, Higuchi R,
Ikenaga N, et al. Precision anatomy for safe approach
to pancreatoduodenectomy for both open and
minimally invasive procedure: A systematic review.
J Hepatobiliary Pancreat Sci. 2021;00:1–­15. https://
doi.org/10.1002/jhbp.901