ms. ref. no.: aanat1426 title: variations in the anatomy ... · artery (celiacomesenteric trunk),...

Ms. Ref. No.: AANAT1426 Title: VARIATIONS IN THE ANATOMY OF THE CELIAC TRUNK: A

SYSTEMATIC REVIEW AND CLINICAL IMPLICATIONS Annals of Anatomy

Received Apr 30, 2013

Decision May 22, 2013

Revision received May 24, 2013

Accepted Jun 15, 2013

Decision letter

Dear Dr. Panagouli,

The reviewers have commented on your above paper. They indicated that it is not

acceptable for publication in its present form.

However, if you feel that you can suitably address the reviewers' comments (included

below), I invite you to revise and resubmit your manuscript.

The comments provided by the reviewers very often considerably help to improve and

strengthen a paper. In addition, the authors' response letter accompanying a revised

version often contains important information which may be regarded as an added

value to the final version of the manuscript. Therefore, Editors decided that the non-

confidential comments of the reviewers and the non-confidential authors' responses

will be published as online supplementary material together with the final version of

an eventually accepted article.

Please carefully address the issues raised in the comments.

If you are submitting a revised manuscript, please also:

a) outline each change made (point by point) as raised in the reviewer comments

AND/OR

b) provide a suitable rebuttal to each reviewer comment not addressed

I look forward to receiving your revised manuscript.

Yours sincerely,

Friedrich Paulsen

Editor-in-Chief

Annals of Anatomy

Reviewers' comments: Reviewer #1: In their Minireview article entitled: VARIATIONS IN THE

ANATOMY OF THE CELIAC TRUNK: A SYSTEMATIC REVIEW AND

CLINICAL IMPLICATIONS, Panagouli et al. systematically investigate anatomical

variations of the branching of the celiac trunk in the existing literature. Additionally,

the authors provide a new classification of anatomical variations of the celiac trunk

and show ethnical variations in the incidence of CT variations.

In my opinion the article is of good quality and describes existing literature very

exactly. However, in my opinion some major issues have to be addressed.

Major comments:

1) According to Table 1, already several classifications of variations of the CT exist.

Please provide information which aspects to existing classifications are added by the

new classification.

2) Please check ethnical descriptions for political correctness. For black people the

description "negro, coloured and black" is used. Furthermore, in my opinion it is not

correct to compare Korean (country), Caucasian (many countries) and Negro

(describing the colour of the skin) (see Table 8). I think race variations have to be

carried out very carefully in such an article or -if not possible- cut out.

3) In my opinion, the number of figures and tables exceeds the format of a minireview.

I would recommend to cut number of figures and tables down. E.g. table 2:

information is already provided in the text of the manuscript. CT variations are

displayed in table 3 and 8.

Minor comments:

1) The signs in the figures are inconsistent. Sometimes there is a number, sometimes

abbreviations with arrows. Please use signs consistent. ----------------------------------------------------------------------------------------------------------------------------

Authors response letter Revision

VARIATIONS IN THE ANATOMY OF THE CELIAC TRUNK: A

SYSTEMATIC REVIEW AND CLINICAL IMPLICATIONS

Eleni Panagouli MD, PhD, Dionysios Venieratos MD, PhD, Associate Professor of

Anatomy, Evangelos Lolis MD, PhD, Panagiotis Skandalakis, MD, PhD, Professor of

Anatomy.

Department of Anatomy, Medical School, University of Athens, Greece, 116 27.

Running title: Review of the variations of celiac trunk

Correspondence to: Eleni Panagouli, Department of Anatomy, Medical School,

University of Athens, Mikras Asias str. 75, 115 27 Athens, Greece.

Tel: 0030 2107462394, fax: 0030 2107462398, e-mail: [email protected]

Authors’ Contributions

E.P. performed the bibliographic search and statistical analysis and participated in

the design of the study. The documentation and comparisons were carried out by E.P.

and E.L. S.P. participated in the design and coordination of the study. D.V. conceived

of the study, elaborated the manuscript in its final form and had the general

supervision of the whole work. All authors read and approved the final manuscript.

ABSTRACT

The normal pattern of the celiac trunk (CT) implies its bifurcation to three branches,

the common hepatic, the splenic and the left gastric artery. According to the available

literature the CT presents several anatomical variations. The purpose of our study is to

investigate the different types of these variations, the correspondent incidences and

the probable influence of genetical factors, as they are presented in the existing

literature. Four databases were searched for eligible articles for the period up to

January 2013 and a total of 36 studies were collected. The CT was trifurcated into the

three basic branches in the 89.42% (10906/12196) of the cases. Bifurcation of the CT

occurred in the 7.40 % of the pooled samples (903/12196). Absence of the CT was the

rarest variation with a percentage of 0.38% (46/12196), hepatosplenomesenteric trunk

was found in 49 out of the 12196 cases (0.40%) and the celiacomesenteric trunk

presented an incidence of 0.76% (93/12196). Other variations of the CT were detected

in the 1.64% of the pooled cases (199/12196). The 14.9% of the cases in the cadaveric

series (489/3278 specimens), the 10.5% in the imaging series (675/6501 specimens)

and the 4.6% (104/2261) in the liver transplantation series presented variations. These

differences are statistically significant (p<0.001). Japanese and Korean population

presented more variations of the CT than Caucasian ones (p<0.05 and p<0.001).

NegroNegro, coloured and black population presented more variations of the CT than

Indian ones (p>0.05).

Using those data, a novel classification of CT variations is proposed.

Keywords: tripod; bifurcation; additional branches; absence; celiacomesenteric trunk;

classification.

INTRODUCTION

The celiac artery or (more commonly referred as) celiac trunk (CT), constitutes a

surgically significant splanchnic branch of the abdominal aorta and thus it has been

studied thoroughly. Knowledge of the variable anatomy of the CT is clinically

Kommentar [t1]: Changed as it was suggested by the Reviewer.

important in the treatment of abdominal aortic aneurysms, in liver, pancreatic and

oesophagogastric surgery, in organ retrievals and in liver transplantations.

The normal pattern of the CT seems to be the so called “tripus Halleri”, namely its

bifurcation to three branches, the common hepatic, the splenic and the left gastric

artery. Higashi et al. (2009) introduced a classification of the possible forms of the

tripus Hallleri in four types: In Type I the CT ended divided into two branches

(splenic and common hepatic arteries), while the left gastric artery emerged earlier

along the trunk. In Type II the three arteries had a common origin while in the two

other types the first branch was the common hepatic artery and the splenic artery

respectively (Table 1). A detailed description of these forms has been made in a

previous paper (Venieratos et al., 2012).

Except the anomalies reported on the normal pattern (Lipshutz 1917; Petrella et al.,

2007; Iezzi et al., 2008; Higashi et al., 2009; Mburu et al., 2010), the CT presents

several anatomical variations such as the absence of one of its branches (bifurcation

or incomplete CT), additional branches, common origin with the superior mesenteric

artery (celiacomesenteric trunk), common origin with the superior and inferior

mesenteric artery (celiac-bimesenteric trunk) and total absence. There are several

reports and studies in the available literature describing and analysing the different

forms of the CT individually or in a sample of population, while there have been

numerous efforts of classification of its ramification types (Lipshutz in 1917; Adachi

in 1928; Morita in 1935; Michels in 1955, Table 1). Since each author proposes a

classification of his own findings, it is natural that However, none of them includes all

the until now observed variations.

The statistical significance of the discrepancies among the different studies on the

frequency of the anatomical variations of the CT is not widely known and it is

controversial whether their presence is dependent on ethnic and gender factors. On the

other hand the existence of diverse nomenclatures may be confusing and misleading.

Consequently, the need for an up-to-date systematic review is evident. Our study

has been designed to take into account the till now reports in the literature, in order to

investigate:

1. The different types of anatomical variations of the CT and the correspondent

incidences.

2. The overall probability of occurrence of any variation type in an extensive sample.

3. The probable influence of factors such as the gender, the race and the type of study.

Kommentar [t2]: This sentence is

changed to provide information which aspects to existing classifications are added

by our classification, as it was requested by

the Reviewer .

Additionally, based on the accrued results, an effort of a more widely and easily

used classification has been made.

MATERIAL AND METHODS

Four databases were searched for eligible articles for the period up to January 2013

(MEDLINE, SCOPUS, ISI web of knowledge, and PUBMED). No publication year

restrictions were imposed. The following terms and combination of them were used:

“celiac artery”, “celiac trunk”, “coeliac”, and “celiac”. The references of all the

articles which were considered relevant were checked to find any studies missed.

Additionally, five anatomical textbooks (Adachi, Michels, Lippert and Pabst, Gray’s

Anatomy, and Bergman) were looked through for any kind of documentation

concerning the CT.

The following criteria for inclusion of data in the study were used:

1) The study must be an original research article or a review examining the

anatomical variations of the CT in a population sample (cadaveric or clinical study).

Studies which were conducted during liver transplantations and provided detailed data

about the variations of the CT were also included. Single case reports and studies with

populations overlapping with other ones were excluded.

2) Only studies concerning adult humans were selected.

3) There were imposed no limitations concerning race, age, sex, journal, language

or publication year. No efforts were made to search unpublished material.

For each study considered as eligible the following parameters were investigated:

year of publication, type of the study (cadaveric, clinical, imaging), demographic

characteristics of the population being studied (gender and race), frequencies and

classification of the reported variations.

The collected data were categorized according to the below mentioned provisional

groups, in order to render the various data as comparable as possible and to avoid

confusion arising from differences in nomenclature:

Group 1: As complete or trifurcated CT (fig. 1) was classified every celiac artery

which gave rise to the three normal branches (common hepatic, left gastric and

splenic artery), regardless of having a common origin (true tripod -“tripus Halleri”) or

one of them emerging first (false tripod; Type I of Lipshutz’s; Adachi’s, Morita’s and

Michel’s classification; all types of Higashi classification, Table 1). This type

constitutes the classical pattern of the CT. The rest of the groups correspond to

variations of the artery.

Group 2: As incomplete or bifurcated CT was classified every celiac artery which

had only two of the three normal branches, the third being a branch of another artery

(Types II, III and IV of Lipshutz’s classification; Types II, V and VI of Adachi’s

classification; Types II, III and IV of Morita’s classification; Types II, IV and V of

Michel’s classification and every other form of bifurcation, Table 1). The different

types of bifurcation were also studied individually, when available data existed.

Group 3: As absence of the CT was classified every case in which the CT is

missing, while its branches rise independently from the abdominal aorta or other

arteries (Type V of Morita’s classification, Table 1).

Group 4: As celiacomesenteric trunk (fig. 2) was classified every case of common

origin of the CT and the superior mesenteric artery (Type IV of Adachi’s

classification; Type VI of Michel’s classification, Table 1).

Group 5: As hepatosplenomesenteric trunk (fig. 3) was classified the common

origin of common hepatic, splenic and superior mesenteric arteries while the left

gastric artery rose alone from the abdominal aorta (Type III of Adachi’s classification,

and Type III of Michel’s classification, Table 1)

Group 6: As other variations of the CT were classified every other form of the CT

which could not be classified into the existed classifications. Examples of these

anomalies could be the origin of more than three branches of the CT (additional

branches, fig.4), common origin of the celiac, superior and inferior mesenteric artery

(celiac-bimesenteric trunk, fig. 5) and every case which was reported in the articles as

‘other’. All these variations were studied as a group and each one individually.

Additionally, an effort was made to categorize the collected data according to the

race and gender of the specimens and the type of study.

After the evaluation of data, the results were recorded in the form of Tables. The

total number as well as the frequency and percentage of each category were calculated.

For comparing continuous variables, the t-test was applied and for nominal variables

the x2 test. All the statistical analysis was done by SPSS 15.0.

RESULTS

Our search retrieved 136 titles which met the search criteria. From them, 48 were

case reports, 33 did not have available abstract or full text and 18 were irrelevant. Out

Kommentar [t3]: Figure 2 is removed

according to the recommendations of the

Reviewer to cut down the number of figures.

Kommentar [t4]: Figure 3 is removed according to the recommendations of the






of the 37 studies left, two articles (Kaneko et al., 1991; Bordei et al. 2002) were

excluded because they were conducted in fetuses. Moreover, five articles (Troupis et

al. 2008; Malnar et al. 2009; Higashi et al. 2010; Kornafel et al. 2010; Bharath et al.,

2011) could not be included due to missing information, one more (Shoumura et al.

1991) because the research was performed on overlapping populations with another

eligible study (Chen et al. 2009) and one review article (Yi et al. 2008) was also

excluded, as it was actually a case report.

Additionally, after an overview of the available books, two eligible studies were

discovered (Adachi 1928; Michels 1955), while the classical reference book of

Bergman et al. (2006) contained citations of six eligible studies of the CT (Rossi and

Cavi 1904; Leriche and Villemin, 1907; Descomps 1910; Picquand 1910; Rio de

Branco 1912; Poynter 1922). Unfortunately, no eligible studies (due to absence of

abstract or full text) or citations were retrieved by the classical book of Lippert and

Pabst.

Thus, a total of 36 studies (fully meeting the inclusion criteria) were collected and

were taken into consideration in the final analysis. Among them, 25 were performed

in cadaveric material (Rossi and Cavi 1904; Leriche and Villemin, 1907; Descomps

1910; Picquand 1910; Rio de Branco 1912; Eaton 1917; Lipshutz 1917; Poynter 1922;

Adachi 1928; Tsukamoto 1929; Michels, 1946; Imakoshi 1949; Michels 1955;

Kozhevnikova 1977; Katsume et al. 1978; Nelson et al. 1988; Shvedavchenko et al.

2001; Saeed et al. 2003; Petrella et al. 2007; Chen et al. 2009; Silveira et al. 2009;

Chitra 2010; Mburu et al. 2010; Prakash et al. 2012; Venieratos et al. 2012) and

represented a total of 3278 specimens, 7 were imaging studies in living patients either

by CT or angiography (Koops et al. 2004; Matsuki et al. 2004; Ferrari et al. 2007;

Iezzi et al. 2008; Song et al. 2010; Ugurel et al. 2010; Natsume et al., 2011) and

represented a total of 6501 specimens, three were performed during liver

transplantations (Hiatt et al., 1994; Jones and Hardy, 2001; López-Andújar et al.,

2007), with a total of 2261 specimens and one was a combination of arteriography,

corrosion and dissection (Vandamme and Bonte 1985), with a total of 156 specimens.

The classification of the eligible articles according to the type of the study is shown in

Table 2.

In most of the studies the race or gender of the specimens was not clearly defined,

as it is presented in Table 23. Ιn the majority of the cases the ethnicity was assumed,

based on the country or university were the study was conducted (if mentioned),

Kommentar [t7]: Table 2 is removed


Reviewer to cut down the number of tables.

Kommentar [t8]: Table 3 is renamed as Table 2 is removed.

allowing thus the processing of seeking correlations. The comparisons made are based

on different populations. On the other hand, even when the number of males and

females was reported, the corresponding incidences according to gender were rarely

mentioned. Particularly, only 3 studies (Lipshutz, 1917; Silveira et al., 2009;

Venieratos et al., 2011) contained information about the distribution of the CT forms

in males and females. Consequently, correlations and comparisons based on the

gender were not feasible due to deficient records.

After the final evaluation of the data and pooling the results of the eligible studies, a

total of 12196 specimens arose. The CT was found to be complete and trifurcated into

the three basic branches (common hepatic, splenic and left gastric artery, Group 1) in

the 89.42% (10906/12196) of the cases (Table 4a3a). The rest of the cases, namely the

10.6% (1290/12196) presented variations of the CT (Groups 2-6).

More specifically, incomplete CT (Group 2) occurred in 903 cases, representing the

7.40 % of the pooled samples (Table 4a3a). Absence of the CT (Group 3) was the

rarest variation (among the 5 groups) with a percentage of 0.38% (46/12196 - Table

4a3a), while hepatosplenomesenteric trunk (Group 5) seemed to be less rare as it was

observed in 49 out of the 12196 cases (0.40% - Table 4b3b). The celiacomesenteric

trunk (Group 4) was more frequent, with an incidence of 0.76% (93/12196 - Table

4b3b).

Other variations (Group 6) of the CT were detected in the 1.64% of the pooled

cases (199/12196 - Table 4b3b) and they were reported in the 13 out of the 36 studies

(Table 5). These variations included additional branches of the CT ([129 cases,

1.06%; Michels, 1946 (4/50); Nelson et al., 1988 (15/50); Shvedavchenko et al., 2001

(40/120); Saeed et al., 2003 (4/52); Koops et al., 2004 (7/604); Petrella et al., 2007

(9/89); Silveira et al., 2009 (1/21); Chitra, 2010 (20/50); Mburu et al., 2010 (25/123);

Venieratos et al., 2012 (4/77) ), ], splenogastromesenteric trunk ([6 cases, 0.05%;

Chen et al., 2009 (2/974); Song et al., 2010 (3/5002); Natsume et al., 2011 (1/175), )],

one case of splenogastric trunk giving rise to a common inferior phrenic trunk

([0.008%; Saeed et al., 2003, (1/52), )], as well as variations mentioned as

“ambiguous anatomy” ([63 cases, 0.52%; Song et al., 2010, 63/5002). ]. These cases

were reported by the authors (Song et al., 2010) as ambiguous anatomy and included

specimens where the common hepatic artery was absent (n=55) or its origin could not

be determined because of persistent anastomotic channels ( n = 8).

Kommentar [t9]: This sentence is

added in order to clarify the comparisons

between different populations.

Kommentar [t10]: Table 4 is renamed as Table 2 is removed.

Kommentar [t11]: Table 5 is removed according to the recommendations of the


Kommentar [t12]: Table 5 is removed



Because of that the literature included in

this table is added in the text.

Kommentar [t13]: This sentence is added because table 5were it was included

is deleted.

Concerning the cases belonging to Group 2 (bifurcation of the CT), exact

information about the different forms of bifurcation was recorded in the 19 out of the

36 articles, corresponding to a total number of 9829 specimens. The observed patterns

of bifurcation and their corresponding incidences are presented in Table 64 and

figure 26. The most commonly discovered types were the following: hepatosplenic

trunk with the left gastric artery arising independently from the abdominal aorta

(328/9829, 3.34%), combination of splenogastric and hepatomesenteric trunk

(186/9829 1.90%) and splenogastric trunk with the common hepatic artery arising

from the superior mesenteric artery (111/9829, 1.13%).

The distribution of the variations of the CT according to the type of the study is

presented in Table 7Table 5. The 14.9% of the cases in the cadaveric series (489/3278

specimens), the 10.5% in the imaging series (675/6501 specimens) and the 4.6%

(104/2261) in the liver transplantation series presented variations (Groups 2-6). The

difference between the incidence of the variations among the three types of studies

was found to be significant (p<0.001). Arteriography, corrosion and dissection studies

were not included, as only one study of 156 specimens was retrieved (Vandamme and

Bonte, 1985).

The ethnicity and origin of the cadavers was assumed in 23 studies (10462). Most of

the specimens were of Korean origin (5002, Song et al., 2010), while 3480 were of

Caucasian origin (white race without explicitly defined ethnicity), 1749 were

Japanese, 100 were Indian and 131 were categorized as Negro, coloured and black

(without explicitly defined ethnicity as well)Negroes. The distribution of the

variations of the CT are shown in Table 86. The CT presented more variations at the

Japanese series than at the Caucasian ones and a statistical significant difference was

determined (p<0.05). Koreans also presented more variations than Caucasians

(p<0.001). No statistically significant difference was found between Korean and

Japanese series (p>0.05), as expected since they belong to the same racial minority..

Series of negro, coloured and blackNegro and Indian origin comprised a much less

number of specimens. Thus, we decided that a comparison between these two series

(and not between them and other, much more large series) was feasible. Such a

comparison showed that the Indian series had a lower incidence of variations but this

difference was not significant (p>0.05).

DISCUSSION

Kommentar [t14]: Table 6 is renamed as Table 2 and 5 are removed.

Kommentar [t15]: Figure 6 is renamed

as figures 2-5 are removed.


Kommentar [t17]: Changed as it was

suggested by the Reviewer. The phrase “negro” is accordingly changed in Table 8.

In Table 2 the races remained as they were

referred by the authors of each study.

Kommentar [t18]: Added in order to

clarify the comparisons between different

populations.

Kommentar [t19]: Table 8 is renamed

as Table 2 and 5 are removed.

Kommentar [t20]: Added in order to

clarify the comparisons between different

populations.

Our study composes a systematic review and looks into the anatomical variations of

the CT as they are recorded in 36 anatomical studies. A total number of 12196 cases

occurred, much larger than the till now revised (Table 97). The results showed that the

CT follows the described as normal pattern and trifurcates in the classical branches

(common hepatic, splenic and left gastric artery) in the 89.42 % (10906/12196) of the

cases. This percentage reaches 85.1% in the cadaveric studies (2741/3278), 89.6%

(5826/6501) in the imaging studies and 95.4% (2157/2261) in the liver transplantation

studies.

The CT, according to our study is expected to present variations (Groups 2-6) in

the 10.6% of the population (1290/12196 specimens). More specifically, variations

occurred in the in the 14.9% (489/3278) in the cadaveric series, in the 10.5% in the

imaging series (675/6501) and in the 4.6% (104/2261) in the liver transplantation

series. Although the number of imaging studies (7) was smaller than that of cadaveric

ones (23), the number of specimens was bigger (6501 and 3278 specimens

respectively). On the other hand, liver transplantation studies might be only 3, but

they were represented by a sufficient number of specimens (2261). Nevertheless, the

variations were found to be more frequent in the cadaveric series and this difference

was statistically significant (p<0.001). It should also be point out that the range of

variations reported in cadaveric studies (5.8% - 46%, Table 7Table 5), it is wider than

that of the imaging (4.1%-15%, Table 7Table 5) or liver transplantation studies (1.7%

-6.6%, Table 7Table 5). Anatomical studies, when made correctly, must reveal all

existing variations, as the aim of any anatomist is exactly this. On the other hand, in

imaging studies, some small arteries may not appear clearly enough to be recorded

and in addition some overlaying vessels may erroneously be considered as one vessel,

whilst artifacts are rather common in such images. Finally, in surgical studies

concerning mainly liver transplantation, the attention of the surgeon is focused to the

surgical field and the operation itself, whereby some variation outside this field may

pass unobserved. For these reasons, we disagree with Matusz et al. (2012) and

comment that any differences concerning such a rare variation as the absence of CT

must be purely fortuitous.

The different incidences of the recorded anomalies among the different studies,

indicate that there is a genetic factor influencing the existence of the CT variations.

The impact of gender was not possible to be assessed, due to the lack of sufficient

information contained in the available data. Most of the studies did not refer to the

Kommentar [t21]: Table 9 is renamed

as Table 2 and 5 are removed.

distribution of the variations according to the gender. Eaton (1917) and Chen et al.

(2009) reported that there were not found any differences between male and females

in their series (206 and 974 specimens respectively) which was also the case in our

previous study (Venieratos et al. 2012). The ethnicity and origin of the specimens

could only be assumed in most of the studies (23/36). Japanese and Korean population

(which are considered as belonging to the same racial minority) presented more

variations of the CT than Caucasian ones and the difference was statistically

significant (p<0.05 and p<0.001). In a similar manner, NegroNegro, coloured and

black population presented more variations of the CT than Indian ones (p>0.05).

Consequently, ethnicity and racial differences seem to affect the existence or not of

variations of the CT. Nevertheless, no difference between White and “Coloured”

subpopulations was observed in the study of Eaton (1917).

The most common variation of the CT included the bifurcation of the artery in two

branches instead of three (categorized as Group 2, 7.40%, 903/12196). Several types

of bifurcation were recorded, concerning mostly the origin of the third branch. These

types are described as follows, in order of occurrence: hepatosplenic trunk with the

left gastric artery arising independently from the abdominal aorta (328/9829, 3.34%),

combination of splenogastric and hepatomesenteric trunk (186/9829 1.90%),

splenogastric trunk with the common hepatic artery arising from the superior

mesenteric artery (111/9829, 1.13%), splenogastric trunk with the common hepatic

artery arising independently from the abdominal aorta (23/9829, 0.23%),

hepatogastric trunk together with splenomesenteric trunk (9/9829, 0.09%),

hepatogastric trunk with the splenic artery arising independently from the abdominal

aorta (8/9829, 0.08%), hepatogastric trunk with the splenic artery arising

independently from the superior mesenteric artery (3/9829, 0.03%), hepatosplenic

trunk with no normal left gastric artery (1/9829, 0.01%) and hepatosplenic trunk

combined with gastromesenteric trunk (1/9829, 0.01%).

The rest of the observed anomalies of the CT were found to be rarer than its

bifurcation. The celiacomesenteric trunk and the hepatosplenomesenteric trunk

(Group 4, 5) occurred with an incidence of 0.76% (93/12196) and 0.40% (49/12196)

respectively, followed by the complete absence of the CT (0.38%, 46/12196, Group

3).

Variations of the CT which could not be classified into the existing classifications

were categorized in the present study as “other variations of the CT” (Group 6,

Kommentar [t22]: Added in order to clarify the comparisons between different

populations.

1.64 %, 199/12196). The most common of them was the additional branches of the

CT (1.06%, 129/12196). Extremely rare was the presence of a splenogastromesenteric

trunk (0.05%, 6/12196), while a single case of a splenogastric trunk giving rise to a

common inferior phrenic trunk was recorded (0.008%). Additionally, Song et al.

(2010) reported variations of the CT which were named as “ambiguous anatomy”

(0.52%, 63/12196). According to them, these cases included specimens where the

common hepatic artery was absent (n=55) or its origin could not be determined

because of persistent anastomotic channels (n = 8).

Based on the above mentioned findings which occurred after researching the

available literature we propose a new classification which includes all the possible

forms of the CT (Table 108).

The classification is composed of 10 types. These Types are created by

modification of the provisional set of groups (Groups 1-6) which were used in the

results section for comparison of the various data. The numbering of these 10 Types

was not arbitrary, but purposefully selected to be in accordance to the incidence of the

corresponding variation. Thus, all these Types were categorized with a descending

incidence.

In Type I (fairly identical with Group 1) belongs the normal form of the CT,

namely its trifurcation. The forms of this type are based on the classification of

Higashi et al. (2009). The rest of the types (Types II-X) correspond to variations of

the CT, as they were accrued from our search in the available literature (Groups 2-6).

Type II contains the different forms of bifurcation of the CT, as they were recorded in

Group 2. Each of the Types III, V, VIII and IX corresponds to the variations of the

CT which were categorized as “other variations” (Group 6). Type V includes the

cases described as “ambiguous anatomy” and is named as “Variations in the origin of

the common hepatic artery” in order to avoid confusion. The cases of

celiacomesenteric trunk constitutes Type IV (Group 4), those of

hepatosplenomesenteric trunk (Group 5) Type VI and those of absence of the CT

(Group 3) Type VII. Except the variations described in the eligible studies, we

considered useful to add another variation of the CT, the celiac-bimesenteric trunk,

namely common origin of the celiac, superior and inferior mesenteric artery, as Type

X. Our research retrieved only one case report describing this anomaly (Nonent et al.,

2001).


It should be pointed out that none of the already existed classifications of the CT

contain all the recorded in the literature variations. For example, the different forms of

trifurcation of the CT are presented only in the classification of Higashi et al. (2009),

where the other variations of the CT are missing (Table 1). Additionally, only Morita

(1935) refers to the absence of the CT in his classification (Table 1). All the different

types of bifurcation and rare variations such as additional branches, variations in the

origin of the common hepatic artery, splenogastromesenteric trunk, splenogastric

trunk giving rise to a common inferior phrenic trunk and celiac-bimesenteric trunk

which are included in our classification are missing from the previous ones. The

purpose of our classification was to respond to this gap and additionally to introduce

an easy and clarified nomenclature.

The abdominal aorta arises in the embryo from the two dorsal aortae, which fuse to

form the descending aorta, at the end of the first month of embryonic life. Each

primitive dorsal aorta gives rise to several branches, such as the lateral and ventral

splanchnic arteries. As the viscera which were supplied from the above mentioned

arteries, descend into the abdomen, the origin of these arteries moves too (Standring

et al., 2008). According to Tandler (1904) the multiple anatomical variations of the

CT might be a result of the unusual regression or persistence of the primitive

embryonic arterial system (primitive splachnic arteries).

The knowledge of the anatomy of the celiac artery and its branching pattern

(including variations) is important for a number of current medical procedures of

clinical interest, as in the interpretation of CT of MR images (Yi et al. 2008; Chen et

al. 2009). The new technology in imaging modalities results in detailed pictures of the

normal or variant pattern of celiac trunk and its branches.

Interventional radiologists should be aware of the position of the CT as the

vertebral level could serve as a landmark for the localization of its orifice, in cases

where a catheter is to be inserted into it. For similar reasons, they should also be

aware of the celiac trunk’s branching pattern and its eventual variations when

performing a diagnostic or therapeutic angiography.

Investigation of upper gastrointestinal bleeding requires CT catheterization and

subsequent catheterization of left gastric, common hepatic and splenic artery.

Embolization is an option when active bleeding is noticed. In cases of

pseudoaneurysms after liver trauma, selective embolization is the treatment of choice

and requires celiac trunk-hepatic artery catheterization.

Kommentar [t24]: These sentences are

added to provide information which aspects to existing classifications are added by our

classification, as it was requested by the

Reviewer .

Pseudoaneurysms of CT branches, mainly hepatic, gastroduodenal and splenic

arteries may complicate several rather severe clinical circumstances including:

pancreatitis; pancreatic leak following pancreatojejunostomy or pancreatogastrostomy

after a pancreatoduodenectomy; leak from the pancreatic stump after a distal

pancreatectomy. These pseudoaneurysms can also be treated by selective

embolization. Arterial variations or the CT’s branching pattern could create

unexpected difficulties and could constitute misleading factors during the procedure.

Finally, transarterial hepatic artery chemoembolization is a useful treatment option in

cases of hepatocellular cancer and the origin and course of the hepatic artery should

be known in advance.

Transplant surgeons are often dealing with the arteries branching from CT and they

should be aware of the position, the course and the variations of these vessels (Yi et al.

2008). Complete dissection of proper and common hepatic artery takes place during

liver transplantation. In organ retrievals, the retrieving surgeon should be skilled

enough and extremely careful in order to dissect, preserve and not to damage proper

and common hepatic artery and the CT itself. Especially during the cold phase of

dissection the danger of damaging the vessels is higher. If there are arterial anomalies,

the surgeon may have to reconstruct the arteries supplying the donor liver before the

implantation. In pancreas retrievals, the splenic, the gastroduodenal and the superior

mesenteric arteries must be retrieved with the pancreas as they provide its blood

supply.

In hepatobiliary and pancreatic surgery the surgeon should know the detailed

anatomy of the CT branches in order to dissect them during liver or pancreas

resections and any variation could result in vascular damage complicating the

operation and patient’s postoperative course (Yi et al. 2008; Chen et al. 2009). In

addition, total gastrectomy and esophagogastic resections require ligation of the left

gastric vessels in their origin.

Any lymph node dissection for malignant esophageal, gastric, hepatobiliary or

pancreatic cancer requires detailed knowledge of the vascular anatomy of the area and

possible variations in order to be performed.

In vascular surgery, repair of thoracoabdominal aneurysms, either open or

endovascular with stent prosthesis, must take into consideration the anatomy of the

CT. Using both ways of repair, blood flow through the CT must be maintained. In

open repair, CT might be cannulated, connected to extracorporeal circulation device

and then reimplanted in the graft. On the other hand, the design of a vascular

endoprosthesis for endovascular repair of a thoracoabdominal aneurism must take into

account the position of the CT. Any variations regarding branches of the CT that

originate directly from the aorta or a common trunk with the SMA could complicate

the procedures.

ACKNOWLEDGEMENTS

The authors wish to thank Mrs. Vasiliki Bitsika who helped at the development of

the figures.

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Figure legends

Figure 1: Complete or trifurcated celiac trunk (CT) (Group 1).

True tripod: common hepatic (1), splenic (2) and left gastric artery (3) have a

common origin. False tripod: one of the three branches emerge first (here the left

gastric artery (3)).

SMA: superior mesenteric artery, AA: abdominal aorta.

Figure 2: Celiacomesenteric trunk (Group 4): common origin of the celiac trunk

(CT) and the superior mesenteric artery (SMA).

1: common hepatic artery, 2: splenic artery, 3: left gastric artery, AA: abdominal

aorta.

Figure 3: Hepatosplenomesenteric trunk (Group 5): common origin of common

hepatic (1), splenic (2) and superior mesenteric arteries (SMA) while the left gastric

artery (3) rose alone from the abdominal aorta (AA).

Kommentar [t25]: The signs in the figures are changed, according to the

comments of the Reviewer.

Figure 4: Additional branches of the celiac trunk (CT).

1: common hepatic artery, 2: splenic artery, 3: left gastric artery, 4: additional branch,

AA: abdominal aorta.

Figure 5: celiac-bimesenteric trunk: common origin of the celiac (CT), superior

(SMA) and inferior mesenteric artery (IMA).

1: common hepatic artery, 2: splenic artery, 3: left gastric artery, SMA: superior

mesenteric artery, AA: abdominal aorta.

Figure 26: Different types of bifurcation of the celiac trunk (Group 2).

1: common hepatic artery, 2: splenic artery, 3: left gastric artery, SMA: superior

mesenteric artery, AA: abdominal aorta, Hs: hepatosplenic trunk, LGA: left gastric

artery, Gm: gastromesenteric trunk, Sg: splenogastric trunk, CHA: common hepatic

artery, Hm: hepatomesenteric trunk, Hg: hepatogastric trunk, SA: splenic artery and

Sm: splenomesenteric trunk.

Kommentar [t26]: Figure legends of figures 2-5 are deleted as the corresponding

figures were removed according to the

recommendations of the Reviewer to cut down the number of figures.

Kommentar [t27]: Figure 6 is renamed

as figures 2-5 are removed.

ms. ref. no.: aanat1426 title: variations in the anatomy ... · artery (celiacomesenteric trunk),...

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