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J Vet Clin 28(5) : 526-529 (2011) 526 Incomplete Brachiocephalic Trunk in a Korean Water Deer Dong-Choon Ahn, Hyun-Jin Tae, Byung-Yong Park, Jeoung-Ha Sim*, Jong-Taek Kim** and In-Shik Kim 1 Korean Zoonoses Research Institute and College of Veterinary Medicine, Chonbuk National University, Jeonju, Chonbuk 560-756, Korea *Department of Nursing, Jesus University, Jeonju 560-714, Korea **College of Veterinary Medicine, Kangwon National University, Chuncheon, Gangwon 200-791, Korea (Accepted: Aug 22, 2011) Abstract : The brachiocephalic trunk (Bct) branches from the aortic arch (Aa) and consists, in ruminants, of the common trunk of the left subclavian artery (LSb), the bicarotid artery (Bc) or left and right common carotid artery (LCc and RCc), and the right subclavian artery (RSb). This pattern differs from the primitive mammalian Aa pattern due to the fact that the analogs of the LCc and LSb migrate cranially and merge with the common trunk of the RCc and RSb in the embryonic stage. A Bct having a septal remnant that consisted of the tunica media was observed in a female Korean water deer (Hydropotes inermis argyropus), which was deemed to have resulted from an incomplete merging of the vessel walls between a carnivoran-type Bct and an incomplete LSb. This is the first report of an abnormal Bct in a Korean water deer. Key words : brachiocephalic trunk, Korean water deer, septum. Introduction The brachiocephalic trunk (Bct) is the first vessel branching from the aortic arch. The branching pattern of the Bct varies in different mammalian species (3,10). In primates, rodents, and rabbits, the Bct is formed from the common trunk of the right common carotid artery (RCc) and the right subclavian artery (RSb), while the left common carotid artery (LCc) and the left subclavian artery (LSb) branch off individually from the aortic arch. This pattern is known as the ‘primitive mammalian pat- tern’ (12). Previously, several authors used the term ‘innomi- nate artery’ to designate the Bct in these mammals. In carnivores, the Bct ramifies the LCc first, and then divides into the RCc and RSb. In pigs, the Bct is divided into the RSb and the bicarotid artery (Bc) which is the common trunk of both common carotid arteries. In ruminants, the LSb is the first to branch from the Bct and is followed by the Bc and RSb. The Korean water deer (Hydroptes inermis argyropus) has a simi- lar pattern except that it lacks a branching Bc from the Bct (1). These differences are likely related to the migration of the LCc and LSb, and merger of these vessels with the Bct as the Aa descends below the thoracic aperture owing to the descent of the heart during the embryonic period (2,7,8,12). In order to final configuration of the branching pattern was formed in ruminants, modifications such as fusion are inevitable not only between the vessel walls of Bct and LCc, but also between the Bct and LSb (2,6). If these modifications do not develop nor- mally, abnormalities may result. We present the first report of an incomplete Bct with two lumina separated by a septum in a female Korean water deer. Case A female Korean water deer, weighing 16.4 kg and estimated to be about 31 months old based on a comparison between the eruption and abrasion of the teeth with the delivery season (4), was killed in a traffic accident in Kangwon prefecture. The structure of the thoracic organs, including the heart, was nor- mal. When the deer was dissected to harvest the arterial silicon cast, a Bct with two asymmetrical lumina formed by an abnor- mal septal structure was found. The vessel of the Bct was observed as a single trunk in appearance and its branching pat- tern was normal as previous report (1). The septum was sepa- rating the lumen of Bct from the Aa to the branching point of LSb. As the results, larger lumen continued into the lumina of LCc, RCc, and RSb, while smaller one for the LSb. Because this larger lumen cast was similar to the carnivoran Bct, the term ‘carnivoran-type Bct’ is used to designate the definitive but incomplete Bct in this report. In addition, the term ‘incom- plete LSb’ is also adopted to describe the smaller lumen cast. To histologically examine the vessel wall, the arterial wall was immersed in 10% neutral buffered formalin for 48 hours, embedded in paraffin, sectioned into 5-um-thick slices, and stained by hematoxylin and eosin. Morphological measure- ments were taken on the silicon cast using Vernier calipers and on the tissue slide under a microscope (Leica, DM 2500, Ger- many) equipped with an image analysis program (isolution, 1 Corresponding author. E-mail : [email protected]

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Page 1: Incomplete Brachiocephalic Trunk in a Korean Water Deer · female Korean water deer (Hydropotes inermis argyropus), which was deemed to have resulted from an incomplete merging of

J Vet Clin 28(5) : 526-529 (2011)

526

Incomplete Brachiocephalic Trunk in a Korean Water Deer

Dong-Choon Ahn, Hyun-Jin Tae, Byung-Yong Park, Jeoung-Ha Sim*, Jong-Taek Kim** and In-Shik Kim1

Korean Zoonoses Research Institute and College of Veterinary Medicine, Chonbuk National University,

Jeonju, Chonbuk 560-756, Korea

*Department of Nursing, Jesus University, Jeonju 560-714, Korea

**College of Veterinary Medicine, Kangwon National University, Chuncheon, Gangwon 200-791, Korea

(Accepted: Aug 22, 2011)

Abstract : The brachiocephalic trunk (Bct) branches from the aortic arch (Aa) and consists, in ruminants, of the commontrunk of the left subclavian artery (LSb), the bicarotid artery (Bc) or left and right common carotid artery (LCc andRCc), and the right subclavian artery (RSb). This pattern differs from the primitive mammalian Aa pattern due tothe fact that the analogs of the LCc and LSb migrate cranially and merge with the common trunk of the RCc andRSb in the embryonic stage. A Bct having a septal remnant that consisted of the tunica media was observed in afemale Korean water deer (Hydropotes inermis argyropus), which was deemed to have resulted from an incompletemerging of the vessel walls between a carnivoran-type Bct and an incomplete LSb. This is the first report of an abnormalBct in a Korean water deer.

Key words : brachiocephalic trunk, Korean water deer, septum.

Introduction

The brachiocephalic trunk (Bct) is the first vessel branching

from the aortic arch. The branching pattern of the Bct varies in

different mammalian species (3,10). In primates, rodents, and

rabbits, the Bct is formed from the common trunk of the right

common carotid artery (RCc) and the right subclavian artery

(RSb), while the left common carotid artery (LCc) and the left

subclavian artery (LSb) branch off individually from the aortic

arch. This pattern is known as the ‘primitive mammalian pat-

tern’ (12). Previously, several authors used the term ‘innomi-

nate artery’ to designate the Bct in these mammals. In

carnivores, the Bct ramifies the LCc first, and then divides into

the RCc and RSb. In pigs, the Bct is divided into the RSb and

the bicarotid artery (Bc) which is the common trunk of both

common carotid arteries. In ruminants, the LSb is the first to

branch from the Bct and is followed by the Bc and RSb. The

Korean water deer (Hydroptes inermis argyropus) has a simi-

lar pattern except that it lacks a branching Bc from the Bct (1).

These differences are likely related to the migration of the LCc

and LSb, and merger of these vessels with the Bct as the Aa

descends below the thoracic aperture owing to the descent of

the heart during the embryonic period (2,7,8,12). In order to

final configuration of the branching pattern was formed in

ruminants, modifications such as fusion are inevitable not only

between the vessel walls of Bct and LCc, but also between the

Bct and LSb (2,6). If these modifications do not develop nor-

mally, abnormalities may result.

We present the first report of an incomplete Bct with two

lumina separated by a septum in a female Korean water deer.

Case

A female Korean water deer, weighing 16.4 kg and estimated

to be about 31 months old based on a comparison between the

eruption and abrasion of the teeth with the delivery season (4),

was killed in a traffic accident in Kangwon prefecture. The

structure of the thoracic organs, including the heart, was nor-

mal. When the deer was dissected to harvest the arterial silicon

cast, a Bct with two asymmetrical lumina formed by an abnor-

mal septal structure was found. The vessel of the Bct was

observed as a single trunk in appearance and its branching pat-

tern was normal as previous report (1). The septum was sepa-

rating the lumen of Bct from the Aa to the branching point of

LSb. As the results, larger lumen continued into the lumina of

LCc, RCc, and RSb, while smaller one for the LSb. Because

this larger lumen cast was similar to the carnivoran Bct, the

term ‘carnivoran-type Bct’ is used to designate the definitive

but incomplete Bct in this report. In addition, the term ‘incom-

plete LSb’ is also adopted to describe the smaller lumen cast.

To histologically examine the vessel wall, the arterial wall was

immersed in 10% neutral buffered formalin for 48 hours,

embedded in paraffin, sectioned into 5-um-thick slices, and

stained by hematoxylin and eosin. Morphological measure-

ments were taken on the silicon cast using Vernier calipers and

on the tissue slide under a microscope (Leica, DM 2500, Ger-

many) equipped with an image analysis program (isolution,

1Corresponding author.E-mail : [email protected]

Page 2: Incomplete Brachiocephalic Trunk in a Korean Water Deer · female Korean water deer (Hydropotes inermis argyropus), which was deemed to have resulted from an incomplete merging of

Incomplete Brachiocephalic Trunk in a Korean Water Deer 527

Leica, Germany).

On the cast, the gap length and width due to the septal struc-

ture were 40.0 mm and 7.0 mm, respectively (Fig 1). The

lumina of the carnivoran-type Bct and incomplete LSb were not

round because of the septal gap. The lumen of the carnivoran-

type Bct at a distance of 1 cm from the Aa was 8.45 mm in

mediolateral diameter and 9.25 mm in ventrodorsal diameter,

while the incomplete LSb was 4.35 mm mediolaterally and

7.55 mm ventrodorsally. Based on measurements from the three

normal casts kept in our laboratory, the Bct length and diame-

ter from the Aa to the branching point of the LSb were

63.8 ± 3.5 mm and 9.9 ± 0.7 mm, respectively.

Upon examination of the tissue slide from the vessels, it was

found that the tunica adventitia and tunica media were present;

however, the tunica intima was lost. The thickness of the tunica

media from the lateral wall of the carnivoran-type Bct was

203.5 ± 9.7 µm, while the lateral wall of the incomplete LSb

was 141.5 ± 17.6 µm. The septal structure was observed as a

confluence of the two internal halves of the tunica media and its

thickness was 176.4 ± 14.3 µm, in which the thickness of the

carnivoran-type Bct side was 116.1 ± 10.1 µm and the incom-

plete LSb side was 60.3 ± 7.5 µm (Fig 2).

Discussion

The Aa and its branches originate from the aortic sac, pha-

ryngeal arch arteries, and seventh dorsal intersegmental arter-

ies. In ruminants and horses, the Bct is the only artery that

branches from the Aa and gives off first the LSb, then Bc and

RSb. The Korean water deer has a branching pattern in which

the LCc and RCc are separately originated from the Bct and not

formed with the Bc, which differs from other domestic rumi-

nants (1). There are four remodeling steps in the formation of

the final Aa and its branches in animals with only one branch of

the Bct from the Aa (12). In the first step, the primitive aortic

arch is formed and three vessels, the innominate artery, the

LCc, and the LSb, are given off from the aortic arch. Victums

(12) regard this as the ‘primitive mammalian pattern’. In this

step, the left seventh dorsal intersegmental artery becomes the

LSb and migrates cranially from a position caudal to the duc-

tus arteriosus. In the second step, as the heart moves to a cau-

dal position, the LCc moves cranially. The proximal end of the

LCc and the ‘innominate artery’ are then fused to form the car-

nivoran-type Bct, which is very short. In this step, the LSb also

originates from the primitive aortic arch and moves to the level

where the ductus arteriosus connects the pulmonary trunk to the

dorsal aorta. Therefore, the two vessels, the Bct and LSb, orig-

inate from the primitive aortic arch. In the third step, the car-

nivoran-type Bct is considerably elongated compared to the

preceding step and the Bc appears by fusion of the two com-

mon carotid arteries. The LSb migrates more cranially to the

Fig 2. The septal structure (S) consisted of confluence of internal

halves of tunica media from two arteries, carnivoran-type brachio-

cephalic trunk (Bct) and left subclavian artery (LSb). The septal

structure must be cut for harvesting the silicon cast. H & E stain.

Scale bar = 300 µm.

Fig 1. A casting of arteries having incompletely unified brachio-

cephalic trunk. The septal structure divided the lumen of brachio-

cephalic trunk from the aortic arch to the branching point of left

subclavian artery (arrow). Aa; aortic arch, Bct; brachiocephalic

trunk, LSb; left subclavian artery, LCc; left common carotid artery,

RCc; right common carotid artery, Hi; highest intercostal artery,

Ds; dorsal scapular artery, Dc; deep cervical artery, Ax; axillary

artery, Sc; superficial cervical artery, It; internal thoracic artery,

Dorsal View.

Page 3: Incomplete Brachiocephalic Trunk in a Korean Water Deer · female Korean water deer (Hydropotes inermis argyropus), which was deemed to have resulted from an incomplete merging of

528 Dong-Choon Ahn, Hyun-Jin Tae, Byung-Yong Park, Jeoung-Ha Sim, Jong-Taek Kim and In-Shik Kim

ductus arteriosus. In the final step, the proximal part of the LSb

joins to the carnivoran-type Bct, so only the Bct branches

from the aortic arch. The RSb is considerably shorter than in

the earlier stages and the length of the Bc and the Bct also

show individual variations. In mammals, the migration of these

vessels is thought to be caused by the descent of the heart

(2,7,8,12).

To form the final shape of the aortic arch and brachiocepha-

lic trunk in ruminants, the migration should be followed by

modification between the vessel walls of the Bct and LSb

(2,6,8,12). As the vessel wall structure is already formed, sev-

eral possibilities might be achievable for fusion. One is simply

transposition of one vessel onto the other artery. If transposi-

tion occurs, the length of the artery to be joined might be main-

tained, and the growth of the main vessel would be disturbed.

However, the length of the LSb in adult ruminants is very short

and the Bct is elongated after the embryonic period. Therefore,

this possibility can be eliminated. Another is fusion by apopto-

sis in the wall between the two vessels. Poelmann and his col-

leagues (9,11) reported that apoptosis of both the vessel wall

proper and the surrounding mesenchyme is an important mech-

anism in the breakdown of specific segments. If this does not

occur normally, abnormalities may result.

In this case, the tunica adventitia and the outer layer of the

tunica media were observed as individual streams, while the

inner layer of the tunica media of two vessels, the carnivoran-

type Bct and LSb, met and formed the septal structure. It might

be conjectured that modification, such as apoptosis, was incom-

pletely achieved in this area. Because the migration and merg-

ing should have occurred in the early embryonic period, the

actual fusion length of the wall may be shorter than expected.

However, the fact that the length of the septal structure was as

long as 40 mm suggests that normal modifications were not

complete and even the remnants had growth potential.

The length of the septal structure in this case is shorter than

that of normal Bct stalks from the Aa to the branching point of

the LSb. This might have been caused by an abnormal descent

of the heart; however, we observed that the location of the

heart, the branching pattern of the carnivoran-type Bct, and the

incomplete LSb were normal. In addition, the other thoracic

organs were normal. These results suggest that the possibility of

an abnormal descent of the heart is low.

The lateral wall of the tunica media in the carnivoran-type

Bct was thicker than that of the LSb. The ventrodorsal diame-

ter of the lumen of the carnivoran-type Bct in this case was

similar to that of a normal Bct; however, the mediolateral diam-

eter was smaller than normal. In addition, the cast of the incom-

plete LSb had a flatter surface and smaller diameter than that of

the carnivoran-type or normal Bct. These results are in contrast

with the comments suggested by Molin et al (9). They observed

that the vessels destined to disappear as a result of a high fre-

quency of apoptosis always have a slightly smaller diameter.

Our results suggest that modifications, such as apoptosis,

should have occurred where the walls met each other.

Histological analysis revealed a lack of the tunica intima and

cell configurations in the tunica media, which may be due to

the long time after death (at least 3 days) and high tempera-

tures that the specimen experienced for defrosting, casting, and

dissection.

To our knowledge this is the first case of an incomplete Bct

in the Korean water deer or any other ruminant.

Acknowledgment

We thank Ki-Soo Cheong in “Gangwon Veterinary Services”

for donation of the animals used in this study.

References

1. Ahn DC, Kim HC, Tae HJ, Kang HS, Kim NS, Park

SY, Kim IS. Branching pattern of aortic arch in the

Korean water deer. J Vet Med Sci 2008; 70: 1051-1055.

2. Hammond WS. The developmental transformations of

the aortic arches in the calf (Bos taurus), with especial

reference to the formation of the arch of the aorta. Am

J Anat 1937; 62: 149-177.

3. Hiruma T, Nakajima Y, Nakamura H. Development of

pharyngeal arch arteries in early mouse embryo. J Anat

2002; 201: 15-29.

4. Jensen W. How old is my deer? North Dakota Outdoors

1996; 59: 2-6.

5. Kent GC, Carr RK. Comparative Anatomy of the Verte-

brates. 9th ed. New York: McGraw Hill. 2001: 314-350.

6. Latshaw, W.K. Veterinary Developmental Anatomy; A

Clinically Oriented Approach, 1st ed. Philadelphia: B.C.

Decker Inc. 1987: 181-188.

7. Lippert H, Pabst R. Aortic arch. In: Arterial variations in

man; Classifications and frequency, 1st ed. Munich: JF

Bergmann-Verlag. 1985: 3-10.

8. McGeady TA, Quinn PJ, FitzPatrick ES, Ryan MT,

Cahalan S. Veterinary Embryology, 1st ed. Oxford:

Blackwell Publishing. 2006: 105-135.

9. Molin DGM, DeRuiter MC, Wisse LJ, Moharmad A,

Doetschman T, Poelmann RE, Gittenberger-de Groot AC.

Altered apoptosis pattern during pharyngeal arch artery re-

modeling is associated with aortic arch malformation in

Tgf beta 2 knock-out mice. Cardiovas Res 2002; 56:

312-322.

10. Parsons FG. On the arrangement of the branches of the

mammalian aortic arch. J Anat (Lond) 1902; 36: 389-399.

11. Poelmann RE, Gittenberger-de Groot AC. Apoptosis as

an instrument in cardiovascular development. Birth

Defects Res 2005; 75: 305-313.

12. Vitums A. Development and transformation of the aortic

arches in the equine embryos with special attention to

the formation of the definitive arch of the aorta and the

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Incomplete Brachiocephalic Trunk in a Korean Water Deer 529

한국고라니의 불완전한 상완머리동맥

안동춘·태현진·박병용·심정하*·김종택**·김인식1

전북대학교 수의과대학, 인수공통전염병연구소, *예수대학교 간호학부, **강원대학교 수의과대학

요 약 :새김질동물류의 상완머리동맥은 대동맥활에서 분지하는 유일한 동맥으로 왼빗장밑동맥, 양목동맥 또는 왼·

오른온목동맥, 오른빗장밑동맥을 분지한다. 이런 분지 양상은 발생초기에 왼온목동맥과 왼빗장밑동맥이 심장 내림현상

에 따라 차례로 앞쪽으로 이동하여 일명 무명동맥과 합류함으로써 생긴다. 본 증례의 약 31개월령 한국고라니 암컷에

서는 상완머리동맥과 왼빗장밑동맥이 합쳐져 외형상 하나의 혈관을 이루고 있었으나 두 동맥의 중간막 안쪽층이 남아

있었으며, 이에 따라 불완전한 상완머리동맥으로 남아 있었음을 볼 수 있었다. 이러한 기형은 왼빗장밑동맥이 정상적

으로 이동 하였으나 합쳐지는 과정이 불완전하게 된 경우라고 볼 수 있으며, 한국고라니에서 처음 보고하는 바이다.

주요어 :상완머리동맥, 중격, 한국고라니