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Cervico-pectoral Ectopia Cordis in Two Holstein Calves
T. Hiraga, M. Abe, K. Iwasa, K. Takehana and A. Tanigaki
Vet Pathol 1993 30: 529
DOI: 10.1177/030098589303000606
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Vet Path ol 30: 529- 534 ( 1993)
Cervico-pectoral Ectopia Cordis in Two Holstein Calves
T. HIRAG A ,
M.
AB E,
K.
K.
IWASA ,
TAKEH A NA , AND A . TANI GAKI
Department of Veterinary Medicine, Veterinary Anatomy, Rakuno Ga kuen Unive rsity, Ebetsu, Hokkaido, Japan
Abstract. Two Holstein calves affected with cerv ico-pecto ral ectopia cord is, a male (No. 1)delivered stillborn
and a female (No .2) died I hou r after birth, were examined macroscopically and radiographically to assess the
sever ity and elucida te the teratogenesis of the anomaly. T he heart of one calf was cove red by the intact
pericardi um and skin and d isplaced to the cauda lmost porti on of the ventrocervical region , j ust cranial to an
enlarged thoracic inlet. T he cranial vena cava and the vena azygos were dupli cated. The sternum was bilaterally
divided into two part s fused only at the xyphoid process and was semicircular. The heart of the other calf,
cove red solely by the pericardiu m, was exposed ventrally from an oval openin g in the body wall j ust cranial to
a defective Y-shaped stern um. In both calves, the arterial branching patt ern from the aorti c arch was interm ediate
between the patt erns of the dog and pig, and in each case a single pulmonary vein emptied into the left atrium .
Pronounced or slight torticollis, cleft palate, and abnormalities in the urogenital system were also found . From
an embryological perspect ive, cerv ical and pectoral ectopia cordis have a common path ogenesis; the cervical
type occurs at a slightly earlier fetal stage than the pectora l type.
Key words: Catt le; congenital malforma tion ; ectopia cordis ; pathogenesis.
Ecto p ia co rdis (EC), a co nd itio n d efin ed as th e a bno rm al po siti on of th e heart a n yw he re o utsi de th e th oracic cavi ty , is su bdivided into th ree typ es accordi ng
to th e si te o f di spl acem ent: ce rvical, pect oral , a nd a bd om in al. In ca tt le , the ce rvica l typ e is th e m ost pre va lent. 3.8.1 0.1I A rare in termed ia te typ e o f EC , partiall y
cerv ica l a nd partiall y pect oral , has been d ocumented
in on ly o ne bo vine case .v
Two exa m ples o f th e interm ediate typ e we re prese nte d a t o ur laborato ry recentl y. N ecropsy o f tw o neonatal ca lves re vealed EC characte rized by th e reloc ati on o f th e heart between th e ce rv ica l region and th e
pect oral regio n. T o eluc idate possibl e e m bry o logica l
impli cati on s in th e teratogen esis o fEC, the gr o ss anato my o f th ese animal s wa s co m pa red with that of th e
ca lves wi t h th e ot he r typ es of EC d efect s.
nums were radiographed with soft x rays (Softex K-2, Softex
Co., Tok yo, Japan).
Results
Calf No. I
Thi s ca lf was co m p lete ly d e veloped a nd weighed 50
kg (us ua l size for a m ale neonate Hol st ein) . The ski n
was intact , a nd th e hair coat was normal. H ow e ver,
pronounced torticolli s to th e right wa s ev iden t, and a
swe lli ng wa s apparent in th e ca ud alm o st cervi cal regio n just a few ce n timete rs cra n ia l to the enlarged th oracic inl et (Fig. I) .
The left a nd right ste rnocep ha lic muscles , originatin g
bil aterall y from th e ste rn u m , fused wit h th e braehi oceph ali c muscles. The fused pairs o f muscles were thin
a nd fatty a nd cra n ia lly di verged at th e swe lli ng in the
ca uda l ce rvica l region (Fig. I ). The fibrou s peri card ium
was co n necte d to th e m and ib les by severa l broad, fla t
ligam ents. The ste rn u m was a b normally se m icircu lar
a nd was attache d to th e fibro us pe ricard ium at the
cranial m argin b y wide , th in sheetlike ligaments. The
pe rica rdi al cavity , a lt ho ugh intact , was ex tre mely large
(F'Ig. 2) .
T he heart was ro und, weighe d 350 g, wa s envelo pe d
Materials and Methods
Within a 34-month period, two calves with severe ectopia
cordis (EC) were born on separate farm s in Hokkaido (northern Japan). Deat h was ascribed to severe complications from
the EC. Bot h calves were bro ught dead to the lab oratory.
Calf No . I, a Holstein male, was delivered stillborn by Caesarean section on 21 Apri l 1987 and was the third offspring
of a multiparous dam that had previously borne two viable,
nor mal calves. Calf No. 2, a Holstein heifer born 2 Febr uary
1990, died I hour after birt h; the dam had a history of seven
nor mal deliveries.
In preparat ion for postmortem exa mination, calf No. I
was perfused with 2% form alin via the right femoral artery,
and calf No.2 was perfused via the left commo n carotid
a rtery. T he skeletal systems were macerated, and the ster-
in th e peri cardium , an d was si t ua ted in th e swolle n
pa rt of t he ve nt roeervica l region underneath th e su bc uta neous la yer a nd skin . In side th e spac io us pericard ial cavity , th e heart was characte rized by a d ouble
a pex, which pointed eit he r cra ni a lly or ca udally, d epend ing o n the general position of th e a n imal (Fig. 2).
529
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530
Hiraga ct al.
Vet Path ol 30:6. 1993
A
Fig. 4. Sche ma o f th e ste rn ums traced fro m so ft x-ray
pictures. A = normal ca lf; B = cerv ica l EC ca lf; C = pectoral
EC ca lf; D = ca lf No. I ; E = ca lf No .2; • = ste rne b rae ; a nd
0 = cart ilage . Bar = 10 em . (A and B" and C' " are reproduced
by permi ssio n.)
In contrast to the apex, however, the base of the heart
was somew hat an chored by the great vesse ls just beneath the VIth cerv ical vert ebra. Th e lungs comprised
two left and six right lobes, with the cranialmost two
of the right lobes protruding into th e pericardial cavi ty
(Fig. 2).
Immediat ely after the aorta eme rged from th e perica rdium, the bra chiocephalic trunk and then the left
subclav ian arte ry branched off. Th e brachiocephalic
trunk branched from a com mo n site into the left and
right co mmo n carotid arteries and th e right subclavian
artery (Fig. 3). Th e cranial vena cava and th e vena
azygos were duplicated. Becau se of the extrapectoral
displacem ent of the heart, the th ora cic portion of the
ca uda l vena cava was con siderably elongated , but this
did not resu lt in an y noti ceabl e d iminution of the diam eter of the vessel. A single pulmonary vein emptied
into the left atrium (Fig. 3).
l--
Fig . 2. Hea rt , peri card ial cavity; ca lf No . I. The heart,
its a pex pointing ca uda lly, and two lo bes o f th e right lun g
(arrowh ead s) occ upy th e intact pericardial cavity . The fibrou s
peri card ium is co n nec ted with th e ste rn um by a wid e ligam ent (* ) and se ve ra l thin ligaments. Bar = 5 em .
Fig. 1. Ventra l v iew , cervica l regio n; ca lf No . I. Severe
torticollis an d a swo llen pa rt of th e neck are observe d . Beca use of the split of th e ste rn ocep ha lic muscles (Sc) a t th e
swelling (*), bo th sides a tta ch to the left and right cra n ia l
end s of the stern um witho ut co vering th e peri card ium . Bar =
5 em .
Fig . 3. Right d orsal view , heart and grea t vessels; ca lf
No . I . T he left subclavian artery (Ls) a rises ind ep endentl y
fro m t he ao rtic a rch, a nd th e br ach iocephal ic trunk bra nches
in to th e left (L) and th e right (R) co m mo n caroti d and th e
rig ht subclavia n (Rs) arteries at a co m mo n site a long th e
trun k. The left (La) a nd right (Ra) az ygos vei ns em pty into
th e left and right cran ia l vena ca vae , resp ecti vely. Vp = co m mon pulmon a ry ve in. Ba r = 5 em .
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Vel " athol 30:6. 1993
531
Bo vine Ectopia Cord is
T he ste rn um parted cra nioca uda lly into two eq ua l
pieces and was fused on ly a t the xyp hoi d process. Co nseq uen tly, th e gross a ppea rance of th e ste rn um was
semicircular. The bone com pr ised 19 irregular sternebrae , as de term ined radi ographically (Fig. 4, D). Several thin, me m branous liga ment s bridged th e space
between the left a nd right pieces of the ste rn um a nd
ta utly connected th e perica rd ium to th e defecti ve ste rnum (Fig . 2).
In ad d it io n to the pr im a ry deformities in th e neck
a nd ches t of th e an ima l, cle ft palat e a nd bilat eral cry ptorchid ism were presen t.
Ca lf No . 2
This ca lf was a fully developed female Holstein born
at full term a nd weighed 41 kg. However, th e heart,
prot ected solely by th e peri cardium , was exposed ven trall y from an ova l ope ni ng (7 x 5 ern) in th e bod y
wa ll a t the cerv ico-pectoral region (Fig. 5).
The bilat eral ste rnocepha lic mu scles originated craniall y fro m th e right tip of th e a bnorma l V- shap ed
ste rn um (Figs. 6, 7). The left m . pect oral descenden s
origina ted fro m th e left mar gin of th e dermal hole on
th e cra nia l side of th e opening (F ig. 7). The fibrous
pericard ium enclosi ng th e heart was a ttached to th e
rim o f th e dermal ope n ing (Figs . 5,6). T he perica rd ial
ca vity was imperfectly for me d becau se o f partial adhesion between the parietal and visceral pericard ia (Fig.
8). No ligaments exte nde d fro m th e per icard ium.
Th e hea rt was grossly enlarged , wit h a weight of7 50
g. It pr otruded throu gh th e oval openi ng in th e bod y
an d was suspe nde d so lely by th e grea t vessels (Figs. 5,
6), and tilt ed dor socaudall y in such a manner as to
di rect th e a pex crani oventra lly. T he lung appeared normal.
Th e branching pattern o f vess els fro m th e ar ch o f
th e ao rta in calf N o. 2 was co m pa ra ble to that found
in ca lf No. I, with th e not ab le exce ption of a shorter
int er val betw een th e sites of origin o f th e brachi ocepha lic trunk a nd th e left subclav ia n arte ry (Fig. 8). O nly
one pulm on ar y vei n em ptied into th e left at rium . The
cranial ve na cava was normal, but a right vena azygos ,
ra ther th an the norm al left one, was pr esen t.
T he stern um was di vid ed lon gitudinally in to two
parts th at exte nde d b ilaterall y fro m th e manubrium to
th e m idd le of the bod y and formed an obvious V- shap e.
T he cra nial margin of the bon e had a smoothly finis hed
edge a nd form ed th e ca uda lmost hal f o f the opening
in the skin thro ugh wh ich th e heart was exposed (Fig .
7). T he Y-sha ped ste rn um was determ ined by rad iogra ph ic exa m ina tio n to be formed by 10 irregul ar ster neb rae (Fig . 4, E).
Addi tio na l defect s included slight torticolli s, a partial cleft palate , and a n a bno rma lly lar ge clitori s.
Fig. 5. Head , neck , ventra l th or a x; calf No .2. T he extrem ely enlarged hea rt pro tr udes ve ntr ally from the thorax
a nd is suspended on ly by the grea t vesse ls. Ba r = 10 em .
Discu ssion
T he pec ulia r a na to m ica l defects present in the two
ca lves were co m pared with a no ma lies associated with
ce rv ical a nd pectoral ecto pia cord is (EC) see n in n ine
other bo vine cases previo usly investigated in our laboratory.! '" T hese defects of th e heart , artery, veins ,
a nd stern um a nd othe r m iscellan eou s abno rmal ities
a re sum marized in Table I. In co ntras t to rep or ted
cas es o f bovine EC, th e di spl acem ent of th e heart in
th ese two calve s to ok a middle positi on , between th ose
of cerv ica l and pect or al EC A number of co m plication s found in ca lf No . I a re co m mo n in bo vin e cervical EC, includi ng th e d oubl e a pex o f th e hea rt, th e
ligam ents connec t ing the mand ib les and th e sternum ,
a nd th e duplication o f the cra n ial vena ca va and th e
ve na azygos. The a no ma lies o f ca lf No . 2 were closer
to th ose seen in bovine pect oral EC A dermal opening
exposing the heart is co m mon in cases ofEC involvi ng
th e chest. 1.2.19.23.27
In most rep orts o f bovine cer vical EC, th e a pex of
th e heart pointed in a cra n ial di rection, an d the base
tilted ca uda lly.3.4.11.1 2.14.'8.22.25.26 In calf No . I, a la rge
per ica rd ial ca vi ty per m itt ed a ran ge o f mo vemen t of
th e ap ex. T his uncon ven tional fi ndi ng has been previo usly re ported .10T he defects in the peri ca rd ial ca vity
in ca lf NO.2 were si m ilar to the absence of th e cavity
in a calf with pectoral EC I9
Veteri na ry textbooks"> ro uti ne ly define three pa ttern s of a rteria l bran ching along th e a rch of th e ao rta
in th e d og, pig, and cow . In cas es of bov ine cervical
EC however, th e bran ch ing freq uently tak es on th e
ca ni ne pattcrn -! '" or in so me cases a hybrid pattern
with features of both the dog a nd pig pauerns.s-P-"
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532
Hiraga ct al.
Vel Pat hoi 30:6. 1993
Fig. 6. Ven tral view, cervi cal and pectoral region ; calf No .2. Both left and right ste rnocepha lic m uscles (Sc) originate
fro m the right cranial end of th e stern um . Th e opening through which the heart protrudes is ova l with smooth margins.
13ar = IO cm .
Fig. 7. Dorsal view , stern um , ste rna l ribs, and pectoral and sternoce phalic (Sc) mu scles; ca lf No .2. The opening is
formed crani all y by the left pectoral descend en s (Pd) and caudally by th e cranial border of th e ste rn um . Bar = 5 em ,
Fig. 8. Left view, heart and large arteries; calf No. 2. Th e bran ching patt ern along the arch o f the aort a is co m parable
to that found in calf No. I. Th e fibrou s pericardium partially ad hered to the epicard ium, so th at the pericard ial cavit y was
imperfect. L and R = left and right co m mo n carotid arteries. Ls and Rs = left and right subclavian arteries. Bar = 5 cm.
Fig. 9. Schema of bra nching patt ern of the art eries from
the ao rt ic ar ch. A = dog type; 13 = pig type; C = catt le type;
D = int erm edi at e type betw een ca nine and porcin e; E =
intermed ia te type between por cine and bovin e; D = ao rta
and brach iocephal ic trun k; I%l = left subclav ian arte ry; I IlID =
right subclav ian artery; • = bicarotid artery; D = left co mmon carotid artery; ~ = right com mon carotid artery ; and
.. = direct ion of blood now.
However , calves with pector al EC di splay either a hybrid pig-cattl e bran ching pattern 1.2. 19.23 or th e catt le
type." In both animals in th e present study, a hybrid
dog-pig pattern was present (Fig. 9).
The mechanism responsible for cervical EC has been
identified as the delay ed descent of th e heart during
em bryonic development. v-" In th e bovine em bryo,
descent of the heart is norm ally co m pleted at abo ut
th e time a fetu s has a crown- ru m p length (CR L) of 14
mrn .? In th e morph ogeni c modifi cati on exerte d by th e
em bryonic vascular pattern to form th e definiti ve adult
pattern , th e left subclavian artery switches its site of
derivation when th e em bryo has a CRL of 17-22 mm. ?
T his switch involves a change in th e site of origin of
th e left subclavian artery from th e aortic arch-a primitive em bryo nic vasc ular pattern -to th e brach iocephali c trunk. Th e formation of th e bicarotid arte ries
is initiated after the em bryo has a CRL of2 5 mrn .? In
bovine feta l life, th e CRLs of 14 mm , 17-22 mm , and
25 mm approxima tely correspond to gestational da ys
36, 37- 39, and 40 , respecti vely.' Thus, cerv ica l EC is
eq ua ted with de velopment al failu re befor e em bryo nic
day 36, whereas pectoral EC is associated with developme nt subseq uent to da y 40. In calf Nos. I and 2,
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Vel Pat hol
30:6. 1993
533
Bovine Ectopia Cordis
T ab le I. Defects of hea rt , a rtery, ve ins, a nd ste rn um and o ther a no ma lies d ocumen ted in calves with ce rv ical and
pectora l ectopia cordis (EC) , includ ing th e present tw o cases (Nos. I, 2).
Defects
Cervico-pectoral EC
Cervical EC
(8 cases" )
Calf No. I
Heart positi on
C rania l to ca udal
ce rvical regio n
Ca uda l cervical
region
Weight (g)
Apex
Pericardia l cavity
Artery branching
pattern from
aort ic arch
Vei ns
C rania l vena cava
300-580
Do ub le
Norma l
Dog type
Bilatera l
or no rm al
Bilatera l, right
or left side
Se veral (normal)
Azygos ve in
Pu lmonary ve in
Stern um
Shape
Num ber of ste rne brae
Ot her defects
Calf No. 2
Pectoral EC
(one case' ")
Cervico-pectoral
regio n
Pecto ral
regio n
350
750
600
Double
No rmal (expande d)
Dog-pig type
Single (no rma l)
Imperfect
Dog-pig type
Double
Absent
Pig-eattl e type
Bila teral
Norma l
Normal
Bila teral
Right side
Right side
Sing le
Sing le
Seve ra l
(no rma l)
In verted trian gle.
tra pezo id , etc.
Sem icircle
Y-shape
Key ho le
13- 26
19
Tortico llis,
cle ft palat e, and
cryptorchidism
10
Torticollis,
cle ft pala te, and
enlarged clitoris
II
T ort icolli s a nd
brach ygnath ism
Torticollis,
cle ft pa late , etc.
EC is beli eved to ha ve ta ke n place bet ween fet al days
36 an d 40 .
In ca tt le witho ut EC, dupli cati on of th e cra nial ve na
cava or ve na azygos is a n extre me ly rar e a no maly. l5.21
Dupl icati ve vei ns ha ve been co nsi de red th e result of
co mpensation for a morphogenic failure to complete
a nasto mosis between th e left and rig ht a nterior card inal a nd supracard ina l ve ins. As in th e ca lves in this
study , a co m mon pulm onary ve in was reported , a lbe it
inco nsiste ntly, in both ca lves with cerv ica l EC3.26 a nd
ca lves with pectoral ECI .23 As suggested by th e fat e of
e mbryo nic vessels in the modificatio n necessary to esta blish the basic ad ult circ ulatory pattern , th e fai lure
of modi ficat ion at th e proper time or th e total fai lure
of m odifi cat ion may be th e basis for vascular a no m ali es. In EC, th e abno rmalities of th e vesse ls near th e
heart m ay be att rib uted to developmental failure in
th e ea rly em bryologica l stage .P-"
In a com prehensive treati se o n ossification of th e
bovine ske leto n," th e early phase of sternal development in th e no rma l bo vine fetus was describ ed as follo ws. At feta l da y 50, th e precu rsor of th e ste rn um is
ident ified as bilat er al ca rtilagino us ba rs. T his pa ir of
cartilagi no us ste rna l ba rs, fully forme d by day 53, a re
fuse d a lmost co m plete ly by feta l day 64. T hese o bse rvations and th e present arteria l findi ngs indicate th at
fusio n of the bilateral ste rnal ba rs is retarded , if not
blocked , by a prem ature j ux tapos itio n ing of th e hea rt
a t th e th oracic inl et. T h is idea co ntras ts with a n ea rlier
pr opositi on that incomplet e fus ion of th e tw o halves
o f th e ste rn um could be regarded as a pr im ary ca use
of cervica l EC1 2.1 3 Becau se of th e strict seq ue nce of
events necessary to confer th e uncomprom ised ca pac ity for differe ntiation, organogenesis, and fusio n of eac h
implicated part in turn, th e incompleti on of fusio n of
th e ste rna l pr imord ial bars is ruled out as playing any
im porta nt role in th e ce rv ica l di splacem ent o f th e heart
in bo vine EC
T he ca use of a bro ad m anubrium and pa ired ste rne brae, wide ly repo rted in ca lves with cervical EC, has
been asc ribed to th e mech an ical action of EC itse lf.4.11- 13.22 T he genera l a ppearance o f th e ste rn ums
(Fig . 4, B) ra nges fro m tha t of a n in verted trian gle to
a trapezoid a nd other sha pes. In pect or al EC, ho wever ,
a ring-sh ap ed stern um form s an ope ni ng in th e bon e
(F ig. 4, C), facilita ting th e protrusion of th e hea rt fro m
the th o rax. I.2.10.16.19.23 In co ntrast to the ste rnu ms cha racterizi ng cervica l EC a nd pectoral EC, the stern ums
o f th e ca lves in th e present study were di spro port ionately short for th eir wid ths. Furthermore, eac h of th e
two ste rn ums had a di stin cti ve sha pe , o ne sem icircula r
(Fig . 4, D) and th e o the r Y-sha ped (Fig. 4, E), a nd bo th
resulted fro m a la rge incis ura o n th e cranial end . T he
result an t two sections of eac h ste rnum me t so lely at
th e xy phoi d process o r at mid-body. These pa rticula r
ma lformatio ns suggest th at th e m anner o f attach me nt
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534
Hi raga ct al.
of the bilateral cervical muscles to the cranial proje ctions of the sternum plays a decisive role in sternomorphogenesis. In calf Nos . I and 2, the EC was classified as interm ediat e (neither pectoral nor cerv ical),
and the morphologic design of their sternums also reflected the intermediate typ e of EC (Fig. 4).
To date, onl y three cases, including th e two calves
in the current study, of bovine EC intermediate between the cervical and pectoral types hav e been reported. In the only other case," the main findings were
displacem ent of the heart to a position just cranial to
th e sternum, left cardiac hypopl asia , double outlet right
ventricle, and a partial defect in the pericardium enveloping the heart. EC in calf No. I was thought to be
closer to the cervical type and that in calf No. 2 closer
to the pectoral type than was th e oth er case."
The results of this study support the view that cervical ectopia cordis is det ermined in the bo vine fetu s
before gestation day 36, that the pectoral type is determined after the 40th fetal day , and that th e nonpectoral-noncervical intermediate type occurs between
fetal da ys 36 and 40 . Further studies are needed to
assess th e roles played by breed , genetics , nutritional
deficiencies, and detrimental environmental influences
on the development of ectopia cordis.
Acknowledgements
We thank the Yakumo Bran ch o f th e Donan Agricult ural
Mutual Aid Associatio n and Kami yub et su T own O ffice for
supplying th e ca lves . Special th an ks arc give n to Dr. H. W.
Leip old , Departm ent of Path ology, Kan sas Sta te University,
for his enco urage me nt and advice.
References
2
3
4
5
6
7
Abe M , Shim izu T , Hi raga T , Iwasa K, Ta keha na K,
Kob ayashi K: A case of sterna l ecto pia co rd is in a ca lf.
1 Co li Dai rying 9:1 01-1 06,1 981
Bogdaschew N: Ecto pia extrasterna lis cordis beim Kalbe.
Ana t An z 72:403-408, 1931
Bowen 1M , Ad rian RW : Ecto pia co rd is in ca tt le. 1 Am
Vet Med Assoc 141:11 62-11 67,1 962
Drommer W: Morp hologische und rontg cnologischc
U nte rsuchungen an di ceph alen Doppclmi flbildungen
beim Rind . Zentralbl Vct crin arrn cd Reihe A 14:515527 , 1967
Evans H E, Sack WO: Prenatal development o f do mes tic
and lab orator y mammal s: growth curves, externa l featu res and selected refere nces . Ana t Hi stol Embryo l 2: 1145 , 1973
Fiedler HH , Seid ler D: Ecto pia cor d is cra nialis m it Anomalien der herznah en Gefafls ta m me bei einem Kalb.
Dtsch T ierarztl Wochen sch r 81:619-621 , 1974
Ge tty R: Sisson and Grossma n's Ana to my of the Domestic Ani ma ls, 5t h cd ., vo l. 1, 2, pp. 565-5 66, 96296 3, 1309-131 0, 1598-1 599. WB Sa unde rs, Phil ad elphia , PA, 1975
Vet Patho l 30:6. 1993
8 G udgliick G : Mi13bildungen des Herzen s einsc hlie13lich
Mi13bildungen der gro13en Gefafse des Herzbereiches. In :
Handbuch der Speziellen Path ologischen Anatomi c der
Hau stiere, cd . Dobberstein 1, Pallaske G, and St unz i H,
3rd ed., vol. 2, pp. 15-40. Paul Par ey, Berl in, Ge rma ny,
1970
9 Hammond WS: Th e development tran sformati on s of
the aortic arches in the ca lf (B as taurus), with especial
reference to the form ati on of the arch o f the ao rta . Am
1 Ana t 62:14 9-1 77,1 937
10 Herzog A, Wied ekin g I F: Ecto pia co rd is co ngenita bei m
Rind . G iessener Bcitr Erbpatho l Zuchthyg 1/ 2: 1- 24, 1970
II Hiraga T , Abc M: Eight calves of cervical ecto pia cordis
and their stern ums . Jp n 1 Vet Sci 48: 1199-1 206, 1986
12 Hughes HV: Ecto pia cor d is in the calf. 1 Co rnp Path ol
Ther 47: 14 1- 15 1, 1934
13 Hu ghes HV: Th e stern um in ecto pia cor dis. Vet 1 92:
22 5-226 , 1936
14 Immi sch I: Exokardie beim Kalb e. Dtsc h Tierarztl
Wochen schr 16:4 69-4 70, 1908
15 Keml er AG , Martin l E: Incidence o f co ngeni ta l ca rd iac
defects in bovin e fetu ses. Am 1 Vet Res 33: 24 9-251 ,
1972
16 Kurtz Hl , Ellery l C: Ecto pia co rd is in a bov ine fetu s.
A m 1 Vet Res 30:4 71-4 73 ,1 969
17 Lind say FEF : Obse rva tions on the loci of ossification in
the prenat al and postn at al bovine skeleto n. II. T he ste rnum . Br Vet 1 125:422-4 28, 1969
18 Mill edge R D, East in CE, Reeves I T: Ph ysiologic and
rad iograph ic stud ies of cerv ical ecto pia co rdis in a calf.
1 Am Vet Med Assoc 152:1 61-1 67,1 968
19 Nak ayam a Y: A case of bovine sterna l ecto pia cordis .
MA Th esis, Rakun o Gak uen University, Ebets u, Ja pan,
1985
20 Rittenbach P: Ecto pia cord is in Kombinati on mit mehrfachen weiteren Herzan om alien bei einem Kalb . Monat sch Vcterina rrncd 19:85 8-861 , 1964
2 1 Sekeles E: Doubl e cra nial vena cav a in a cow : case report
and revie w of the literatu re. Zentra lbl Vctcrinar rncd Reihe
A 29:4 94-5 03, 1982
22 Vitum s A: Ecto pic heart of a Sho rtho rn bull. An at An z
114:4 8-61 , 1964
23 Wil ken s H: Ecto pia co rdis th ora cal is fissistern ali s beim
Kalb e. T iera rztl U msc h 9: 389-392 , 1954
24 Wil kens H, M unster W: Ar terie n. In: Leh rbu ch der Anatomic der Hau stiere, ed . Nickel R, Schurnrner A, and
Seiferle E, vo l. 3, pp . 76- 190. Paul Par ey, Berlin , German y, 1976
25 Wyrost P: Th e result s of stud ies on conge nital cerv ical
situs o f the heart in do mes tic ani ma ls. Folia Morph ol
(Prag ue) 29: 220-22 3, 1981
26 Wyrost P, Rad ek 1: Co ngen ital cerv ical situs of the heart
in a 2.5 years-o ld cow. Fo lia Mor ph ol (Wa rsaw) 41: 7387, 1982
27 Zietzschman n 0: Ein Fall vo n Ectopia cordis nud a beim
Rind sfetu s. Dtsch T ierarztl Wochensch r 42: 179-1 80,
1934
Requ est rep rint s from Dr. T . Hira ga, Department of Veterin ar y Ana to my, Ra kun o Ga kuen U nive rsity, 582 Bunk yod ai
Mid or im ach i, Ebets u, Hokkai do 069 (Jap an).
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