235l$. lp. 235 243, with 4 flgures Printed in Great Britain

- ,mrlmparative anatomy of the cardiac foramen ovale in cats

ffi-e[ildae), dogs (Canidae), bears (Ursidae) and hyaenaslffiJS,aenidae)

r l L i . . s , i T \ IR A . MACDONALD AND MARCUS JOHNSTONE

tir*r,nrl. i,L, . ,t' preclinical Veterinary Sciences, The Royal (Dick) Schoot of Veterinary Studies, University of Edinburgh'

, i l tt i l i l t i t"r;;"-l- i K

: September 1994)

I r ' 4 r l

", rir r"---.ire of the foramen ovale from 16 species representing 4 carnivore families, the Felidae, Canidae,

,ririiruui,irj .1d Hyaenidae, was studied using the scanning electron microscope. The Felidae were represented

nN tu i:.:sric cat fetuses (Felis catus),2 snow leopard neonates (Unciauncia), an ocelot neonate (Leopardus

,rnar ri1i,r,,,ir I lion neonates (Panthera leo), a panther neonate (Panthera pardus) and 3 tigers (Neofelis tigris),

nulr*n-r: r.! I fetuses and a neonate. The Canidae were represented by a golden jackal neonate (Canis

/l111irnirili,,r ::rewborn wolf (Canis lupus),S domestic dog fetuses (Canis.familiaris),3 red fox neonates (Vulpes

/14tirlil*1 j:.: a dhole neonate (Cuon alpinus). The Ursidae were represented by a brown bear neonate (Ursus

,ri r f ii . ;av-old grizzly bear cub (Ursus arctos horribilis), a polar bear neonate (Utsus maritimus), and 2

ilulrlutir:trrr: --,. bear fetuses (species unknown). The Hyaenidae were represented by a striped hyaena neonate

ir ir,iiriirlr,lL .'.tt€na).In each species, the foramen ovale, when viewed from the terminal part of the caudal vena

,,1r 1u- tr*l :he appearance of a short tunnel. A thin fold of tissue, the developed remains of the embryonic

*rllxiullrrrlm ::-:rrum, extended from the distal end of the caudal vena cava for a variable distance into the Iumen

rrr, )ur r...rtrium and contributed towards the'tunnel'appearance in all specimens. It constituted alarge

ilr,,'iil,,$'r-_ _: of the tube, and its distal end was straight-edged. There was fibrous material underlying the

rlrlluuulilrrlllrr;.- -n of the flap, the apparent morphology of which suggested that it comprised cardiac muscle' In

,rlruurNNti ,[,r-.is. the pulmonary veins drained from close beside the interatrial septum and this venous drainage

utr111n1gi -. be directed along the length of the flap of tissue on its dorsal surface. Collapse of the'tunnel'of

tlurilLr lffir -:r primum effected closure of the foramen ovale in most of the neonates studied. When closed, the

6ns4iiur 1-: appeared to be anchored to the interatrial septum along the surface of the crista dividens which lay

qr )1u E.. rtrium. The straight edge at the end of the'tunnel'remnant was not usually attached and, when

wr1fliltrii -:-:d. formed a small blind-ended pouch ending at the attachment of the flap to the crista dividens'

i l i i t i l i _ _ r l T I O N

lLru :r:--;t ion of the mammalian fetus differs from

iirlllil ' .:,: adult in a number of important ways' Each

lli lllelE f consequence of gas exchange occurring in

lllru "rlr,i.i-;::a rather than in the lungs of the prenatal

llluunrum;u ')r1 genated blood coming in the umbilical

,rrrutln r. i:, the placenta passes through the liver via the

Lilrfilr]lluril,. ,::rosus into the caudal vena cava' It is then

lu]l]lliiii:lfl:]r *::J bv the heart to the fetal tissues through

two specialisations within the fetal circulation which

enable it to bypass the lungs: the foramen ovale and

the ductus arteriosus. The former (Fig. 1) provides an

open channel from the caudal vena cava through to

the left atrium and allows blood to be shunted directly

to the left side of the heart (Amoroso et al' 1942;

Franklin et aI. 1942). The second fetal shunt, the

ductus arteriosus, enables the deoxygenated blood

from the right ventricle to be shunted away from the

lungs and into the aorta (Fig' lA). At birth the

,,'*xffi.i : -.:ce to Dr Alastair A. Macdonald, Department ol Preclinical Veterinary Sciences, The Royal (Dick) School of Veterinary

tuturtulus. --:

University of Edinburgh, Summerhall, Edinburgh EH9 1QH, UK'

236 A. A. Macdonald and M. Johnstone

ADuctus

arteriosus

Caudalvenac€IVA

Fig. 1. (l) Schematic diagram of the heart of a tiger fetus with the

lefi atrium opened. The heart is oriented to show the relative

positions of the major arteries and veins, the foramen ovale and the

short tunnel-shaped fold of tissue representing the septum primum

which lies distal to it. (B) Schematic diagram ofa horizontal section,

at right angles to ,4, through the left and right atria ofthe heart of

a tiger fetus. The arrangement of the caudal vena cava, cnsta

dividens (C) and the short tunnel-like fold of tissue (septum

primum, SI) extending into the left atrium from the foramen ovale

is illustrated.

placenta is abandoned, the lungs expand and take

over the role of respiration, and the two shunts in the

heart, the foramen ovale and ductus arteriosus,

normally close.Surprisingly, relatively little is known about the

anatomy of the foramen ovale and its associated

structures; it has been studied largely in man and a

number of the domestic animals (M osca, I 9 14 ; Patten'

t93l; Amoroso et al. 1942; Franklin et

Ottaway, 1944 Macdonald, 1988; M

1988). Although comparable studies have

out on the dog (Chausse, 1916; Ottaway, I

is relatively little comparative informationForamen ovale for other carnivores (Amoroso et al. 1942;

al. 1944; Franklin, 1946). Anatomical di

the structure ofthe fold oftissue distal to thc

were found between the families

Suiformes (Macdonald, 1988, 1994) and

B

raised questions with respect to the

similar anatomical differences existing

lies of the carnivora. The scanning

scope was used to obtain information on

graphical and low-powered microscopic

the opening and its associated tissues' The

nomenclature used to describe species th

paper was that published by Corbett & Hin

M A T E R I A L S A N D M E T H O D S

We studied 35 hearts from 16 species

carnivore families, the Felidae' Canidae,

the Hyaenidae. Fetal and neonatal size is i

the crown-rump length (CRL) of the ani

The Felidae were represented by hearts

fetuses (Felis catus) (University of

specimen nos AAM137-AAMI45)' 2

snow leopards (Uncia uncia) (Edin

specimen nos AAM271 and LAM272),

ocelot neonate (Leopardus pardalisl

historisches Museum, Berlin - specimen nc

CRL : 15.5 cm), 2 lion neonates (P

(Liverpool Museum-sPecimen no. I

CRL: 37 cm', SurabaYaAAM86), I male Panther neonate (P

(Zoological Museum, Bogor-specimen

CRL : 38 cm), and 3 rigets (Neofelis

prising 2 male fetuses (Natural History

London-specimen nos 86'718, CRL:2

86.720. CRL : 30.5 cm) and a male

History Museum, London-specimen no-

CRL:28 cm) .The Canidae were rePresented bY

male golden jackal neonate (Canis

museum van Natuurlijke Historie,

no. 790, CRL : 16 cm), I newborn male

/apzs) (Natural HistorY Museum,

no. 70 .3 .30 .2 .3 , CRL :22cm) ,8 dog

familiaris) (Royal (Dick) School of V-specimen nos. AAM129-AAMI35), 3

neonates (Vulpes vulpes), a male and

ling pair (Rijksmuseum van Natuurlijke

Ccu'diac foranten ovqle in carnivores

, - : . . -specimen nos. 12888 a/b, CRL: 13.5 cm)

- . male cub (Rijksmuseum van Natuurlijke

1 r-i. Leiden specimen no. a2K2, CRL:

-' -:r). and a male dhole neonate (Cuon alpinus)

il . r,::ruseuffr van Natuurlijke Historie, Leiden

inu- 1:n no. 20551, CRL : 19 cm).--..

Ursidae were represented by hearts from I'i.;L: rrr-')\r/r1 bear cub (Ursus arctos) (Zoologisches

r ls-1. Berlin specimen no. 10874, CRL :

-: a 1 d male grizzly bear cub (Ursus arctos

ii " - r) (Zoologisches Museum, Berlin-specimenr- j-14. CRL : 20.5 cm), 1 male polar bear

,rr: r: .3 ' Li'sus maritimus) (Rijksmuseum van Natuur-

r,, : i :.torie, Leiden-specimen no. 819, CRL:

1l -: .rnd 2 male bear fetuses (species unknown)

-. :::-.ol Museum-specimen nos 143.446, CRL :-

- : . . rnd 143.441, CRL:20 cm).-':=

Hraenidae were represented by a heart from I

iuu : :.ilp€d hyaena neonate (H1,aena hyaena) (Zoolo-

uLln" :., \ luseum, Berlin specimenno. BERNONUM,i l _ : 1 3 c m ) .-.::

:uboptimal condition under which material in

lirr:.r-: collections was originally gathered, fixed':xrr -,. J: unknown) and preserved (in alcohol or

, .,:rmalin) precluded the detailed study of

ulttrr:,r-lCturo. However, in most specimens there was,irr ,,rerficial damage either to the topography or

::ru ' .,, powered microscopic appeafance of the

ruu-- The foramen ovale and associated caudal vena

ir,ri ,, r. ,. 3fe dissected free of the walls of the atria and'rffirF.:i 1or study in the scanning electron microscope

Lr',trr-,:: -s05). The specimens were first placed in a

, , r r r - . : r o f 3"h g lutara ldehyde in 0.1 l t sodium

riru ,: .ate buffer (pH 7.3) overnight and then im-

mlrl-,{: in 2 % guanidine hydrochloride and 2oh tanntc

LLrl - ' : a second night (Murakami et al. 1977). They

rrllrLri.i: .r.3rr washed in 0.1 rr,r sodium cacodylate buffer

,r,i :. .thred in I 7o osmium tetroxide. After fixation,

iru : ! re S w€re dehydrated through a graded series of

Lur"r . r-s. dried in a critical point drier using carbon

,i , r: , Cohen, 1979), and sputter coated with 20 pm

u : :rl ladium (Echlin, 1975).

, , T S

' : : .:n€r&l anatomy of the heart of the carnivore

i,: -, . i l lustrated in Figure 1. In each species, the-- -:n ovale, when viewed from the terminal part of

:rr ,: ldal vena cava had the appearance of the

:ur .-- --i to a short tunnel. This entrance was formed': - - : icaudally) by atrial tissue associated with the

,i. .L - :. \ ena cava and in part (cranially) by the curved

iu: - -i: Jf interatrial seDtum termed the crista dividens

(Figs 1 8,2a, b,3f, 4h, c). The crista dividens had an

edge which tended to be narrow in the middle and

broadened out towards its attachments on the atrial

walls. A thin fold of tissue, the developed remains of

the embryonic septum primum, extended from the

distal end of the caudal vena cava for a variable

distance into the lumen of the left atrium and

contributed towards the 'tunnel' appearance in all

specimens (Figs 1-3). It was unfenestrated in all

animals except for 1 polar bear specimen (Ursus

maritimus) and its distal edge had a smooth, rounded

appearance. The thin fold constituted about 75oh of

the inner surface of the 'tunnel', the wall of the

interatrial septum contributing the remaining 'floor'.

Felidae

The fold of tissue representing the septum primum

was thin-walled in all specimens of the domestic cat

(Felis catus) (Fig. 2 c). The dimpled appearance of the

fold suggested that a branched fibrous substrate lay

below the endothelial layer. The pulmonary veins

drained over the surface of the fold from near their

attachment adjacent to the caudal vena cava and the

interatrial septum. In the snow leopard (Uncia uncia)

the fold of tissue was quite thick and the underlying

fibrous arrangement of the subendothelial tissue

suggested that it comprised cardiac tissue which had

contracted (Fie. 24. The venous drainage from the

pulmonary veins of this species seemed to be directed

to flow along the length of the flap of tissue.

Although the fold of tissue representing the septum

primum of the ocelot (Leopardus pardalrs') was

embedded in blood (Fig. 2e), careful brushing

revealed that the collapsed fold of tissue was straight

edged and thin. It had been covered in the venous

drainage from the pulmonary vein which emptied

over it from its opening on the roof of the atrium

adjacent to the attachment of the caudal vena cava.

The septum primum fold in the lion (Panthera leo)

was simple and ended in a straight edge (Fig. 2fl. The

length of the flap in I specimen seemed barely long

enough to reach the crista dividens. The pulmonary

veins drained from close beside the interatrial septum

and seemed to direct the blood flow along the length

of the flap of tissue on its dorsal surface. The specimen

from the panther (Panthera pardas) also had a septum

primum which seemed too short to cover the opening

of the foramen. The pulmonary vein emptied over it

from its attachment to the interatrial septum and the

caudal vena cava. The septum primum of one of the

tigers (Panthera tigris) demonstrated branched fibrous

material underlying the endothelium in the proximal

238 A. A. Macdonald and M. Johnstone

Fig. 2. (a) Scanning electron micrograph of the heart of a domestic cat (Felis catus) fetvs illustrating the caudal vena cava (Y),(R), coronary sinus (H), crista dividens (CD) of the interatrial septum, and the septum primum (SI), the fold of tissue attached toovale which stretches into the left atrium. Bar, 1 mm. (b) Scanning electron micrograph of the heart of a panther (Pantheraillustrating the caudal vena cava (V), left atrium (L), the crista dividens (CD) ofthe interatrial septum, and the septumshort tunnel-like fold of tissue attached to the foramen ovale stretching into the left atrium. Bar, 1 mm. (c) Scanning electronof the heart of a domestic cat (Felis catus) fetus illustrating the straight edge (arrow) of the septum primum (SI) and behind thatedge of the crista dividens (CD) of the interatrial septum. Bar, 1 mm. (d) Scanning electron micrograph of the heart of a l-wk(Uncia uncia) illustrating the folded straight edge of the septum primum (SI). Bar, I mm. (e) Scanning electron micrograph ofedge (arrow) of the septum primum (SI) of a newborn ocelot (Leopardus pardalis) partly hidden in blood clot. Bar, I mm. (/|electron micrograph of the straight edge of the septum primum (SI) of a hon (Panthera leo) neonate. Bar, I mm, @)micrograph of the straight edge of the septum primum (SI) of a tiger (Panthera trgrus) fetus. Bar, 1 mm.

part of the flap, the orientation of the fibres beingaround the circumference of the tunnel. Distally theflap was straight edged (Fig. 2g). One pulmonary veindrained onto the fold of tissue from the dorsal surfaceof the atrium, medial to the caudal vena cava andclose to the interatrial septtrm; another vein seemed to

drann on\o \\e.wa\\ o\. \\e a\irrrrn'\\ s\a\ a wav \\a\

the flow would be against the ventralwall of the tunnel.

Canidae

In the domestic dog (C anis familiaris) tllietepresentng \\e septum pr\munn

239r',trdia( foranten ovale in carnivores

Scanning electron mrcrograph of the heart of a domestic dog (Canis.famlllarls) fetus illustrating the caudal vena cava (V)' left

- . the site of drainage tiom the pulmonary veins (P), and the septum primum (SI), the short tunnel-like fold ol tissue attached to

- - - . : nova les t r e t ch ing in to the le f t a t r i um .Ba r , Imm. (b )Scann inge lec t r onm ic rog rapho f t hehea r to f ab rownbea r (U rsusa rc tos )

- : ustrating the caudal vena cava (V), left atrium (L), the site ofdrainage from the pulmonary veins (P)' and the tunnel-like septum

- SII stretching into the left atrium. Bar, I mm. (c) Scanning electron micrograph of the heart of a wolf (Canis lupus) neonate

" .= .g thes t ra i gh tedgeo i t hesep tumpr imum(S I ) .Ba r , lmm. ( / )Scann inge lec t r onm ic rog rapho f t hehea r to fa red fox (Vu lpesvu lpes )

,:: raring the straight eoge of ihe ,.ptu- p.i-.r- (SI). Bar, 1 mm. (e) Scanning electron micrograph of the heart of a hyaena (Hyaena

:..jonate illustrating the (lblded) straight edge of the septum primum (SI). Bar, 1 mm. (/) Scanning electron micrograph of the heart

.- : tCuon atpinus)neonate viewed from the caudal u.nu.uuu and illustrating the right atrium (R), the crista dividens (CD) of the

: :i septum, and the septum primum (SI) blown back slightly from the left atiium. Bar, 1 mm. (g) Scanning electron micrograph of

:- . of a l-d-old grizzly bear (Ursus arcto,s horribilii cub illustrating the straight edge of the septum primum (SI)' Bar, 1 mm (ft)

-.::lectron micrograph of the heart of a polar bear (Ursus maritilnus) neonate illustrating a fenestration (arrow) lying proximal to

". ;ht edge of the septum primum (SI). Bar, i mm.

::n individual animals. There was fibrous ma-'- :nderlying the endothelium of the flap. The

-,n of the pulmonary vein was such that it

. - -J along the length of the flap (Fig. 3 4)' Like the

- .ile golden jackal (Canis aureus) had a thin

, r * -- primum flap with a straight edge' In the

specimen of the wolf (Canis lupus) Ihe branched

fibrous material running from the wall of the atrium

around the circumference of the tunnel shape of the

fold of tissue beneath the endothelium could be clearly

seen from the left atrium (Fig. 3c). One pulmonary

vein was positioned in the roof of the attiumto empty

240 A. A. Macdonald and M. Johnstone

Fig.4. (a) Scanning electron micrograph of the left atrium of atiger (Panthera rrgrlb) fetus illustrating the septum prrmum

over the foramen ovale. The leading edge (arrow) is indicated. Bar, 1 mm. (6) Scanning electron micrograph ofthe heart ofa

(panthera tElrs) viewed from the right atrium illustrating the septum primum (SI) collapsed over, but incompletely closing

ovale. Note the crista dividens (CD). Bar, I mm. (c) Scanning electron micrograph of the heart of a wolf (Can r's lupus) neonale

the caudal vena cava illustrating the septum primum (SI) collapsed over and closing the foramen ovale' Note the crista divi

I mm.

along the dorsal side of the fold. The red fox (Vulpes

vulpes) had a fold of tissue representing the septumprimum which was thin and ended in a straight edge(Fig. 3d). There was a pulmonary vein emptying into

the atrium close to the interatrial septum and the

attachment of the caudal vena cava. A similar

situation pertained in the dhole (Cuon alpinus).However, the length of the septum primum fold of

tissue was insufficient to cover the foramen ovale in

the specimen studied (Fig. 3/).

Ursidae

In the brown bear (Ursus arctos) the septum primum

fold was large enough to cover the opening (Fig. 3b).There was also evidence of a fibrous substrate from

the slight wrinkled appearance of the tissue underlyingthe endothelium. This was also apparent in the sample

from the grizzly bear (Ursus arctos horribllts) (Fig.

3g). The septum primum fold of the polar bear was

fenestrated, and had 3 holes situated along the straight

leading edge of the septum primum (Fig. 3r). Two of

the holes appeared to be formed from a single opening

bridged by a thread of tissue extending from the

unfenestrated main portion of the flap to the leading

edge; the third hole similarly appeared to be separatedfrom the adjacent opening by a single thread of tissue'

There were no holes in the septum primum of either of

the 2 bears ofunknown species. Both appeared to be

in the later stages of closure. In both animals the

attachment to the interatrial septum was made near

the crista dividens and therefore because the distal end

of the flap was not anchored to the interatrial septum'

it formed a narrow pouch. There was a largepulmonary vein emptying into the atrium close to the

interatrial septum and the attachment of the caudal

vena cava; its blood flow appeared to be

along the dorsal surface of the tissue flap-

Hyaenidae

The hyaena septum primum was thin and

enough to cover the foramen. The way in

wrinkles were arranged in this fold of tissue

that the endothelial surface covered fibrous

nonfibrous tissue (Fig. 3e)' There was a

vein emptying into the atrium close to the i

septum and the attachment of the caudal

Closure of the foramen ovale

Collapse of the 'tunnel' of the septum

closure of the foramen ovale in most of thc

studied (Figs 2d-f, 3c,g,h, 4c). ln a

neonates the 'tunnel' had either notbeen fixed in an open position. Closureproduced by the tissue fold hinging along

edge of the opening which was adj

terminal portion of the caudal vena

attached, the fold appeared to be

interatrial septum along that surface of

dividens which lay in the left atrium. The

at the end of the 'tunnel' remnant was

attached and, when gently lifted, formed

blind-ended pouch back to the fold's

the crista dividens (Figs 2d,f, 3 c, g, h, 4cl-

D I S C U S S I O N

The primary function of the foramenheart of the fetus is to conveY ox

returning from the placenta, into the left

Cardiac foramen ovale in carnivores

LuuuLr*- -rereby to supply oxygen to the coronary

Irr s*. 'nd the brain (Rudolph, 1985). There are very

r'',h !.-,runts of the anatomy of this cardiac structure

il re-res other than man and a number of theriL{ilundr;J animals (Mosca, l9l4; Franklin et al. 1942'llliltu:l;.r.ri:, t a]r.1944 Macdonald et al. 1988). Before therilnnrpflriat- study almost nothing of a detailed com-'lillltirilr[--n 3 nature appears to have been published on the

ilLiltnw.:.r: ,iith regard to the carnivores. Brief accountsrrr -[ ]!$---t ons of the foramen ovale (or its neonatalililnilrf,rDi,i-::i in the domestic cat (Felis domestica), lion

rlr|lLr tr.,,. tiger (Neofelis tigris), domestic dog (Canis'11r1rlr1il|lml[J"r,i,r.i'"--,r. red fox (vulpes vulpes), brown beat (ursus

rirrr;i,r .-,d spotted hyaena (crocuta crocuta) were

: b1' Simi6 (1938), Franklin et al. (1942),' r zrl. (1944), Franklin (1946) and Schiller

"'lllluc m::cnt study has demonstrated that the general: -': the septum primum in the cats, dogs,

umc rvaena examined differs from that seen ln:i:he domestic animals (Franklin et al. 1942::"- t',. 1944; Macdonald et al. 1988). The distal' ' ' " " " / '

Lrr :tr septum primum was straight-edged in all.iul!r-rr-,,-rres and did not feature the network of

oeen in the cow, sheep and horse. Its tunnel-

:rire was similar in general shape to that seenr,urldir ::gs. but much shorter in relative length

r-c. 1988, 1994).By contrast, its size seemed

$n :-r than the simple flap of tissue seen in the

F::ten, 1931). Few precise details are avall-Lir ,r :,;her members of the Order Carnivora.

, similarity of shape may be deduced fromilsrurr.ilon of the heart from a 3-v-old huntineL i : i,-rr! pictus) and the descriptions of the closed

:''"ale in a 1-month-old spotted hyaena;,:st and an oriental small-clawed otter

n, "ror€a) (Macalister, 1873).lrlimrme :ierences in the lensth of the tunnel-like

'ilrrc a ere observed between individual animals.

:he source of these differences may have

mi,r: ;losely related to differences in the stage oft of the animal rather than to any inherent

' differences. Support for this possibility:::: recent studies in the rat; there is a spurt-- -: the length and thickness of the septum: - ,d at the time of birth (Momma et al. 1992).: ::rterpretation may be made of some of the

:r.rm the present study; intraspecies dif--: the length and thickness of the septumr.tre seen in the newborn lion. tiser and fox

lllllflm urs,-,rlogical structure of the tissue fold was not

241

in other species, however, and cardiac muscle has been

found beneath the endothelial layer in the human,

horse and sheep fetus (Patten, l93l1' Leach, 1940;

Macdonald et al. 1988). One experiment demonstratedthat the fold of tissue from newborn lambs if rapidlyremoved could be observed to contract rhythmicallyin vitro (Barclay & Franklin, 1938). We detected thepresence of wrinkles on the endothelium of the septumprimum in each of the carnivore families studiedwhich was consistent with cardiac tissue also beingpresent as the substrate of the septum primum in thecarnivore fetus and neonate. However, these obser-vations are at odds with the comment by Simid (1938)

that no cardiac tissue was present in the membranesealing the foramen ovale of her I wk lion.

Physiological studies carried out on the lamb fetushave shown that it is blood from the umbilical vein,traversing the ductus venosus and hepatic veins, andpreferentially entering the left heart via the foramenovale, which supplies the coronary arteries and brain(Edelstone & Rudolph, 1979; Rudolph, 1985). Theseobservations supported earlier views derived fromanatomical and early physiological studies of the catfetus, that the crista dividens at the entrance to theheart (Figs I B, 2a, b, 3f, 4b, c) divides the blood flowtravelling within the thoracic part of the caudal venacava into 2 streams, one being directed into the rightatrium and the other through the foramen ovale intothe left atrium (Windle & Becker, 1940; see Amorosoet al. 1942). Recent ultrasonographic studies on thehuman fetus have demonstrated that blood from theductus venosus and left hepatic veins flows directlythrough the foramen ovale to the left atrium (Kiserud

etal.1992). The topographic anatomy of the carnivoreheart and the tunnel-like construction of the septumprimum would suggest that, as in man and thedomestic ungulates, the foramen ovale of the carni-vore fetus functions to shunt the more highlyoxygenated blood returning from the placenta intothe left atrium and thus to the coronary arteries andthe brain.

The results of the present study also show that thestructure of the neonatal carnivore's septum primumis such that it normally ensures closure of the foramenovale after birth; the tissue fold was unfenestrated inall the specimens studied with the exception of thepolar bear (Fig. 3 fr), and its size was sufficient to coverthe opening in all instances with the exception of thedhole (Fig. 3fl. The arrangements of the pulmonaryveins in the roof of the right atrium also seemed to bepositioned in such a way as to facilitate the flatteningof the tissue fold over the foramen by the rush ofblood returning to the heart from the inflated lungs.*li in the present study. It has been examined

242 A. A. Macdonald and M' Johnstone

The results of a study carried out by Chausse (1916)

demonstrated that the foramen ovale was successfully

closed in all but 5oh of the 62 neonate dogs studied'

In a more recent study, Oliviera et al. (1980) suggested

that the process of functional closure was very rapid

with closure occurring within 48 h in 72 % of the dogs

studied, and complete closure being achieved in all

subjects by 21 d after birth.

The site of anatomical closure of the flap of tissue

is not indicated in these reports. However, Macalister

(1873) found during the dissection of an oriental

small-clawed ottet (Aonyx cinerea) that 'the foramen

ovale is closed, but in the left auricle the upper edge of

the crescentic valve (of the foramen ovale) is not

attached, and allows of a blowpipe being introduced

for a short distance'. Similar observations were made

for the tiger and hunting dog(Lycaon pictus) by Simi6

(1938), and have been seen in a number of species

during the present study. These results indicate that

the site of anatomical closure is likely to be that part

of the crista dividens lying in the left atrium' The

mechanism by which adhesion occurs between the

septum primum and the interatrial septum remains

unclear.The lack of significant differences between the

carnivore species studied was not expected' Recent

studies of the phylogeny of the carnivora have

indicated a closer relationship between the Felidae

and the Hyaenidae, and between the Canidae and the

Ursidae than between the members of either of these

larger groupings (Wozencraft, 1989; Wyss & Flynn,

1993). The anatomical similarities between the for-

amen ovale of these 4 families may be instructive' The

potential usefulness of placental and other fetal

membranes in assessing phylogenetic relationships

above the family level has been recognised for some

time (Mossman, 1937, 1953, 1987)' The relative

conservatism of morphology of fetal membranes, and

the reason why significant differences in placental

structures are rarely found within families may be

explained by the concept that the growth and function

of these structures is restricted to the environment of

the uterus, and therefore not directly subject to the

selective pressures of the external environment(Mossman, 1953, lg87). Similar arguments may be

extended to an analysis of foramen ovale morphology'

In conclusion, the results of this study demonstrate

that the shape of the septum primum flap of tissue in

a range of carnivore species was similar and appeared

to be consistent with that found in other families of

carnivores. It formed a somewhat longer tunnel than

is found in the human heart but was shorter than

those of the pigs and peccaries' It was more

significantly different from those seen in

and equids. The anatomy of this fold

drainage from the lungs such that when

expand with air at birth, the mass flow of

appeared to be arranged in relation to

from the pulmonary veins into the left

contribute to 'blowing' the flap over

opening, thereby functionally closing the

A C K N O W L E D G E M E N T S

institutions: Kibun Binatang, Surabaya;

Museum; Natural HistorY Museum,

We gratefully acknowledge the assistance g

"rr.utott and administrative staff of thc

This project was supported in part by thc

Trust-. the Carnegie Trust for the Unir

Royal Zoological Society of Scotland;

Museum, Bogor; das Zoologisches Museu

Undergo at Birth' Oxford: Blackwell'

CnausssP (1916) Recherches sur la persistane drr

fiir Naturkunde der Humbolt-UniversititThe assistance and technical expertise of

S. Mitchell and C. Warwick are much

Scotland, the Balloch Trust and the

Edinburgh.

R E F E R E N C E S

Auonoso EC, Blnclev AE, FnlNrr'rN KJ,

The bifurcation of the posterior caval channel i

foetal heart. Journal of Anatomy 76' 240_247 '

Blncr.ev AE, FneNruN KJ (1933) The time of

of the foramen ovale in the lamb. Joumal d25G258.

BARcLAY AE, FuNruN KJ, Pntcnlno MML (

Circulation and Cardiovascular System, and the

chez quelques animaux domestiqtue. Compte

des Sciences, Paris 162,48G481'

Connr.r AL (1979) Critical point drying principles

Scanning Electron Microscopy 2, 303-323'

Consrrr GB, Hrr.r JE (1991) A World List of

system in the viable foetal lamb Journal of A

M,rc,lt-nrtn A (1873) On the anatomy of Aonyx-

3rd edn. London: British Museum (Natural

EcHLIN P (1975) Sputter coating techniques for

microscopy. Scanning Electron Miuoscopy 2'

EosI-sroNp DI, RuoorpH AM (1979) Preferenti{

ductus venoqus blood to the brain and hearr

American Journal of Physiology 231 , H'|T+HT!'-

FRANKTIN KJ (1946) Patent foramen ovale and

a lion cub. Journal of Anatomy 80' 209'

FuNrln KJ, AMoRoso EC, BencrlY AE,

The valve ofthe foramen ovale and its relation to

entries. Vetirinary Journal 98' 2941'

Krssruo T. Erc-NnsSH, Brl,ls HG, Hslrnvrr LR

ovale: an ultrasonographic study of its relatim

vena cava, ductus venosus and hepatic veirs'

Obstetrics and Gynecology 2, 389-396'

Llecn EH (1940) Footnote. 1n Fr'rNrunt KJ'

Prichard MML. Some observations on the

Roval lrish Academy, Ser 2, l, 539-54'7 '

Cardiac foramen ovale in carnivores

i l r r r , . " -p AA (1988) Comparat ive anatomy of the foramen', rru - :he Snina. Anatomy and Embrl,olsgy l7g, 53 57.

ri,i,ri t' .-D .{A (1994) The placenta and cardiac foramen ovale ofrllrf :i!:.:-isa (Babyrousa babyrussa). Anatomy and Embryology,1 :r-:": :

rilillrrilLrr' , ) -{A, FoworN AL, Oussv J, Srrvnn M, RossoerB pDre i -:-i foramen ovale of the letal and neonatal foal. Equinerrrrr,,'- i ' j-; Journal 20.255 260.

Nttirumir.- :'. Iro T, MoRr y, yAlaalruu y (199D perinataliuuuurlrr'i .: of the cardiovascular system. Early Human De-r ' r i rh 1n: : : 29. 167 l '70.

rilllllLlrlttliil + r. -911) Sulla conformazione della valvola del foro ovaleruilr ;r.:: di alcuni animali domestici. Atti detta Societd deirdfrrr', :: e Matematici, Modena l, 10_24.

Itlllttumruw; .l\\' (1937) Comparative morphogenesis of the fetalrllrul!10lrffr-l_ :s and accessory uterine structures. Contributions to

rfililMmftl+. :i\. t1953) The genital system and the fetal membranesru :riir'rr;-: ,or mammalian phylogeny and taxonomy. Journal ofittunmm-. :: 34,289 298.

rlillil@ttu$i -:- ,\- t1987) Vertebrate Fetal Membranes. New Brunswick.Lrlt]liillMll r*,.:. : Rutgers University Press.

rl]llttltu{{is'.r,L I. \'_.\N{,{Moro K, Irostrrsue T, InrNo S ( 1977) Modified,fiumm-: -(:_:um conductive staining method for non-conductivelri.ttttut ,:r:imens. Archives oJ Histology and Cytologv 40, 35 40.

tllurlrI|u]u0rrw r,j l. Prrro p, SrLvA E, Onsr AM, Mrlro Drls S, Drrmr

z+)

RM (1 980) Observaciones anat6micas sobre el cierre del foramenoval en el perro (Canis familiaris). Zenttalblatt ftir Veterindr-medizin C Anqtomia, Histologia, Embrvologia 9,321 324.

Orrowey CW (1944) The anatomical closure of the foramen ovalein the equine and bovine heart: a comparative study withobservations on fetal and adult states. Veterinary Journal 100,1 i 1 - 1 1 8 , 1 3 0 - 1 3 4 .

Orrowny CW (1949) Patent foramen ovale in a puppy. VeterinaryReco rd6 l , 503 504 .

PrrraN BM(1931) The closure of the foramen ovale. AmericanJournal of Anatomy 48, 1944.

Runorps AM (1985) Distribution and regulation of blood flow inthe fetal and neonatal lamb. Circulation Research 57, 8ll 821.

Sculrren HJ (1959) Das Herz des Lowen (Felis leo L.). Morpho-logisches Jahrbuch 100, 163-184.

Srunj V (1938) Zur Anatomie des Carnivorenherzens. GegenbaursM o r p ho lo g is c he s J ahrb uc h 82. 499,536.

WINTTE WF, Bocxnn RF (1940) The course of the blood throughthe fetal heart; an experimental study in the cat and guinea pig.Anatomi(al Record 71, 417426.

WozrNcnmr WC (1989) The phylogeny of the recent carnivores. InCarnivore Behavior, Ecology, and Evolution (ed. J. L. Gittleman),pp.495-535. London: Chapman and Hal l .

Wyss AR, FryNN JJ (1993) A phylogenetic analysis and definitionof the carnivora. ln Mammal Phylogenlt; placentals (eds F. S.Szalay, M. J. Novacek & M. C. McKenna), pp. 32 52. NewYork: Springer.