Evolution ofthe Ventricles

Solomon Victor, FRCS, FRCPVijaya M. Nayak, MSRaveen Rajasingh, MPhil

We studied the evolution of ventricles by macroscopic examination of the hearts ofmarine cartilaginous and bony fish, and by angiocardiography and gross examination ofthe hearts of air-breathing freshwater fish, frogs, turtles, snakes, and crocodiles.A right-sided, thin-walled ventricular lumen is seen in the fish, frog, turtle, and snake.

In fish, there is external symmetry of the ventricle, internal asymmetry, and a thick-walled left ventricle with a small inlet chamber. In animals such as frogs, turtles, andsnakes, the left ventricle exists as a small-cavitied contractile sponge. The high pressuregenerated by this spongy left ventricle, the direction of the jet, the ventriculoarterial ori-entation, and the bulbar spiral valve in the frog help to separate the systemic and pul-monary circulations. In the crocodile, the right aorta is connected to the left ventricle,and there is a complete interventricular septum and an improved left ventricular lumenwhen compared with turtles and snakes.

The heart is housed in a rigid pericardial cavity in the shark, possibly to protect it fromchanging underwater pressure. The pericardial cavity in various species permits move-ments of the heart-which vary depending on the ventriculoarterial orientation and needfor the ventricle to generate torque or spin on the ejected blood- that favor run-off intothe appropriate arteries and their branches. In the lower species, it is not clear whetherthe spongy myocardium contributes to myocardial oxygenation. In human beings,spongy myocardium constitutes a rare form of congenital heart disease. (Tex Heart InstJ 1999;26:168-75)

W e describe our macroscopic and angiocardiographic findings related to

the evolution of the cardiac ventricles in fish, frogs, snakes, turtles, andcrocodiles. In addition, we discuss ways in which the ventricular devel-

opment in these animals relates to that in human beings.

Materials and Methods

Key words: Animal;evolution; heart/anatomy;heart ventricle; myocardium;regional blood flow;ventricle, single; ventricle,spongy

From: The Department ofCardiovascular Surgery,The Heart Institute,Chennai- 600 010, India

Address for reprints:Solomon Victor, FRCS,FRCF? 15 East Street,Kilpauk Garden Colony,Chennai - 600 010, India

C 1999 by the Texas HeartsInstitute, Houston

The anatomical terms are applied herein as they are in human anatomy and can beenvisioned by imagining the animal held head-up with the belly facing the observ-er.

Fish. The hearts of 24 marine cartilaginous fish (12 hammerhead sharks, 6 dogsharks, and 6 tiger sharks) and 6 marine bony fish (Scomberemorus commersonii)were studied by laying each fish on its back and opening the pericardial cavity bymeans of a vertical midline incision. The truncus was divided longitudinally andthe incision was continued caudally into the right-sided lumen of the ventricle.Transverse and coronal sections of the ventricles were examined macroscopically.The heart was studied similarly in 6 air-breathing freshwater fish, Channa striata,

which can survive outside water due to an accessory nongill respiratory appara-

tus. Each of these freshwater fish was anesthetized with ketamine, after which oxy-

gen was insufflated into the oral cavity. Angiocardiography was performed using a

digital computerized imaging system, with contrast medium injected through theduct of Cuvier. Later, the heart was dissected in the same manner as were those ofthe marine fish.

Frogs. Twelve frogs were anesthetized with the use of ether, and anesthesia was

maintained with oxygen and ether. The frogs were intubated and were manuallyventilated by digital closing and opening of a hole in the inlet tube. Each frog waslaid on its back, and its heart was explored through a ventral midline incision in

the chest wall and pericardium. Angiocardiography was performed by injectingcontrast medium into the ventral abdominal vein, hepatocardiac channel, sinus

venosus, pulmocutaneous branch, and left atrium. Later, the truncus and bulbus

168 Evolution of the Ventricles

GuestEditorial

Volume 26, Number 3, 1999

were incised longitudinally, and the incision wascontinued along the inferior border of the heart intothe lumen of the ventricle. Coronal and transversesections of the heart were examined macroscopically.

Turtles and Snakes. Six pond turtles and 4 ratsnakes were anesthetized with the use of ether in-halation, followed by intubation and ventilation aswas done in the frogs. The heart was exposed byremoving the ventral plate of each turtle and by aventral midline incision in each snake. The peri-cardium was then opened. Angiocardiography wasperformed with the contrast medium injected man-ually into the right or left atrium, and images wereobtained by digital computerized imaging. The pul-monary artery was incised longitudinally, and theincision was extended into the right ventricle. Acoronal section of the ventricle was then obtainedthrough the ventricular septal defect. Anterior andposterior flaps of the ventricle, thus created, facili-tated macroscopic inspection of the ventricular lu-men and wall, related arteries, and valves.

Crocodiles. Two crocodiles were anesthetized withketamine, followed by intubation and manual venti-lation. Each heart was exposed through a ventralmidline incision. Angiocardiography was performedby manual injection of contrast material into theright or left atrium with the use of digital computer-ized imaging. Later, the right ventricle was examinedthrough a longitudinal incision, which was begun inthe pulmonary artery and extended into the lumenof the right ventricle. The left ventricle was exposedthrough a long-axis incision close and parallel to theanterior descending coronary artery; the left ventric-ular wall and the mitral and aortic valves were exam-ined macroscopically.

Findings

Marine Cartilaginous Fish. The heart of the marinecartilaginous fish (hammerhead shark, dog shark,and tiger shark) is housed in a pericardial cavity witha ventral wall that also serves as a cartilaginous chestwall. The heart is symmetrical, with 2 ducts ofCuvier. There is a large venous sinus under the sep-tum transversum between each lobe of the liver andthe corresponding hepatic vein. The sinus venosus istriangular, and its caudal wall is adherent to thetransverse septum. There is a common atrium thatbears isomeric appendages on either side. Externally,the ventricle has right and left faces separated by ananterior ridge, along which runs a coronary arterythat resembles morphologically the left anterior des-cending coronary artery in a human being.A conical bulbar chamber leads craniad to a trun-

cus arteriosus. We use the term bulbus to refer to thischamber, which is visibly demarcated from the main

ventricle and is caudal to the row of craniad semilu-nar valves. Downward extension of the longitudinalarteriotomy opens the bulbus, which has 3 longitu-dinal ridges. Caudal to the bulbus, there is a ventric-ular lumen in the right side of the externallysymmetrical heart. This lumen is the morphologicequivalent of the human right ventricle. Its innerwall has a curvilinear band with anterior trabecula-tions, resembling the trabecula septomarginalis seenin the right ventricular surface of the mammalianand human interventricular septum. This band bor-ders a ventricular septal defect that leads through anoblique passage, craniad to the leftwardly situatedcommon atrioventricular orifice. The left side of theventricle consists of spongy myocardium with nolumen except for a small chamber beneath the com-mon atrioventricular orifice. This chamber commu-nicates with the right ventricular lumen through theventricular septal defect. The common atrioventric-ular orifice has 2 bridging leaflets connected toprimitive papillary muscles on either side, with in-tervening chordae tendineae.Marine Bony Fish. In the marine bony fish

(Scomberemorus commersonii), the heart is medianand symmetrical. The pericardial sac is fibrous allaround and is detached from the chest wall. Thehepatic veins drain directly from the liver into thesinus venosus without an interposed venous sac.Craniad to the ventricular chamber is an onion-bulb-shaped chamber that is the conus, separatedfrom the ventricle by a tricuspid semilunar valve. Weuse the term conus to denote a chamber that is crani-ad to the semilunar truncal valve and has no intrin-sic contractility. Caudal to the semilunar valve is apitted bulbar septum. There is no trabecula sep-tomarginalis. The common atrioventricular orificewith 2 bridging leaflets is nearly flush with the innerwall of the ventricular lumen, which is right sided.The left wall of this chamber and the apex of theventricle are thick walled and without a lumen,except for a tiny inlet chamber that communicateswith the right ventricular lumen. The conus contin-ues as a truncus, which is devoid of the lateralbranches evident in the marine cartilaginous fish,except near its termination.Air-Breathing Freshwater Fish. The heart of the air-

breathing freshwater fish is externally symmetrical.A median dorsal ridge develops inside the sinusvenosus at the junction of the 2 ducts of Cuvier. Thesinus venosus is less dominant than that seen inmarine fish. A common atrium with 2 appendagesopens through a left-sided common atrioventricularorifice into the right-sided lumen in the ventricle.The left wall of this ventricular lumen is thick andspongy. There is a left-sided inlet chamber that issmall and smooth (Fig. lA). During angiocardiogra-

Evolution of the Ventricles 169Texas Heart Institutejournal

phy, not only the right-sided lumen but also thespongy left wall of the ventricle fills with contrastmedium (Fig. 1 B). The contrast from the lumen andthe spongy wall is ejected into the truncus, whichhas an elastic dilated conus shaped like an onion

"Truncus

Ventricle

Fig. 1 A) The conus and lumen of the "right" ventricle of afreshwater fish (Channa striata) is opened longitudinally,revealing the spongy left wall and a small inlet chamber ofthe "left" ventricle (LV) beneath the common atrioventricular(AV) orifice. B) Angiocardiogram of a freshwater fish revealscontrast material filling the entire spongy "left" ventricle andthe lumen of the right ventricle.

bulb. The conus is distended during ventricular sys-tole and is emptied during ventricular diastole.

Frog. The frog heart is asymmetrical, due to a D-loop. The bulbus is situated on the right side and hasa spiral valve inside. The spiral valve is situatedbetween the 2 rows of semilunar valves at the caudaland craniad limits of the bulbus. The ventricle has athin-walled lumen on the right side and a left wallthat is spongy with no cavity. Contrast medium emp-ties from the right atrium into the lumen of theventricle and is ejected through the bulbus into thepulmocutaneous branch, guided by the spiral valve.Contrast material from the left atrium is absorbedby the spongy left wall of the ventricle during dias-tole (Figs. 2A and 2B). During systole, the spongesqueezes its contents through the bulbus (Fig. 2C)into the carotid and systemic arteries. Figure 3Ashows that during diastole the spongy "left" ventricleis pink with oxygenated blood and the cavitied "right"ventricle is dark with deoxygenated blood. Duringsystole, both ventricles become pale (Fig. 3B).

Turtle. In the turtle, the entire heart lies to theright of midline to accommodate the retractile neck.Two atria are separated by a complete interatrial sep-tum. In addition, there are 2 ventricles, each with asmooth inlet chamber and a spongy wall. No conusor bulbus is seen. The 2 inlet chambers conjoinacross a ventricular septal defect. The spongy wall ofthe right ventricle is thin, whereas that of the leftventricle is thick. From the lower edge of the inter-atrial septum, 2 leaflets are suspended, resembling aSt. Jude bileaflet mitral valve. Rudimentary papil-lary muscles are also present.During diastole, the 2 leaflets hang down, block

the ventricular septal defect, and separate the inletchambers. Contrast medium flows from each atri-um into the corresponding ventricle, filling therespective inlet chambers and soaking their spongywalls. Two aortae and 1 pulmonary artery areanatomically connected to the right ventricle.During systole, the right and left leaflets ofthe atrio-ventricular valve close the corresponding atrioven-tricular orifices. The left ventricular sponge squeezesits contents across the ventricular septal defect andthrough the right ventricular inlet chamber into the2 aortae. A bulbotrabecular septum helps the venousblood make a U-turn from the inlet of the right ven-tricle into the outflow tract and the pulmonary ar-tery.

Snake. The snake heart lies largely to the left ofmidline and has an asymmetrical ventricular masswith no bulbus or conus. Three intertwined vesselsemanate from the base of the heart. Two atria arecompletely separated by the interatrial septum,which suspends a bileaflet valve similar to that in theturtle. The right ventricle has a large lumen and a

170 Evolution of the Ventricles Volume 26, Number 3, 1999

LA

LV

Fig. 2 Angiocardiogram of a frog shows contrast medium from the left side of the atrium (LA) coursing through radial passages inthe spongy "left" ventricle during early ventricular diastole (A). The left ventricular (LV) sponge is fully soaked during ventricular enddiastole (B), and ejects during systole (C) through the bulbus (arrow) and the 2 divisions of the truncus (arrowheads) into thesystemic circulation.

thin spongy wall. There is a bulbotrabecular septum.The venous blood flows ventral to this septum into

- , _,;,: ;Uthepulmonary artery. The left ventricle is a thickdense sponge except for a tiny smooth inlet cham-ber (Fig. 4). The left ventricle fills with blood dur-ing ventricular diastole (Fig. 5). During systole, thesponge then ejects its contents across the ventricularseptal defect and the inlet of the right ventricle intothe 2 aortae, which are anatomically connected tothe right ventricle (Fig. 6).

Crocodile. The heart of the crocodile lies largely tothe left of midline and is asymmetrical. The septa-

B t v tion of the atria and ventricles is complete. The rightaortic arch is connected to the left ventricle, and the

;-~~_left aortic arch and the pulmonary artery are con-nected to the right ventricle. The 2 aortae and the^, 6,;_pulmonary artery are intertwined.Under experimental conditions, contrast medium

ejected from the right ventricle flows only into the.. - _pulmonary artery and does not enter the left aorticarch, which is anatomically connected to the rightventricle. Contrast material ejected by the left ven-tricle opacifies both aortae; the right aortic arch fills

_ _.....theleft aortic arch through the foramen of Panizza,which connects the 2 aortae close to their origin.The left ventricle has a good-sized lumen with a rel-atively thick wall, partly spongy and partly compact(Fig. 7). The papillary support for the mitral valve isdevoid of chordae tendineae and is close to the

-Li_ leaflets in the upper third of the ventricle. The rightventricle also has a good-sized lumen, but with a

thin wall. There is a cogwheel type of infundibularfig. 3 A) During diastole, the spongy"left" ventricle (LV) is valvular mechanism reported earlier that shuts offpink with oxygenated blood and the nrght" ventnicle (RV) Isdarker with deoxygenated blood. B) Both the "right " and the the pulmonary circulation when the crocodile is"left" ventricles of the frog become pale during systole. under water, to enable the right ventricle to eject its

contents into the left aortic arch. I

Evolution of the Ventricles 171Texas Heart Institutejournal

Fig. 4 Coronal section of a snake heart, showing the spongyleft ventricle (LV), with a very small inlet chamber beneath theleft atrioventricular (AV) orifice.

Fig. 5 Contrast flows from the left atrium (LA) into the leftventricular sponge of the snake through radial channels duringearly ventricular diastole (A). The left ventricle (LV) is fullysoaked during late diastole (B).

Discussion

Pericardial CavityMarine cartilaginous fish have a rigid cartilaginouspericardial cavity, possibly to protect the heart againstthe variations in pressure that occur under water atdifferent depths. Large venous sacs in the hepaticvenous system act as capacitance reservoirs and help

the venous circulation adapt to changes in pressure.2Conversely, marine bony fish and freshwater fish,which do not dive to great depths, have a fibrouspericardium, and the capacitance sacs are absent fromthe hepatic venous system. Instead, the venous sacsare situated at the confluence of the cardinal veins,on either side.The role of variable intrapericardial pressure levels

during the cardiac cycle has received scant attention inresearch. Negative intrapericardial pressure duringventricular systole may possibly aid venous returnthrough an "aspiration" effect.3 4The pericardial cavityalso allows complex movement of the cardiac cham-bers-that is, it permits rotary movement of the leftventricle-which provides varying torque or spin tothe ejected blood. This spin creates appropriate flowpatterns for the blood to smoothly negotiate the curveof the aorta and its branches.5 The flow pattern variesfrom species to species. In fish with a straight truncus,the twist is not apparent. In human beings, the twist-ing of the left ventricle is obvious and is responsiblefor the complex pattern of blood flow in the aorta andits branches.5 The right ventricular mechanism isadapted to lower pressure and to the simpler arrange-ment of the pulmonary arteries. The carina-like fork-ing of the pulmonary artery clearly aids smooth flowinto its right and left branches.

Two VentriclesFish,6 frogs,7 turtles, and snakes8,9 are generally con-sidered to have single ventricles.6,10-13 This erroneousimpression has arisen because only the visible singlelumen inside the ventricle has been taken into ac-count and not the presence of a contractile, spongyleft ventricle.The inner wall of the "single" lumen in the heart of

the fish clearly bears a trabecula septomarginalis and,hence, constitutes the right ventricular surface of theinterventricular septum. There is no lumen on theleft side of the septum. Instead, the left side of theventricular wall is thick and spongy and representsthe noncavitied left ventricle. There is a chamberbetween the common atrioventricular canal on theleft and the ventricular septal defect bounded by thetrabecula septomarginalis. This is a small, left ven-tricular inlet chamber that communicates with theright ventricular lumen through the ventricular sep-tal defect.During ontogeny, the human heart bears similari-

ties to that of the fish, including a small-cavitied leftventricle. It is of interest that angiocardiography inthe live fish reveals a spongy "left" ventricle that alsofills with contrast material. Although we have notbeen able to study the heart of lungfish,6,13 it is likely,in light of our angiocardiographic findings in frogs,turtles, and snakes, that the spongy left ventricle in

172 Evolution of the Ventricles Volume 26, Number 3, 1999

LA:a

LV "

.4

.-

W.

A::

A.]

Fig. 6 The spongy left ventricle (LV) of the snake, seen in the lateral view during early (A), mid (B), and late systole (C). The contrastflows from the left ventricle through the ventricular septal defect into the 2 aortae seen overlapping each other (arrow) connectedto the right ventricle.

LA = left atrium

Fig. 7 Thick spongy wall of a crocodile' left ventricle (LVW witha good-sized lumen.

the lungfish would facilitate ejection of arterial bloodinto the cranial circulation, aided by septation in theoutflow tract.

Features of the frog heart are similar to those of thefish, with a single ventricular lumen, an inner trabec-ulated surface, and a thick-walled spongy left ventri-cle with no lumen (as shown by angiocardiography).The D-loop displaces the bulbus to the right side,between the right and left atrial appendages. Foxonand Walls7 have speculated about how the "single"ventricular lumen handles both venous and arterialblood. Our angiocardiographic study reveals a clearseparation of systemic and pulmonary circulations inthe anesthetized, ventilated frog.The turtle and the snake also appear to have a sin-

gle ventricular lumen.6,8,9,12 This lumen consists of a"cavum venosum" (right ventricular inlet) beneaththe venous atrioventricular orifice, a "cavum arterio-

sum" (left ventricular inlet) beneath the arterial atrio-ventricular orifice, and a "cavum pulmonale" (rightventricular outlet) beneath the pulmonary valve.Amid speculation8 9 about the way in which the arte-rial and venous blood are separated in a single ven-tricular chamber, White8 postulated that a muscularridge of an incomplete interventricular septumopposed the ventral wall and helped to divide thecavum pulmonale from the cavum venosum. Thus,purely venous blood was thought to enter the pul-monary circulation. It was assumed that the rightaortic arch received the arterial blood and the leftarch received mixed venous blood. However, oxygen-saturation studies3 have shown that both aortae carryoxygenated blood. Our angiocardiographic findingsconfirm that the pulmonary and systemic circula-tions are separate in anesthetized, ventilated animals.Angiocardiography also shows that the cavum arte-riosum beneath the arterial atrioventricular orificeaccommodates only a fraction of the left atrial blood,which is largely absorbed by the spongy left ventricle.The ventricle ejects this blood into the 2 aortae, usingthe cavum arteriosum and the cavum venosum as itsoutflow tract.The hearts of the turtle and the snake, then, have a

right ventricle with a large lumen and a thin free wall.The "left" ventricle is largely spongy with a smallinlet chamber. The right ventricular surface of thespongy left ventricle is the right surface of the bulbarand trabecular components of the interventricularseptum with an anterior cavum pulmonale. The sinusand membranous components of the interventricularseptum are absent, resulting in a ventricular septaldefect. This defect connects the cavum arteriosumand the cavum venosum, which serve during systole

Evolution of the Ventricles 173Texa-s Heart Institutejournal

as the outflow tract for the spongy left ventricle.During diastole, the atrioventricular valve leafletshang down and functionally separate the cavumarteriosum from the cavum pulmonale, divertingthe venous and arterial blood to the appropriate ven-tricles. The thick spongy wall of the left ventricleabsorbs the left atrial blood.

Role of the SpongeA question arises with regard to the sponge that con-stitutes the left ventricle in these species: is itdesigned to pump, to facilitate myocardial oxygena-tion, or both? Angiocardiography confirms thepumping action. These species have coronary arter-ies. In fact, fish have a morphologic equivalent ofthe human left anterior descending and right coro-nary arteries that can be identified easily. Theoxygenating function (if any) of the spongy myo-cardium needs to be studied and correlated with theoxygenation of the endocardial surface ofthe humanheart. The existence of sinusoids in the humanmyocardium is disputed.'4 More information is nec-essary in order to establish whether the sinusoids, ifpresent, are related to the spaces in the spongymyocardium in the process of evolution. Trans-myocardial revascularization through mechanicalchannels, created with needles or lasers, has beencompared to the natural myocardial perfusion insnakes.'5 Although we are certain of the ejectionfunction of the sponge, we do not know whether thespongy structure oxygenates the myocardium.Moreover, crude channels cannot be equated withcomplex sinusoids. It should also be noted that inthe frog, snake, and turtle, the thick left ventricularsponge fills with oxygenated blood and the thinspongy layer of the right ventricular wall fills withdeoxygenated blood (Fig. 3A). If the sponge con-tributes to oxygenation, the right ventricle wouldneed to extract oxygen from the deoxygenatedvenous blood. Perhaps the thin wall of the right ven-tricle is perfused only by the coronary arteries. Inother species, such as the turtle and the crocodile,the ventral mesocardium persists as the gubernacu-lum cordis and supplies blood to the myocardium.

Human Spongy VentncleSpongy ventricle is a rare congenital heart disease inhuman beingsl6 and may present in adults. It is pos-sibly due to the persistence of the spongy myocardi-um seen in phylogeny and ontogeny. Genes relatedto the formation of the ventricles have been identi-fied.'7 These genes control the regression of thespongy myocardium, resulting in cavitation of theventricle. Of note, the resorption process leavesbehind competent chordopapillary support for theatrioventricular valves and exhibits an evolutionary

pattern that is evident in the valve design of variousspecies.18-20

Evolutionary Design and AnticipationWe conclude that there is a design in the evolutionof the venous connections of the heart,2' pectinatemuscles,22 atrioventricular valves,'8 left ventriculartendons,23 outflow tracts,24 and great arteries.25One neglected aspect in the study of evolution is

that of anticipation.26'27 Fish atria and ventriclesappear to have a built-in provision for becomingupdated to the human 4-chambered structure. Thistransformation is achieved in stages: the truncusyields the great arteries, appropriate shifting takesplace in the great arteries, the left ventricle decreasesin sponginess and increases in the size of its lumen,the chordopapillary apparatus becomes more sophis-ticated, the coronary circulation undergoes changes,and the ventricular septal defect closes. This evolu-tionary progression points to a master design andplan for countless millennia.

References

1. Axelsson M, Franklin CE. From anatomy to angioscopy:164 years of crocodilian cardiovascular research, recent ad-vances, and speculations. Comp Biochem Physiol 1997;1 1 8A:5 1-62.

2. Victor S, Raveen R, Nayak VM. Evolution of the liver andthe hepatic venous outflow. Third International Congresson the Budd-Chiari Syndrome [abstract]. Chennai, Febru-ary8-11, 1998:30-1.

3. Hughes GM. Comparative physiology ofvertebrate respira-tion. Cambridge: Harvard University Press, 1963:103-18.

4. Shabetai R. Diseases of the pericardium. In: AlexanderRW, Schlant RC, Fuster V, editors. Hurst's the heart, arter-ies and veins. 9th edition. New York: McGraw-Hill, 1998:2170.

5. Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Long-more DB. Helical and retrograde secondary flow patternsin the aortic arch studied by three-directional magneticresonance velocity mapping. Circulation 1993;88(5 Pt1):2235-47.

6. Robb JS. Comparative basic cardiology. New York: Grune& Stratton, 1965:49-50.

7. Foxon GE, Walls EW. The radiographic demonstration ofthe mode of action of the heart of the frog. J Anat 1947;81:111-7.

8. White FN. Circulation in the reptilian heart (squamata).Anat Rec 1959;135:129-34.

9. Johansen K, Hol R. A cineradiographic study of the snakeheart. Circ Res 1960;8:253-9.

10. Victor S, Nayak VM, Neelamani M, Raveen R, Kabeer M.Single ventricle is not single during evolution. IndianHeartJ 1996;48:551.

11. Victor S, Nayak VM, Raveen R. Evolutionary anticipationof biventricular status [abstract]. 13th Biennial Asian Con-gress on Thoracic and Cardiovascular Surgery. Sydney,Australia. October 1997:108.

12. Kotpal RL. Modern textbook ofzoology-vertebrates. 2ndedition. Meerut, India: Rastogi Publications, 1998:167,203.

174 Evolution of the Ventricles Volume 26, Number 3, 1999

13. Weichert CK. Anatomy of the chordates. 4th edition. NewYork: McGraw-Hill, 1970:548, 551, 553.

14. TsangJC, Chiu RC. The phantom of "myocardial sinusoids":a historical reappraisal. Ann Thorac Surg 1995;60:1831-5.

15. Sen PK, Udwadia TE, Kinare SG, Parulkar GB. Trans-myocardial acupuncture: a new approach to myocardialrevascularization. J Thorac Cardiovasc Surg 1965;50:181-9.

16. Shah CP, Nagi KS, Thakur RK, Boughner DR, Xie B.Spongy left ventricular myocardium in an adult. Tex HeartInstJ 1998;25:150-1.

17. Roberts R, Schwartz RJ. Principles of molecular biologyand cardiac development. In: Alexander RW, Schlant RC,Fuster V, editors. Hurst's the heart, arteries and veins. 9thedition. New York: McGraw-Hill, 1998:190.

18. Victor S, Nayak VM, Raveen R, Gladstone M. Bicuspidevolution of the arterial and venous atrioventricular valves. JHeart Valve Dis 1995;4:78-87.

19. Victor S, Nayak VM. The tricuspid valve is bicuspid. JHeart Valve Dis 1994;3:27-36.

20. Victor S, Nayak VM. Definition and function of commis-sures, slits and scallops of the mitral valve: analysis in 100hearts. Asia Pacific J Thorac Cardiovasc Surg 1994;3:10-6.

21. Victor S, Nayak VM, Raveen R. Evolution of the venousconnections of the heart. Asia Pacific Heart J 1998;7:59.

22. Victor S, Nayak VM. Musculi pectinati: design, functionand surgical considerations [abstract]. 13th Biennial AsianCongress on Thoracic and Cardiovascular Surgery. October1997:107.

23. Nayak VM, Victor S. Vestigial bands in the left ventricle.Asia Pacific Heart J 1997;6:121-3.

24. Nayak VM, Victor S. Conotruncal variations in the normalheart. Asia Pacific Heart J 1998;7:61.

25. Victor S, Nayak VM, Raveen R. Unfolding of the master-plan for evolution of the great arteries [abstract]. The 3rdCongress of the Asian Vascular Society, Beijing, China. May8-10, 1998:129.

26. Victor S. Acknowledging the intellect. Chennai: The HinduMagazine, December 7, 1997:2.

27. Victor S. Anticipation and planning in evolution. Bhavan'sJ 1999;45:63-6.

Editorial Commentary

Comparative Anatomy and Physiology:Evolution Revisited

Even though comparative anatomy of the cardiovas-cular system has been studied extensively for severalyears, communication between experts ofvarious dis-ciplines has still been quite limited. Such imperfectconditions nearly guarantee recurrent frustrationsand disparate conclusions, mainly due to the lack ofmethodological and semantic consistency and thelimited opportunities for interdisciplinary communi-cation and coordinated programs of investigation.The accompanying article about the phylogenetic

evolution of the ventriclesi illustrates this impasse.Victor and colleagues' present a fascinating andadmirable collection of individual observations.Their studies cross the treacherous borders betweenbasic biology (including the theory of evolution),comparative anatomy (applying both macroscopicand angiographic examination), comparative physi-ology (gathering information about oxygen satura-

tions, hemodynamic pressures, coronary physiology,myocardial metabolism, and adaptive changes in themarine environment), and comparative embryology(taking into account even recent concepts in molecu-lar biology and genetic control). While congratulat-ing Victor's group for their generous contribution, Iwould like to send out a call to interested investiga-tors concerning the need to abide by specific require-ments implicit in each discipline-both to overcome

the pitfalls of a Leonardo da Vinci-style instinctiveapproach to the study of nature, and to encourage an

interdisciplinary approach to the task of assimilatingthe progress of related disciplines.

Clearly, the theory of evolution cannot be revisitedtoday without considering the fundamental contri-butions of molecular developmental biology, as ele-gantly manifested in a recently published book on thesubject.2 The realization that genetic control of cellu-lar differentiation and morphogenesis transcends thespecificity of species presents a new opportunity toclarify the evolutionary theory of the cardiovascularsystem. Still, it seems appropriate to recognize thatsuch novel experiments as targeted gene ablation andrandom mutagenic screens can proceed safely andproductively only if the results of more traditionalmorphologic studies in anatomy and embryology aretaken into full account.3 At the same time, modernimaging techniques (including scanning electron mi-croscopy, angiography, echocardiography, nuclearmagnetic resonance, and computerized tomography)should be adapted to the study of comparative anato-my, and morphologic descriptions should be precisewith regard to 3-dimensional relationships and therelative sizes of cardiac cavities. Moreover, those whoprovide such descriptions should be respectful ofgen-erally agreed-upon current concepts, especially interms of nomenclature and the definition of anatom-ic structures.The use of the term conus provides a classic exam-

ple of nebulous terminology, as illustrated by Victor'sarticle.' Unlike Victor and associates, most modernauthors tend to use the term conus to mean anembryologic structure, rather than an anatomicstructure in the fully developed heart. Conversely,infundibulum is a term commonly used to identifythe outflow tract of fully developed ventricles, not todescribe an embryologic structure.4

Evolution of the Ventricles 175Texas Heart Institutejournal

The integration of related disciplines to produce anupdate on such complex issues would seem to beimperative, as exemplified by a recent book con-cerning coronary artery anomalies, wherein phylo-genetic and embryologic premises are proposed asthe logical foundation for the anatomical and clinicalsections.5 Therefore, I strongly encourage researchscientists and clinicians in the fields of comparativebiology, embryology, human anatomy, pathologicanatomy, cardiology, and cardiac surgery to enhanceprogress in the study of fundamental issues by join-ing together to establish interdisciplinary teams andmethods of research and communication.

References1. Victor S, Nayak VM, Raveen R. Evolution of the ventricles.

Tex Heart InstJ 1999;26:168-75.2. Harvey RP, Rosenthal N, editors. Heart development. San

Diego: Academic Press, 1999:1-488.3. de la Cruz MV, Markwald R, editors. Living morphogenesis

of the heart. Boston: Birkhauser, 1999:1-229.4. de la Cruz MV, Moreno-Rodriguez R, Angelini P. Phy-

logeny of the coronary arteries. In: Angelini P, editor.Coronary artery anomalies: a comprehensive approach.Philadelphia: Lippincott Williams & Wilkins, 1999:1-9.

5. Roberts WC. Foreword. In: Angelini P, editor. Coronaryartery anomalies: a comprehensive approach. Philadelphia:Lippincott Williams & Wilkins, 1999:vii.

Paolo Angelini, MD,Associate Professor ofInternal Medicine,Baylor College ofMedicine;StaffCardiologist,St. Luke's Episcopal Hospital andTexas Heart Institute;Houston

176 Evolution of the Ventricles Volume 26, Number 3, 1999