Guest Editorial Evolution of the Ventricles Solomon Victor, FRCS, FRCP We studied the evolution of ventricles by macroscopic examination of the hearts of Vijaya M. Nayak, MS marine cartilaginous and bony fish, and by angiocardiography and gross examination of Raveen Rajasingh, MPhil the 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, and snakes, the left ventricle exists as a small-cavitied contractile sponge. The high pressure generated 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 lumen when compared with turtles and snakes. The heart is housed in a rigid pericardial cavity in the shark, possibly to protect it from changing underwater pressure. The pericardial cavity in various species permits move- ments of the heart-which vary depending on the ventriculoarterial orientation and need for the ventricle to generate torque or spin on the ejected blood- that favor run-off into the appropriate arteries and their branches. In the lower species, it is not clear whether the spongy myocardium contributes to myocardial oxygenation. In human beings, spongy myocardium constitutes a rare form of congenital heart disease. (Tex Heart Inst J 1999;26:168-75) W e describe our macroscopic and angiocardiographic findings related to the evolution ofthe cardiac ventricles in fish, frogs, snakes, turtles, and crocodiles. In addition, we discuss ways in which the ventricular devel- opment in these animals relates to that in human beings. Materials and Methods The anatomical terms are applied herein as they are in human anatomy and can be envisioned 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 dog sharks, 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 by Key words: Animal; evolution; heart/anatomy; means of a vertical midline incision. The truncus was divided longitudinally and heart ventricle; myocardium; the incision was continued caudally into the right-sided lumen of the ventricle. regional blood flow; Transverse and coronal sections of the ventricles were examined macroscopically. ventricle, single; ventricle, spongy 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- From: The Department of Cardiovascular Surgery, gen was insufflated into the oral cavity. Angiocardiography was performed using a The Heart Institute, digital computerized imaging system, with contrast medium injected through the Chennai- 600 010, India duct of Cuvier. Later, the heart was dissected in the same manner as were those of the marine fish. Address for reprints: Frogs. Twelve frogs were anesthetized with the use of ether, and anesthesia was Solomon Victor, FRCS, maintained with oxygen and ether. The frogs were intubated and were manually FRCF? 15 East Street, Kilpauk Garden Colony, ventilated by digital closing and opening of a hole in the inlet tube. Each frog was Chennai - 600 010, India laid on its back, and its heart was explored through a ventral midline incision in the chest wall and pericardium. Angiocardiography was performed by injecting C 1999 by the Texas Hearts contrast medium into the ventral abdominal vein, hepatocardiac channel, sinus Institute, Houston venosus, pulmocutaneous branch, and left atrium. Later, the truncus and bulbus 168 Evolution of the Ventricles Volume 26, Number 3, 1999 were incised longitudinally, and the incision was ventricle and is caudal to the row of craniad semilu- continued along the inferior border ofthe heart into nar valves. Downward extension of the longitudinal the lumen of the ventricle. Coronal and transverse arteriotomy opens the bulbus, which has 3 longitu- sections ofthe heart were examined macroscopically. dinal ridges. Caudal to the bulbus, there is a ventric- Turtles and Snakes. Six pond turtles and 4 rat ular lumen in the right side of the externally snakes were anesthetized with the use of ether in- symmetrical heart. This lumen is the morphologic halation, followed by intubation and ventilation as equivalent of the human right ventricle. Its inner was done in the frogs. The heart was exposed by wall has a curvilinear band with anterior trabecula- removing the ventral plate of each turtle and by a tions, resembling the trabecula septomarginalis seen ventral midline incision in each snake. The peri- in the right ventricular surface of the mammalian cardium was then opened. Angiocardiography was and human interventricular septum. This band bor- performed with the contrast medium injected man- ders a ventricular septal defect that leads through an ually into the right or left atrium, and images were oblique passage, craniad to the leftwardly situated obtained by digital computerized imaging. The pul- common atrioventricular orifice. The left side of the monary artery was incised longitudinally, and the ventricle consists of spongy myocardium with no incision was extended into the right ventricle. A lumen except for a small chamber beneath the com- coronal section of the ventricle was then obtained mon atrioventricular orifice. This chamber commu- through the ventricular septal defect. Anterior and nicates with the right ventricular lumen through the posterior flaps of the ventricle, thus created, facili- ventricular septal defect. The common atrioventric- tated macroscopic inspection of the ventricular lu- ular orifice has 2 bridging leaflets connected to men and wall, related arteries, and valves. primitive papillary muscles on either side, with in- Crocodiles. Two crocodiles were anesthetized with tervening chordae tendineae. ketamine, followed by intubation and manual venti- Marine Bony Fish. In the marine bony fish lation. Each heart was exposed through a ventral (Scomberemorus commersonii), the heart is median midline incision. Angiocardiography was performed and symmetrical. The pericardial sac is fibrous all by manual injection of contrast material into the around and is detached from the chest wall. The right or left atrium with the use ofdigital computer- hepatic veins drain directly from the liver into the ized imaging. Later, the right ventricle was examined sinus venosus without an interposed venous sac. through a longitudinal incision, which was begun in Craniad to the ventricular chamber is an onion- the pulmonary artery and extended into the lumen bulb-shaped chamber that is the conus, separated of the right ventricle. The left ventricle was exposed from the ventricle by a tricuspid semilunar valve. We through a long-axis incision close and parallel to the use the term conus to denote a chamber that is crani- anterior descending coronary artery; the left ventric- ad to the semilunar truncal valve and has no intrin- ular wall and the mitral and aortic valves were exam- sic contractility. Caudal to the semilunar valve is a ined macroscopically. pitted bulbar septum. There is no trabecula sep- tomarginalis. The common atrioventricular orifice Findings with 2 bridging leaflets is nearly flush with the inner wall of the ventricular lumen, which is right sided. Marine Cartilaginous Fish. The heart ofthe marine The left wall of this chamber and the apex of the cartilaginous fish (hammerhead shark, dog shark, ventricle are thick walled and without a lumen, and tiger shark) is housed in a pericardial cavity with except for a tiny inlet chamber that communicates a ventral wall that also serves as a cartilaginous chest with the right ventricular lumen. The conus contin- wall. The heart is symmetrical, with 2 ducts of ues as a truncus, which is devoid of the lateral Cuvier. There is a large venous sinus under the sep- branches evident in the marine cartilaginous fish, tum transversum between each lobe of the liver and except near its termination. the corresponding hepatic vein. The sinus venosus is Air-Breathing Freshwater Fish. The heart ofthe air- triangular, and its caudal wall is adherent to the breathing freshwater fish is externally symmetrical. transverse septum. There is a common atrium that A median dorsal ridge develops inside the sinus bears isomeric appendages on either side. Externally, venosus at the junction ofthe 2 ducts ofCuvier. The the ventricle has right and left faces separated by an sinus venosus is less dominant than that seen in anterior ridge, along which runs a coronary artery marine fish. A common atrium with 2 appendages that resembles morphologically the left anterior des- opens through a left-sided common atrioventricular cending coronary artery in a human being. orifice into the right-sided lumen in the ventricle. A conical bulbar chamber leads craniad to a trun- The left wall of this ventricular lumen is thick and cus arteriosus. We use the term bulbus to refer to this spongy. There is a left-sided inlet chamber that is chamber, which is visibly demarcated from the main small and smooth (Fig. lA). During angiocardiogra- Texas Heart Institutejournal Evolution of the Ventricles 169 phy, not only the right-sided lumen but also the bulb. The conus is distended during ventricular sys- spongy left wall of the ventricle fills with contrast tole and is emptied during ventricular diastole. medium (Fig. 1 B). The contrast from the lumen and Frog. The frog heart is asymmetrical, due to a D- the spongy wall is ejected into the truncus, which loop.