anatomy and pathology of the whale heart with special reference to the coronary circulation

Anatomy and Pathology of the Whale Heart with Special Reference to the Coronary Circulation

R. C. TRUEX, F. G . NOLAN, R. C. TRUEX, JR., H. P. SCHNEIDER AND H. I. PERLMUTTER Department o f Anatomy and Cardiovascular Research Institute of Hahnemann Medical College, Philadelphia, Pennsyluania, and The Marine Heart Research Foundation, Los Angeles, California

The unique position of the whale in the animal kingdom has long stimulated the curiosity and challenged the research in- terest of the scientific world. These enig- matic mammals, whose remote ancestors lived on land, have, during the evolution- ary process of adapting to a marine en- vironment, modified some of their organ systems. It is not surprising, therefore, that observations have been made upon the anatomy, pathology and physiology of the cetacean circulatory and respiratory systems.

Knox (1838) observed the great size of the heart in one adult and one fetus of the fin whale (Balaena borealis Knox). He stated the adult heart equalled in size an ordinary sized washing-tub, while the fetal heart was peculiar in form, being much flattened, and scarcely exhibiting the appearance of an apex. Pouchet and Beauregard ( 1889, 1892) called attention to the completion of an arterial circle on the ventral surface of the cardiac infundib- ulum in two young whales (Balaenoptera musculus and rostrata). These authors also noted anastomoses between the marginal arteries and the ventral interventricular arteries in both specimens. White and Kerr (15-27) examined the coronary vessels in the heart of an adult sperm whale, but found no evidence of coronary artery disease. Walmsley (38) exposed and measured the outside diameters of the coronary arteries in a 320 pound heart of an adult female fin whale (Balaenoptera physalus). He also gave an excellent description of the heart and coronary circulation in a fin whale fetus with a body length of 143 cm. Walmsley stated that the coronary veins have the usual mammalian distribution

although they are typical of the cetacean venous system in that multiple channels replace veins which are single in most mammals.

Race, Edwards, Halden, Wilson and Lui- be1 (59) recently completed a study on the aorta, coronary arteries, venous drainage, and cardiac muscle fibers in a 256-pound heart of an adult male sperm whale (Physeter catodon). They also studied the heart of a sperm whale fetus with a body length of 2.1 meters. These authors measured the adult heart and coronary circulation and graphically illustrated their results. Although they observed large, multiple anastomoses between the left and right coronary arteries, they stated they found no evidence of atherosclerosis or calcification in any arteries.

The cardiac conduction system of the whale has been examined morphologically by several investigations (White and Kerr, 15-77; Ogata, 17; Ogata and Sassa, 19; Walmsley, 38; Race et al., 59; Truex, 61). Electrocardiograms have been recorded from the live Beluga, fin, gray, and pilot whales (King, Jenks and White, 53; White, King and Jenks, 53; Kanwisher and Senft, 60; Nolan and Truex, unpublished data). For physiological experiments on smaller aquatic mammals the reader is referred to the interesting papers of Irving (39), Scholander (4O), Scholander and Irving (41), and Irving, Scholander and Grin- nell (41).

The above anatomical and pathologic investigations on the whale heart and coronary circulation were of necessity based

Supported by U.S.P.H. grants H-1575, H-3816, H-4753 and the Marine Heart Research Founda- tion.

325

326 R. C. TRUEX AND OTHERS

upon a limited number of suitable specimens, often obtained by chance and studied under difficult circumstances. Early in 1959 we had the good fortune to obtain numerous fresh hearts from several species of whales taken for scientific and com- mercial purposes. The hearts of several fetuses, 6 adult fin, and three pilot whales were partially dissected and studied, but are not included in measurements reported in the present communicatjon.

MATERIALS AND METHODS

The present investigation is based upon 10 adult whale hearts of three different species : (sei, or Balaenoptera borealis; gray, or Eschrichtius gibbosus; and sperm, or Physeter catodon); 7 specimens were from male and three from female animals. The aorta, pulmonary and caval vessels were Uniformly measured and trimmed prior to weighing each heart. Six hearts were dissected as fresh specimens, three after formalin perfusion, and one heart with latex injected into the coronary arteries. Variable amounts of fat ( 15 to 40 pounds) were carefully removed from the atrioventricular and interventricular sulci to expose all of the epicardial branches of the two coronary arteries and the cardiac veins. Each of the major arteries and veins as well as their smaller rami were opened and inspected for evidence of disease. The pattern of the coronary circulation of each heart was diagrammed, after which the 4 chambers were opened, inspected and measured. The essential measurements and data for each of the 10 hearts are presented in figure 1.

RESULTS

The cetacean heart is somewhat flattened when removed from the body and emptied of blood, and is globular in shape. The dorsal surface of the gray, sei, and sperm whale hearts preisented a distinct interventricular cleft. In addition the heart of the sperm whale exhibited a bifid apex. Preliminary studies on the very large hearts of the gray and fin whale (figs. 2, 3, and 4) were engrossing and informative, but phys- ically exhausting due to the bulk of these fresh specimens. The pattern and distribution of the coronary vessels were easily determined by the crude but effective per-

fusion method shown in figures 3 and 4. Structures within the atria and ventricles were exposed with little effort and are of phenomenal size. However, this early ex- perience with large hearts weighing up to 750 pounds convinced the authors it would be prudent to concentrate their energies on the smaller hearts of the sei and sperm whales.

Caliper measurements of all the cardiac valves and papillary muscles were completed, but for the sake of brevity, are omitted from the essential data shown in figure 1. The animals were all young adults although neither their exact ages nor body weights were determined. In a general way the 4 chambered cetacean heart resembled that of the land mammals. The left and right atria were capacious and their auricles had thin distensible walls reenforced by numerous, thick, pectinate muscle strands. The capacity of the right ventricle approximates that of the left ventricle, while the most unexpected observation was the variable thicknesses of the ventricular myocardium (fig. 1). In view of the enormous work demanded of the whale heart under several atmospheres of environmental pressure, we had antici- pated a uniformly thick ventricular wall. Contrary to our expectations, the anterior and lateral walls of the two ventricles as well as their apices, had areas that were surprisingly thin, whereas the myocardiumi was thick at the atrioventricular junction and within the muscular interventriculai: septum. Each whale heart, like their dis- tant ungulate cousins on land, had a heavy muscular moderator band that spanned the lumen of the right ventricle (fig. 5).

Coronary circulation The left coronary artery was dominant

in both gray whales and one sperm whale. The right coronary artery was dominant in one sperm whale heart and in another was the only coronary artery arising from the aorta. In the remaining 5 hearts the two coronary arteries were of equal size and distribution. As in most mammalian heartis, the left coronary artery of the whalle provided nourishment to the left atriuin and ventricle, while the right atrium arid ventricle were supplied by the right coronary artery (figs. 6 and 7). Both coronairy

ANATOMY-PATHOLOGY OF WHALE HEART

ANATOMIC MEASUREMENTS OF 10 WHALE HEARTS

2 0 1 10.5

327

(Physeter cotodon)

11.9

3 @ a # _ _ ~ _ _ _ _ Body Length (in meters)------------13,1 Heort Weight (in Ibs.1---------------

132 200

13 150 20 28 30

60 83 25

25 70 15

200 250

112 90 38

Circumference Heort tin em)--------- 137 Diometer Pulmonary Artery (in mml- - -- -I 87 Pulmonory Wall Thickness (in mm)--- - ---I2 Diameter Aorta (in mm I- - - --- - - - - I 90 Aortic Wall Thickness (in mm)-- - - - - - - -18 Diameter Right Coronory Artery (in mml--- 30 Diometer Left Coronory Artery (in mm)----32 Left Ventricle Thickness (in mrn)

43 Lateral wall _-_------------- Atrioventricular Junction- - - ---- - --78 Apex _ _ _ _ _ _ _ _ _ _ - _ _ - - - - - - _ _ 24

Right Ventricle Thickness (in mm) 30

Atrioventricular Junction---- - - - -- - 68 Lef t A-V Orifice (in mm)----------- 188 Right A-V Orifice (in mm)---------263 Moderator Bond (in mm)

Anterior Wall-- -_--- --------- Apex-- - _ _ -_ _ _ _----- - -----I 2

Length _ _ _ _ ______- - - - ----- 206 Width _ _ _ _ _ ___----- - ------ Thickness _ _ _ _ _ _ _ ___-- - _--- -23 68

162 206

26 175 20 33 36

53 90 16

15 60 13

250 285

232 75 28

I70 I75 17

200 18 32 38

60 84 24

23 78 23

307 306

255 78 25

I76 2 50

18 265

I8 34 44

90 9 0 26

60 82 24

400 360

230 70 30

l o * 2.3 '50 165 !37

12 I87

19 33 36

67 58 24

50 45 24

210 254

254 64 50 -

SPERM WHALE

I59 158 238

I 3 200

17 35 22

45 59 21

24 32 22

244 254

207 78 25 -

I54 I70 I69

13 187

18 45 49

47 80 23

26 43 17

275 250

262 66 30 -

~ __ 12.5 143 175

262 I I

210 18

33 35

44 88 25

43 38 14

250 28 1

147 66 40 -

5 9 11.6 113 150 200

I I 190

14 44 -- -

42 71 30

26 34 12 I90 280

I 5 4 60 30 -

Fig. 1 Size of cardiac structures and vessels.

arteries provided a rich arterial supply to the interventricular septum by means of the large ventral and dorsal interventricular arteries. The parent arteries then anastomosed with each other. Multiple large intercoronary anastomoses (5 to 15 mm in diameter) were demonstrated dor- sally in the atrioventricular sulcus (fig. 7), while smaller anastomotic vessels were present on the ventral surface of the pulmonary artery, and along the ventral and dorsal interventricular sulci.

Careful dissection of the arteries over the base of the pulmonary artery and along the interventricular sulci revealed arteriovenous communications 2-8 mm in diameter. Such channels were located entirely within the epicardium and were observed in all 10 hearts. The largest and most conspicuous arteriovenous channels were noted in the hearts of the sperm whale. In the one heart with latex injected into the coronary arteries under minimal pressure, the latex was observed in all of the arteries but also in the large veins that ac- companied the arteries within the inter-

ventricular sulci and proximal ventral wall of the right ventricle (fig. 17).

Gray whale. The basic coronary arterial pattern shown in figures 6 and 7 was found in the two hearts of the gray whale. The participating arteries were smooth walled and devoid of any evidence of atherosclerosis or calcification. The ventral interventricular and right marginal arteries (fig. 6 ) have counterparts in the human heart, while the left marginal artery may correspond to an enlargement of one of the left ventricular branches observed in the human heart. Additional ventricular arteries were present on both the ventral and dorsal surfaces of the left and right ventricles (figs. 6 and 7).

The venous drainage of the ventricular myocardium is accomplished by large epicardial veins that lie adjacent to, and parallel the course of, the major arteries. The plicated walls of the larger veins were ex- tremely thin. Numerous anastomotic veins of variable size were present at the apex, and on both the ventral and dorsal surfaces of the ventricles as shown in figures

328 R. C. TRUEX AND OTHERS

8 and 9. It was not uncommon to observe large veins (8-10 mm in diameter) that emerged abruptly from the deeper layers of the myocardium to terminate in the interventricular and marginal epicardial veins. The basic venous pattern (figs. 8 and 9) was similar in both gray whale hearts. As in higher land mammals, most of the interventricular septum, left ventricle, and the dorsolateral wall of the right ventricle were drained by tributaries of the coronary sinus. The ostium of the coronary sinus was of considerable size (fig. 4 ) and was located in the dorsal wall of the right atrium. The ventral and lateral walls of the right ventricle were drained by two to 4 veins. These vessels pene- trated deeply into the epicardial fat of the atrioventricular sulcus and terminated in the ventral wall of the right atrium above the annulus fibrosus. Small veins from the lower portions of the right and left atria terminated in the circumflex tributaries of the coronary sinus. The roof and inter- atrial surfaces of the right atrium presented ostia of several minimal cardiac veins similar to those observed in the heart of dog and man (Truex and Schwartz, '51; Truex and Angulo, '52).

The smaller heart of the sei whale had a coronary vascular pattern and distribution similar to that of the larger gray whale (figs. 6, 7, 8, and 9). The coronary arteries possessed numerous in- terarterial anastomoses between the two parent vessels, had small arteriovenous communications, but showed no evidence of arterial disease. The wide venous channels were placed deep in the epicardium of the interventricular and atrioventricular sulci, whereas the ventral and dorsal surfaces of both ventricles had a veritable network of small, anastomosing veins. The marginal and circumflex veins were present, but in all three specimens the dorsal interventricular vein was the largest tribu- tary of the coronary sinus.

Sperm whale. The coronary circulation of these 5 hearts presented the basic arterial and venous patterns shown in figures 10, 11, 12, and 13. However, each specimen possessed its own anatomic peculiar- ities and vascular variations. The coronary arteries and their myocardial branches were conspicuous in this species due to

Sei whale.

their large size and convoluted appearance. Only the larger arteries were included in figures 10 and 11. Unfortunately the thick arterial network to the interventricular septum could not be shown adequately in these two views. Abundant intercoronary anastomoses between the left and right coronary arteries were present over the base of the pulmonary artery, in the interventricular and atrioventricular sulci, and at the b s d apex. We were im- pressed particularly by the frequency and large size of the anastomoses between major branches of the left coronary artery in all 4 specimens (figs. 10 and 16). We have not observed such prominent inter- communications between branches of one coronary artery in any of the other aquatic or land mammals studied to date. The female sperm whale heart with only a right coronary artery arising from the aorta was a most interesting specimen for similar anomalies are observed only rarely in man. In this whale heart the single coronary artery gave rise to circumflex, interventricular and marginal arteries (figs. 14 and 15). These branches, though all arising from one parent vessel, formed a basic pattern of cardiac distribution similar to that found in the other sperm whale hearts that possessed both a left and right coronary artery. The arteries were ex- plored thoroughly, but no evidence of atherosclerosis or calcification was found in this specimen. As demonstrated in figure 17 and noted above, the sperm whale hearts all had numerous arteriovenous anastomoses. Atheromatous plaques were present to a varying degree in each of the hearts of the 4 male sperm whales as de- scribed below.

The venous drainage of the sperm whale heart is shown in figures 12 and 13. The marginal veins were smaller, while the interventricular and left circumflex veins were of considerable size. The network of small epicardial veins observed in the hearts of the sei whale was here replaced by a more open network composed of larger veins. This observation was in marked contrast to our findings in the gray and sei whales. The venous radicals in the heart of the sperm whale were neither as large nor as numerous as the arteries that supplied the myocardium.

ANATOMY-PATHOLOGY O F WHALE HEART 3219

Pathology The epicardial arteries of each heart

were opened and examined for evidence of coronary artery disease. The intima and walls of all of the arteries of the gray and sei whales were smooth and devoid of disease. The aorta, coronary orifices, and lumens of the major proximal branches of the left and right coronary arteries of all of the sperm whale hearts also appeared smooth and entirely normal.

However, in the more distal portions of the marginal, interventricular, and ventricular arteries of each of the 4 male sperm hearts we observed multiple atheromatous intimal plaques. In one specimen the plaques were of small size (fig. 19) and located most commonly a,t the ostium of a smaller branch of the parent vessel. In two specimens multiple medium-sized plaques were observed (figs. 21 and 22). The elongated, yellowish, intimal plaques were always oriented parallel to the long axis of the artery. In no artery did we observe an annular type lesion that formed a ring within the lumen of the vessel.

Microscopic sections of the atheromatous plaques, prepared by a variety of dif- ferential stains, demonstrated a histolog- ical appearance (figs. 23 and 24) quite similar to that observed in human coronary arteries with atherosclerosis. The plaques were composed of proliferated tis- sues that involved chiefly the intima and subintimal layers. The fibrous elements predominated, particularly collagen fibers. Numerous fibroblasts and macropha.ges were distributed between the abundant connective tissue fibers. Hemorrhage and blood pigments often were observed within the confines of the larger plaques, although we observed no evidence of necrosis or calcification within the walls of the arteries. The internal elastic membrane had lost its integrity and was replaced by a loosely fenestrated fibrous layer (fig. 23). In some instances the inner layers of the tunica media were also involved, and in such regions there was no sharp demarca- tion between the tunica intima and tunica media. The clear areas between the wavy fibrous layers within the plaque, and along the intimo-medial junction (fig. 24), resulted from the extraction of lipids during

tissue dehydration and embedding. Frozan sections stained with Scharlach R demom- strated an abundance of minute fat drop- lets within the plaques that were arranged in stratified layers between the fibrous elements. Larger deposits of fat were also observed within the plaques as well as along the intimo-medial junction.

In only one specimen did we observe evidence of myocardial infarction and necrosis. The heart of one sperm whale possessed a circumscribed lesion that had de- stroyed the proximal and dorsal portion of the muscular interventricular septum and adjacent wall of the left ventricle. Thk entire thickness of the septum had been replaced in an area of 10 X 15 cm by a foul smelling mass of cheesy material in- terlaced by fibrous strands. The margins of the necrotic area were not sharply de- marcated from the cardiac muscle fibers of the surrounding myocardium. The gross pathologic appearance of the area was that of a recent dorsal myocardial infarction undergoing necrosis. In this specimen the coronary arteries had demonstrated multiple medium-sized atheromatous plaques, and also nematode worms had been found in the cardiac veins (figs. 5 and 18). We were unable to isolate and identify the specific artery, or arteries and veins, re- sponsible for the infarcted area in this heart.

Parasitism Examination of the small proximal veins

on the dorsal surface of two sperm whale hearts revealed the presence of nematode worms. The lumen of one vein was entirely occluded by one large worm that was 2.5 mm in diameter and 125 mm in length (fig. 18). The right ventricle of this same specimen contained 15 additional uniden- tified nematode worms, 90 to 129 mm in length (fig. 5).

DISCUSSION

Although gross body measurements and organ weights have been made in several species of whales, little scientific informa- tion has accumulated concerning the heart and circulation of these mammals. To the authors knowledge this is the only study based upon several whale hearts. We have recorded some of the cardiac measure-

330 R. C. TRUEX AND OTIIERS

ments (fig. 1) and presented the basic coronary vascular patterns (figs. 6 to 13) of the whale as only a starting point for future investigations on additional animals.

The homologies between the coronary circulation of the cetacean and human hearts can be appreciated best by a careful examination of these illustrations. For example, the ventral interventricular and left circumflex arteries have an origin and distribution similar to the anterior descend- ing and circumflex branches 0f the human left coronary artery. In a similar manner the left circumflex vein corresponds to the great cardiac vein of the human heart; the dorsal interventricular vein corresponds to the middle cardiac vein, while the right marginal vein is analogous to the small cardiac vein of man. The right ventricular veins, though few in number, simulate the human anterior cardiac veins, but in the cetacean heart they possess more extensive anastomoses with the large tributaries of the coronary sinus.

The greatest difference between the whale and human coronary circulation is manifest in the multiple, large intercoronary arterial anastomoses, anastomoses between large branches of one coronary artery, and the unusual venous drainage of the whale heart. One can demonstrate small intercoronary anastomoses on the dorsum of the human heart, but never finger-sized vessels comparable to those always observed in the same region of the whale heart. One can only speculate whether such interarteria'l anastomoses are of small caliber in man because of the smaller size of the human heart and coronary arteries as compared to these structures in the whale. The large anastomoses between the tortuous major branches of the left coronary artery of the sperm whale are unique even among the whales, and are normally absent in the human heart.

The occurrence of arteriovenous anastomoses in all of the whale hearts merits additional consideration. The size, location and frequency of such anatomic communications indicates they must have some important, but still unknown, functional significance. One can only surmise that they may play an important role in

the shunting of arterial blood into the venous system during myocardial engorgement or distention. It is well known that both the baleen and toothed whales ex- hale carbon dioxide and take in atmos- pheric air when they surface to "b10~" several times. Blow holes, located on the top of the head, remain tightly closed when the whale is submerged, and the animal must perform all of his bodily functions on stored oxygen. It is possible that venous blood may cause distention and engorgement of the right ventricle and right atrium during prolonged sub- mersion. Under such circumstances the ventricular walls would be compressed, and would offer increased resistance to coronary arterial flow. Under these circumstances the arteriovenous shunts might act as safety valves that direct the arterial blood into the low pressured venous system.

Comparative aspects of the coronary circulation merit a more extensive study, for several authors have recently observed anomalous arteriovenous communications in the human heart (Walther, Starkey, Zervopolus and Gibbons, '57; Schultz, '58; Steinberg, Baldwin and Dotter, '58; Ed- wards, '58; Zuhdi, Kraft, Carey and Allen, '60). Such anomalous human arteriovenous anastomoses correspond in location to those we have observed in the normal coronary circulation of the whale heart. The phylogenetic significance and possible re- lationship between the arteriovenous anastomoses observed in the aquatic and land mammals including man, must await fur- ther investigation.

Marine nematodes have been found in the hearts of several aquatic mammals. Heart and lung worms most commonly are observed in those aquatic mammals that live on a fish diet such as seals, sea lions, and dolphins. (Fasut, '37; Lyster, '40; Dougherty and Herman, '47; Ander- son, '52; Margolis, '54; Brown, McIntyre, DelliQuadri and Schroeder, '60). Nem- atodes have been recorded previously in the right ventricle of the sperm whale heart (see Margolis, '54), but to our knowledge they have never before been observed within the epicardial cardiac veins. Para- sitic nematodes in the right heart could migrate with relative ease into the ostium

ANATOMY-PATHOLOGY OF WHALE HEART 331

of the fist-sized coronary sinus and its large venous tributaries during atrial di- astole.

We believe the existence of atheromatous plaques in the coronary arteries of the male sperm whale to be a most significant finding. Future studies, on a more extensive series of whale specimens of both sexes, must be made before one can de- termine the validity of such factors as age and sex upon atherosclerosis. How- ever, it should be noted that the sperm whale dives deeper, remains submerged longer (50-60 minutes), has a squid and fish diet, and an erratic temperament that set him apart from the other species of whale. One can only speculate as to the special roles played by stress, diet, and temperament in these toothed denizens of the deep. We look forward to the examination of the coronary arteries of truly aged sperm whale bulls. Such aged bulls live an isolated life in the frigid arctic and antarctic waters, and presumably have been driven from the herds by younger males. Time and study alone will reveal whether such aged animals possess a more advanced degree of coronary atherosclerosis.

We cannot explain the absence of plaques in the coronary arteries of the sperm whale as reported by White and Kerr (15-17) and Race et al. (59). The presence of atherosclerosis in our 4 male specimens may have resulted from a for- tuitous sampling of specimens, or a more thorough examination of all the distal arterial branches. We reiterate, the intimal atheromatous changes were always con- fined to those distal arteries that feed branches directly into the ventricular myocardium. Unless these small arteries are opened and examined with care one would miss the vascular pathology de- scribed and illustrated in this communica- tion. An extensive search will be made for evidence of myocardial infarction in our continuing studies.

We realize we have created as many puzzling problems as we have solved. We have derived some solace from the knowledge that many investigators who studied whales before us have often been amazed, bewildered, and perplexed by seemingly unsolvable questions. We sub-

scribe whole-heartedly to the words of a noted predecessor in this field, P. D. Scho- lander (59) who stated: When playing around in the ocean, dolphins are pleas- ing to the eye no end, but let it only add to your thrill that these rascals are a graveyard to our wits. For is not finding out infinitely more exciting than knowing the answer?

SUMMARY AND CONCLUSIONS The present study of the adult whale

heart and coronary circulation was made upon 10 specimens of three different species (sei, gray, and sperm whales) with heart weights that ranged from 100 to 350 pounds. Branches of the coronary arteries and cardiac veins were dissected, diagrammed and examined for evidence of arterial disease. Essential measurements of the heart and blood vessels are presented, while the basic patterns of the cardiac arterial and venous systems are illustrated and compared to those of man.

The right and left coronary arteries were of equal size and distribution in 5 hearts; the left coronary was dominant in three, and the right coronary artery was dominant in one specimen. An anomalous right coronary artery was the only coronary vessel present in one sperm whale heart. Large intercoronary anastomoses between the left and right coronary arteries were demonstrated in 9 hearts, while anastomoses between the major branches of the left coronary artery were a prominent feature of the circulation in the heart of the sperm whale. Arterio- venous communications were observed in all 10 specimens, and provide a possible phylogenetic explanation for the trouble- some arteriovenous anomalies recently en- countered in the human coronary circulation. Marine nematode heart worms were observed in the right ventricle and cardiac veins in two of the sperm whale hearts. One male sperm whale heart demonstrated a large recent myocardial infarct in the interventricular septum. The significance of these results are discussed.

The coronary arteries of the sei and gray whales were devoid of atherosclerosis and calcification. However, we observed multiple, yellowish colored, intimal atherom atous plaques in the more distal ventric-

332 R. C . TRUEX AND OTHERS

ular branches of both coronary arteries in the hearts of the 4 male sperm whales. The factors of sex, age, species, stress, and diet appear to be strongly implicated in cetacean arterial atherosclerosis, but the significance of each factor must await more adequate sampling and future investigation.

ACKNOWLEDGMENTS

The authors are indebted to the U. S . Department of Interior, Fish and Wildlife Service for special permission to euthanize and study the California gray whale; to Charles and John Caito of the Del Monte Whaling Station, Richmond, California for laboratory facilities and technical assistance; to the British Columbia Packers, Whaling Division, Vancouver and Coal Harbour, B. C., for their valued assistance in providing laboratory space and fresh specimens for this study; to Carlernst Diedrich, Bruce McNeil, Lindsley Parsons, Hector Cowie, Hanibul Anderson, Captain Edward Karlsen, Captain Arne Borgen, Richard Cohen, Faith Hartman, Martha Q. Smythe, Audrey Gourley, Theresa Malin- owski, and Ilona Bauer for their coopera- tion and professional assistance.

We express our sincere appreciation to Miss Marjorie Stodgell, Steven Gigliotto, Louis Sunny, and Walter Guzejko for their valued medical art and photographic assistance in preparing the illustrations used in this publication.

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ANATOMY-PATHOLOGY OF WHALE HEART 333

Walther, R. J., G. W. Starkey, E. Zervopolus and White, P. D., R. L. King and J. L. Jenks 1953 G. A. Gibbons 1957 Coronary arteriovenous Thesrelation of heart size to the time intervals fistula: Clinical and uhvsiologic reuort of two of the heart beat. with uarticular reference patients, with review of the- literature. Am. J. Med., 22: 213-222. Med., 248: 69-70.

to the elephant and the whale. New Eng. J.

White, P. D., and W. 3. Ken 1915-1917 The Zuhdi, N., D. Kraft, J. Carey and A. Greer 1960 heart of the suerm whale with esuecial refer- Coronary arteriovenous-like communications. ence to the A-V conduction system. Heart, A.M.A. Arch. Surg., 80: 178-180. 6: 207-216.

PLATE 1

EXPLANATION OF FIGURES

2 Ventral surface: 250-pound heart of a male gray whale. A hypertrophied human heart of 400 gm is superimposed on the right atrium to illustrate comparative heart slze of the two specimens. The major arteries and veins are concealed by large amounts of fat in the atrioventxicular and interventricular sulci as well as along the margins of both ventricles. The letters used in all figures indicate the 4 heart chambers (Le., RA, right atrium; RV, right ventricle; LA, left atrium; LV, left ventricle). Distention of myocardium of right ventricle by two inch hose inserted in right coronary artery of fresh fin whale heart (300 lbs.). The left ventricle could be distended in a similar manner .with water pressure from a three inch hose placed in the left coronary artery. This effective method was used to demonstrate both the arterial and venous patterns of several fresh specimens.

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ANATOMY-PATHOLOGY OF WHALE HEART R. C. Truex, F. G. Nolan, R. C. Truex, Jr., H. P. Schneider and H. I. Perlmutter

PLATE 1

335

PLATE 2


4 Ostium of coronary sinus ( C S ) in the right atrium of a fin whale heart weighing 300 pounds. Openings of the three largest venous tributaries ( f i g s . 9 and 13) of the coronary sinus are clearly shown. Venous return is illustrated during irrigation of myocardium with equal pressures in the left and right coronary arteries. The right atrioventricular orifice and posterior papillary muscle of the right ventricle are seen on the Tight side of the figure.

Right ventricle of sperm whale heart (specimen number two, in fig. 1). The coronary circulation of this specimen is shown in figures 10, 11, 12, and 13. Marine nematodes were present in the right ventricle (F and G, fig. 5) , and cardiac veins (fig. IS) of this heart. The specimen also demonstrated a recent, large infarction of the interventricular septum. The anterior ( A ) and posterior ( C ) papillary muscles; moderator band ( B ) ; papillary muscle of the conus (D); and valves of the pulmonary artery ( E ) are identified.

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PLATE 2

337

PLATE 3


6 Coronary arteries on ventral surface of a 250-pound gray whale heart. The major arteries are identified and their respective diameters are indicated.

7 Coronary arteries on dorsal surface of gray whale heart. Same specimen as shown in figure 6 above. Note intercoronary anastomoses in dorsal atrioventricular and interventricular sulci, and at apex.

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ANATOMY-PATHOLOGY OF WHALE HEART R. C. Truex, F. G . Nolan. R. C. Truex, Jr., H. P. Schneider and H. I. Perlmutter

PLATE 3

R. Ventricular (7-13 rnm)

R. Marginal (12 mm)

Ventral Interientricular a. (20-28 mm) 6

339

PLATE 4

EXPLANATION O F FIGURES

8 Cardiac veins on ventral surface of a 250-pound gray whale heart. The major veins are identified and their respective diameters are indicated. Anastomoses between the ventricular veins and coronary arteries (fig. 17) were present in all the hearts of the gray, sei, and sperm whales.

Cardiac veins on the dorsal surface of gray whale heart. Same specimen as shown in figures 6, 7, and 8. Note large size of dorsal interventricular vein and ostium of coronary sinus.

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ANATOMY-PATHOLOGY OF WHALE HEART R. C. Truex, F. G . Nolan, R. C. Truex, Jr., H. P. Schneider and H. I. Perlmutter

Aorta -

Circumflex (24 mm)

L. Marginal v. (16-20 mrn)

Dorsal 1nt;rventricular v. (27-40 mm)

PLATE 4

9

34 1

PLATE 5


10 Coronary arteries on ventral surface of a sperm whale heart. The tortuous major arteries are identified, and the prominent intercoronary anastomoses are clearly shown. The sperm whale hearts also possessed large anastomotic communications between major branches of the left coronary artery (fig. 16).

Coronary arteries on dorsal surface of a sperm whale heart. Same specimen as shown in figures 5 , 10, 12, arid 13. This heart also demonstrated a recent large infarct in the dorsaI and proximal part of the interventricular septum. Note bifid apex of the sperm whale heart.

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342


PLATE 5

a.

cular aa.

I0

343

PLATE 6


12 Cardiac veins on ventral surface of sperm whale heart. The major veins are identified. The right ventricular veins terminate in the right atrial cavity and also have large communications with the tributaries of the coronary sinus.

Cardiac veins terminating in coronary sinus on dorsal surface of sperm whale heart. Although there are variations i n vessel size and their arrangement, the basic pattern of venous drainage is similar in the three species of whales studied (e.g., compare figs. 8 and 9 with figs. 12 and 13).

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PLATE 6

nflex v.

vv.

12

345

PLATE 7


14 Anomalous coronary circulation of heart. The heart of this female sperm whale had a single right coronary artery that supplied the myocardium of all 4 chambers. Although arising from a single coronary artery, the major branches conform to the basic arterial pattern and distribution observed in other whale hearts (e.g., compare figs. 14 and 15 with the arterial patterns shown in figs. 6, 7, 10, and 11).

Branches of a single right coronary artery on the dorsal surface of sperm whale heart. Same specimen as shown in figure 14.

15

346


PLATE 7

a.

Circumflex a

Marginal a.

15 347

PLATE 8


16 Anastomoses between major branches of the left coronary artery of a sperm whale heart injected with latex. The large latex communications between the ventral interventricular ( l ) , ventricular, and circumflex ( 2 ) arteries are clearly shown after careful removal of the vessel walls. Large amounts of the thick latex, injected into the arteries, were recovered in the adjacent more flattened cardiac veins (3).

Arteriovenous anastomoses on ventral surface of right ventricle of a sperm whale heart with latex injection of coronary arteries. The auricle of the right atrium (1) and right coronary artery ( 2 ) .are identified adjacent to the pulmonary artery. The smaller arteries shown in the illustration communicated directly with the injected vein held in the center of the figure. Such arteriovenous anastomoses were demonstrated in all 10 whale hearts, and were most often located over the base of the pulmonary artery, and along the atrioventricular and interventricular sulci. Similar anastomoses, requir- ing surgical correction have been observed recently in the human heart (see text).

18 Marine nematode obstructing the lumen of a cardiac vein (1) on the dorsal surface of the left ventricle of a sperm whale heart. Same heart illustrated in figures 5, 10, 11, 12, and 13. The dorsal interventricular artery ( 2 ) is identified. Deep to the area shown in this figure we observed a large, recently infarcted region within the interventricular septum.

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PLATE 8

349

PLATE 9


19 Two small intimal atheromatous plaques (arrows) in a branch of the right marginal artery of a male sperm whale. Multiple plaques were observed in many of the smaller arteries over both ventricles in the hearts of the 4 male sperm whale specimens. Magnification of gross specimens in figures 19-22 is indicated by metric scale.

Medium-sized intimal atheromatous plaque (arrow) in a left ventricular artery of a male sperm whale. Note proximity of plaque to the orifice of a smaller branch of the parent vessel.

Large intimal plaque (arrow) in ventral interventricular artery of a male sperm whale. The large plaques were always parallel to the long axis of the artery. No annular intimal lesions were observed in this study. Note abundant amount of periarterial adipose tissue so common to the cetacean coronary circulation.

Multiple, large, intimal atheromata (arrows) in a branch of the dorsal interventricular artery of a sperm whale heart. The lumen of the artery was partially occluded in each instance, however, complete occlusion of an artery was not observed.

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21

22

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PLATE 9

351

PLATE 10


23 Microscopic section of intimal atheromatous plaque. Fibroblasts, macrophages, and blood pigments account for the cellular and mottled appearance. Note absence of internal elastic membrane. Male sperm whale. Hematoxylin and eosin stain. x 30. Photomicrograph demonstrating fibrous structure of the intimal atheromatous plaque. The darkly stained collagen fibers predominate within the plaque, tunica intima, deeper layers of the tunica media, and tunica adventitia. Male sperm whale heart. Van Gieson stain. >( 20.

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ANATOMY-PATHOLOGY OF WHALE HEART R. c. Truex, F. G. Nolan, R. C. Truex, Jr., H. P. Schneider and H. I. Perlmutter

PLATE 10

353

anatomy and pathology of the whale heart with special reference to the coronary circulation

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