Path. vet. 5: 313-326 (1968)

From the Laboratory for Experimental Surgery, Free University of Amsterdam, the Netherlands (Head, Prof. G. den OTTER, M.D.)

Anomalous Origin of the Coronary Arteries in Animals

The literature contains numerous recorded instances of anomalous origin of the coronary arteries in domestic animalsls. 15a especially cattle, and in human being$, 1%1L18-21, 23, 27,31.37, 39,42, more frequentIy in the latter. I did not find any report of such anomaly in swine. Anomalous origin of the coronary arteries is reported in this paper in 10 cattle, 1 domestic pig, and 1 deer.

Review of Literature GODGLuCK15reviewed the veterinary literature to 1941 and added a description of a case of anomalous origin of the right coronary artery from the pulmonary trunk in a cow. VINKet al.38 reported 8 cases of such an anomaly, all in cattle. V I T U M Sstudied ~~ a cow’s heart with such an anomaly associated with significant anastomosis between the two coronary arteries. FISHER and P I R I Ereported ~~ anomalies of the coronary arteries in 9 cattle; among these were 2 cases of anomalous origin of the right coronary artery from the pulmonary trunk. b S C H K E B g , REID30, SCHAUDER~~, and RUBLI~~. 34 reported in cattle aneurysms of the coronary arteries, sometimes communicating with one of the ventricular cavities. S C H ~ N D U described B E ~ ~ such an anomaly in a cow but classified it with anomalies of the ventricles. The reports of cases in cattle are discussed in a comprehensive review by GODGLuCK15a, but 3 other reports not mentioned by him need to be cited here. ALTMANN~ found an aneurysmic left coronary artery communicating with the right ventricle in a 2I/,-year-old ox.

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CHRISTENSEN and DALGAARD-MIKKELSENgreported 2 cases of ectasia of a coronary artery-the left in one case and the right in the othercommunicating with the right ventricle in cattle. E M S B reported O~~ ectasia of both coronary arteries in a 6-year-old cow; the left artery was 25 and the right 12 mm in diameter instead of the normal 12 and 5 mm respectively. BAR ONE^ recorded hypoplasia of the left coronary artery associated with hyperplasia of the right coronary artery in a mule. CERVEN+ and KAMAN~ studied the heart of a calf with a common stem of the coronary arteries.

Development of the Coronary Arteries In general, MARTIN'S^* classic theory of the development of the coronary arteries in the rabbit is accepted by investigators of cardiac anomalies. MARTIN stated that the coronary arteries develop as endothelial sprouts, situated near the distal bulbus cushions. GRANT^^ described the communication between the arteries and the veins in the rabbit’s heart. He found that development of the truncus septum was already established before the primordia of the coronary arteries were seen. BEN NETT^ studied the development of the sinusoids and their communications with the arteries in the pig. GOLDSMITH and BUTLER^^ described the development of the coronary circulatory system in the embryonic pig. They stated that all vessels arose by endothelial budding from preexisting endothelial sprouts and that the main vessels existed as short sprouts in the 12 mm stage. In accordance with GRANT^^ and GOLDSMITH and BUTLER^^, PAT TEN^^ reported that septation of the truncus arteriosus in the pig was completed before the 10mm stage.

Gross Anatomy of the Coronary Arteries The gross anatomy of the coronary arteries of animals is recorded in the Handbook of Comparative Anatomy by ELLENBERGER and BAUM~Z and in the handbook of Comparative Basic Cardiology by R o B B ~Both ~ . books give a survey of the normal picture of the course of the coronary arteries in cattle and pigs. More detailed studies of

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Figs. I and 2. Diagram of the normal origin and division of the coronary arteries in the ox (1)and pig (2) for comparison with all subsequent figures.

these vessels in the pig and dog were published by LUMB and SINGdog and man by B R O ~ W E R ~and , in pig by BERG^. The pattern of origin of the coronary arteries is usually constant in both ox (Fig. 1) and pig (Fig. 2). The position of the orifice of the right coronary artery may vary a little. The secondary and further branches of the coronary arteries do not have a constant source. Some branches may originate in the Ieft and some in the right coronary stem. In my illustrations and in the text the veterinary Latin terms as described in the Basle Nomina Anatomica40 are used: L E T A R Y ~23, ~ ~ in

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to

notations in Figures

A.O. : Aorta A.P. : Arteria pulmonalis-pulmonary trunk L. : Left or anterior R. : Right or posterior I : origin a. coronaria sinistra I1 : origin a. coronaria dextra 1 : ramus descendens anterioris 2 : ramus circumflexus 3 : ramus septalis 4 : ramus septalis 5 : ramus descendens posterioris 6 : ramus circumflexus 7 : ramus septalis

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R

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A

4 L

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Fig. 3. Diagram showing aneurysm of both coronary arteries (stippled areas) which are joined by an anastomosis (arrow). Fig. 4. Diagram showing absence of the orifice of the left coronary artery. The wavy lines indicate the anastomoses mentioned in the text.

Report of Cases Case 1; Fig. 3; Heart 183 The heart of a 6-month-old pig of unknown history had aneurysmatic stems of both coronary arteries, with an anastomosis between these aneurysms but without other externally visible anomaly. The origins of both coronary arteries were normally situated. The orifices, stems, and secondary branches of the arteries were wide. A very wide vessel connected the stems of both coronary arteries on the surface of the conus arteriosus, 3 cm below the ring of the semilunar valves of the pulmonary trunk. The ramus descendens of the left and the ramus circumflexus of the right coronary artery were very wide also, but their courses were normal. The ostium aortae had abnormaIly large cusps; there was aIso a slight fibrous subaortic stenosis. The pulmonary ostium was normal.

Case 2; Fig. 4; Heart A 4-month-old calf of unknown history came to emergency slaughter. At autopsy all of its organs and muscles were congested, a

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R

Fig.5. Diagram showing absence of the orifice of the right coronary artery. Note the branch of the left c.a. passing between the aorta and the pulmonary trunk to supply the branches of the right c.a. Fig. 6. Diagram to show origin of the right coronary artery in the pulmonary trunk (A.P.) instead of in the aorta (A.O.) The wavy lines represent the anastomoses mentioned in the text.

clear indication of a circulatory insufficiency.Its heart lacked an orifice for the left coronary artery. The orifice of the right coronary artery was normally situated. A branch of the right artery passed between the pulmonary trunk and the aorta and served as the stem of the left artery; the further course of this left artery was normal. There was an anastomosis between the septal branches of the right artery and another one between one of the septal branches and the ramus dexter. Otherwise, the heart appeared normal.

Case 3; Fig. 5; Heart - (fragment) The heart of a cow of unknown history and at least 6 years old lacked any macroscopic anomaly externally. The orifice of the left coronary artery was correctly situated, but that of the right coronary artery was lacking. A branch of the left artery passed between the aorta and the pulmonary trunk and served as the stem of the right artery; the further course of which was normal. There was no other anomaly.

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Fig. 7. Diagram depicting origin of the left coronary artery from the pulmonary trunk instead of from the aorta. Fig. 8. Diagram showing aneurysmal anastomoses (stippled area) between the coronary arteries. The small rectangles indicate islands of normal tissue amid the aneurysms.

Case 4; Fig. 6; Heart 1505 The heart of a cow of unknown history and at least 3 years old was enlarged to about 1l/z times the normal size. The only malformation was an anomalous origin of the right coronary artery, which arose exactly above the right cusp of the pulmonary trunk, but thereafter had a normal course. There were some slight anastomoses between the small rani of the right and left coronary arteries. The main vessels were of normal diameter.

Case 5; Fig. 7; Heart 163 The heart of a 2-month-old calf of unknown history was free of any macroscopic anomaly. The only malformation was an anomalous origin of the left coronary artery, which arose exactly above the caudal cusp of the pulmonary trunk but thereafter had a normal course. The two coronary arteries did not anastomose grossly and were of normal diameter.

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Fig. 9.Diagram showing anastomosis (stippled area) between left coronary artery and left ventricle. Fig. 10. Diagram showing hypoplasia of the aorta and origin of the right coronary artery from the aortic wall.

Case 6 ;Fig. 8 ;Heart 1693 A cow of at least 3 years of age and unknown history had a much larger than normal heart (1 1/2 x). The right coronary artery originated exactly above the right cusp of the pulmonary trunk. The courses of both coronary arteries were normal but there were many aneurysmal anastomoses between them. The main branches varied in diameter from 8 to 12 mm and the secondary branches between 5 and 8 mm. Obvious coronary arteroventricular anastomosis was lacking. Case 7; Fig. 9; Heart 1687

A cow at least 3 years old and of unknown history had a very large heart. An aneurysmatic left coronary artery anastomosed with the left ventricle. The points of origin and courses of both coronary arteries were normal. The rami circumflexi were of normal diameter. The origin and the common stem of the left coronary artery and the ramus descendens sinister were very wide; the latter ended in a large aneurysm that opened by a valve into the left ventricle at the apex.

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R 45

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Fig. f 1. Diagram showing hypopIasia of the pulmonary trunk and common origin of both coronary arteries from an aneurysm indicated by dotted lines. Fig. 12. Diagram showing common origin of both coronary arteries.

Case 8; Fig. 10; Heart 1689 The heart of a 2-day-old hog deer (Axisporcinw) that died unexpectedly, had several malformations. These were remarkable hypoplasia of the aorta, a small high ventricular septal defect, premature closure of the foramen ovale secundum, relative hyperplasia of the pulmonary trunk, and origin of the right coronary artery from the aortic wall 2 cm distal to the cusp of the right semilunar valve. The origin of the left coronary artery was correctly situated; its diameter conformed with the hypoplasia of the aorta. The course of the coronary arteries resembled those of normal bovine arteries.

Case 9; Fig. 11; Heart 1607

A 2-day-old calf of unknown history had hypoplasia of the pulmonary trunk, 4 caval veins and situs inversus. The heart had a large high ventricular septal defect. The aorta had 3 normal semilunar cusps, was situated above the right ventricle, and was widened. An aneurysm (6 cm in diameter) 3 cm distal to the aortic cusps gave common origin to the right and left coronary arteries which were otherwise normal.

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Fig. 13. Diagram showing common origin of both coronary arteries. The concentric circles indicate stenosis of the pulmonary trunk. Fig. 14. Diagram indicating hypoplasia of the right coronary artery and hypoplasia of the aorta.

Case 10; Fig. 12; Heart 93 The heart of a 6-month-old calf of unknown history had a high ventricular septa1 defect. The coronary arteries had a common origin immediately distal and a little to the left of the right semilunar cusp of the aorta but were otherwise normal. The aorta was in a slight dextroposition; the pulmonary trunk and the aorta had normal semilunar cusps with 3 leaflets. Case 11; Fig. 13; Heart 1610 The heart was from a Cmonth-old calf of unknown history. It was an extreme case of tetralogy of Fallot, with a common origin of the coronary arteries, at a little distance from the caudal cusp of the aorta. The short common branch divided into 3 sub-branches, 2 of which followed the expected course of the left coronary artery and 1 that of the right artery; the latter lay to the right and craniad of the aorta. A small vessel formed an anastomosis between the aorta ascendens and the main stem of the left coronary artery. The aorta originated in the right ventricle (double outlet ventricle). The pulmonary trunk had a severe valvular and subvalvular stenosis.

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Case 12; Fig. 14; Heart 1688 The heart of a 6-week-old calf of unknown history had hypoplasia of the right coronary artery, hyperplasia of the left coronary artery, high ventricular septal defect, transposition and hypoplasia of the aorta (double outlet ventricle), stenosis of the isthmus aortae, and patency of the ductus Botalli s. arteriosus. The origin of the right coronary artery was hypoplastic and its septal and circumflex branches were poorly developed. The left coronary artery was slightly hyperplastic. Its common stem was divided into 2 branches, a ramus circumflexus cranialis and a ramus circumflexus caudalis. The latter divided into the ramus descendens sinister (anterioris), a ramus septalis, and a ramus descendens dexter (posterioris). The lesions observed in the 12 cases are summarized in Table I. TubZe I. Summary of Lesions in 12 Malformed Hearts* Figure Heart 3 183 Pig 4 5 6 1505

Anomalies of the coronary arteries anastomosis left c.a. with r.c.a. one origin of the c.a. (r.c.a.) one origin of the c.a. (1.c.a.) origin of the r.c.a. in the pulmonary trunk origin of the 1.c.a. in the pulmonary trunk origin of the r.c.a. in the pulmonary trunk origin of the 1.c.a. is aneurismatic high origin of the r.c.a.

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1693

9 10

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1687 1689 deer 1607

high origin of the r. and 1.c.a.

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common origin of both the c.a.

13 14

1610 1688

one common stem of the c.a. hypoplasia of the r.c.a. hyperplasia of the 1.c.a.

Other Anomalies

aneurisms aneurisms ventricular septal defect ; hypoplasia of the aorta situs inversusventricular septal defecthypoplasia pulmonary trunk high ventricular septal defect Tetralogy of Fallot double outlet ventricle; hypoplasia of the aorta; stenosis of the isthmus aortae

* All cases are bovine except the ones marked pig or deer.

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Discussion In the light of my findings a tenable general theory of the genesis of the coronary arteries does not exist. In my material anomalous origin of 1 or both of the coronary arteries from the pulmonary trunk occurred only in the uncomplicate cases (Table I). Such a position did not occur in association with other cardiac malformations. If these anomalies be developed under the influence of an abnormal septation of the truncus arteriosus, one may expect an anomalous origin of one or both the coronary arteries from the pulmonary trunk. However, such a condition is unknown in my collection of congenital anomalies of the heart of cattle and pigs. It is, therefore, my opinion that the theory of anomalous septation of the truncus arteriosusl9 10915 as a cause of an anomalous origin of the coronary arteries is not tenable. This opinion is in accordance with GRANT^^ and PAT TEN^^ who state that the septation of the truncus arteriosus is already established before the primordia of the coronary arteries appear. The hypothesis of the development of more than two coronary arterieslgs 2092% 31 and the closure of most of them except the two remaining ones may be true but it has not been proved. BECKER5 reported small arteries which have their origin in the pulmonary trunk, but in our cases more than two main arteries did not occur. The hypothesis of abnormal potentials's 8, 21,399 42, positive or negative, of the bulbus-truncus cushions to form the primordia of the coronary arteries may be right but has also not been proved. All our cases may be developed under such conditions. The endothelial cell of the embryo has many potentials;however, we know very little about the mechanism of these processes. The reasons for the finding of different types of these anomalies in different species of animals and the human being is also not very clear. One of the reasons may be that veterinary cases are found in slaughterhouses, where predominantly healthy animals are examined, whereas human cases are chiefly found in the postmortem examination of patients who died of disease. Another reason may be a difference in the embryogenesis of the arteries. Since we know there is an important differencein the gross anatomy of the arteries, it seems reasonable to expect that the second factor will be very important. A more detailed comparative anatomical and embryological study of the heart is necessary in order to solve these problems.

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Twelve different cases of anomalous origin of the coronary arteries in animals are reported, 10 from cattle, 1from a pig, and 1 from a deer. The etiology of these anomalies is not yet clear. The hypothesis of abnormal potential of development of the bulbus-truncus cushions may be right, though it has not been proved.

Zwammenfassung Es wird iiber 12 verschiedene Falle von Anomalien des Herzarterienursprunges bei Tieren berichtet, und zwar bei 10 Rindern, einem Schwein und einem Reh. Die Atiologie dieser Anomalien ist noch unklar. Moglicherweise ist die Hypothese eines anomalen Entwicklungspotentials der Bulbus-Truncus-Polster korrekt, jedoch ist sie noch nicht bewiesen worden.

Acknowledgements Our thanks are due to Drs. P. ZWART and A.P. van der LINDEwho supplied the hearts 1689 and 1687.

References 1. ABRIKOSSOFF, A. : Aneurysma des linken Herzventrikels mit abnormer Abgangsstelle der linken Koronararterie von der Pulmonalis bei einem fiinfmonatlichen Kinde. Virchotus Arch. 203: 413-420 (1911). 2. ALTMANN, L. : Mit der rechten Herzkammer anastomosierendes Aneurisma der Arteria coronaria sinistra. AZZatorvosi Lapok 49: 99 (1926). Abstract in Jahresb. Vet. Med. 4G: 638 (1926). 3. BARONE, R.: Une anomalie rare des vaisseaux du cmur chez une mule. Rec. Mid. vN. 128: 93-96 (1952). 4. BENNETT, H.S.: The development of the supply to the heart in the embryo pig. Amer. J. Anat. 60: 27-54 (1936). 5. BECKER,A.: Mededeling Anatomendag 11, XII, Amsterdam (1966). 6. BERG,R. : Zur Morphologie der Koronargefasse des Schweines unter besonderer Beriicksichtigung ihres Verhaltens zum Myokard. Arch. exp. Vet.-Med. 19: 1145-1307 (1965). 7. BROUWER, H.A. : De normale en pathologische anatomie en histologie van de arteriele component van het coronaire circulatie systeem. Thesis, Utrecht (1963). 8. CERVEN+,C. and KAMAN, J. : Common stem of the coronary arteries in a calf. Anat. A n r . 113: 29-35 (1963). S.: To tilfaelde af kronisk 9. CHRISTENSEN,N.O. and DALGAARD-MIKKELSEN, ektasi af en af koronararterieme ved paa kongenitalt grundlag opstaaet kom-

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munikation til h ~ j r eventrikel hos oksen. Medlemsbl. danske Dyrlageforen. 28: 187-211 (1945). 10. CRONK,E.S.; SINCLAIR,J.G. and RIGDON,R.H.: An anomalous coronary artery arising from the pulmonary artery. Amer. Heart J. 42: 906-911 (1951). 11. DUTRA,F.R.: Anomalies o f coronary arteries. Arch. intern. Med. 85: 955-965 (1950). 12. ELLENBBRGER, W. und BAUM,H. : Handbuch der Vergleichende Anatomie der Haustiere (August Hirschwald, Berlin 1915). 13. EMSBO, P.: Misdannelse af Arterie coronariae cordis. Skand. Vet. Tidskr. 35: 211-233; 257-272 (1945). 14. FISHER, E.W. and PIRIE,H.M. : Cardiovascular lesions in cattle. Ann. N.Y. Acad. Sci. 127: 606-622 (1965). 15. GODGLUCK, G.: Uber den Abgang der rechten Kranzarterie aus der Pulmonalis und gleichzeitiger Reduction der Pulmonalisklappen bei einem Rinde. Arch. Tierbeilk. 77: 231-243 (1942). 15a. GODGL~CK, G. : Missbildungen der Koronararterien. pp. 29-30 in: Handbuch der speziellen pathologischen Anatomie der Haustiere (DOBBERSTEIN, J.; PALLASKE, G. and STUNZI, H. eds.) Vol. 2, 3rd edition. (Paul Parey, Berlin 1963). 16. GOLDSMITH, J.B. and BUTLER, H.W.: The development of the cardiac coronary circulation system. Anaer.J. Anad. GO: 185-202 (1937). 17. GRANT,R.T.: Development of the cardiac coronary vessels in the rabbit. Heart 13: 261-271 (1926). 18. GRANT,R.T. : An unusual anomaly of the coronary vessels in the malformed heart of a child. Heart 13: 273-283 (1926). 19. GRXTZER, G.: Der Seitenbahnenkreislauf an einem Herzen mit einer Kranzschlagader. Virchows Arch. 262: 608-614 (1926). 20. HACKENSELLNER, H.A. : Ober accessorische, von der Arteria pulmonalis abgehende Herzgefasse und ihre Bedeutung fur das Verstandnis der formalen Genese des Ursprunges einer oder beider Coronaraiterien von der Lungenschlagader. Frankf. Z. Path. 66: 463-470 (1955). 21, LIMBOURGH, M. : Ober den Ursprung der Kranzarterien des Herzens aus der Arteria pulmonalis. Beitr. path. Anat. YOU: 191-194 (1938). 22. LUMB, G. and SINGLBTARY, H.: Blood supply to cardiac conduction tissue in pig and man. Surgical Forum 12: 218-220 (1961). 23. LUMB, G. and SINGLETARY, H.: Blood supply to the atrioventricular node and bundle of His: Comparative study in pig, dog and man. Amer. J. Putb. 41: 65-75 (1962). 24. MARTIN,H.: Recherches anatomiques et embroloques sur les arttres coronaires du cceur chez les vertkbrks. ThCse, Paris (1894). 25. PATTEN,B.M. : Embryology of the Pig, 3rd ed. (Blakiston, Philadelphia 1948). 26. PETRAN,T.: Ein Fall von Mangel der A. coronaria cordis dextra. Virchom Arch. 278: 158-164 (1930). 27. PIRINGER-KUCHINKA, A. : Typische Varietat der Koronararterien. Anat. An?. 98: 97-104 (1951). 28. POLLAK, E.: Zur KeMtnis der Anomalien und Fehlbildungen der Kranzarterien des Herzens. Inaug. Diss. Wiirzburg (1959). 0.: Kongenitale Anomalie der rechten Ventrikelwand und Koro29. RASCHKE,

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nararterie beim Rinde. 2. Fleiscb. Milcbh. 25: 354-356 (1915). 30. REID, C. : Abnormal left coronary artery of ox heart communicating directly with the cavity of the left ventricle near the apex. J. Anat. 57: 12-17 (1923). 31. RICHTER,C.: uber das Fehlen einer Kranzarterie. Vircbows Arch. 299: 637-642 (1937). 32. ROBB,J.S.: Comparative Basic Cardiology (Grune & Stratton, New York 1965). 33, RUBLI,H. : Einzigartige Missbildung eines Zweiges der Arteria coronaria sinistra beim Kalbherzen. Anat. A n x . 77: 169-177 (1933). 34. RUBLI,H. : Noch eine Missbildung der Arteria coronaria sinistra beim Kalbherzen. Anaf. An?. 78: 47-51 (1934). W. : Bisher unbekannte Missbildung der Arteria coronaria sinistra 35. SCHAUDER, des Rindes. Anat. Anx. 58: 540-552 (1924). 36. SCHONDUBE, W. : Verdoppelung des rechten Ventrikels mit Missbildung der Kranzarterien. Frank$ 2. Patb. 27: 197-225 (1922). R.M. : Het coronair arterioveneus aneurisma. Ned. T. Geneesk. 37. SCHUILENBURG, 109: 924-931 (1965). 38. VINK,H.H.; Vos, J.J. TH.; HEIDA,G. and DE VRIES,J.: Oorsprong der Kroonslagaderen uit de longslagader. Ned. T . Geneed 85: 44404441 (1941). 39. VITUMS, A. : Anomalous origin of the right coronary artery in a cow. ZbZ. Vet. Med. 10: 185-194 (1963). M.W.: Nomina Anatomica Parisiensa (1955) et B.N.A. (1895) 40. WOERDEMAN, ed. Oosthoek Comp., Utrecbt (1957). 41. WOLFFHUGEL, K.: Ursprung der Arteria coronaria cordis dextra aus der Arteria pulmonalis bei einem Rinde. Z. Fleisch MiZcbbyg. 72: 38-42 (1901). 42. WUTHRICH, R. : Uber den Abgang der Arteria coronaria sinistra aus der Arteria pulmonalis. Zugleich ein Beitrag zum Problem des plotzlichen Todes. Cardiohgia 18: 193-212 (1951). Author’s address: Dr. CJ. VAN NIK,Loevestein 15, Leidwdorp (The Netherlands).