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Case Reports Double outlet right ventricle and other associated congenital cardiac anomalies in an American Miniature Horse foal M. K. CHAFFIN*. M. W. MlLLERf and E. L. MORRIS
Departments of *Large Animal Medicine and Surgery and fSmall Animal Medicine and Surgery, Texas Veterinary Medical Center, College of Veterinary Medicine, Texas A& M University, College Station, TX 77843-4476 USA.
Introduction CONGENITAL cardiac anomalies are uncommon in the horse, accounting for only 3.5% of all congenital defects (Crowe and Swerczek 1985). Ventricular septal defects (VSD) are the most common congenital cardiac anomaly in the horse, and have been thoroughly described (Rooney and Franks 1964; Glazier, Farrelly; and O'Connor 1975; Huston, Saperstein and Leipold 1977; Crowe and Swerczek 1985). Other reported congenital cardiac anomalies include patent ductus arteriosus (Rooney and Franks 1964; Buergelt, Carmichael, Tashjian and Das 1970; Glazier, Farrelly and Neylon 1974; Machida, Yasuda and Too 1987), tetralogy of Fallot (Greene, Wray and Greenway 197% truncus arteriosus (Greene et a/. 1975; Rooney and Franks 1964). pseudotruncus arteriosus (Bayly et al. 1982). atrial septal defects (Rooney and Franks 1964), valvular defects (Rooney and Franks 1964; Critchley 1976; Button, Gross, Allert and Kitzman 1978; Bayly et a/. 1982; Reef, Mann and Orsini 1987), ventricular hypoplasia (Musselman and LoGuidice 1984). double outflow right ventricle (Vitums 1970), pulmonary atresia (Vitums, Grant, Stone and Spencer 1973; Vitums and Bayly 1982) and aortic anomalies (Scott, Chaffee, Eyster and Kneller 1978). We can find no reports of congenital cardiac anomalies in American Miniature Horses, or reports of anomalous pulmonary venous connection in the horse. The purpose of this report is to describe an American Miniature Horse foal with double outlet right ventricle (DORV), subpulmonary ventricular septal defect. subpulmonary muscular stenosis, atrial septal defect, anomalous pulmonary venous connection, and a single coronary artery.
Case history A 2-day-old, male American Miniature Horse foal was referred to
the Texas Veterinary Medical Center at Texas A&M University for evaluation of cyanosis and a loud systolic cardiac murmur. The foal was born unassisted and without complications, but demonstrated tachypnoea and syncope when handled.
Clinical findings The foal was bright, alert and responsive when examined. Rectal temperature was 38.3"C; pulse and respiratory rates were 200 and 100/min, respectively. Hydration was normal and the foal sucked vigorously. Mucous membranes were cyanotic, but capillary refill time was normal. When handled, the foal would struggle briefly,
become tachypnoeic, and collapse. Thoracic auscultation revealed normal pulmonary sounds and a grade V/VI holosystolic murmur with the point of maximal intensity located at the left cardiac base. Results of a complete blood count and serum biochemistry and electrolyte profiles were within normal limits. A radial immunodiffusion test demonstrated adequate passive transfer of immunoglobulins (IgG concentration, 2050 mg/dl). Blood gas analysis of a sample obtained from the great metatarsal artery demonstrated hypoxaemia ( Pao2, 23.6 mmHg). After placement of an intranasal insufflation tube, the foal was given 100% 0 2 at 3 litres/min for 15 min. Mucous membranes remained cyanotic, and subsequent arterial blood gas analysis (during O2 therapy) revealed persistent hypoxaemia ( Pao2, 23.8 mmHg), suggesting the presence of a right-to-left shunt (Krotje 1987; Shapiro, Harrison, Cane and Templin 1989; Bonagura 1989). Thoracic radiographs revealed a mildly increased interstitial pattern in the right caudal lung field, normal pulmonary vasculature and generalised cardiomegaly. The electrocardiogram was normal.
Echocardiography Two-dimensional echocardiography documented marked right ventricular hypertrophy, a 13-mm diameter membranous ventricular septal defect (VSD), and a 12-mm diameter atrial septal defect (ASD) in the area of the fossa ovalis. A thin, loose flap of tissue was imaged on the left atrial side of the ASD. Colour-flow and spectral Doppler echocardiography demonstrated left-to-right shunting of blood across the ASD and left-to-right shunting of blood across the VSD into the outflow tract of the pulmonary artery. A peak pressure gradient of 67 mmHg between the left and right ventricle was estimated based on spectral Doppler recordings. Only one major vessel could be adequately visualised leaving the heart and a tentative diagnosis of truncus or pseudotruncus arteriosus, ASD and VSD was made.
Cardiac catheterisation Cardiac catheterisation was performed under isoflurane general anaesthesia. The right jugular vein and carotid artery were surgically exposed and catheterised with a seven french NIH and seven french pigtail catheter, respectively. Advancement of the carotid catheter across the aortic valve resulted in catheterisation of the anatomical right ventricle. Advancement of the jugular venous catheter across the tricuspid valve also resulted in catheterisation of the anatomical right ventricle. The left ventricle
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Fig I : Angiograms of an American miniature horse foal with multiple congenital cardiac anomalies. ( a ) Selective right ventricular angiogram demonstrating opacification of the right ventricle and preferential filling of the aorta. A lesser amiiuni of contrast is seen in the pulnzonary artery. The single coronary artery is seen cranial to the aortic sinus (arrow).(h) The aortic catheter is placed across the ventricular septal defect into the left ventricle. Contrast medium can he seen in the leji ventricle and has preferentiaMy jilled the pulmonary artery via the suhpulmonary VSD. Contrast material also can he seen in (he right Lrentricular orutlon~tract and proximal aorta
Fig 2: Photographs of the hear1 of an American Miniature Horse $)a1 with multiple congenital cardiac anomalies. ( a ) Cranial \tiew, of the intact heari demonstrating the parallel course of the initial segments of the aorta (Aoi and pulmonary artery (PA),as well as the single coronary artery arising from the right aortic sinus (arrowhead). (h) Cross-sectional view of the heart at the level of the ventricular septal defect (arrow) and Lrntricular ourflow tracts. Note that both the aorta and pulmonary artery Iea\,e the right ventricle. There is muscular stenosis ofthe right ,,entricular outflonj rract (arrowheads)just below the pulmonay ltalve
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was catheterised by manipulating the carotid catheter across the aortic valve and through the VSD. Injection of contrast material (I5 ml, 100 kg/cm': Renograffin-76, Squibb Diagnostics, New Brunswick, NJ, USA) into the right ventricle opacified the right ventricle, aorta, a single coronary artery and, to a lesser extent, the pulmonary artery (Fig la). Injection of contrast material into the left ventricle opacified the left ventricle, pulmonary artery and, to a lesser extent, the aorta (Fig Ib). The ante-mortem diagnoses were VSD, septum secundum ASD, single coronary artery and double outlet right ventricle (DORV). The prognosis for long-term survival and performance was poor, and at the owner's request. the foal was destroyed while still under anaesthesia. Pathology
Post-mortem examination confirmed DORV, single coronary artery, membranous VSD and septum secundum ASD. The initial segments of the aorta and pulmonary artery were parallel to each other (Fig 2a). Further from the heart, the aorta was cranial and to the right of the pulmonary artery. The aorta arose from the anatomical right ventricle and had a normal tricuspid semilunar valve. The pulmonary artery also arose from the anatomical right ventricle and had a normal semilunar valve. A 13-mm diameter VSD was present at the uppermost aspect of the septum, just below the pulmonary valve. The outflow tract to the pulmonary artery was narrowed by muscular hypertrophy immediately below the pulmonary valve and above the VSD (Fig 2b). A circular, 14mm diameter, septum secundum ASD was present at the level of the fossa ovalis. A small, thin flap of tissue partly covered the defect, leaving a 7-mm opening. This flap was freely movable between the atria. The ductus arteriosus was not patent. The coronary circulation arose from a single coronary artery originating from the right aortic sinus (Fig 2a). There was no evidence of a coronary ostium in either of the other two aortic sinuses. The single coronary artery consisted of a short ( 3 4 mm) initial segment which divided to form the left cranial descending coronary artery (paraconal interventricular) and the right coronary artery. The right coronary artery had a normal course along the right coronary groove. At the level of the coronary sinus, the right coronary artery bifurcated into a subsinuosal interventricular artery (normal in pigs and horses) and an artery that continued along the left coronary groove, a position similar to that normally occupied by the left circumflex coronary artery. Careful dissection of the pulmonary venous system revealed that 6 separate pulmonary veins entered the left atrium normally. The pulmonary vein arising from the cranial or apical portion of the right lung entered the dorsal aspect of the right atrium caudal to the azygous vein and cranial to the intervenous tubercle. The previously identified ASD was located caudal to the intervenous tubercle in the area of the fossa ovalis, differentiating it from a sinus venosus ASD. Histological examination of the lungs revealed no abnormalities.
Discussion Double outlet right ventricle describes a specific type of ventriculoarterial connection in which the aorta and the pulmonary trunk are connected to the morphological right ventricle. A great artery is considered to be connected to a ventricle when >50% of its circumference originates from that ventricle (Becker and Anderson I98 I ; Perloff 1987). This cardiac anomaly has been dessribed in man (Becker and Anderson 1981; Perloff 1987), dogs (Turk, Miller and Hegreberg 198I ; Bonagura 1989), cats (Jeraj ef al. 1978), cattle (Godgluck 1962). pigs (Olafson 1939) and one horse (Vitums 1970). The estimated incidence of DORV in man is 0.09 per 1000 live births (Mitchell, Korones and Berendes 1971) or 4.5% of necropsy cases of congenital cardiac anomalies (Van Praagh e f al. 1982). There is
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some evidence to suggest that DORV arises due to arrest of the normal rotation of the semilunar valve region during embryogenesis (Bostrom and Hutchins 1988). The complex anatomy of DORV is classified based on three essential gross morphological features: the relationships of the great arteries to the ventricles, the relationships of the VSD to the great arteries and the presence or absence of obstruction to right ventricular outflow. There are 4 types of relationships between the great arteries and the ventricles: ( I ) aorta is to the right of and caudal to the pulmonary trunk, (2) great arteries are side by side with the aorta to the right of the pulmonary trunk, (3) aorta is to the right of and cranial to the pulmonary trunk, and (4) aorta is to the left of and cranial to the pulmonary trunk. A VSD provides the morphological left ventricle with its only outlet. The VSD is either subaortic, subpulmonary, beneath both great arteries (doubly committed), beneath neither great artery (uncommitted) or absent altogether. These 4 locations combined with the 4 relationships of the great arteries result in 16 possible combinations of DORV (Perloff 1987). The aorta and pulmonary artery of this foal were side-by-side with the aorta to the right of the pulmonary trunk. This is the usual arrangement in people with DORV. The origin of the pulmonary trunk from the right ventricle and the lack of fibrous continuity between the semilunar valves and the atrioventricular valves differentiated this heart from those with complete transposition of the great vessels (Perloff 1987). In people with DORV, the VSD is most commonly in the subaortic position (Sridaromont et al. 1978). The VSD in this foal was located in the subpulmonary position. In DORV with the great vessels side-by-side and the aorta to the right of the pulmonary trunk, a subpulmonary VSD is referred to as the Taussig-Bing anomaly. With this arrangement, the oxygenated blood from the left ventricle selectively enters the pulmonary trunk because the VSD is committed to the pulmonary artery (Sridaromont ef a / . 1976, 1978). The Taussig-Bing anomaly accounts for approximately 8% of all people with DORV (Sridaromont et a/. 1978) and clinical manifestations resemble those of complete transposition of the great arteries. Cyanosis is present at or shortly after birth because of obligatory flow of unoxygenated blood from the right ventricle into the aorta (Beuren 1960). Left ventricular blood selectively enters the pulmonary artery, unless pulmonary stenosis shunts some of the left ventricular outflow into the aorta. Muscular subpulmonary stenosis was present in this foal's heart just above the VSD. Pulmonary stenosis has been reported in 41-72% of people with DORV (Sridaromont e f ul. 1978; Van Praagh et al. 1982), but is uncommon in people with a subpulmonic VSD (Argawala et ul. 1973). Partial anomalous pulmonary venous connection (PAPVC) is a communication of one or more, but not all, of the pulmonary veins to the right atrium or cavae. This anomaly has been reported in dogs (Hilwig and Bishop 1975) and is estimated to be present in 0.6% of all people (Lucas 1983). In people, PAPVC is commonly associated with a sinus venosus-type ASD (Nugent et ul. 1985). Isolated, uncomplicated PAPVC involving a single pulmonary vein is usually undetected since only 20% or less of pulmonary venous blood would return to the right atrium. Diagnosis is difficult; electrocardiography and echocardiography may detect volume overload of the right heart, but a selective angiogram with a venous catheter placed in the anomalously connected pulmonary vein is needed to document the site of connection (Nugent et a / . 1985). Surgical treatment involves the placement of a contoured intracardiac patch to divert anomalously delivered pulmonary venous blood into the left atrium through a surgically created ASD (Murphy, Kerr and Kirklin 1971). Atrial septa1 defects have been reported i n horses (Rooney and Franks 1964; Physick-Sheard, Maxie, Palmer and Gaul 1985), cattle (Gopal et a / . 1986), pigs (Hsu and Du 1982), dogs (Hamlin, Smith and Smetzer 1963;jeraj et a / . 1980; Lombard,
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Ackerman and Berry 1989), cats (Farrow 1984) and an antelope (Chaffin, Miller, Jensen and Hall 1990). Four types of ASD can occur: patent foramen ovale, ostium primum ASD, ostium secundum ASD and sinus venosus ASD. The last three types are differentiated by their location in the atrial septum (Chaffin et al. 1990). The ASD in our foal was of the ostium secundum type, located in the fossa ovalis (midseptal) region of the septum with normal septal tissue between the defect and the atrioventricular valves (Hamlin et al. 1963; Pyle 1983). The large size of the defect and presence of a left-to-right shunt differentiated it from patent foramen ovale (Pyle 1983). Atrial septal defects usually result in left-to-right shunts because the right ventricular walls are thinner and more compliant and the orifice of the tricuspid valve has a larger cross-sectional area than does the mitral valve. Resultant volume overload of the right atrium, right ventricle, pulmonary artery and pulmonary veins leads to enlargement of these structures (Bonagura 1989). In man, ASD is a common anomaly associated with DORV (Van Praagh et al. 1982). Anomalies of coronary arteries have occurred in people (Ogden and Goodyear 1970 Ogden I970 Vlodaver, Neufeld and Edwards 1975; Lipton et al. 1979; Dabizzi et al. 1980; Roberts 1986) and dogs (Buchanan 1990), and have been associated with pulmonary stenosis in dogs (Buchanan 1990) and DORV in people (Van Praagh et al. 1982). Single right (R) or left (L) coronary arteries are classified on the basis of the location of the branch that crosses to the opposite side (Lipton et al. 1979). The distribution of the coronary circulation in our foal did not match any of the typical classifications reported for people or dogs (Lipton et al. 1979; Dabizzi et al. 1980), but most closely resembled the type RI circulation described for people (Lipton et al. 1979). This may reflect interspecies differences in normal coronary artery distribution. Horses and pigs have a right dominant coronary system, while people, dogs, cats and cattle have a left dominant coronary system. One report describes a Thoroughbred yearling with a single right coronary artery (Rooney and Franks 1964), similar to the type R2A described for people and dogs (Lipton et al. 1979; Buchanan 1990). that presumably resulted in left ventricular failure. Several echocardiographic formats including M-mode (Reef 1985, 1987, 1991; Clark, Reef, Sweeney and Lichtensteiger 1987; Reef et al. 1987; Lombard, Scarratt and Buergelt 1983; Bayly et al. 1982; Pipers, Hamlin and Reef 1979), 2-dimensional real-time (Reef et al. 1987; Clark et al. 1987; Reef 1985, 1987, 1991; Carlstein 1987; Pipers, Reef and Wilson 1985; Bayly et al. I982), Doppler (Moise 1989; Reef 1991) and contrast echocardiography (Reef et al. 1987; Kvart, Carlsein, Jeffcott and Nilsfors 1985; Bonagura and Pipers 1983) have been used to document congenital cardiac malformations in the horse. In the present foal, 2-dimensional real-time echocardiographic evaluation detected the VSD and ASD and suggested an anomaly of the ventricular outflow tracts. In addition, colour-flow and spectral Doppler echocardiography documented the left-to-right shunts through the VSD and the ASD. The definitive nature of this defect, however, could only be determined by angiocardiography and post-mortem examination. In conclusion, this 2-day-old American Miniature Horse foal had cyanosis, exercise-induced syncope, and a systolic heart murmur. Echocardiography and selective angiocardiography detected DORV, VSD, ASD and a single coronary artery. Postmortem examination confirmed each of these findings, demonstrated subpulmonary muscular stenosis and documented the presence of partial anomalous pulmonary venous connection to the right atrium. The arrangements of the VSD and the great vessels resembled the Taussig-Bing anomaly as described in man. As the popularity of the American Miniature Horse increases, veterinarians may encounter more congenital cardiac anomalies.
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Acknowledgement We thank Dr Rebecca Heaton for referral of this case. References Argawala. 8.. Doyle, E X , Danilowicz. D.. Spencer, F.C. and Mills, N.M. (1973) Double outlet right ventricle with pulmonic stenosis and anteriorly positioned aorta (Taussig-Bing variant). Am. J. Cardiol. 32. 850-854. Bayly, W.M.. Reed. S.M.. Leathers. C.W.. Brown, C.M., Traub. J.L.. Paradis. M.R. and Palmer, G.H. (1982) Multiple congenital heart anomalies in five Arabian foals. J . Am. ver. med. Assoc. 181,684-689. Becker. A.E. and Anderson, R.H. (1981) Pathology of Congenifal Heart Disease. Butterworths and Co. Ltd.. London. pp 297-307. Beuren, A. (1960) Differential diagnosis of the Taussig-Bing heart from the complete transposition of the great vessels with a posteriorly overriding pulmonary artery. Circulation 21, 1071-1087. Bonagura, J.D. (1989) Congenital heart disease. In: Te.rrhook i f ' Veterinary Inrernal Medicine, Diseases of rhe Dog and Car. 3rd edn. Ed: S.J. Ettinger. W.B. Saunders Co. Philadelphia. pp 976-1030. Bonagura, J.D. and Pipers. F.S. (1983) Diagnosis of cardiac lesions by contrast echocardiography.J. Am. ver. med. Assoc. 182,396-402. Bostrom, M.P.G. and Hutchins. G.M. (1988) Arrested rotation of the outflow tract may explain double-outlet right ventricle. Circulation 77. 1258-1265. Buchanan, J.W. (1990) Pulmonic stenosis caused by single coronary artery in dogs: Four cases (1965-1984). J. Am. vet. med. Assoc. 196. 115-120. Buergelt. C.D.. Carmichael. J.A.. Tashjian. R.J. and Da$. K.M. (1970) Spontaneous rupture of the left pulmonary artery in a horse with patent ductus arteriosus. J. Am. set. med. Assoc. 157,313-320.
Button. C., Gross, D.R., Allen. J.A. and Kitzman, J.V. (1978) Tricuspid atresia in a foal. J. Am. vet. med. Assoc. 172.825-830. Carlstein. J.C. (1987) no-dimensional. real-time echocardiography in the horse. Vet. Radiol. 28.76-78. Chaffin. M.K.. Miller. M.W.. Jenson. J.M.and Hall, D.G. (1990) Echocardiographic diagnosis of atrial septal defect in a newborn bongo (Boocerus eurycerus) with hypogammaglobulinemia and septicemia. J. Zoo Wildlve Med. 21,358-365. Clark, E.S.. Reef, V.B.. Sweeney. C.R. and Lichtensteiger. C. (1987) Aortic valve 191,841-844. insufficiency in a one-year-old colt. J. Am. vet. med. ASSCJC. Critchley. K.L. (1976) An interventricular septal defect, pulmonary stenosis and bicuspid pulmonary valve in a Welsh pony foal. Equine vet. J. 8. 176-178. Crowe. M.W. and Swerczek, T.W. (1985) Equine congenital defects. Am. J. iw. Res. 46,353-358.
Dabizzi, R.P., Caprioli. G.. Aiazzi. L.. Castelli. C.. Baldrighi, G., Parenzan. L. and Baldrighi. V. (1980) Distribution and anomalies of coronary arteries in tetralogy of Fallot. Circularion 61.95-102. Farrow, C.S. (1984) Atrial septal defect in a kitten. Mod. ver. Pracr. 65,281-282. Glazier, D.B.. Fmeily. B.T. and Neylon, J.F. (1974) Patent ductus arteriosus in an eight-month-old foal. Ir. r'er. J. 28. 12-13. Glazier, D.B., Farrelly. B.T. and O'Connor. J. (1975) Ventricular septal defect in a 7year-old gelding. J. Am. vef.med. Assoc. 167,49-50. Godgluck. G. (1962) Missbildungen des Herzens bei Tieren. Dtsch fierarzfl.Wschr. 69.98-102.
Gopal, T.. Leipold. H.W. and Dennis, S.M. (1986) Congenital cardiac defects in calves.Am. J. ver. Res. 47, 1120-1121. Greene. H.J., Wray. D.D. and Greenway, G. A. (1975) n o equine congenital cardiac anomalies. IK vet. J. 29. 115-117. Hamlin. R.L.. Smith, C.R. and Smetzer. D.L. (1963) Ostium secundum type interatrial septal defects in the dog. J. Am. r'et. med. Assoc. 143. 149-157. Hilwig. R.L. and Bishop, S.P. (1975) Anomalous pulmonary venous return in a Great Dane. Am. J. ver. Rex 36, 229-233. Hsu. F.S. and Du. S.J. (1982) Congenital heart disease in swine. Vet. Pafhol. 19.676686.
Huston. R., Saperstein. G. and Leipold. H.W. (1977) Congenital defects in foals. J. equineMed. Surg. 1, 146-161. Jerdj. K., Ogburn, P.N., Jessen. C.A.. Miller, J.D. and Schenk, M.P. (1978) Double outlet right ventricle in acat. J. Am. vet. med. Assoc. 173, 1356-1360. Jeraj, K., Ogburn. P.N., Johnston, G.R.. Edwards. W.. Yano. B., Brunson. D.. Wallace, L. and McGrath. C. (1980) Atrial septal defect (sinus venosus typebin a dog. J. Am. set. med. Assoc. 177, 342-346. Krotje, L.J. (1987) Cyanosis: physiology and pdthOgeneSiS. Comp. Conr. Ed. Pract. Vet. 9.271-278. Kvan. C.. Carlsten, J., Jeffcott. L.B. and Nilsfors. L. (1985) Diagnostic value of contrast echocardiography in the horse. Equine vet. J . 17. 357-360. Lipton, M.J.. Barry. W.H., Obrez, 1.. Silverman. J.F. and Wexler. L. (1979) Isolated
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406 single coronary artery: diagnosis, angiographic classification. and clinical significance. Radifdogy 130. 39-47. Lombard. C.W., Scarratt. W.K. and Buergelt. C.D. (1983) Ventricular septal defects in the horse. J.Am. vet. med. Assoc. 183. 562-565. Lombard. C.W.. Ackerman. N. and Berry. C.R. (1989) Pulmonic stenosis and rightto-left atrial shunt in three dogs. J. Am. vet. med. Assoc. 1. 71 -75. Lucas. R.V.. Jr (1983) Anomalous venous connections. pulmonary and systemic. In: MOSS'Heart Disease in Infants, Children and Adolescents. Eds: F.H. Adams and G.C. Emmanouilides. The Williams and Wilkins Co. Baltimore, pp 458. Machida. N.. Yasuda. J. and Too, K. (1987) Auscultatory and phonocardiographic studies on the cardiovascular system of the newborn thoroughbred foal. Jpn J. wr, Res. 35. 235-250. Mitchell. S.C.. Komnes, S.B. and Berendes, H.W. (1971) Congenital h e m disease in 56.109 births; incidence and natural history. Circrtlation43,323-332. Moise. N.S. (1989) Doppler echocardiographic evaluation of congenital cardiac disease. J. vet. intern. Med. 3. 195-207. Murphy, J.W.. Kerr. A.R. and Kirklin. J.W. (1971) lntracardiac repair for anomalous pulmonary venous connection of right lung to inferior vena cava. Ann. Thorac. Surg. 11. 38-42. Musselman. E.E. and LoGuidice. R.J. ( 1984) Hypoplastic left ventricular syndrome in a foal. .I.Am. vet. med. Assoc. 185.542-543. Nugent. E.W.. Plauth. W.H., Edwards. J.E.. Schlant. R.C. and Williams. W.H. (1985) Congenital heart disease. In: The Hearr. 6th edn. Ed: J.W. Hurst. McGraw-Hill Inc. New York, pp 580-728. Ogden. J.A. (1970) Congenital anomalies of the coronary arteries. Am. J. Cardiol. 25.474-479.
Ogden, J.A. and Goodyear. A.V.N. (1970) Patterns of distribution of the single coronary artery. Yale J. Bio/. Med. 43. I 1-2 I . Olafson. I? (1939) Congenital cardiac anomalies in animals. Bit// int. Ass. Med. Mtts. 19. 129-134. Perloff. J.K. (1987) The Clinical Remgnition c f l Congenifal Heart Disease. W.B. Saunders Co.. Philadelphia, pp 443-466. Maxie. M.G.. Palmer, N.C. and Gaul, C. (1985) Atrial septal tent ostium primum type with hypoplasiic right ventricle in a Welsh pony foal. Can. J. conrp. Med. 49.429-433. Pipers. F.S., Hamlin, R.L. and Reef. V.B. (1979) Echocardiographic detection of cardiovascular lesions in the horse. J. equine Med. Surg. 3.68-77. Pipers, F.S.. Reef. V.B. and Wilson, J. (1985) Echocardiographic detection of ventricular septal defects in large animals. J. Am. vet. med. Assoc. 187. 8 10-816.
Pyle. R.L. ( 1983) Congenital heart disease. In: Testbook of Vererinury lnrenral Medicine. Diseases ofthe Dog and Cat. 2nd edn. Ed: S.J.Eltinger. WE Saunders Co, Philadelphia. pp 933-959. Reef, V.B. (1985) Cardiovascular disease in the equine neonate. Ver. Clirtic,sN. Am. (Large Anim. Pract.) 1. 117-129. Reef, V.B. (1987) Mitral valve insufficiency associated with ruptured chordae tendineae in three foals. J . Am. vet. m d . A.wJ~..191. 329-33 I, Reef. V.B. (1991) Echocardiographic findings in horses with congenital cardiac diseae. Conrp Cnnt. Ed. Pracl. Vet. 1. 109-1 17. Reef, V.B.. Mann. P.C. and Orsini. P.G. (1987) Echocardiographic detection of tricuspid atresia in two foals. J. Am. vet. med. Assoi,. 191, 225-228. Roberts. W. (1986) Major anomalies of coronary arterial origin seen in adulthood. Am. Hearr J. 111.941-963. Rooney. J.R. and Franks, J.R. (1964) Congenital cardiac anomalies in horses. Vet, Pathol. 1.454-464. Scott, E.A.. Chaffee. A,. Eyster. G.E. and Kneller. S.K. (1978) Interruption of aortic arch in two foals. J. Am. wr. med. Assoc. 172.347-350. Shapiro, B.A.. Harrison, R.A.. Cane. R.D. and Templin. R. (1989) Cliniwl Applicatian of BlfJod Gases. 4th edn. Year Book Medical Publishers Inc.. Chicago. pp 101-135. Sridaromont. S.. Feldt. R.H.. Ritter. D.G..Davis, G.D.and Edwards, J.E. (1976) Double-outlet right ventricle: Hemodynamic and anatomic correlations. Am ./. Cardiol. 38. 85-94. Sriddromont. S.. Ridder. D.G.. Feldt. R.H.. Davis. C.D. and Edwards, J.E. (197X) Double outlet right ventricle: Anatomic and angiocardiogrdphic correlations. Mayo Clin. Proc. 53.555-571. Turk, J.R., Miller, L.M. and Hegreberg. G.A. (1981) Double outlet right ventricle in a dog. .I.Am. Animal Hospital Assoc. 17. 789-792. Van Praagh. S.. Davidoff. A.. Chin. A., Shiel, F.S.. Reynolds. J. and Van Pradgh. R. (1982) Double outlet right ventricle: anatomic types and development implications based on a study of 101 autopsied cases. Coettr 8. 389. Vitums, A. (1970) Origin of the aorta and pulmonary trunk from the right ventricle in a horse. Ver. Pathol. 7.482-491. Vitums. A. and Bayly, W.M. (1982) Pulmonary atresia with dextroposition of the aorta and ventricular septal defect in three Arabian foals. Vet.Pathd 19, 160-168. Vitums. A,. Grant. B.D..Stone, E.C. and Spencer. G.R. (1973) Transposition of the aond and atresia of the pulmonary trunk in a horse. Cornell Vet. 63.41-57. Vlodaver. Z., Neufeld, H.N. and Edwards. J.E. (1975) C'oronap Arterial Variations in the Normal Heart and Congenital Heart Disease. Academic Press Inc. New York.
Receivedjiv publication: 9.9.91 Accepted: 23.12.91
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Eqrrir~rwf. .I. (1992) 24 (5)402-406
Case Reports Double outlet right ventricle and other associated congenital cardiac anomalies in an American Miniature Horse foal M. K. CHAFFIN*. M. W. MlLLERf and E. L. MORRIS
Departments of *Large Animal Medicine and Surgery and fSmall Animal Medicine and Surgery, Texas Veterinary Medical Center, College of Veterinary Medicine, Texas A& M University, College Station, TX 77843-4476 USA.
Introduction CONGENITAL cardiac anomalies are uncommon in the horse, accounting for only 3.5% of all congenital defects (Crowe and Swerczek 1985). Ventricular septal defects (VSD) are the most common congenital cardiac anomaly in the horse, and have been thoroughly described (Rooney and Franks 1964; Glazier, Farrelly; and O'Connor 1975; Huston, Saperstein and Leipold 1977; Crowe and Swerczek 1985). Other reported congenital cardiac anomalies include patent ductus arteriosus (Rooney and Franks 1964; Buergelt, Carmichael, Tashjian and Das 1970; Glazier, Farrelly and Neylon 1974; Machida, Yasuda and Too 1987), tetralogy of Fallot (Greene, Wray and Greenway 197% truncus arteriosus (Greene et a/. 1975; Rooney and Franks 1964). pseudotruncus arteriosus (Bayly et al. 1982). atrial septal defects (Rooney and Franks 1964), valvular defects (Rooney and Franks 1964; Critchley 1976; Button, Gross, Allert and Kitzman 1978; Bayly et a/. 1982; Reef, Mann and Orsini 1987), ventricular hypoplasia (Musselman and LoGuidice 1984). double outflow right ventricle (Vitums 1970), pulmonary atresia (Vitums, Grant, Stone and Spencer 1973; Vitums and Bayly 1982) and aortic anomalies (Scott, Chaffee, Eyster and Kneller 1978). We can find no reports of congenital cardiac anomalies in American Miniature Horses, or reports of anomalous pulmonary venous connection in the horse. The purpose of this report is to describe an American Miniature Horse foal with double outlet right ventricle (DORV), subpulmonary ventricular septal defect. subpulmonary muscular stenosis, atrial septal defect, anomalous pulmonary venous connection, and a single coronary artery.
Case history A 2-day-old, male American Miniature Horse foal was referred to
the Texas Veterinary Medical Center at Texas A&M University for evaluation of cyanosis and a loud systolic cardiac murmur. The foal was born unassisted and without complications, but demonstrated tachypnoea and syncope when handled.
Clinical findings The foal was bright, alert and responsive when examined. Rectal temperature was 38.3"C; pulse and respiratory rates were 200 and 100/min, respectively. Hydration was normal and the foal sucked vigorously. Mucous membranes were cyanotic, but capillary refill time was normal. When handled, the foal would struggle briefly,
become tachypnoeic, and collapse. Thoracic auscultation revealed normal pulmonary sounds and a grade V/VI holosystolic murmur with the point of maximal intensity located at the left cardiac base. Results of a complete blood count and serum biochemistry and electrolyte profiles were within normal limits. A radial immunodiffusion test demonstrated adequate passive transfer of immunoglobulins (IgG concentration, 2050 mg/dl). Blood gas analysis of a sample obtained from the great metatarsal artery demonstrated hypoxaemia ( Pao2, 23.6 mmHg). After placement of an intranasal insufflation tube, the foal was given 100% 0 2 at 3 litres/min for 15 min. Mucous membranes remained cyanotic, and subsequent arterial blood gas analysis (during O2 therapy) revealed persistent hypoxaemia ( Pao2, 23.8 mmHg), suggesting the presence of a right-to-left shunt (Krotje 1987; Shapiro, Harrison, Cane and Templin 1989; Bonagura 1989). Thoracic radiographs revealed a mildly increased interstitial pattern in the right caudal lung field, normal pulmonary vasculature and generalised cardiomegaly. The electrocardiogram was normal.
Echocardiography Two-dimensional echocardiography documented marked right ventricular hypertrophy, a 13-mm diameter membranous ventricular septal defect (VSD), and a 12-mm diameter atrial septal defect (ASD) in the area of the fossa ovalis. A thin, loose flap of tissue was imaged on the left atrial side of the ASD. Colour-flow and spectral Doppler echocardiography demonstrated left-to-right shunting of blood across the ASD and left-to-right shunting of blood across the VSD into the outflow tract of the pulmonary artery. A peak pressure gradient of 67 mmHg between the left and right ventricle was estimated based on spectral Doppler recordings. Only one major vessel could be adequately visualised leaving the heart and a tentative diagnosis of truncus or pseudotruncus arteriosus, ASD and VSD was made.
Cardiac catheterisation Cardiac catheterisation was performed under isoflurane general anaesthesia. The right jugular vein and carotid artery were surgically exposed and catheterised with a seven french NIH and seven french pigtail catheter, respectively. Advancement of the carotid catheter across the aortic valve resulted in catheterisation of the anatomical right ventricle. Advancement of the jugular venous catheter across the tricuspid valve also resulted in catheterisation of the anatomical right ventricle. The left ventricle
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Fig I : Angiograms of an American miniature horse foal with multiple congenital cardiac anomalies. ( a ) Selective right ventricular angiogram demonstrating opacification of the right ventricle and preferential filling of the aorta. A lesser amiiuni of contrast is seen in the pulnzonary artery. The single coronary artery is seen cranial to the aortic sinus (arrow).(h) The aortic catheter is placed across the ventricular septal defect into the left ventricle. Contrast medium can he seen in the leji ventricle and has preferentiaMy jilled the pulmonary artery via the suhpulmonary VSD. Contrast material also can he seen in (he right Lrentricular orutlon~tract and proximal aorta
Fig 2: Photographs of the hear1 of an American Miniature Horse $)a1 with multiple congenital cardiac anomalies. ( a ) Cranial \tiew, of the intact heari demonstrating the parallel course of the initial segments of the aorta (Aoi and pulmonary artery (PA),as well as the single coronary artery arising from the right aortic sinus (arrowhead). (h) Cross-sectional view of the heart at the level of the ventricular septal defect (arrow) and Lrntricular ourflow tracts. Note that both the aorta and pulmonary artery Iea\,e the right ventricle. There is muscular stenosis ofthe right ,,entricular outflonj rract (arrowheads)just below the pulmonay ltalve
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was catheterised by manipulating the carotid catheter across the aortic valve and through the VSD. Injection of contrast material (I5 ml, 100 kg/cm': Renograffin-76, Squibb Diagnostics, New Brunswick, NJ, USA) into the right ventricle opacified the right ventricle, aorta, a single coronary artery and, to a lesser extent, the pulmonary artery (Fig la). Injection of contrast material into the left ventricle opacified the left ventricle, pulmonary artery and, to a lesser extent, the aorta (Fig Ib). The ante-mortem diagnoses were VSD, septum secundum ASD, single coronary artery and double outlet right ventricle (DORV). The prognosis for long-term survival and performance was poor, and at the owner's request. the foal was destroyed while still under anaesthesia. Pathology
Post-mortem examination confirmed DORV, single coronary artery, membranous VSD and septum secundum ASD. The initial segments of the aorta and pulmonary artery were parallel to each other (Fig 2a). Further from the heart, the aorta was cranial and to the right of the pulmonary artery. The aorta arose from the anatomical right ventricle and had a normal tricuspid semilunar valve. The pulmonary artery also arose from the anatomical right ventricle and had a normal semilunar valve. A 13-mm diameter VSD was present at the uppermost aspect of the septum, just below the pulmonary valve. The outflow tract to the pulmonary artery was narrowed by muscular hypertrophy immediately below the pulmonary valve and above the VSD (Fig 2b). A circular, 14mm diameter, septum secundum ASD was present at the level of the fossa ovalis. A small, thin flap of tissue partly covered the defect, leaving a 7-mm opening. This flap was freely movable between the atria. The ductus arteriosus was not patent. The coronary circulation arose from a single coronary artery originating from the right aortic sinus (Fig 2a). There was no evidence of a coronary ostium in either of the other two aortic sinuses. The single coronary artery consisted of a short ( 3 4 mm) initial segment which divided to form the left cranial descending coronary artery (paraconal interventricular) and the right coronary artery. The right coronary artery had a normal course along the right coronary groove. At the level of the coronary sinus, the right coronary artery bifurcated into a subsinuosal interventricular artery (normal in pigs and horses) and an artery that continued along the left coronary groove, a position similar to that normally occupied by the left circumflex coronary artery. Careful dissection of the pulmonary venous system revealed that 6 separate pulmonary veins entered the left atrium normally. The pulmonary vein arising from the cranial or apical portion of the right lung entered the dorsal aspect of the right atrium caudal to the azygous vein and cranial to the intervenous tubercle. The previously identified ASD was located caudal to the intervenous tubercle in the area of the fossa ovalis, differentiating it from a sinus venosus ASD. Histological examination of the lungs revealed no abnormalities.
Discussion Double outlet right ventricle describes a specific type of ventriculoarterial connection in which the aorta and the pulmonary trunk are connected to the morphological right ventricle. A great artery is considered to be connected to a ventricle when >50% of its circumference originates from that ventricle (Becker and Anderson I98 I ; Perloff 1987). This cardiac anomaly has been dessribed in man (Becker and Anderson 1981; Perloff 1987), dogs (Turk, Miller and Hegreberg 198I ; Bonagura 1989), cats (Jeraj ef al. 1978), cattle (Godgluck 1962). pigs (Olafson 1939) and one horse (Vitums 1970). The estimated incidence of DORV in man is 0.09 per 1000 live births (Mitchell, Korones and Berendes 1971) or 4.5% of necropsy cases of congenital cardiac anomalies (Van Praagh e f al. 1982). There is
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some evidence to suggest that DORV arises due to arrest of the normal rotation of the semilunar valve region during embryogenesis (Bostrom and Hutchins 1988). The complex anatomy of DORV is classified based on three essential gross morphological features: the relationships of the great arteries to the ventricles, the relationships of the VSD to the great arteries and the presence or absence of obstruction to right ventricular outflow. There are 4 types of relationships between the great arteries and the ventricles: ( I ) aorta is to the right of and caudal to the pulmonary trunk, (2) great arteries are side by side with the aorta to the right of the pulmonary trunk, (3) aorta is to the right of and cranial to the pulmonary trunk, and (4) aorta is to the left of and cranial to the pulmonary trunk. A VSD provides the morphological left ventricle with its only outlet. The VSD is either subaortic, subpulmonary, beneath both great arteries (doubly committed), beneath neither great artery (uncommitted) or absent altogether. These 4 locations combined with the 4 relationships of the great arteries result in 16 possible combinations of DORV (Perloff 1987). The aorta and pulmonary artery of this foal were side-by-side with the aorta to the right of the pulmonary trunk. This is the usual arrangement in people with DORV. The origin of the pulmonary trunk from the right ventricle and the lack of fibrous continuity between the semilunar valves and the atrioventricular valves differentiated this heart from those with complete transposition of the great vessels (Perloff 1987). In people with DORV, the VSD is most commonly in the subaortic position (Sridaromont et al. 1978). The VSD in this foal was located in the subpulmonary position. In DORV with the great vessels side-by-side and the aorta to the right of the pulmonary trunk, a subpulmonary VSD is referred to as the Taussig-Bing anomaly. With this arrangement, the oxygenated blood from the left ventricle selectively enters the pulmonary trunk because the VSD is committed to the pulmonary artery (Sridaromont ef a / . 1976, 1978). The Taussig-Bing anomaly accounts for approximately 8% of all people with DORV (Sridaromont et a/. 1978) and clinical manifestations resemble those of complete transposition of the great arteries. Cyanosis is present at or shortly after birth because of obligatory flow of unoxygenated blood from the right ventricle into the aorta (Beuren 1960). Left ventricular blood selectively enters the pulmonary artery, unless pulmonary stenosis shunts some of the left ventricular outflow into the aorta. Muscular subpulmonary stenosis was present in this foal's heart just above the VSD. Pulmonary stenosis has been reported in 41-72% of people with DORV (Sridaromont e f ul. 1978; Van Praagh et al. 1982), but is uncommon in people with a subpulmonic VSD (Argawala et ul. 1973). Partial anomalous pulmonary venous connection (PAPVC) is a communication of one or more, but not all, of the pulmonary veins to the right atrium or cavae. This anomaly has been reported in dogs (Hilwig and Bishop 1975) and is estimated to be present in 0.6% of all people (Lucas 1983). In people, PAPVC is commonly associated with a sinus venosus-type ASD (Nugent et ul. 1985). Isolated, uncomplicated PAPVC involving a single pulmonary vein is usually undetected since only 20% or less of pulmonary venous blood would return to the right atrium. Diagnosis is difficult; electrocardiography and echocardiography may detect volume overload of the right heart, but a selective angiogram with a venous catheter placed in the anomalously connected pulmonary vein is needed to document the site of connection (Nugent et a / . 1985). Surgical treatment involves the placement of a contoured intracardiac patch to divert anomalously delivered pulmonary venous blood into the left atrium through a surgically created ASD (Murphy, Kerr and Kirklin 1971). Atrial septa1 defects have been reported i n horses (Rooney and Franks 1964; Physick-Sheard, Maxie, Palmer and Gaul 1985), cattle (Gopal et a / . 1986), pigs (Hsu and Du 1982), dogs (Hamlin, Smith and Smetzer 1963;jeraj et a / . 1980; Lombard,
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Ackerman and Berry 1989), cats (Farrow 1984) and an antelope (Chaffin, Miller, Jensen and Hall 1990). Four types of ASD can occur: patent foramen ovale, ostium primum ASD, ostium secundum ASD and sinus venosus ASD. The last three types are differentiated by their location in the atrial septum (Chaffin et al. 1990). The ASD in our foal was of the ostium secundum type, located in the fossa ovalis (midseptal) region of the septum with normal septal tissue between the defect and the atrioventricular valves (Hamlin et al. 1963; Pyle 1983). The large size of the defect and presence of a left-to-right shunt differentiated it from patent foramen ovale (Pyle 1983). Atrial septal defects usually result in left-to-right shunts because the right ventricular walls are thinner and more compliant and the orifice of the tricuspid valve has a larger cross-sectional area than does the mitral valve. Resultant volume overload of the right atrium, right ventricle, pulmonary artery and pulmonary veins leads to enlargement of these structures (Bonagura 1989). In man, ASD is a common anomaly associated with DORV (Van Praagh et al. 1982). Anomalies of coronary arteries have occurred in people (Ogden and Goodyear 1970 Ogden I970 Vlodaver, Neufeld and Edwards 1975; Lipton et al. 1979; Dabizzi et al. 1980; Roberts 1986) and dogs (Buchanan 1990), and have been associated with pulmonary stenosis in dogs (Buchanan 1990) and DORV in people (Van Praagh et al. 1982). Single right (R) or left (L) coronary arteries are classified on the basis of the location of the branch that crosses to the opposite side (Lipton et al. 1979). The distribution of the coronary circulation in our foal did not match any of the typical classifications reported for people or dogs (Lipton et al. 1979; Dabizzi et al. 1980), but most closely resembled the type RI circulation described for people (Lipton et al. 1979). This may reflect interspecies differences in normal coronary artery distribution. Horses and pigs have a right dominant coronary system, while people, dogs, cats and cattle have a left dominant coronary system. One report describes a Thoroughbred yearling with a single right coronary artery (Rooney and Franks 1964), similar to the type R2A described for people and dogs (Lipton et al. 1979; Buchanan 1990). that presumably resulted in left ventricular failure. Several echocardiographic formats including M-mode (Reef 1985, 1987, 1991; Clark, Reef, Sweeney and Lichtensteiger 1987; Reef et al. 1987; Lombard, Scarratt and Buergelt 1983; Bayly et al. 1982; Pipers, Hamlin and Reef 1979), 2-dimensional real-time (Reef et al. 1987; Clark et al. 1987; Reef 1985, 1987, 1991; Carlstein 1987; Pipers, Reef and Wilson 1985; Bayly et al. I982), Doppler (Moise 1989; Reef 1991) and contrast echocardiography (Reef et al. 1987; Kvart, Carlsein, Jeffcott and Nilsfors 1985; Bonagura and Pipers 1983) have been used to document congenital cardiac malformations in the horse. In the present foal, 2-dimensional real-time echocardiographic evaluation detected the VSD and ASD and suggested an anomaly of the ventricular outflow tracts. In addition, colour-flow and spectral Doppler echocardiography documented the left-to-right shunts through the VSD and the ASD. The definitive nature of this defect, however, could only be determined by angiocardiography and post-mortem examination. In conclusion, this 2-day-old American Miniature Horse foal had cyanosis, exercise-induced syncope, and a systolic heart murmur. Echocardiography and selective angiocardiography detected DORV, VSD, ASD and a single coronary artery. Postmortem examination confirmed each of these findings, demonstrated subpulmonary muscular stenosis and documented the presence of partial anomalous pulmonary venous connection to the right atrium. The arrangements of the VSD and the great vessels resembled the Taussig-Bing anomaly as described in man. As the popularity of the American Miniature Horse increases, veterinarians may encounter more congenital cardiac anomalies.
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Acknowledgement We thank Dr Rebecca Heaton for referral of this case. References Argawala. 8.. Doyle, E X , Danilowicz. D.. Spencer, F.C. and Mills, N.M. (1973) Double outlet right ventricle with pulmonic stenosis and anteriorly positioned aorta (Taussig-Bing variant). Am. J. Cardiol. 32. 850-854. Bayly, W.M.. Reed. S.M.. Leathers. C.W.. Brown, C.M., Traub. J.L.. Paradis. M.R. and Palmer, G.H. (1982) Multiple congenital heart anomalies in five Arabian foals. J . Am. ver. med. Assoc. 181,684-689. Becker. A.E. and Anderson, R.H. (1981) Pathology of Congenifal Heart Disease. Butterworths and Co. Ltd.. London. pp 297-307. Beuren, A. (1960) Differential diagnosis of the Taussig-Bing heart from the complete transposition of the great vessels with a posteriorly overriding pulmonary artery. Circulation 21, 1071-1087. Bonagura, J.D. (1989) Congenital heart disease. In: Te.rrhook i f ' Veterinary Inrernal Medicine, Diseases of rhe Dog and Car. 3rd edn. Ed: S.J. Ettinger. W.B. Saunders Co. Philadelphia. pp 976-1030. Bonagura, J.D. and Pipers. F.S. (1983) Diagnosis of cardiac lesions by contrast echocardiography.J. Am. ver. med. Assoc. 182,396-402. Bostrom, M.P.G. and Hutchins. G.M. (1988) Arrested rotation of the outflow tract may explain double-outlet right ventricle. Circulation 77. 1258-1265. Buchanan, J.W. (1990) Pulmonic stenosis caused by single coronary artery in dogs: Four cases (1965-1984). J. Am. vet. med. Assoc. 196. 115-120. Buergelt. C.D.. Carmichael. J.A.. Tashjian. R.J. and Da$. K.M. (1970) Spontaneous rupture of the left pulmonary artery in a horse with patent ductus arteriosus. J. Am. set. med. Assoc. 157,313-320.
Button. C., Gross, D.R., Allen. J.A. and Kitzman, J.V. (1978) Tricuspid atresia in a foal. J. Am. vet. med. Assoc. 172.825-830. Carlstein. J.C. (1987) no-dimensional. real-time echocardiography in the horse. Vet. Radiol. 28.76-78. Chaffin. M.K.. Miller. M.W.. Jenson. J.M.and Hall, D.G. (1990) Echocardiographic diagnosis of atrial septal defect in a newborn bongo (Boocerus eurycerus) with hypogammaglobulinemia and septicemia. J. Zoo Wildlve Med. 21,358-365. Clark, E.S.. Reef, V.B.. Sweeney. C.R. and Lichtensteiger. C. (1987) Aortic valve 191,841-844. insufficiency in a one-year-old colt. J. Am. vet. med. ASSCJC. Critchley. K.L. (1976) An interventricular septal defect, pulmonary stenosis and bicuspid pulmonary valve in a Welsh pony foal. Equine vet. J. 8. 176-178. Crowe. M.W. and Swerczek, T.W. (1985) Equine congenital defects. Am. J. iw. Res. 46,353-358.
Dabizzi, R.P., Caprioli. G.. Aiazzi. L.. Castelli. C.. Baldrighi, G., Parenzan. L. and Baldrighi. V. (1980) Distribution and anomalies of coronary arteries in tetralogy of Fallot. Circularion 61.95-102. Farrow, C.S. (1984) Atrial septal defect in a kitten. Mod. ver. Pracr. 65,281-282. Glazier, D.B.. Fmeily. B.T. and Neylon, J.F. (1974) Patent ductus arteriosus in an eight-month-old foal. Ir. r'er. J. 28. 12-13. Glazier, D.B., Farrelly. B.T. and O'Connor. J. (1975) Ventricular septal defect in a 7year-old gelding. J. Am. vef.med. Assoc. 167,49-50. Godgluck. G. (1962) Missbildungen des Herzens bei Tieren. Dtsch fierarzfl.Wschr. 69.98-102.
Gopal, T.. Leipold. H.W. and Dennis, S.M. (1986) Congenital cardiac defects in calves.Am. J. ver. Res. 47, 1120-1121. Greene. H.J., Wray. D.D. and Greenway, G. A. (1975) n o equine congenital cardiac anomalies. IK vet. J. 29. 115-117. Hamlin. R.L.. Smith, C.R. and Smetzer. D.L. (1963) Ostium secundum type interatrial septal defects in the dog. J. Am. r'et. med. Assoc. 143. 149-157. Hilwig. R.L. and Bishop, S.P. (1975) Anomalous pulmonary venous return in a Great Dane. Am. J. ver. Rex 36, 229-233. Hsu. F.S. and Du. S.J. (1982) Congenital heart disease in swine. Vet. Pafhol. 19.676686.
Huston. R., Saperstein. G. and Leipold. H.W. (1977) Congenital defects in foals. J. equineMed. Surg. 1, 146-161. Jerdj. K., Ogburn, P.N., Jessen. C.A.. Miller, J.D. and Schenk, M.P. (1978) Double outlet right ventricle in acat. J. Am. vet. med. Assoc. 173, 1356-1360. Jeraj, K., Ogburn. P.N., Johnston, G.R.. Edwards. W.. Yano. B., Brunson. D.. Wallace, L. and McGrath. C. (1980) Atrial septal defect (sinus venosus typebin a dog. J. Am. set. med. Assoc. 177, 342-346. Krotje, L.J. (1987) Cyanosis: physiology and pdthOgeneSiS. Comp. Conr. Ed. Pract. Vet. 9.271-278. Kvan. C.. Carlsten, J., Jeffcott. L.B. and Nilsfors. L. (1985) Diagnostic value of contrast echocardiography in the horse. Equine vet. J . 17. 357-360. Lipton, M.J.. Barry. W.H., Obrez, 1.. Silverman. J.F. and Wexler. L. (1979) Isolated
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406 single coronary artery: diagnosis, angiographic classification. and clinical significance. Radifdogy 130. 39-47. Lombard. C.W., Scarratt. W.K. and Buergelt. C.D. (1983) Ventricular septal defects in the horse. J.Am. vet. med. Assoc. 183. 562-565. Lombard. C.W.. Ackerman. N. and Berry. C.R. (1989) Pulmonic stenosis and rightto-left atrial shunt in three dogs. J. Am. vet. med. Assoc. 1. 71 -75. Lucas. R.V.. Jr (1983) Anomalous venous connections. pulmonary and systemic. In: MOSS'Heart Disease in Infants, Children and Adolescents. Eds: F.H. Adams and G.C. Emmanouilides. The Williams and Wilkins Co. Baltimore, pp 458. Machida. N.. Yasuda. J. and Too, K. (1987) Auscultatory and phonocardiographic studies on the cardiovascular system of the newborn thoroughbred foal. Jpn J. wr, Res. 35. 235-250. Mitchell. S.C.. Komnes, S.B. and Berendes, H.W. (1971) Congenital h e m disease in 56.109 births; incidence and natural history. Circrtlation43,323-332. Moise. N.S. (1989) Doppler echocardiographic evaluation of congenital cardiac disease. J. vet. intern. Med. 3. 195-207. Murphy, J.W.. Kerr. A.R. and Kirklin. J.W. (1971) lntracardiac repair for anomalous pulmonary venous connection of right lung to inferior vena cava. Ann. Thorac. Surg. 11. 38-42. Musselman. E.E. and LoGuidice. R.J. ( 1984) Hypoplastic left ventricular syndrome in a foal. .I.Am. vet. med. Assoc. 185.542-543. Nugent. E.W.. Plauth. W.H., Edwards. J.E.. Schlant. R.C. and Williams. W.H. (1985) Congenital heart disease. In: The Hearr. 6th edn. Ed: J.W. Hurst. McGraw-Hill Inc. New York, pp 580-728. Ogden. J.A. (1970) Congenital anomalies of the coronary arteries. Am. J. Cardiol. 25.474-479.
Ogden, J.A. and Goodyear. A.V.N. (1970) Patterns of distribution of the single coronary artery. Yale J. Bio/. Med. 43. I 1-2 I . Olafson. I? (1939) Congenital cardiac anomalies in animals. Bit// int. Ass. Med. Mtts. 19. 129-134. Perloff. J.K. (1987) The Clinical Remgnition c f l Congenifal Heart Disease. W.B. Saunders Co.. Philadelphia, pp 443-466. Maxie. M.G.. Palmer, N.C. and Gaul, C. (1985) Atrial septal tent ostium primum type with hypoplasiic right ventricle in a Welsh pony foal. Can. J. conrp. Med. 49.429-433. Pipers. F.S., Hamlin, R.L. and Reef. V.B. (1979) Echocardiographic detection of cardiovascular lesions in the horse. J. equine Med. Surg. 3.68-77. Pipers, F.S.. Reef. V.B. and Wilson, J. (1985) Echocardiographic detection of ventricular septal defects in large animals. J. Am. vet. med. Assoc. 187. 8 10-816.
Pyle. R.L. ( 1983) Congenital heart disease. In: Testbook of Vererinury lnrenral Medicine. Diseases ofthe Dog and Cat. 2nd edn. Ed: S.J.Eltinger. WE Saunders Co, Philadelphia. pp 933-959. Reef, V.B. (1985) Cardiovascular disease in the equine neonate. Ver. Clirtic,sN. Am. (Large Anim. Pract.) 1. 117-129. Reef, V.B. (1987) Mitral valve insufficiency associated with ruptured chordae tendineae in three foals. J . Am. vet. m d . A.wJ~..191. 329-33 I, Reef. V.B. (1991) Echocardiographic findings in horses with congenital cardiac diseae. Conrp Cnnt. Ed. Pracl. Vet. 1. 109-1 17. Reef, V.B.. Mann. P.C. and Orsini. P.G. (1987) Echocardiographic detection of tricuspid atresia in two foals. J. Am. vet. med. Assoi,. 191, 225-228. Roberts. W. (1986) Major anomalies of coronary arterial origin seen in adulthood. Am. Hearr J. 111.941-963. Rooney. J.R. and Franks, J.R. (1964) Congenital cardiac anomalies in horses. Vet, Pathol. 1.454-464. Scott, E.A.. Chaffee. A,. Eyster. G.E. and Kneller. S.K. (1978) Interruption of aortic arch in two foals. J. Am. wr. med. Assoc. 172.347-350. Shapiro, B.A.. Harrison, R.A.. Cane. R.D. and Templin. R. (1989) Cliniwl Applicatian of BlfJod Gases. 4th edn. Year Book Medical Publishers Inc.. Chicago. pp 101-135. Sridaromont. S.. Feldt. R.H.. Ritter. D.G..Davis, G.D.and Edwards, J.E. (1976) Double-outlet right ventricle: Hemodynamic and anatomic correlations. Am ./. Cardiol. 38. 85-94. Sriddromont. S.. Ridder. D.G.. Feldt. R.H.. Davis. C.D. and Edwards, J.E. (197X) Double outlet right ventricle: Anatomic and angiocardiogrdphic correlations. Mayo Clin. Proc. 53.555-571. Turk, J.R., Miller, L.M. and Hegreberg. G.A. (1981) Double outlet right ventricle in a dog. .I.Am. Animal Hospital Assoc. 17. 789-792. Van Praagh. S.. Davidoff. A.. Chin. A., Shiel, F.S.. Reynolds. J. and Van Pradgh. R. (1982) Double outlet right ventricle: anatomic types and development implications based on a study of 101 autopsied cases. Coettr 8. 389. Vitums, A. (1970) Origin of the aorta and pulmonary trunk from the right ventricle in a horse. Ver. Pathol. 7.482-491. Vitums. A. and Bayly, W.M. (1982) Pulmonary atresia with dextroposition of the aorta and ventricular septal defect in three Arabian foals. Vet.Pathd 19, 160-168. Vitums. A,. Grant. B.D..Stone, E.C. and Spencer. G.R. (1973) Transposition of the aond and atresia of the pulmonary trunk in a horse. Cornell Vet. 63.41-57. Vlodaver. Z., Neufeld, H.N. and Edwards. J.E. (1975) C'oronap Arterial Variations in the Normal Heart and Congenital Heart Disease. Academic Press Inc. New York.
Receivedjiv publication: 9.9.91 Accepted: 23.12.91
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