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Atrioventricular Canal Defect (incomplete form of endocardial cushion defect) and Ostium Secundum Type Interatrial Septal defect in a dog
Journal of Veterinary Cardiology, Vol.4, No. 2, November 2002
ESVC Atrioventricular Canal Defect (incomplete form of endocardial cushion defect) and Ostium Secundum Type Interatrial Septal defect in a dog C.N. Amberger & C.E. Boujon, Chris Amberger, DVM, DECVIM-CA(Cardiology) and Claude Boujon, DVM, FVH(Pathology)
Abstract A four-year-old German shepherd mixed-breed dog was presented with an asymptomatic heart murmur. An atrial septal defect associated with tricuspid and mitral dysplasia (atrioventricular canal defect) was diagnosed. The pulmonary to systemic blood flow ratio was in the range of 2.5:1 (Qp:Qs ratio). Echocardiography and flow pattern across the valves as well as the direction of the shunt allows a better description of the physiopathological consequences of this rare congenital heart disease. Additionally, an Ostium Secundum Type interatrial septum defect was found at necropsy.
Key words : Atrioventricular canal defect, Ostium Secundum Type atrial septum defect, dog, echocardiography
Introduction Atrioventricular (AV) canal defect is the consequence of the failure of the dorsal endocardial cushion to fuse with the septum primum to close the ostium primum in the atrial septum during the partitioning of the heart and chamber formation, between the third and the fourth week of fetal life1. The term AV canal defect designates a group of lesions in which the AV septum is absent or incomplete. Complete endocardial cushion defects include a septum primum atrial septal defect, a ventricular septal defect and an abnormal five-leaflet AV-valve2. Common AV canal with communication of all four cardiac chambers has been described in cats 3 but not in dogs. Reported cases in dogs of incomplete AV canal defects include ostium primum defects and dysplastic septal mitral leaflets4,5. Patients with atrioventricular canal defects have severe left to right shunting2. Blood flows from the left ventricle to the right ventricle in systole through the septum primum atrial septal defect, and is enhanced by the mitral regurgitation of the dysplastic septal leaflet. Additionally, failure of the septum secundum to grow normally results in the ostium secundum remaining open
and is termed an ostium secundum atrial septal defect. This defect seems to be more frequent than ostium primum defects in dogs6,7.
Case Report A 4-year-old male German shepherd mixed-breed dog was referred after changing owners for evaluation of a cardiac murmur. There was a history of minor exercise intolerance when the dog played with another young animal. The dog was alert with a normal temperature (38.4°C), mild hypokinetic pulse (100/min) and normal respiratory rate (44/min). The mucous membranes were slightly cyanotic with normal capillary refill time (< 2 sec.). The peripheral veins and respiratory sounds were normal. Cardiac auscultation revealed a grade V/VI systolic murmur, louder over the tricuspid area (PM 4 ICS), with bilateral radiation and a thrill. Electrocardiographic findings showed a normal sinus rhythm (95/min) with increased P-duration (0.06 sec), first degree AV-block (PR = 0.15 sec), right bundle branch block (Mean complex negative in Lead I, II, III, QRS
Small Animal Practice 96, rue de la Servette CH-1202 Geneva-Switzerland
37
Chris Amberger, Claude Boujon
Figure 1 - ECG (Lead II, 1 mV/cm, paper speed 100 mm/sec) showing RBBB and Phonocardiogramm (70/140 Hz) with diamond-shaped holosystolic ejection murmur.
Figure 2 - Left lateral and dorsoventral radiographs of the cardiac silhouette showing right ventricular and atrial enlargement as well as pulmonary overcirculation. a
b
38
duration 0.12 sec with mean electrical axis -100°). A systolic crescendo-decrescendo murmur was recorded on phonocardiography (Figure 1), with elevated systolic time intervals (PEP/LVET 0.4). Thoracic radiography revealed right-sided cardiomegaly (short axis length greater than 6 vertebrae on the Buchanan’s Index) and pulmonary overcirculation (Figure 2). The arterial blood pressure was normal (Systolic/Diastolic/Mean 135/82/99 mmHg, HR 100 bpm). Echocardiography: On 2-D echocardiography, from the right parasternal long axis view, the right ventricle (RV) was enlarged and the heart showed generalized hypokinetic motion. Due to volume overload, the heart rate was quite slow, as the increase of cardiac output or stroke volume directly reduces heart frequency (optimal rate by increased end-diastolic volume). Atrial septal defect and bilateral AV-valve dysplasia with malposition of the septal leaflets, particularly of the tricuspid valve, were present (Figure 3a). The main abnormalities measured with 2D-guided M-mode were an increased internal dimension of the right ventricle and a moderate increase of the left ventricle dimensions (EDVI = 115 ml/m2, ESVI 56 ml/m2, eccentric hypertrophy) (Table 1). In color Doppler, a turbulent regurgitant flow coming from the left septal cusp of the mitral valve toward the dysplastic annulus mimicked a VSD-jet with positive flow on the right side of the heart (Figure 3b), with a velocity of 2.5 m/sec (25 mmHg). No positive flow was evident between left and right atria, as the ASD was more than twothirds of the size of the septum. The pulmonic flow velocity was increased (> 1.5 m/sec) and turbulent, with associated ejection murmur, and pulmonary hypertension was present (Tricuspid regurgitation over 4 m/sec (N<2.8 m/sec), corresponding to a RV-RA pressure gradient of 64 mmHg). From the left parasternal standard view, ASD with dilation of the right atrium, dysplastic AV-valves and right ventricular dilation were evident (Figure 4). Tricuspid and mitral regurgitation were both present, with normal E/A ratio and increased inflow velocities, as well as aortic flow, with a non-turbulent PWD-shape (Table 1). Qp:Qs ratio as determined by cardiac output via aorta and pulmonary artery systolic flow velocity integral was 2.5:1, which demonstrates an increased right cardiac output with a left-to-right shunt8. Because the major problem was generalized volume overload (LR-shunt and bilateral AV-insufficiency), the dog was treated with ACE-inhibitors (Benazepril 0.25 mg/kg SID) and controlled every three to four months over an 18month period. The dog was doing very well on monotherapy, was completely asymptomatic, although it did develop an additional ventricular arrhythmia (monomorphic right ventricular extrasystole), with increased endsystolic volume index, pulmonic flow velocity, Qp:Qs ratio and transvalvular AV-valve flow and regurgitation (Table 1). Because of the development of a behavioral disorder (childdirected aggression) the dog had to be euthanatized at the age of 6 years.
Chris Amberger, Claude Boujon
Figure 1 - ECG (Lead II, 1 mV/cm, paper speed 100 mm/sec) showing RBBB and Phonocardiogramm (70/140 Hz) with diamond-shaped holosystolic ejection murmur.
Figure 2 - Left lateral and dorsoventral radiographs of the cardiac silhouette showing right ventricular and atrial enlargement as well as pulmonary overcirculation. a
b
38
Journal of Veterinary Cardiology, Vol.4, No. 2, November 2002 duration 0.12 sec with mean electrical axis -100°). A systolic crescendo-decrescendo murmur was recorded on phonocardiography (Figure 1), with elevated systolic time intervals (PEP/LVET 0.4). Thoracic radiography revealed right-sided cardiomegaly (short axis length greater than 6 vertebrae on the Buchanan’s Index) and pulmonary overcirculation (Figure 2). The arterial blood pressure was normal (Systolic/Diastolic/Mean 135/82/99 mmHg, HR 100 bpm). Echocardiography: On 2-D echocardiography, from the right parasternal long axis view, the right ventricle (RV) was enlarged and the heart showed generalized hypokinetic motion. Due to volume overload, the heart rate was quite slow, as the increase of cardiac output or stroke volume directly reduces heart frequency (optimal rate by increased end-diastolic volume). Atrial septal defect and bilateral AV-valve dysplasia with malposition of the septal leaflets, particularly of the tricuspid valve, were present (Figure 3a). The main abnormalities measured with 2D-guided M-mode were an increased internal dimension of the right ventricle and a moderate increase of the left ventricle dimensions (EDVI = 115 ml/m2, ESVI 56 ml/m2, eccentric hypertrophy) (Table 1). In color Doppler, a turbulent regurgitant flow coming from the left septal cusp of the mitral valve toward the dysplastic annulus mimicked a VSD-jet with positive flow on the right side of the heart (Figure 3b), with a velocity of 2.5 m/sec (25 mmHg). No positive flow was evident between left and right atria, as the ASD was more than twothirds of the size of the septum. The pulmonic flow velocity was increased (> 1.5 m/sec) and turbulent, with associated ejection murmur, and pulmonary hypertension was present (Tricuspid regurgitation over 4 m/sec (N<2.8 m/sec), corresponding to a RV-RA pressure gradient of 64 mmHg). From the left parasternal standard view, ASD with dilation of the right atrium, dysplastic AV-valves and right ventricular dilation were evident (Figure 4). Tricuspid and mitral regurgitation were both present, with normal E/A ratio and increased inflow velocities, as well as aortic flow, with a non-turbulent PWD-shape (Table 1). Qp:Qs ratio as determined by cardiac output via aorta and pulmonary artery systolic flow velocity integral was 2.5:1, which demonstrates an increased right cardiac output with a left-to-right shunt8. Because the major problem was generalized volume overload (LR-shunt and bilateral AV-insufficiency), the dog was treated with ACE-inhibitors (Benazepril 0.25 mg/kg SID) and controlled every three to four months over an 18month period. The dog was doing very well on monotherapy, was completely asymptomatic, although it did develop an additional ventricular arrhythmia (monomorphic right ventricular extrasystole), with increased endsystolic volume index, pulmonic flow velocity, Qp:Qs ratio and transvalvular AV-valve flow and regurgitation (Table 1). Because of the development of a behavioral disorder (childdirected aggression) the dog had to be euthanatized at the age of 6 years.
Table 1 - Echocardiographic values with references. Echocardiographic findings (M-Mode and Pulse Wave Doppler, Continuous Wave Doppler for velocities over 1.5 m/sec).
Body weight (kg) Heart rate (bpm) RVIDd (mm) IVSd (mm) LVIDd (mm) LVWd (mm) IVSs (mm) LVIDs (mm) LVWs (mm) FS (%) Aod (mm) Las (mm) Vmax, Pulmonary (m/sec) Vmax, Aortic (m/sec) Vmax, Mitral (m/sec) Vreg, Mitral (m/sec-mmHg) Vmax, Tricuspid (m/sec) Vreg, Tricuspid (m/sec-mmHg)
Patient (initial exam) 25.7 90 NSR 24.1 11.4 45.8 9.7 14.8 29.4 13.3 36 22.4 25.1 1.15 1.31 1.5 4.8-92 1.4 4.2-70
(after 15 month) 26.6 120 VPC’s 32.7 9.9 46.8 9.5 15.1 34.6 12.8 26 22.3 40.1 2.58 1.12 1.85 6.0-144 1.6 4.6-85
Reference values* (Mean +/- SD) 25 70-140 14.4 +/-2.7 8.7 +/- 0.9 44.8+/-2.9 7.9+/-1.0 13.0+/-1.5 31.0+/-2.5 12.1+/-1.2 28-40 24.6+/-1.6 21.8+/-2.4 1.0 +/-0.15 1.19+/-0.18 0.81+/-0.14 0.63+/-.018
* Lombard CW : Normal values of the canine M-mode echocardiogram. Am J Vet Res 1984;45: 2015, and with data from Henik RA, Echocardiography and Doppler Ultrasound, in Tilley LP and Goodwin LK (eds): Manual of Canine and Feline Cardiology, 3rd Ed. W.B. Saunders, Philadelphia 2001.
Pathological findings: The heart showed a severe eccentric hypertrophy of the right ventricle and atrium and a mild eccentric hypertrophy of the left ventricle (Figure 5). Intracardiac anomalies included the interatrial septum, the tricuspid and the mitral valves. An interatrial septum defect of ostium primum type, 25 mm in diameter, was found (Figure 6). There was a fibrous zone on the inferior border of the defect, including the septal cusp of the mitral valve and was bound by fibrous tissue to the septal cusp of the tricuspid valve. The caudal and the septal leaflets of the tricuspid valve were fused. The septal leaflet of the mitral valve was adhered directly to the septum. Both AV-valves were dislocated toward the apex and all leaflets were thick and nodular and showed histologically a myxoid degeneration. Their cordae tendinae were too short and thick with normal insertion. Moreover, there was an additional atrial septum defect 12 mm proximal to the first one (Figure 6). This defect corresponds to an ostium secundum type and was 15 x 10mm large. Macroscopically, the liver was rather small, with a finely irregular surface with a very hard consistency. Histologically the architecture of the liver was modified. The hepatocytes were variable in size, blood stasis and intrahepatic porto-portal shunt and fibrosis were observed. Lymphocytes and haemosiderin containing macrophages were present in the periportal area, and a light fibrosis of the central veins was present. No macroscopic abnormalities were found in the lungs.
Discussion In this patient, an incomplete form of an endocardial cushion defect and ostium secundum type interatrial septal defect were observed. Because the endocardial cushions
contribute to the development of the atrial and ventricular septa and to the septal leaflets of the mitral and tricuspid valve, anomalous development may result in a septum primum atrial septal defect and AV-valve dysplasia, with abnormal leaflets, myxoid degeneration and short thickened cordae tendinae9,10. AV-valve dysplasia explains the AV-valvular regurgitation. The severe left to right shunting of blood through the interatrial septum defect and AV-valvular regurgitation lead to volume overload and to eccentric hypertrophy of both ventricles and the right atrium. The severe atrial volume overload increased also enddiastolic volume, and the heart rate was kept relatively slow due to the increase of the cardiac output (CI over 10 L/min/m2). Despite the complex malformation, the left ventricular function was sufficient to provide normal arterial pressure and peripheral perfusion. Measurement of Qp/Qs from Doppler derived pulmonary and aortic blood flow may provide some information about the quantification of the shunt. Qp/Qs ratio over 2 are considered haemodynamically significant, but the error done on the pulmonic side may be important11. The resulting pulmonary hypertension was well tolerated, and the dog did not develop Eisenmenger’s syndrome at that age. There was still no ascites or peripheral venous engorgement at that time. Histologically, however, signs of beginning liver cirrhosis were observed, probably of cardiac origin. It seems that this particular cardiac abnormality has similarities with the pathophysiology of mitral and tricuspid dysplasia12 and may be well compensated for a long time in dogs. Generally, only the most severely affected animals develop congestive heart failure and atrial arrhythmias within the first year of age in these AV-valve dysplasia. 39
Chris Amberger, Claude Boujon
Figure 3(a-b) - 2D right parasternal long axis view: The interventricular septum is too short, both atrioventricular valve insertions are displaced toward the axis of the heart. The interatrial septum is incomplete.There is a systolic turbulent colorflow Doppler from the mitral valve regurgitation with a high velocity left to right shunt at the atrial level similar to VSD-shunt. a
The presence of P-mitrale and first degree AV block reflect atrial dilation and alteration in the conductive system. In dogs, definitive morphologic data about right bundle branch block are missing13. An isolated case report described RBB in a dog with ASD13. These ECG change are probably mostly compatible with a manifestation of right ventricular overload rather than a true conduction delay in the RBB15,16. There was no presence of splintered QRS-complex despite of the tricuspid abnormality17. The difficulty of interpretation of this cardiac malformation was due to the mix of systolic regurgitation from mitral and tricuspid valves associated with the absence of an interatrial septum at the valvular level. As the pars membranacea of the interventricular septum was very thin (but without defect), the severe color flow Doppler aliasing mimicked a VSD jet with a positive flow from left to right. In fact, the regurgitative jet from the mitral valve goes through the ASD into the right ventricle, and only the velocity of the jet allows the differentiation to be made (Figure 3c). In dogs with a VSD and mild pulmonary hypertension, the pressure gradient between the LV and the RV should be above 50 to 80 mmHg, corresponding to a velocity of 3.5 to 4.5 m/sec. In this dog, it was impossible to find a flow velocity over 2-2.5 m/sec. This was due to the fact that the flow was not coming from the left ventricle, but from the left atrium due to mitral regurgitation, and the direction of this jet was very turbulent because of the simultaneous presence of tricuspid regurgitation. The list of differential diagnoses in this patient included complete atrioventricular canal defect2, common atrium 18, and ostium primum defect associated with mitral and tricuspid dysplasia6. The definitive confirmation of the diagnosis was made by necropsy. There have been only few cases of atrioventricular canal described in dogs4,5,19. To our knowledge, this clinical report is the first with incomplete atrioventricular canal defect (mitral and tricuspid dysplasia associated with ostium primum ASD) in combination with an ostium secundum ASD. 40
b
Figure (3c) - Schematic drawing of the haemodynamics associated with a partial atrioventricular canal defect, with left to right shunting trough the atrial septal defect over the septum membranaceum, with additional turbulence from bilateral AV-valve insufficiency due to dysplastic septal leaflets.
Figure 4 - Left parasternal 4-chamber view showing abnormal AV-valve insertion and severe dilation of the right atrium.
Chris Amberger, Claude Boujon
Journal of Veterinary Cardiology, Vol.4, No. 2, November 2002
Figure 3(a-b) - 2D right parasternal long axis view: The interventricular septum is too short, both atrioventricular valve insertions are displaced toward the axis of the heart. The interatrial septum is incomplete.There is a systolic turbulent colorflow Doppler from the mitral valve regurgitation with a high velocity left to right shunt at the atrial level similar to VSD-shunt. a
The presence of P-mitrale and first degree AV block reflect atrial dilation and alteration in the conductive system. In dogs, definitive morphologic data about right bundle branch block are missing13. An isolated case report described RBB in a dog with ASD13. These ECG change are probably mostly compatible with a manifestation of right ventricular overload rather than a true conduction delay in the RBB15,16. There was no presence of splintered QRS-complex despite of the tricuspid abnormality17. The difficulty of interpretation of this cardiac malformation was due to the mix of systolic regurgitation from mitral and tricuspid valves associated with the absence of an interatrial septum at the valvular level. As the pars membranacea of the interventricular septum was very thin (but without defect), the severe color flow Doppler aliasing mimicked a VSD jet with a positive flow from left to right. In fact, the regurgitative jet from the mitral valve goes through the ASD into the right ventricle, and only the velocity of the jet allows the differentiation to be made (Figure 3c). In dogs with a VSD and mild pulmonary hypertension, the pressure gradient between the LV and the RV should be above 50 to 80 mmHg, corresponding to a velocity of 3.5 to 4.5 m/sec. In this dog, it was impossible to find a flow velocity over 2-2.5 m/sec. This was due to the fact that the flow was not coming from the left ventricle, but from the left atrium due to mitral regurgitation, and the direction of this jet was very turbulent because of the simultaneous presence of tricuspid regurgitation. The list of differential diagnoses in this patient included complete atrioventricular canal defect2, common atrium 18, and ostium primum defect associated with mitral and tricuspid dysplasia6. The definitive confirmation of the diagnosis was made by necropsy. There have been only few cases of atrioventricular canal described in dogs4,5,19. To our knowledge, this clinical report is the first with incomplete atrioventricular canal defect (mitral and tricuspid dysplasia associated with ostium primum ASD) in combination with an ostium secundum ASD. 40
Figure 5 - External view of the heart: cardiomegaly with eccentric hypertrophy of right ventricle (RV) and atrium (RA) and, to a lesser extent, of the left ventricle (LV).
b
Figure (3c) - Schematic drawing of the haemodynamics associated with a partial atrioventricular canal defect, with left to right shunting trough the atrial septal defect over the septum membranaceum, with additional turbulence from bilateral AV-valve insufficiency due to dysplastic septal leaflets.
Figure 4 - Left parasternal 4-chamber view showing abnormal AV-valve insertion and severe dilation of the right atrium.
Figure 6 - View of the interatrial septum with both ostium primum (* ) and secundum (D) septal defects and AV valvular dysplasia (¨). Right atrium (RA), right ventricle (RV) and interventricular septum (IVS).
Abbreviations: PWD: Pulsed wave Doppler CWD: Continuous wave Doppler ESVI: Endsystolic Volume Index, ESVI = ESV(ml)/BSA(m2) EDVI : Enddiastolic Volume Index, EDVI = EDV(ml)/BSA(m2) Both are LV-stroke volume calculated with M-mode LVIDd and LVIDs using Teicholz Method (LVVd(s) = (7 x LVIDd(s)3)/(LVIDd(s) + 2.4) divided by Body surface area (BSA). PEP: Left Ventricular pre-ejection period (isovolumic contraction). LVET: Left ventricular ejection time (cardiac systole). CI: Cardiac index, Cardiac output (flow/min) divided by heart rate equal average stroke volume. Cardiac output is divided by BSA to produce an index that is the same for animals of different size. ASD: atrium septal defect - VSD: ventricle septal defect.
References 1. King AS. Development of the heart and Great Vessels, in The Cardiorespiratory System. Blackwell Science Ltd, Oxford, 1999: 369-376 2. Kittleson MD, Atrioventricular Canal Defect in Kittleson MD and Kienle RD. Small Animal Cardiovascular Medicine, Mosby Inc, St Louis 1998; 283-284 3. Liu SK, Ettinger S. Persistent Common Atrioventricular Canal in Two Cats. J Am Vet Med Assoc 1968; 153/5: 556-562 4. Monnet E, Orton C, Gaynor J, Boon J, Petersen D, Gaudagnoli M. Diagnosis and surgical repair of partial atrioventricular septal defects in two dogs. J Am Vet Med Assoc 1997; 211/5: 569-572 5. Nakayama T, Wakao Y, Uechi M, Muto M, Kageyama T, Tanaka K, Kawabata M, Takahashi M. A case report of surgical treatment of a dog with atrioventricular septal defect (incomplete form of endocardial cushion defect). J Vet Med Schi 1994; 56/5: 981-984 6. Kittleson MD, Atrial Septal Defects in Kittleson MD and Kienle RD. Small Animal Cardiovascular Medicine Mosby, Inc, St Louis 1998; 231-233 7. Hamlin RL, Smith CR, Smetzer D. Ostium Secundum Type Interatrial Septal Defects in the Dog. J Am Vet Med Assoc 1963; 143/2: 149-157 8. Kirberger RM, Berry WL. Atrial septal defect in a dog: the value of Doppler echocardiography. J S Afr Vet Assoc 1992; 63/1: 43-48 9. Robinson WF, Maxie MG. The cardiovascular system, in Jubb KVF, Kennedy PC, Palmer N (Eds). Pathology of Domestic Animal. 4th Ed., Academic Press Inc., San Diego 1992: 3: 9-17 10. Liu S-K, Tilley P. Dysplasia of the tricuspid valve in dog and cat. J Am Vet Med Assoc 1976 (169): 623-630 11. Bonagura, JD, Advance in Doppler Echocardiography, Proc. 20th annual ACVIM forum 2002: 746-748 12. Bonagura J, Lehmkuhl L. Dysplasia of the Atrioventricular valves, in Fox PR, Sisson D, Moise NS (Eds) Textbook of Canine and Feline Cardiology. Philadelphia, W.B. Saunders; 1999: 520-526 13. Miller MS, Tilley LP, Smith FWK, Fox PR: Intraventricular conduction defects, in Fox PR, Sisson D, Moise NS (Eds) Textbook of Canine and Feline Cardiology. Philadelphia, W.B. Saunders; 1999: 84-86 14. Troy GC, Turnwald GH. Atrial Fibrillation and Abnormal Ventricular Conduction Presented as Right Bundle Branch Block in a Dog with an Atrial Septum Primum Defect. J Am Anim Hosp Assoc 1979; 15: 417-420 15. Volpi A, Ferrario G, Dubini D et al. Atrial septal defect of the ostium secundum associated with incomplete left bundle branch block. G Ital Cardiol 1983; 13(6): 472-474 16. Sung RJ, Tamer DM, Agha AS et al. Etiology of the electrocardiographic pattern of “incomplete right bundle branch block” in atrial septal defect: an electropyhsiologic study. J Pediatr 1975(87):1182-1186 17. Kornreich BG, Moise NS Right atrioventricular valve malformation in dogs and cats: electrocardiographic survey with emphasis on splintered QRS complexes . J Vet Intern Med 1997: 11(4): 226-230 18. Fernandez del Palacio MJ, Costa A, Talavera J et al. Common Atrium in a Dog, J Vet Intern Med 2001; 15: 57-62 19. Santamarina G, Espino L, Mila M, Suarez ML. Partial atrioventricular canal defect in a dog. J Small Anim Pract 2002: 43, 17-21
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ESVC Atrioventricular Canal Defect (incomplete form of endocardial cushion defect) and Ostium Secundum Type Interatrial Septal defect in a dog C.N. Amberger & C.E. Boujon, Chris Amberger, DVM, DECVIM-CA(Cardiology) and Claude Boujon, DVM, FVH(Pathology)
Abstract A four-year-old German shepherd mixed-breed dog was presented with an asymptomatic heart murmur. An atrial septal defect associated with tricuspid and mitral dysplasia (atrioventricular canal defect) was diagnosed. The pulmonary to systemic blood flow ratio was in the range of 2.5:1 (Qp:Qs ratio). Echocardiography and flow pattern across the valves as well as the direction of the shunt allows a better description of the physiopathological consequences of this rare congenital heart disease. Additionally, an Ostium Secundum Type interatrial septum defect was found at necropsy.
Key words : Atrioventricular canal defect, Ostium Secundum Type atrial septum defect, dog, echocardiography
Introduction Atrioventricular (AV) canal defect is the consequence of the failure of the dorsal endocardial cushion to fuse with the septum primum to close the ostium primum in the atrial septum during the partitioning of the heart and chamber formation, between the third and the fourth week of fetal life1. The term AV canal defect designates a group of lesions in which the AV septum is absent or incomplete. Complete endocardial cushion defects include a septum primum atrial septal defect, a ventricular septal defect and an abnormal five-leaflet AV-valve2. Common AV canal with communication of all four cardiac chambers has been described in cats 3 but not in dogs. Reported cases in dogs of incomplete AV canal defects include ostium primum defects and dysplastic septal mitral leaflets4,5. Patients with atrioventricular canal defects have severe left to right shunting2. Blood flows from the left ventricle to the right ventricle in systole through the septum primum atrial septal defect, and is enhanced by the mitral regurgitation of the dysplastic septal leaflet. Additionally, failure of the septum secundum to grow normally results in the ostium secundum remaining open
and is termed an ostium secundum atrial septal defect. This defect seems to be more frequent than ostium primum defects in dogs6,7.
Case Report A 4-year-old male German shepherd mixed-breed dog was referred after changing owners for evaluation of a cardiac murmur. There was a history of minor exercise intolerance when the dog played with another young animal. The dog was alert with a normal temperature (38.4°C), mild hypokinetic pulse (100/min) and normal respiratory rate (44/min). The mucous membranes were slightly cyanotic with normal capillary refill time (< 2 sec.). The peripheral veins and respiratory sounds were normal. Cardiac auscultation revealed a grade V/VI systolic murmur, louder over the tricuspid area (PM 4 ICS), with bilateral radiation and a thrill. Electrocardiographic findings showed a normal sinus rhythm (95/min) with increased P-duration (0.06 sec), first degree AV-block (PR = 0.15 sec), right bundle branch block (Mean complex negative in Lead I, II, III, QRS
Small Animal Practice 96, rue de la Servette CH-1202 Geneva-Switzerland
37
Chris Amberger, Claude Boujon
Figure 1 - ECG (Lead II, 1 mV/cm, paper speed 100 mm/sec) showing RBBB and Phonocardiogramm (70/140 Hz) with diamond-shaped holosystolic ejection murmur.
Figure 2 - Left lateral and dorsoventral radiographs of the cardiac silhouette showing right ventricular and atrial enlargement as well as pulmonary overcirculation. a
b
38
duration 0.12 sec with mean electrical axis -100°). A systolic crescendo-decrescendo murmur was recorded on phonocardiography (Figure 1), with elevated systolic time intervals (PEP/LVET 0.4). Thoracic radiography revealed right-sided cardiomegaly (short axis length greater than 6 vertebrae on the Buchanan’s Index) and pulmonary overcirculation (Figure 2). The arterial blood pressure was normal (Systolic/Diastolic/Mean 135/82/99 mmHg, HR 100 bpm). Echocardiography: On 2-D echocardiography, from the right parasternal long axis view, the right ventricle (RV) was enlarged and the heart showed generalized hypokinetic motion. Due to volume overload, the heart rate was quite slow, as the increase of cardiac output or stroke volume directly reduces heart frequency (optimal rate by increased end-diastolic volume). Atrial septal defect and bilateral AV-valve dysplasia with malposition of the septal leaflets, particularly of the tricuspid valve, were present (Figure 3a). The main abnormalities measured with 2D-guided M-mode were an increased internal dimension of the right ventricle and a moderate increase of the left ventricle dimensions (EDVI = 115 ml/m2, ESVI 56 ml/m2, eccentric hypertrophy) (Table 1). In color Doppler, a turbulent regurgitant flow coming from the left septal cusp of the mitral valve toward the dysplastic annulus mimicked a VSD-jet with positive flow on the right side of the heart (Figure 3b), with a velocity of 2.5 m/sec (25 mmHg). No positive flow was evident between left and right atria, as the ASD was more than twothirds of the size of the septum. The pulmonic flow velocity was increased (> 1.5 m/sec) and turbulent, with associated ejection murmur, and pulmonary hypertension was present (Tricuspid regurgitation over 4 m/sec (N<2.8 m/sec), corresponding to a RV-RA pressure gradient of 64 mmHg). From the left parasternal standard view, ASD with dilation of the right atrium, dysplastic AV-valves and right ventricular dilation were evident (Figure 4). Tricuspid and mitral regurgitation were both present, with normal E/A ratio and increased inflow velocities, as well as aortic flow, with a non-turbulent PWD-shape (Table 1). Qp:Qs ratio as determined by cardiac output via aorta and pulmonary artery systolic flow velocity integral was 2.5:1, which demonstrates an increased right cardiac output with a left-to-right shunt8. Because the major problem was generalized volume overload (LR-shunt and bilateral AV-insufficiency), the dog was treated with ACE-inhibitors (Benazepril 0.25 mg/kg SID) and controlled every three to four months over an 18month period. The dog was doing very well on monotherapy, was completely asymptomatic, although it did develop an additional ventricular arrhythmia (monomorphic right ventricular extrasystole), with increased endsystolic volume index, pulmonic flow velocity, Qp:Qs ratio and transvalvular AV-valve flow and regurgitation (Table 1). Because of the development of a behavioral disorder (childdirected aggression) the dog had to be euthanatized at the age of 6 years.
Chris Amberger, Claude Boujon
Figure 1 - ECG (Lead II, 1 mV/cm, paper speed 100 mm/sec) showing RBBB and Phonocardiogramm (70/140 Hz) with diamond-shaped holosystolic ejection murmur.
Figure 2 - Left lateral and dorsoventral radiographs of the cardiac silhouette showing right ventricular and atrial enlargement as well as pulmonary overcirculation. a
b
38
Journal of Veterinary Cardiology, Vol.4, No. 2, November 2002 duration 0.12 sec with mean electrical axis -100°). A systolic crescendo-decrescendo murmur was recorded on phonocardiography (Figure 1), with elevated systolic time intervals (PEP/LVET 0.4). Thoracic radiography revealed right-sided cardiomegaly (short axis length greater than 6 vertebrae on the Buchanan’s Index) and pulmonary overcirculation (Figure 2). The arterial blood pressure was normal (Systolic/Diastolic/Mean 135/82/99 mmHg, HR 100 bpm). Echocardiography: On 2-D echocardiography, from the right parasternal long axis view, the right ventricle (RV) was enlarged and the heart showed generalized hypokinetic motion. Due to volume overload, the heart rate was quite slow, as the increase of cardiac output or stroke volume directly reduces heart frequency (optimal rate by increased end-diastolic volume). Atrial septal defect and bilateral AV-valve dysplasia with malposition of the septal leaflets, particularly of the tricuspid valve, were present (Figure 3a). The main abnormalities measured with 2D-guided M-mode were an increased internal dimension of the right ventricle and a moderate increase of the left ventricle dimensions (EDVI = 115 ml/m2, ESVI 56 ml/m2, eccentric hypertrophy) (Table 1). In color Doppler, a turbulent regurgitant flow coming from the left septal cusp of the mitral valve toward the dysplastic annulus mimicked a VSD-jet with positive flow on the right side of the heart (Figure 3b), with a velocity of 2.5 m/sec (25 mmHg). No positive flow was evident between left and right atria, as the ASD was more than twothirds of the size of the septum. The pulmonic flow velocity was increased (> 1.5 m/sec) and turbulent, with associated ejection murmur, and pulmonary hypertension was present (Tricuspid regurgitation over 4 m/sec (N<2.8 m/sec), corresponding to a RV-RA pressure gradient of 64 mmHg). From the left parasternal standard view, ASD with dilation of the right atrium, dysplastic AV-valves and right ventricular dilation were evident (Figure 4). Tricuspid and mitral regurgitation were both present, with normal E/A ratio and increased inflow velocities, as well as aortic flow, with a non-turbulent PWD-shape (Table 1). Qp:Qs ratio as determined by cardiac output via aorta and pulmonary artery systolic flow velocity integral was 2.5:1, which demonstrates an increased right cardiac output with a left-to-right shunt8. Because the major problem was generalized volume overload (LR-shunt and bilateral AV-insufficiency), the dog was treated with ACE-inhibitors (Benazepril 0.25 mg/kg SID) and controlled every three to four months over an 18month period. The dog was doing very well on monotherapy, was completely asymptomatic, although it did develop an additional ventricular arrhythmia (monomorphic right ventricular extrasystole), with increased endsystolic volume index, pulmonic flow velocity, Qp:Qs ratio and transvalvular AV-valve flow and regurgitation (Table 1). Because of the development of a behavioral disorder (childdirected aggression) the dog had to be euthanatized at the age of 6 years.
Table 1 - Echocardiographic values with references. Echocardiographic findings (M-Mode and Pulse Wave Doppler, Continuous Wave Doppler for velocities over 1.5 m/sec).
Body weight (kg) Heart rate (bpm) RVIDd (mm) IVSd (mm) LVIDd (mm) LVWd (mm) IVSs (mm) LVIDs (mm) LVWs (mm) FS (%) Aod (mm) Las (mm) Vmax, Pulmonary (m/sec) Vmax, Aortic (m/sec) Vmax, Mitral (m/sec) Vreg, Mitral (m/sec-mmHg) Vmax, Tricuspid (m/sec) Vreg, Tricuspid (m/sec-mmHg)
Patient (initial exam) 25.7 90 NSR 24.1 11.4 45.8 9.7 14.8 29.4 13.3 36 22.4 25.1 1.15 1.31 1.5 4.8-92 1.4 4.2-70
(after 15 month) 26.6 120 VPC’s 32.7 9.9 46.8 9.5 15.1 34.6 12.8 26 22.3 40.1 2.58 1.12 1.85 6.0-144 1.6 4.6-85
Reference values* (Mean +/- SD) 25 70-140 14.4 +/-2.7 8.7 +/- 0.9 44.8+/-2.9 7.9+/-1.0 13.0+/-1.5 31.0+/-2.5 12.1+/-1.2 28-40 24.6+/-1.6 21.8+/-2.4 1.0 +/-0.15 1.19+/-0.18 0.81+/-0.14 0.63+/-.018
* Lombard CW : Normal values of the canine M-mode echocardiogram. Am J Vet Res 1984;45: 2015, and with data from Henik RA, Echocardiography and Doppler Ultrasound, in Tilley LP and Goodwin LK (eds): Manual of Canine and Feline Cardiology, 3rd Ed. W.B. Saunders, Philadelphia 2001.
Pathological findings: The heart showed a severe eccentric hypertrophy of the right ventricle and atrium and a mild eccentric hypertrophy of the left ventricle (Figure 5). Intracardiac anomalies included the interatrial septum, the tricuspid and the mitral valves. An interatrial septum defect of ostium primum type, 25 mm in diameter, was found (Figure 6). There was a fibrous zone on the inferior border of the defect, including the septal cusp of the mitral valve and was bound by fibrous tissue to the septal cusp of the tricuspid valve. The caudal and the septal leaflets of the tricuspid valve were fused. The septal leaflet of the mitral valve was adhered directly to the septum. Both AV-valves were dislocated toward the apex and all leaflets were thick and nodular and showed histologically a myxoid degeneration. Their cordae tendinae were too short and thick with normal insertion. Moreover, there was an additional atrial septum defect 12 mm proximal to the first one (Figure 6). This defect corresponds to an ostium secundum type and was 15 x 10mm large. Macroscopically, the liver was rather small, with a finely irregular surface with a very hard consistency. Histologically the architecture of the liver was modified. The hepatocytes were variable in size, blood stasis and intrahepatic porto-portal shunt and fibrosis were observed. Lymphocytes and haemosiderin containing macrophages were present in the periportal area, and a light fibrosis of the central veins was present. No macroscopic abnormalities were found in the lungs.
Discussion In this patient, an incomplete form of an endocardial cushion defect and ostium secundum type interatrial septal defect were observed. Because the endocardial cushions
contribute to the development of the atrial and ventricular septa and to the septal leaflets of the mitral and tricuspid valve, anomalous development may result in a septum primum atrial septal defect and AV-valve dysplasia, with abnormal leaflets, myxoid degeneration and short thickened cordae tendinae9,10. AV-valve dysplasia explains the AV-valvular regurgitation. The severe left to right shunting of blood through the interatrial septum defect and AV-valvular regurgitation lead to volume overload and to eccentric hypertrophy of both ventricles and the right atrium. The severe atrial volume overload increased also enddiastolic volume, and the heart rate was kept relatively slow due to the increase of the cardiac output (CI over 10 L/min/m2). Despite the complex malformation, the left ventricular function was sufficient to provide normal arterial pressure and peripheral perfusion. Measurement of Qp/Qs from Doppler derived pulmonary and aortic blood flow may provide some information about the quantification of the shunt. Qp/Qs ratio over 2 are considered haemodynamically significant, but the error done on the pulmonic side may be important11. The resulting pulmonary hypertension was well tolerated, and the dog did not develop Eisenmenger’s syndrome at that age. There was still no ascites or peripheral venous engorgement at that time. Histologically, however, signs of beginning liver cirrhosis were observed, probably of cardiac origin. It seems that this particular cardiac abnormality has similarities with the pathophysiology of mitral and tricuspid dysplasia12 and may be well compensated for a long time in dogs. Generally, only the most severely affected animals develop congestive heart failure and atrial arrhythmias within the first year of age in these AV-valve dysplasia. 39
Chris Amberger, Claude Boujon
Figure 3(a-b) - 2D right parasternal long axis view: The interventricular septum is too short, both atrioventricular valve insertions are displaced toward the axis of the heart. The interatrial septum is incomplete.There is a systolic turbulent colorflow Doppler from the mitral valve regurgitation with a high velocity left to right shunt at the atrial level similar to VSD-shunt. a
The presence of P-mitrale and first degree AV block reflect atrial dilation and alteration in the conductive system. In dogs, definitive morphologic data about right bundle branch block are missing13. An isolated case report described RBB in a dog with ASD13. These ECG change are probably mostly compatible with a manifestation of right ventricular overload rather than a true conduction delay in the RBB15,16. There was no presence of splintered QRS-complex despite of the tricuspid abnormality17. The difficulty of interpretation of this cardiac malformation was due to the mix of systolic regurgitation from mitral and tricuspid valves associated with the absence of an interatrial septum at the valvular level. As the pars membranacea of the interventricular septum was very thin (but without defect), the severe color flow Doppler aliasing mimicked a VSD jet with a positive flow from left to right. In fact, the regurgitative jet from the mitral valve goes through the ASD into the right ventricle, and only the velocity of the jet allows the differentiation to be made (Figure 3c). In dogs with a VSD and mild pulmonary hypertension, the pressure gradient between the LV and the RV should be above 50 to 80 mmHg, corresponding to a velocity of 3.5 to 4.5 m/sec. In this dog, it was impossible to find a flow velocity over 2-2.5 m/sec. This was due to the fact that the flow was not coming from the left ventricle, but from the left atrium due to mitral regurgitation, and the direction of this jet was very turbulent because of the simultaneous presence of tricuspid regurgitation. The list of differential diagnoses in this patient included complete atrioventricular canal defect2, common atrium 18, and ostium primum defect associated with mitral and tricuspid dysplasia6. The definitive confirmation of the diagnosis was made by necropsy. There have been only few cases of atrioventricular canal described in dogs4,5,19. To our knowledge, this clinical report is the first with incomplete atrioventricular canal defect (mitral and tricuspid dysplasia associated with ostium primum ASD) in combination with an ostium secundum ASD. 40
b
Figure (3c) - Schematic drawing of the haemodynamics associated with a partial atrioventricular canal defect, with left to right shunting trough the atrial septal defect over the septum membranaceum, with additional turbulence from bilateral AV-valve insufficiency due to dysplastic septal leaflets.
Figure 4 - Left parasternal 4-chamber view showing abnormal AV-valve insertion and severe dilation of the right atrium.
Chris Amberger, Claude Boujon
Journal of Veterinary Cardiology, Vol.4, No. 2, November 2002
Figure 3(a-b) - 2D right parasternal long axis view: The interventricular septum is too short, both atrioventricular valve insertions are displaced toward the axis of the heart. The interatrial septum is incomplete.There is a systolic turbulent colorflow Doppler from the mitral valve regurgitation with a high velocity left to right shunt at the atrial level similar to VSD-shunt. a
The presence of P-mitrale and first degree AV block reflect atrial dilation and alteration in the conductive system. In dogs, definitive morphologic data about right bundle branch block are missing13. An isolated case report described RBB in a dog with ASD13. These ECG change are probably mostly compatible with a manifestation of right ventricular overload rather than a true conduction delay in the RBB15,16. There was no presence of splintered QRS-complex despite of the tricuspid abnormality17. The difficulty of interpretation of this cardiac malformation was due to the mix of systolic regurgitation from mitral and tricuspid valves associated with the absence of an interatrial septum at the valvular level. As the pars membranacea of the interventricular septum was very thin (but without defect), the severe color flow Doppler aliasing mimicked a VSD jet with a positive flow from left to right. In fact, the regurgitative jet from the mitral valve goes through the ASD into the right ventricle, and only the velocity of the jet allows the differentiation to be made (Figure 3c). In dogs with a VSD and mild pulmonary hypertension, the pressure gradient between the LV and the RV should be above 50 to 80 mmHg, corresponding to a velocity of 3.5 to 4.5 m/sec. In this dog, it was impossible to find a flow velocity over 2-2.5 m/sec. This was due to the fact that the flow was not coming from the left ventricle, but from the left atrium due to mitral regurgitation, and the direction of this jet was very turbulent because of the simultaneous presence of tricuspid regurgitation. The list of differential diagnoses in this patient included complete atrioventricular canal defect2, common atrium 18, and ostium primum defect associated with mitral and tricuspid dysplasia6. The definitive confirmation of the diagnosis was made by necropsy. There have been only few cases of atrioventricular canal described in dogs4,5,19. To our knowledge, this clinical report is the first with incomplete atrioventricular canal defect (mitral and tricuspid dysplasia associated with ostium primum ASD) in combination with an ostium secundum ASD. 40
Figure 5 - External view of the heart: cardiomegaly with eccentric hypertrophy of right ventricle (RV) and atrium (RA) and, to a lesser extent, of the left ventricle (LV).
b
Figure (3c) - Schematic drawing of the haemodynamics associated with a partial atrioventricular canal defect, with left to right shunting trough the atrial septal defect over the septum membranaceum, with additional turbulence from bilateral AV-valve insufficiency due to dysplastic septal leaflets.
Figure 4 - Left parasternal 4-chamber view showing abnormal AV-valve insertion and severe dilation of the right atrium.
Figure 6 - View of the interatrial septum with both ostium primum (* ) and secundum (D) septal defects and AV valvular dysplasia (¨). Right atrium (RA), right ventricle (RV) and interventricular septum (IVS).
Abbreviations: PWD: Pulsed wave Doppler CWD: Continuous wave Doppler ESVI: Endsystolic Volume Index, ESVI = ESV(ml)/BSA(m2) EDVI : Enddiastolic Volume Index, EDVI = EDV(ml)/BSA(m2) Both are LV-stroke volume calculated with M-mode LVIDd and LVIDs using Teicholz Method (LVVd(s) = (7 x LVIDd(s)3)/(LVIDd(s) + 2.4) divided by Body surface area (BSA). PEP: Left Ventricular pre-ejection period (isovolumic contraction). LVET: Left ventricular ejection time (cardiac systole). CI: Cardiac index, Cardiac output (flow/min) divided by heart rate equal average stroke volume. Cardiac output is divided by BSA to produce an index that is the same for animals of different size. ASD: atrium septal defect - VSD: ventricle septal defect.
References 1. King AS. Development of the heart and Great Vessels, in The Cardiorespiratory System. Blackwell Science Ltd, Oxford, 1999: 369-376 2. Kittleson MD, Atrioventricular Canal Defect in Kittleson MD and Kienle RD. Small Animal Cardiovascular Medicine, Mosby Inc, St Louis 1998; 283-284 3. Liu SK, Ettinger S. Persistent Common Atrioventricular Canal in Two Cats. J Am Vet Med Assoc 1968; 153/5: 556-562 4. Monnet E, Orton C, Gaynor J, Boon J, Petersen D, Gaudagnoli M. Diagnosis and surgical repair of partial atrioventricular septal defects in two dogs. J Am Vet Med Assoc 1997; 211/5: 569-572 5. Nakayama T, Wakao Y, Uechi M, Muto M, Kageyama T, Tanaka K, Kawabata M, Takahashi M. A case report of surgical treatment of a dog with atrioventricular septal defect (incomplete form of endocardial cushion defect). J Vet Med Schi 1994; 56/5: 981-984 6. Kittleson MD, Atrial Septal Defects in Kittleson MD and Kienle RD. Small Animal Cardiovascular Medicine Mosby, Inc, St Louis 1998; 231-233 7. Hamlin RL, Smith CR, Smetzer D. Ostium Secundum Type Interatrial Septal Defects in the Dog. J Am Vet Med Assoc 1963; 143/2: 149-157 8. Kirberger RM, Berry WL. Atrial septal defect in a dog: the value of Doppler echocardiography. J S Afr Vet Assoc 1992; 63/1: 43-48 9. Robinson WF, Maxie MG. The cardiovascular system, in Jubb KVF, Kennedy PC, Palmer N (Eds). Pathology of Domestic Animal. 4th Ed., Academic Press Inc., San Diego 1992: 3: 9-17 10. Liu S-K, Tilley P. Dysplasia of the tricuspid valve in dog and cat. J Am Vet Med Assoc 1976 (169): 623-630 11. Bonagura, JD, Advance in Doppler Echocardiography, Proc. 20th annual ACVIM forum 2002: 746-748 12. Bonagura J, Lehmkuhl L. Dysplasia of the Atrioventricular valves, in Fox PR, Sisson D, Moise NS (Eds) Textbook of Canine and Feline Cardiology. Philadelphia, W.B. Saunders; 1999: 520-526 13. Miller MS, Tilley LP, Smith FWK, Fox PR: Intraventricular conduction defects, in Fox PR, Sisson D, Moise NS (Eds) Textbook of Canine and Feline Cardiology. Philadelphia, W.B. Saunders; 1999: 84-86 14. Troy GC, Turnwald GH. Atrial Fibrillation and Abnormal Ventricular Conduction Presented as Right Bundle Branch Block in a Dog with an Atrial Septum Primum Defect. J Am Anim Hosp Assoc 1979; 15: 417-420 15. Volpi A, Ferrario G, Dubini D et al. Atrial septal defect of the ostium secundum associated with incomplete left bundle branch block. G Ital Cardiol 1983; 13(6): 472-474 16. Sung RJ, Tamer DM, Agha AS et al. Etiology of the electrocardiographic pattern of “incomplete right bundle branch block” in atrial septal defect: an electropyhsiologic study. J Pediatr 1975(87):1182-1186 17. Kornreich BG, Moise NS Right atrioventricular valve malformation in dogs and cats: electrocardiographic survey with emphasis on splintered QRS complexes . J Vet Intern Med 1997: 11(4): 226-230 18. Fernandez del Palacio MJ, Costa A, Talavera J et al. Common Atrium in a Dog, J Vet Intern Med 2001; 15: 57-62 19. Santamarina G, Espino L, Mila M, Suarez ML. Partial atrioventricular canal defect in a dog. J Small Anim Pract 2002: 43, 17-21
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