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Cor Triatriatum Dexter Complicated with Pulmonic Stenosis and Patent Foramen Ovale in A Pitbull Terrier Puppy
Ran Choi*,**, Dong-Guk Lee*, Hyun-Seok Choi** and Changbaig Hyun**1
*Jukjeon Animal Medical Center, Daegu 704-923, Korea
**Section of Small Animal Internal Medicine, College of Veterinary Medicine, Kangwon National University, Chuncheon 201-100, Korea
(Accepted: February 21, 2014)
Abstract : A 2-month-old intact male Pitbull terrier (weighing 1.01 kg) were referred with primary complaints of severe abdominal distension, exercise intolerance, retarded growth, yellow nasal discharge and anorexia. Diagnostic imaging studies found enlarged right atrium partitioned by abnormal membrane, severe pulmonic systolic jets (5.66 m/s of peak velocity) and right-to-left blood shunt at the inter-atrial septum. Based on clinical and diagnostic findings, the case was diagnosed as cor triatriatum dexter complicated with severe pulmonic stenosis and right-to-left shunted patent foramen ovale. Either surgical or interventional therapy has not been attempted, because of unstable patient’s condition.
Using blood transfusion, oxygen supply and cardiac medications (i.e., sildenafil, spironolactone, enalapril), the dog was recovered.
Key words : cor triatriatum dexter, pulmonic stenosis, patent foramen ovale, dog, congenital heart defects.
Introduction
Cor triatriatum is a congenital heart defect, which is char- acterized by the subdivision of atrium by a thin membrane (7). Therefore, dogs with cor triatriatum have three atrial chambers. There are two types of cor triatriatum. Cor triatri- atum sinistrum (CTS) is the condition where the left atrium subdivided into two atria, while cor triatriatum dextrum (CTD) is the condition where the right atrium subdivided into two atria. CTS is more common type of cor triatriatum in cats and humans (4,5,7), while CTD is more common in dogs (3).
Cor triatriatum is taken up 0.1% of all congenital cardiac malformations in humans and is often occurred with other cardiac defects (~50% of cases in humans) (7). Clinical man- ifestations can be differed by type and severity of cor triatria- tum and concurrent other cardiac defects, although dogs with CTD may show typical clinical signs associated with right sided heart failure (e.g. distended caudal vena cava, ascites, hepatomegaly) (3). Successful therapy can be achieved by enlarging the membrane orifice or excising the abnormal membrane to remove flow obstruction (1,2,9).
Case
A 2-month-old intact male Pitbull terrier (weighing 1.01 kg) were referred with primary complaints of severe abdom-
inal distension, exercise intolerance, retarded growth, yellow nasal discharge and anorexia. All other siblings (5 dogs) of litter were died within few days of birth. He is the only one survived dog. No particular other medical history was obtained for this dog. Physical examination on this dog found pale and anemic mucous membrane, ascites, subcutaneous edema, ema- ciation, loud left basal systolic (grade 4/6) and soft left api- cal regurgitant (grade 2/6) murmurs, tachycardia (~200 beats per min) and weak femoral pulsation. The systolic blood pressure of this dog measured by Doppler method (811B, Parks medical, USA) was ~100 mmHg.
Complete blood cell count revealed decreased hematocrit (11.9%, reference 32-55%), decreased red cell counts (2× 10 M/L, reference 4.7-8.5 M/L), decreased hemoglobin (8.4 g/dL, reference 10.3-18 g/dL) and increased reticulocyte (366.6× 10 K/uL, reference 0-60× 10 K/uL). Blood biochemistry re- vealed decreased albumin (1.3 g/dL, reference 2.1-3.6 g/dL) and total protein (3.7 g/dL, reference 4.8-7.2 g/dL), increased alanine transaminase (578 U/L, reference 8-75 u/L) and aspar- ate transaminase (149 U/L, reference 0-50 U/L), increased blood urea nitrogen (64 mg/dL, reference 10-26 mg/dL). Blood gas analysis revealed decreased serum sodium (125 mEq/L, reference 139-150 mEq/L) and total carbon dioxide (16 mmol/
L, reference 17-25 mmol/L).
Electrocardiogram showed normal sinus rhythm and sinus tachycardia (195-210 beats per min). Thoracic radiography revealed generalized cardiomegaly with caudal vena cava dis- tension and massive ascites (Fig 1B). Trachea was dorsally displaced and hypoplastic, although the radiographic position-
1Corresponding author.
E-mail: hyun5188@kangwon.ac.kr
ing was inappropriate due to respiratory distress.
The cardiac apex was severely deviated to the left thorax (Fig 1A). Echocardiography revealed the right atrium subdi-
vided into two atria by membranous structure (Fig 2A). There was small fenestration between distal (DRA) and proximal right atrium (PRA) and the blood flow was entering through Fig 1. Thoracic radiography of this dog. A: Radiography revealed generalized cardiomegaly with left deviation of cardiac apex. B:
Radiography revealed generalized cardiomegaly with marked distended caudal vena cava and severe ascites. The trachea looks hypo- plastic and dorsally displaced, although the radiographic positioning was inappropriate due to respiratory distress.
Fig 2. Echocardiography of this dog. A: Right parasternal long axis of 4 chamber view is showing the right atrium subdivided into two atria by membranous structure. B: Continuous wave Doppler echocardiography at the fenestration between distal (DRA) and prox- imal right atrium (PRA) is showing the blood flow is entering through small fenestration between DRA and PRA. LA, left atrium;
LV, left ventricle; RV, right ventricle.
Fig 3. Echocardiography of this dog. A: Color Doppler imaging taken at right parasternal long axis of 4 chamber view is showing a regur- gitant jet from left ventricle (LV) to atrium (LA) by defected parietal (posterior) cusp of mitral valve. The arrow indicated severe pul- monary systolic jets from right pulmonary artery by marked pulmonary stenosis. B: Color Doppler imaging taken at left apical long axis of 4 chamber view is showing a diverging regurgitant jets from LV to LA by cleft posterior cusp of mitral valve. RV, right ventricle.
small fenestration from DRA to PRA (Fig 2B). Color Dop- pler imaging (CDI) also revealed mild regurgitation from left ventricle (LV) to atrium (LA), especially from parietal (pos- terior) cusp of mitral valve (Fig 3A and 3B). CDI also found a systolic jet from right ventricular outflow tract (pulmonary artery; Fig 4A and 4B). Continuous wave Doppler (CWD) echocardiography for this jet revealed severe pulmonary stenosis (PS, maximal velocity of 5.66 m/s, pressure gradi- ent 128.4 mmHg; Fig 5A) and moderate pulmonary hyper-
tension (PHT, maximal velocity of 2.58 m/s, pressure gradient 26.7 mmHg; Fig 5B). There were weak blood shunt flow between the DRA and the LA. Microbubble contrast study was performed to identify the direction and severity of this shunt. This study revealed the right to left blood shunt through patent foramen ovale between two atria (Fig 4C). M- mode echocardiography of left ventricle (LV) revealed septal flattening and right chamber dilation, due to pressure over- load from PS and CTD (Fig 4D). Based on diagnostic find- Fig 4. Echocardiography of this dog. A: Color Doppler imaging taken at right parasternal short axis of aortic/ pulmonic valve level is showing a systolic jet from right ventricular outflow tract (pulmonary artery). B: Color Doppler imaging taken at right parasternal long axis of 4-chamber view is showing a systolic jet from pulmonary artery (PA). The strong jet is also entering to right pulmonary artery (RPA). C: Microbubble contrast study revealed the right to left shunt through small fenestration (foramen ovale; arrow) between the distal right (DRA) and left atrium (LA). D: M-mode echocardiography of left ventricle (LV) revealed septal flattening and right chamber dilation, due to pressure overload from pulmonic stenosis and cor triatriatum dexter. PRA; proximal right atrium.
Fig 5. Echocardiography of this dog. A: Continuous wave Doppler echocardiography taken at right parasternal short axis of left ventricle and pulmonary artery revealed marked systolic jets (maximal velocity of 5.66 m/s, pressure gradient 128.4 mmHg), indicating severe pulmonic stenosis. A: Continuous wave Doppler echocardiography taken at right parasternal short axis of left ventricle and pulmonary artery revealed marked regurgitant jets (maximal velocity of 2.58 m/s, pressure gradient 26.7 mmHg), indicating moderate pulmonary hypertension.
ings including clinical manifestations of right sided congestive heart failure, generalized cardiomegaly with ascites and dis- tended caudal vena cava, and right atrium divided by mem- branous structure, systolic jets at right ventricular outflow tract, mitral regurgitant jets and mild right-left shunt at the inter-atrial septum, this case was diagnosed as cor triatriatum dexter complicated with pulmonic stenosis, mitral regurgita- tion and right-to-left patent foramen ovale.
Immediate medical treatment was directed to restore circu- latory blood cells by blood transfusion (35 mL whole blood to reach 32% of hematocrit), to reduce the resistance of pul- monary vasculature (sildenafil, 1 mg/kg, q8hr, PO), to inhibit renin-angiotensin-aldosterone system (RAAS; enalapril, 0.5 mg/kg, q12hr, PO; spironolactone, 1 mg/kg, q12hr, PO) and to improve tissue oxygenation (oxygen tank, 5 L/min). The clinical condition of dog was improved after emergency treatment. The dog was released with prescription of sildena- fil (1 mg/kg, q8hr, PO), enalapril (0.5 mg/kg, q12hr, PO) and spironolactone (1 mg/kg, q12hr). After a week, the dog came back for rechecking. Clinical status and laboratory findings were much improved, although the dog was still emaciated.
Ascites and subcutaneous edema was disappeared. The dog was eating and playing better.
The diagnostic imaging studies were repeated but there were no significant changes, despite clinical improvement.
One interesting echocardiographic finding was that the MR was not detected again, so as the left apical murmurs was.
This finding was suggested the MR might be not pathological, but functional, probably because of severe anemia. Interven- tional balloon dilation therapy for CTD and PS has yet been attempted, because the dog was too young and emaciated.
However, the dog was euthanized by the owner’s request after 3 months of medical therapy.
Discussion
CTD has rarely been reported in dogs and occurs from the complete persistence of the right sinus valve of the embry- onic heart (3). During embryogenesis, the right horn of the sinus venosus becomes proximal portion of the RA, while the embryologic right atrium takes up the distal portion of RA. Those two portions of RA are divided by membranous structure and connected through the sinoatrial orifice. The proximal portion of RA receives the venous blood from both vena cava, whereas the distal portion of RA is in contact with the tricuspid valve and the right atrial appendage. CTD occurs if this embryonic membrane between proximal and distal RA has been persisted (7). Therefore, severity of clinical signs can be differed by the size of the communicating orifice between the proximal and distal RA. The smaller the com- municating orifice is, the milder the clinical signs of dog (3).
Diagnosis of CTD may not be straightforward unless good echocardiographical support is available. No typical heart murmurs and ECG findings in dogs with CDT has been yet reported. In this case, there were no typical ECG findings, as
reported in veterinary literatures (1-3). The most obvious heart murmur for this case was loud left basal systolic murmur and mild left apical regurgitant murmur. Authors believed the first murmur might be due to pulmonic stenosis and the sec- ond murmur might be due to mitral regurgitation. In fact, we could not detect any other murmur associated with CTD, as noticed in veterinary literatures (1-3). Typical thoracic radio- graphic findings in dogs with CTD are a distended caudal vena cava without generalized cardiomegaly and persistent ascites (3). In this case, ascites and cardiomegaly on the tho- racic radiography were very obvious at the first presentation, because the dog also had other compound cardiac malforma- tions causing RA/RV dilation. Conclusive findings in echocar- diography are the abnormal membrane and the flow distur- bance through the small fenestration in the partitioned RA (2,8). In this case, the confirmation of abnormal membrane and small fenestration in the partitioned RA was straightfor- ward. However the concurrent cardiac malformations made us confuse to understand the pathological and hemodynamic changes. At the first presentation, authors believed the dog might have mitral valvular dysplasia, because the dog had mild-to-moderate mitral regurgitation (especially posterior cusp) with left apical heart murmur, although we failed to visualize the defected mitral valve. However, the MR turned out not pathological but functional. Authors believed severe anemia at the first presentation might be a cause of MR in this dog, because the MR was disappeared after correction of anemia. According to human literature, severe anemia can cause functional MR (10). Diagnosis of small atrial septal defect (ASD) and PFO is challenging in small dogs and cats.
Microbubble study and transesophageal echocardiography are supportive diagnostic method for small ASD and PFO. In this study, we could not visualize the PFO at the inter-atrial septum. However, we could prove right-to-left shunted blood flow through tiny fenestration at the inter-atrial septum, using microbubble study.
Due to obstruction to venous flow through the abnormal membrane between the PRA and DRA, the venous return may be stagnant and cause to increase in hydrostatic pres- sure within the caudal vena cava and abdominal structures.
Therefore, the most prominent clinical sign associated with CTD is persistent ascites at an early age, as also seen in this case. Other clinical signs associated with CTD are exercise intolerance, lethargy, distended cutaneous abdominal veins, and diarrhea (1-3). Those clinical sings are associated with right-sided congestive heart failure, as similarly noticed in this case. Furthermore, the concurrent pulmonic stenosis in this case might also deteriorate clinical signs associated with right-sided heart failure. Persistently higher RV pressure by CTD with PS in this dog (even after birth) might interfere postnatal closure of the foramen ovale in the inter-atrial sep- tum and resulting in right-to left patent foramen ovale (PFO), although the dog was not apparently cyanotic at the first pre- sentation.
General therapeutic recommendation for solitary CTD is
the enlargement of the membrane orifice or excision of the abnormal membrane to remove flow obstruction, by surgical (9) or trans-catheter intervention (e.g. balloon dilation [1,2]).
Medical treatment should be directed to lessen ascites using furosemide and/or spironolactone. However, in this case, we could not attempt the balloon dilation, immediately, because the dog was too anemic and emaciated and had other concur- rent cardiac defects. Therefore the initial medical treatment was focused to restore patient’s condition and to lessen the clinical signs associated with CTD and other concurrent car- diac defects. Thanks to blood transfusion and cardiac medi- cation, the clinical condition was much improved with time.
We did not remove ascites from this dog, because the dog had very severe hypoabuminemia and proteinemia. We did not also use furosemide for this dog, despite ascites and sub- cutaneous edema, because the dog was too emaciated and hypotensive. Therefore, our cardiac medication was focused to reduce the resistance of pulmonary vasculature (sildenafil) and to inhibit RAAS (enalapril and spironolactone). This treatment was successful to improve clinical condition and to maintain good health condition. However, the dog was euth- anized after 3 months of medical therapy, because of recur- rent ascites.
In conclusion, this case is described CTD complicated with severe PS and right-to-left shunted PFO in a puppy. Although CTD in dogs have been well described in veterinary litera- tures, to author’s the best knowledge, this is the first case report describing CTD complicated with PS and PFO in dogs.
Acknowledgement
This study was supported by Human Resource Training
Project for Regional Innovation from National research foun- dation of Korea (NRF).
References
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핏불테리어종 자견에서 폐동맥 협착과 난원공 개존증이 합병된우측 삼중심방증
최란*,**·이동국*·최현석**·현창백1**
*대구 죽전 동물병원, **강원대학교 수의학과 소동물 내과교실
요 약 : 2개월령 수컷 핏불테리어종 개 (체중 1.01 kg)가 심한 복부 팽만, 운동 불내성, 성장 지연, 노란 비루와 식욕 부진을 주증으로 진료 의뢰 되었다. 영상 진단상에 비정상적인 막으로 분할된 확대된 우심방, 심한 수축기 폐동맥 제 트 혈류 (최고혈류 5.66 m/s) 그리고 심방 중격에서의 우좌 단락혈류가 관찰되었다. 임상증상 및 진단학적 결과에 기 초하여, 본 증례는 심한 폐동맥 협착과 우좌 단락의 난원공 개존증이 합병된 우측 삼중심방증으로 진단 되었다. 비안 정적인 환자의 상태 때문에 수술적 혹은 중재적 치료는 시도되지 않았다. 그 개는 수혈, 산소공급 그리고 심장 관련 약물적 치료(예, 실데나필, 스피로노락톤, 에날라프릴)로 회복되었다.
주요어 : 우측 삼중심방증, 폐동맥 협착, 난원공 개존증, 개, 선천성 심장 결손
