While recognized as a relatively common form of cardiomyopathy in humans, ventricular noncompaction has only been reported as a spontaneously occurring pathology in cats. In two independent reports, LVNC was described in a Maine Coon-cross cat that was heterozygous for the cardiac myosin binding protein C mutation (A31P), in 2017 [6], and in a two-month-old kitten affected by Purkinje fiber dysplasia, in 2009 [5]. Experimentally, LVNC is being studied in transgenic mouse models and in species in which myocardial trabeculation is ordinarily present, such as chicks and adult fish [2, 7, 8, 16,17,18,19,20]. To the author’s best knowledge, this is the first report of LVNC in a canine patient.
Depending on the anatomical distribution, age of clinical onset, and coexistence of other congenital cardiac anomalies, several forms of myocardial noncompaction are described in humans. Based on the ventricle involved, myocardial noncompaction is classified as either left ventricular or biventricular (BVNC), where, in addition to LVNC, RV involvement is confirmed by a ratio of more than 75% between the noncompacted and compacted layers. Left ventricular noncompaction is classified as congenital or acquired (or as pediatric and adult form, respectively), or as isolated (or simple) versus non-isolated (i.e., associated with other cardiac anomalies) [2].
Based on genetics and the typical disease natural history, pediatric LVNC is likely a distinct, primary condition while the adult onset LVNC is a phenotypic variation of other cardiomyopathies [4]. In children, the LVNC is often associated with atrial septal defect, ventricular septal defect, patent ductus arteriosus, Ebstein’s anomaly, atrioventricular and pulmonary valvular abnormalities, ventricular septal defects, persistent left superior vena cava, histiocytoid cardiomyopathy, partial anomalous pulmonary venous return, and coronary ostial stenosis [15, 21].
The present LVNC case revealed several congenital cardiac co-morbidities, similar to what was reported in children. These co-morbidities involve both atrioventricular (tricuspid valve dysplasia) and semilunar valve defects (pulmonic stenosis).
While historically reported only based on gross pathology and histopathological findings, the diagnosis of LVNC is currently mainly attained by echocardiography [3, 22, 23] and, more recently, by cardiac MRI [1, 24,25,26,27,28], which is likely the reason behind the higher incidence of LVNC reported in recent years. Characteristic LVNC echocardiographic features include: (1) a thick, bilayer myocardium, (2) prominent trabeculation, and (3) deep endomyocardial recesses [23]. In the 8-week-old Savannah kitten with Purkinje fiber dysplasia/histiocytoid cardiomyopathy, LVNC was an incidental necropsy finding, with no pre mortem echocardiography performed. In the Maine Coon cross cat, the LVNC was seen on echocardiography at two years of age, as a “moth-eaten” appearance of the LV wall in short-axis view with deep recesses in the inner LV wall on the long axis view, representing hypertrabeculation. This was also subsequently confirmed histopathologically [6]. The cat had biventricular noncompacted cardiomyopathy where the RV was considered to be noncompacted, based on the LVNC criteria.
In the present case, the noncompacted layer of the RV comprised more than 75% of the wall, which corresponds to the biventricular form. However, definitively diagnosing biventricular noncompacted cardiomyopathy in this case was challenging for several reasons: (1) RV hypertrophy induced by the concurrent pulmonic stenosis, (2) trabeculation in the RV was an expected finding in the normal RV myocardium [4], and (3) due to the absence of a specific location compared with LVNC.
In this case, as in the one with Purkinje fiber dysplasia, the diagnosis was only based on gross and histopathological findings that met criteria such as a two-layer structured myocardium, segmental rather than scattered trabeculation within the apical LV, a NC/C ratio > 50%, and the concomitant presence of other congenital heart defects, namely TVD and PS. A disturbed cardiac conduction system comprising His and Purkinje’s fibers [3] can be potentially relevant to LVNC in the cat reported with Purkinje fiber dysplasia [5]. However, in the present canine case there was no evidence of Purkinje fiber involvement. The absence of echocardiographic evidence of LVNC in these two cases is due to the unknown existence of this pathology before 2009 in cats and present in dogs. In the Maine Coon cross cat, the presence of the cardiac myosin binding protein C mutation implied a more detailed examination of the myocardium. Therefore, the serendipity of identifying the noncompaction during echocardiography was superior in this case. In the present case, the size and the young age of the dog associated to the moderate dyspnea limited our ability to describe the specific features related to LVNC on the initial echocardiographic examination.
The three most common complications of LVNC are heart failure, ventricular arrhythmias and systemic embolic events, a so-called “classic triad” [29]. However, the clinical presentation of LVNC is highly variable [4]. Therefore, in the absence of this classic triad, the presence of only non-specific clinical signs such as poor body condition, anorexia, exercise intolerance and dyspnea, and the scarcity of cases reported in the literature with no widely accepted or robust diagnostic criteria, the diagnosis of LVNC is difficult to confirm.
In humans, the differential diagnosis list includes hypertrophic cardiomyopathy and dilated cardiomyopathy. In hypertrophic cardiomyopathy, the NC/C ratio does not usually reach a value higher than 2:1, and the trabeculated regions tend to be segmental in LVNC and diffusely distributed in LV hypertrophy [30]. In the present case, there was no pre or post mortal evidence of dilated cardiomyopathy, and the generalized concentric hypertrophy of the RV was attributable to the PS. While early manifestation of HCM could not be definitively ruled out in this patient, this disease entity is very rare in the dog and our echocardiographic findings were not characteristic for HCM.
Anomalies of the tricuspid valve in humans include tricuspid stenosis, Ebstein’s anomaly, tricuspid valve dysplasia, and double orifice tricuspid valve (DOTV). The latter is a rare congenital cardiac anomaly with three described variants: the “commissural” (the accessory ostium lying within the commissure); the central or “bridge type” (a fibrous bridge dividing the orifice into two ostia), and the “hole” (the accessory ostium lying within a leaflet) [12].The hole type should be distinguished from a simple fenestration or cleft which has no subvalvular apparatus. Usually DOTV is considered as benign and its pathophysiology is determined by concomitant lesions. Most cases are diagnosed incidentally during open-heart surgery or autopsy and it usually coexists with concomitant cardiac anomalies. The occurrence of DOTV is extremely rare and difficult to diagnose by echocardiography; therefore, the condition can be easily overlooked [12,13,14, 31, 32]. The identification of the accessory orifice in the septal leaflet of the tricuspid valve in the present case is compatible with the “hole” variant anomaly described in humans, reflecting the first confirmation of this pathology in a canine patient.
In conclusion, this is the first description of LVNC in a dog, supporting the introduction of ventricular myocardial noncompaction as a differential diagnosis for canine cardiomyopathies
