Morphological variations of the interatrial septum and potential implications in equine cardiology

Abstract

The interatrial septum morphology, shaped by the septum primum and secundum fusion, results in the formation of the fossa ovalis (FO) and its limbus. Incomplete fusion can lead to a patent foramen ovale (PFO), while complete fusion may produce septal ridges and pouches (SPs), with SPs in humans linked to ischemic stroke and atrial arrhythmias. In horses, atrial tachycardia and fibrillation often originate near the FO. This study examines adult equine interatrial septum morphology to enhance understanding the region and guide electrophysiological interventions for equine cardiac arrhythmias. Post-mortem examinations of 62 adult equine hearts, assessed the interatrial septum morphology from both right and left sides, measuring the dimensions of the FO and the craniocaudal length, and dorsoventral height of the SPs. Histological analysis at selected septal locations evaluated the wall's thickness and composition. Significant morphological variations were observed, particularly the consistent presence of right-sided SP. The septum wall comprises three layers, with the central layer containing cardiomyocytes in varied orientations, interspersed with fibroadipose tissue, features potentially contributing to atrial arrhythmias. Understanding the equine interatrial septum morphology is important for optimizing transseptal puncture outcomes, by facilitating accurate intracardiac echocardiography interpretation, guiding precise puncture site selection and improving procedural safety and efficacy.

Keywords: Arrhythmia; Fossa ovalis; Horse; Ridge; Septal pouch; Transeptal puncture.

Fig. 1

Right atrial (RA) landmarks after lateral opening of the sinus venarum cavarum (facies atrialis) (A), right is cranial and top is dorsal. The locations of sample collection for histological evaluation are indicated with three dashed lines annotated as 1, 2 and 3 each corresponding to a specific level: level 1 (1) was located 1 cm caudal to the limbus, level 2 (2) was positioned at the entrance of the right-sided septal pouch (RSP), and level 3 (3) was taken at the RSP. B: Measurements of the fossa ovalis (FO) and RSP are shown. The FO craniocaudal length (white double-headed arrow) and dorsoventral height (black double-headed arrow) were measured caudally to the limbus. The RSP craniocaudal length (yellow double-headed arrow) and dorsoventral height (orange double-headed arrow) were also measured. Right is cranial and top is dorsal. C: After a cut on the craniocaudal axis, the FO and the RSP, covered by the limbus (cross-sectioned), are shown. Right is cranial and top is right. The length of the RSP is indicated by the yellow double-headed arrow. CaVC caudal vena cava, CrVC cranial vena cava, CS coronary sinus opening, CT crista terminalis, RA right atrium, RV right ventricle, TIV tuberculum intervenosum, TV tricuspid valve.

Fig. 2

A left-sided view on the interatrial septum shows macroscopic variations between horses. (A) Smooth endocardial surface, seen in the majority of horses; (B) uneven surface; (C) left-sided septal pouch, indicated with a scalpel holder inside it; and (D) a septal ridge, indicated by the white arrows. Right is caudal and top is dorsal. PV III, ostium III of the pulmonary veins.

Fig. 3

Schematic overview of the interatrial septum in the heart. (A) General illustration of the interatrial septum formed by the fusion of the embryonic septum primum and secundum. (B–I) Different morphological presentations of the interatrial septum and their comparative prevalence among species: equine (Eq), human (Hu), porcine (Por), and ovine (Ov). (B) Smooth septum on both the right and left sides; (C) patent foramen ovale (PFO); (D) single left-sided septal pouch (LSP); (E) single right-sided septal pouch (RSP), the most common presentation in horses; (F) double septal pouch (DSP); (G) Double sided septal pouch with the presence of a left-sided septal ridge (LSR); (H) right-sided septal pouch coexisting with a left-sided septal ridge; (I) left-sided septal ridge. LA, left atrium; RA, right atrium. Adapted from Holda et al., 2018^,.

Fig. 4

Histological sections of the interatrial septum using Masson’s trichrome staining at levels 1 and 2, as shown in Fig. 1A. Right is dorsal, and top is towards the right atrium. (A) Level 1, located 1 cm caudal to the limbus, illustrates the layered structure of the interatrial septum, featuring two subendocardial fibrous layers (yellow double arrows), with a myocardial layer (black double arrow) between them. (B) Level 2, positioned at the entrance of the right-sided septal pouch, exhibits a similar structural organization, with clearly defined fibrous (yellow double arrows) and myocardial (black double arrow) layers. In (A) and (B), the black boxes indicate the area for (C) and (D), respectively. (C,D) Magnified view of the myocardial layer at levels 1 and 2, revealing an undulating (wave-like) arrangement of myocardial fibers. In (C) and (D), the black boxes indicate the area for (E) and (F), respectively. (E–F) A detailed view of the myocardial fibers at Level 1 and Level 2 is shown in longitudinal cut (l) (showing transverse orientation), cross-section (c) (with fibers oriented in a craniocaudal direction), and oblique cut (o) (with fibers oriented obliquely within the interatrial septum). Adipose tissue (a) was observed interspersed between the cells in level 1. LA, left atrium; RA, right atrium.

Fig. 5

Histological sections of the interatrial septum using Masson’s trichrome staining at level 3, as shown in Fig. 1A. The right side is dorsal, and the top is oriented towards the right atrium. (A,B) Level 3, located at the right-sided septal pouch (RSP), shows the RSP in a cross section bordered by the limbus and interatrial septum. (A) Distinct undulating pattern of myocardial tissue is observed. The black box indicates the area magnified in (C). (B) A left-sided septal ridge is present (yellow arrows), with the black box indicating the area magnified in (D). (C) Magnified view of the myocardial layer from (A) showing a significant amount of adipose tissue (a). (D) A close-up of the left-sided septal ridge reveals a large amount of adipose tissue around and between the myocardial fibers. In (C) and (D), the black boxes indicate the area for (E) and (F), respectively. (E) A detailed view of the myocardial fibers in (C) shows them in cross-section (c), oriented in the craniocaudal direction, which is the most common orientation. (F) A detailed view of the myocardial fibers from (D) highlights the intertwining of fibers in cross-section (c) (craniocaudal direction) and fibers in oblique cut (o) (oblique orientation within the interatrial septum). An abundance of adipose tissue was also observed. LA, left atrium.