Short QT intervals in African lions

Abstract

The cardiac conduction system in large carnivores, such as the African lion (Panthera leo), represents a significant knowledge gap in both veterinary science and in cardiac electrophysiology. Short QT intervals have been reported from zoo-kept, anaesthetized lions, and our goal was to record the first ECGs from wild, conscious lions roaming freely, and compare them to zoo-kept lions under the hypothesis that short QT is unique to zoo-kept lions. Macroscopic and histological examinations were performed on heart tissue removed from nine healthy zoo lions. ECGs were recorded from the nine anaesthetized zoo-kept lions, and from 15 anaesthetized and conscious wild lions in Africa. Our histological and topographical description of the lion's heart matched what has previously been published. In conscious lions, the ECG recordings revealed a mean heart rate of 70 ± 4 beats/min, with faster heart rates during the night. PQ and QT intervals were heart rate dependent in the conscious lions. Interestingly, QT intervals recorded in wild lions were markedly longer than QT intervals from zoo lions (398 ± 40 vs. 297 ± 9 ms, respectively; P < 0.0001). Anaesthesia or heart rate did not account for this difference. We provide a comprehensive description of the cardiac anatomy and electrophysiology of wild and zoo-kept lions. QT intervals were significantly shorter in zoo lions, suggesting functional disparities in cardiac electrophysiology between wild and zoo-kept lions, potentially related to physical fitness. These findings underscore the plasticity of cardiac electrophysiology and may be of value when reintroducing endangered species into the wild and when managing lions in human care.

Keywords: Panthera leo; Purkinje; QT; circadian; feline; predator.

FIGURE 1

The lion heart. (a) A caudal view of the lion's heart. The left ventricle (LV), left auricle (LA), the right ventricular outflow tract (RVOT) and the aorta are indicated. Scale bar 1 cm. (b) Facies auricularis, a lateral view of the heart surface marking the tips of the auticulae atriorum, facing the left thoracic wall of the animal. Abbreviations as in (a); RV, right ventricle. Scale bar 1 cm. (c) An oblique basal view showing the cranial caval vein (V.c.cr) and the caudal caval vein (V.c.cau). The black square indicates the section where the sinoatrial node is located. Scale bar 1 cm. (d) The right atrium opened by an incision through the caval veins and the right ventricle by an incision following the septal wall. The triscupidal valve (TV) separates the right atrium and ventricle. The triangle of Koch is indicated by a black triangle. The atrioventricular node is located at the base of the triangle and the bundle of His toward the pointy end. The sinus‐node area is indicated by the black box. Scale bar 1 cm. (e) The left ventricle opened up by two insicions parallel to the septal wall. The mitral valve (MV) marks the transition from the left atrium to ventricle. A network of free‐running Purkinje strands or fibres (PF) is visible within the left ventricle. Scale bar 1 cm.

FIGURE 2

The sinoatrial node and RR intervals during a 24‐h cycle. (a) The sinoatrial node (SAN) is found sub‐epicardially (Epi) under the terminal crest (CT). Endo, endocardium. (b) A section corresponding to the white rectangle in (a), showing a branch of the central sinoatrial node artery (SNA) surrounded by extracellular matrix and islets of SAN cells and nerve fibres (N). (c) A section corresponding to the white rectangle in (b), showing pale, round pacemaker cells (P) as well as short, branching and striated transitional cells (T). (d) RR intervals during a 24‐h cycle from the ECG loggers placed in the freely roaming lions in Kgalagadi Transfrontier Park (n = 12). The red line illustrates the cosinor fit to the data. Error bars indicate the standard deviation. The dark period (18.30 h to 06.00 h) is indicated in grey.

FIGURE 3

Atrioventricular node and PQ intervals. (a) The fibrous body is continuous with the mitral valve (MV) and the triscupidal valve (TV) and separates the atria from the ventricles. A. Septum, atrial septum; V. septum, ventricular septum. (b) A section corresponding to the black rectangle in (a), showing the penetrating bundle of His. (c) Enlargement of the area indicated by the rectangle in (b), showing Purkinje fibres (PF), nerves (N) and capillaries (C). (d) The PQ interval as a function of the RR interval (black symbols) from the ECG loggers placed in the freely roaming lions in Kgalagadi Transfrontier Park (n = 12). For comparison, the PQ interval as function of the RR interval from the individual anaesthetized zoo lions is plotted in red. Error bars indicate the standard deviation.

FIGURE 4

The left ventricle. (a) Transmural section of a lion left ventricle. On the epicardium (Epi), fat cells and several arteries can be observed. Endo, endocardium. (b) Network of free‐running Purkinje fibre strands comparable to the indicated structures in Figure 1e. (c) Zoomed‐in section of the free‐running Purkinje fibre network. (d) Endocardial section corresponding to box D in (a) Purkinje fibres (PF) are found sub‐endocardially surrounded by collagen and thin elastic fibres. CM, cardiomyocytes. (e) A midmyocardial section corresponding to box E in (a). The collagenous streaks are associated with vasculature, not with Purkinje fibres. A indicates an artery. (f) QT interval as a function of RR intervals (black symbols) from the ECG loggers placed in the freely roaming lions in Kgalagadi Transfrontier Park (n = 12). For comparison, the QT interval as function of the RR interval from the individual anaesthetized zoo lions is plotted in red. Error bars indicate the standard deviation.

FIGURE 5

Shorter QT interval in the zoo‐kept lions. (a) Exemplar 7.5‐s ECG trace from a conscious, wild lion. The heart rate is 58 beats/min and the QT interval is 412 ms in this example. (b) PQ intervals from wild lions during conscious circumstances and during anaesthesia at matched heart rates (open circles, n = 12; Student's paired t‐test). For comparison, PQ intervals from the anaesthetized lions bred and housed in captivity is illustrated (red inverted triangles, n = 9; same data are illustrated in Figure 3d; Student's unpaired t‐test). No statistically significant differences were identified. (c) QT intervals from wild lions during conscious circumstances and during anaesthesia at matched heart rates (open circles, n = 12; P‐value from Student's paired t‐test). For comparison, QT intervals from the anaesthetized zoo‐kept lions in Denmark are illustrated (red inverted triangles, n = 9; same data are illustrated in Figure 4f; P‐value from Student's unpaired t‐test).

FIGURE 6

Electrical activity in the lion heart. (a) Position of electrodes in the Einthoven configuration. The vectors are directed from the negative electrode (right front limb) to the positive electrode (left front and left hind limb). A ground electrode (not shown) was placed on the right hind limb. (b) Position of electrodes in the orthogonal configuration. The vectors are directed from the negative electrode to the positive electrode. (c) Electrocardiogram obtained in the Einthoven configuration; 25 mm/s recording speed, 1 mV/cm amplitude. (d) 2D vector loops of the entire 7‐s recording shown in (c). Lead aVF (vertical) is plotted against lead I (horizontal); 0.5 mV/cm. (e) Electrocardiogram obtained in the 3D orthogonal configuration. (f) 3D vector loops based on ECG complexes recorded in the orthogonal configuration. The mean electrical axis is shown as a red arrow. The elevation, which is the angle between the mean electrical axis and the Z‐axis running in a ventral‐to‐dorsal direction, is indicated by Θ. The azimuth is the angle between the X‐axis and the projection of the mean electrical axis on the horizontal plane (grey arrow). For simplification, the angle indicated by Φ in the figure is between the Y‐axis and the projection, so the azimuth is 90 − Φ. (g) Projections of the mean electrical axis on the XY, YZ and XZ planes from all nine lions. All axes are 4 mV long and all vectors originate at (0, 0). The lion in Panel A and B was generated using publicly available deep‐learning algorithms that generate pictures.

FIGURE 7

Early repolarization notch. Enlarged ECG trace from a lead II in an anaesthetized zoo lion. Electrical noise is removed from the signal by aligning complexes to the peak of the R wave and generating an averaged signal from 10–20 beats (Speerschneider & Thomsen, 2013). Note the prominent J wave (arrow) representing early repolarization of the ventricular myocytes and the short QT interval (330 ms). Additionally, P, Q, R and T waves are indicated on the trace.