Introduction

A 6-week-old 252-g (0.56-lb) sexually intact male Netherland Dwarf rabbit was evaluated on an emergency basis because of sudden collapse. Earlier in the morning, the owners had found the rabbit lethargic and disoriented, although it was ambulatory and showed interest in food and water. After a period without observation during the daytime hours, the rabbit was found laterally recumbent and unresponsive but nonsubmerged in a shallow water bowl. The rabbit apparently regained consciousness and was transported to the clinic; during the car ride, it returned to normal mentation, as reported by the owners. The pet had been part of a litter of 3 rabbits; the other 2 rabbits died within 4 hours after birth. Husbandry included twice-daily feeding of a pelleted commercial rabbit food and free-choice timothy hay. Water was available ad libitum. The rabbit was cohoused with a doe, and no medications or supplements had been administered to either rabbit.

On examination, the rabbit was nonresponsive. While the rabbit was moved to a treatment area, it regained consciousness and righted itself, with a return to apparently normal mentation over a period of approximately 15 to 30 seconds. Auscultation revealed an arrhythmia with intermittent dropped beats and an underlying rate of 300 beats/min; physical examination findings were otherwise unremarkable. Three-lead ECG^a (Figure 1) was performed.

Portions of a lead II ECG recording obtained from a 6-week-old 252-g (0.56-lb) Netherland Dwarf rabbit that was unrestrained in sternal recumbency for 3-lead, surface-level ECG. Evaluation was performed on an emergency basis because of the rabbit's multiple episodes of syncope while at rest. Physical examination revealed an arrhythmia consisting of intermittent dropped beats with a heart rate of 300 beats/min. The ECG tracings indicate a calculated rate of 300 beats/min and an initial arrhythmia characterized as a right bundle branch block with a 1:1, normal-to-abnormal (bigeminal) conduction pattern (A and B). Paroxysmal advanced second-degree block, consisting of multiple pauses during which normal P waves are visible without corresponding QRS complexes, is present (C). The tracing terminates during a period of ventricular asystole when the rabbit became syncopal (D). Tracings in all panels (A through D) have been enhanced for visibility (marked EN). Paper speed = 25 mm/s; 2 cm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 258, 11; 10.2460/javma.258.11.1189

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Portions of a lead II ECG recording obtained from a 6-week-old 252-g (0.56-lb) Netherland Dwarf rabbit that was unrestrained in sternal recumbency for 3-lead, surface-level ECG. Evaluation was performed on an emergency basis because of the rabbit's multiple episodes of syncope while at rest. Physical examination revealed an arrhythmia consisting of intermittent dropped beats with a heart rate of 300 beats/min. The ECG tracings indicate a calculated rate of 300 beats/min and an initial arrhythmia characterized as a right bundle branch block with a 1:1, normal-to-abnormal (bigeminal) conduction pattern (A and B). Paroxysmal advanced second-degree block, consisting of multiple pauses during which normal P waves are visible without corresponding QRS complexes, is present (C). The tracing terminates during a period of ventricular asystole when the rabbit became syncopal (D). Tracings in all panels (A through D) have been enhanced for visibility (marked EN). Paper speed = 25 mm/s; 2 cm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 258, 11; 10.2460/javma.258.11.1189

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Portions of a lead II ECG recording obtained from a 6-week-old 252-g (0.56-lb) Netherland Dwarf rabbit that was unrestrained in sternal recumbency for 3-lead, surface-level ECG. Evaluation was performed on an emergency basis because of the rabbit's multiple episodes of syncope while at rest. Physical examination revealed an arrhythmia consisting of intermittent dropped beats with a heart rate of 300 beats/min. The ECG tracings indicate a calculated rate of 300 beats/min and an initial arrhythmia characterized as a right bundle branch block with a 1:1, normal-to-abnormal (bigeminal) conduction pattern (A and B). Paroxysmal advanced second-degree block, consisting of multiple pauses during which normal P waves are visible without corresponding QRS complexes, is present (C). The tracing terminates during a period of ventricular asystole when the rabbit became syncopal (D). Tracings in all panels (A through D) have been enhanced for visibility (marked EN). Paper speed = 25 mm/s; 2 cm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 258, 11; 10.2460/javma.258.11.1189

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ECG Interpretation

Three-lead ECG^a (Figure 1) was performed with the rabbit unrestrained in sternal recumbency. The ECG findings were consistent with a sinus rhythm and a heart rate of 300 beats/min, conducted with a right bundle branch block. The block occurred with a bigeminal pattern, represented by a 1:1 pattern of normal to abnormal complexes. The P-P and R-R intervals were regular throughout this period. Mean electrical axis during this period was not systematically assessed because of a lack of standard positioning; however, the complexes with bundle branch block morphology were shifted in axis relative to the normal complexes, such that the amplitude of negative deflection of the ECG trace in the region of the QRS complex in lead II was reduced. The bundle branch block was punctuated by multiple 0.3- to 0.5-second pauses during which multiple P waves were visible without corresponding ventricular activity. This represented paroxysmal, advanced second-degree atrioventricular (AV) block with a 2:1 or 3:1 conduction ratio. Ventricular asystole ensued and continued to the end of the recording, with P waves appearing at a rate of 300 beats/min and absent QRS complexes. At this point, the rabbit spontaneously collapsed into lateral recumbency and the examination was terminated in anticipation of a resuscitation attempt. The rabbit, however, recovered without intervention.

Thereafter, a CBC, serum biochemical analysis, and point-of-care electrolyte panel^b (including assessments of free magnesium and free calcium concentrations) were performed. Clinicopathologic abnormalities detected included mildly high alanine aminotransferase activity (100 U/L; external source reference interval,¹ 14 to 80 U/L) and mild hypokalemia (serum biochemical analysis, 1.5 mmol/L; point-of-care electrolyte panel, 1.9 mmol/L [external-source reference interval,¹ 3.5 to 7.0 mmol/L, applied for both serum potassium concentrations]). The intention was to measure the rabbit's circulating cardiac troponin I concentration, but this assessment was not performed because of the proportionally large volume of blood required for the testing, relative to the estimated total blood volume of the patient. Fluids (volume not recorded) and B-complex vitamins were both administered SC, and the rabbit was hospitalized with supportive care overnight and evaluated the following morning by a board-certified veterinary cardiologist (JDT) and a zoological medicine specialist (JWC). Echocardiography was not performed owing to financial constraints.

During hospitalization, signs of gastrointestinal stasis developed and the rabbit was treated with 12 mL of lactated Ringer solution SC and 0.1 mL of B-complex vitamins^c SC and provided with small-volume syringe feedings of a rabbit critical care assist feeding formula.^d A 3-lead, recheck ECG revealed normal sinus rhythm.^e The rabbit was discharged from the hospital, and the owners were instructed to administer albuterol syrup^f (0.03 mg/kg [0.01 mg/lb]) PO every 12 hours and a potassium-containing oral gel formulation^g (potassium gluconate, 0.8 mEq/mL) at a dosage of 1.4 mL, PO, every 12 hours for 14 days. Fecal production resumed shortly after hospital discharge.

At a recheck examination 1 month later, there had been no further episodes of collapse, and the rabbit had generally increased energy and playfulness, as reported by the owners. Recheck 6-lead ECG^e was performed (Figure 2); the findings were unremarkable, with normal sinus rhythm and a rate of 300 beats/min. The owners were instructed to administer albuterol syrup (0.03 mg/kg, PO, q 12 h for 7 days, tapering to q 24 h for the following 7 days) to the rabbit at home; if the rabbit had no episodes of collapse, albuterol treatment was to be discontinued. If medical treatment failed, the option of exogenous pacing was to be discussed. Two or 3 transient, self-limiting episodes of lethargy without collapse were observed during the treatment period by the owners. At 3 months after diagnosis of paroxysmal second-degree AV block, the rabbit continued to do well after having been weaned completely from albuterol treatment at 2 weeks after the recheck examination.

Six-lead diagnostic surface-level ECG recording obtained from the rabbit described in Figure 1 at the 1-month recheck examination. All previously identified ECG abnormalities are resolved, and a sinus rhythm with a calculated rate of 300 beats/min is seen throughout the recording. Paper speed = 50 mm/s; 2 cm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 258, 11; 10.2460/javma.258.11.1189

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Six-lead diagnostic surface-level ECG recording obtained from the rabbit described in Figure 1 at the 1-month recheck examination. All previously identified ECG abnormalities are resolved, and a sinus rhythm with a calculated rate of 300 beats/min is seen throughout the recording. Paper speed = 50 mm/s; 2 cm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 258, 11; 10.2460/javma.258.11.1189

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Six-lead diagnostic surface-level ECG recording obtained from the rabbit described in Figure 1 at the 1-month recheck examination. All previously identified ECG abnormalities are resolved, and a sinus rhythm with a calculated rate of 300 beats/min is seen throughout the recording. Paper speed = 50 mm/s; 2 cm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 258, 11; 10.2460/javma.258.11.1189

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Discussion

Descriptions of ECG characteristics in rabbits are limited in the veterinary medical literature, possibly because of the challenging nature of identifying leporine patients with rhythm disturbances and interpreting rapid, low-voltage cardiac activity of animals positioned in nonstandard recumbency.^2,3,4,5 In ECG recordings obtained from healthy rabbits, the sinus rate is typically 190 to 320 beats/min, ST intervals are prolonged (compared with findings for carnivores), and T waves are peaked. The latter 2 findings have been presumptively attributed to the high-potassium and low-sodium content of rabbits’ diets.⁶ Data regarding ECG variables in a population of 46 healthy pet rabbits have been made available as well as recommendations for standardized ECG assessment.⁷

For interpretation of arrhythmias in rabbits, it is often recommended that practitioners refer to principles applied to larger mammals.^4,5 Specific arrhythmias identified in rabbits include atrial fibrillation and ventricular premature complexes, both occurring concurrently with congestive heart failure secondary to cardiomyopathies or valvular disease, and there are anecdotal reports^2,3 of syncope attributable to uncharacterized arrhythmias. The case described in the present report represented the first documented example of one of these syncopal arrhythmias in a rabbit and has suggested possible treatment.

Second-degree AV block can be subclassified as Mobitz type I or II block, 2:1 block, or advanced block.⁸ For the rabbit of the present report, multiple P waves were blocked in succession, indicative of either advanced second-degree AV block or intermittent third-degree AV block. A necessary feature in the diagnosis of third-degree AV block is AV dissociation, wherein atrial depolarization occurs at a rate different from that of the ventricles, the latter of which are driven independently by automaticity of the subatrial tissues. A ventricular escape rhythm was not identified in the rabbit, despite what appeared to be a sufficiently long pause. Ventricular escape rhythms in electrophysiological studies of laboratory rabbits have been identified at a rate of 75 beats/min in a live animal and a mean ± SEM rate of 51.5 ± 10.7 beats/min in isolated, perfused (Langendorff technique) rabbit hearts; however, the rate of ventricular escape rhythms varies according to anatomic origin.^9,10,11 At the termination of the recording for the rabbit of the present report, ventricular asystole ensued without evidence of an escape rhythm.

The bundle branch block QRS complex morphology in the rabbit of the present report suggested an initial infra-Hisian location of the block, with migration of the focus to a more proximal location during paroxysms of advanced AV block. Bundle branch blocks occur distal to the bifurcation of the bundle of His (ie, infra-Hisian block location), whereas general AV block locations are described as nodal (supra-Hisian), Hisian, or infra-Hisian, and those blocks originate at the AV node, within the bundle of His, or within the bundle branches, respectively.⁸ For the case described in the present report, an intermittent shift in the anatomic focus of the block from the right bundle branch to multiple infra-Hisian locations or a Hisian focus was likely, given the complete lack of ventricular depolarization despite continuing P waves during the observed pauses. Owing to the unaltered rate, refractoriness of the ventricular myocardium was not considered an adequate explanation for the lack of ventricular activity during the paroxysms.

Because transient insults or immaturity of the conduction system was suspected, a tapering course of medical treatment for the rabbit of the present report was recommended. Paroxysmal AV block is most often treated by temporary or permanent extrinsic pacing, although positive chronotropic agents—most commonly atropine, a muscarinic receptor antagonist and parasympatholytic drug—have been effective in the short-term management of some cases.¹² The relatively common occurrence of functional gastrointestinal ileus among hospitalized leporine patients is a strong contraindication for administration of atropine because worsening of this condition by the drug's parasympatholytic effect can prove fatal.³ Dopamine, epinephrine, norepinephrine, and isoproterenol have been effective when administered to dogs with experimentally induced chronic AV block and have been used (albeit rarely) as alternative treatments in human cases.^{13,14,15,16,17,18} For the rabbit of the present report, albuterol was selected for long-term management because of its duration of action and availability as an oral preparation. Albuterol is a selective β₂-adrenoceptor agonist that has weak positive inotropic and chronotropic effects through direct stimulation of cardiac β₂-adrenoceptors and indirect vagal withdrawal and baroreceptor activation through nitric oxide-mediated vasodilation.^19,20 Albuterol was considered a lower-risk treatment option for a patient that already had gastrointestinal stasis and proved benign with regard to resumed gastrointestinal motility. In research settings, internal pacing has been accomplished with implanted electrical stimulators in live rabbits, and brief optical pacing has been accomplished in isolated hearts of rabbits.^21,22,23 Pacemaker use in clinical leporine patients has not been documented to the authors’ knowledge.

On the basis of the case described in the present report, paroxysmal second-degree AV block may be the cause of arrhythmic syncope in rabbits and may be successfully managed with oral administration of albuterol. For the rabbit of the present report, the underlying disorder was not definitively located. Limiting factors in interpretation of this case included the lack of echocardiographic data or assessment of circulating cardiac troponin I concentration as well as the lack of 6-lead diagnostic ECG data collected at the time of emergent presentation.