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Hillary K. Hammond Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO

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Marisa K. Ames Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO

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Kursten V. Pierce Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO

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Gretel Tovar Lopez Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO

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Matthew S. Johnston Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO

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Introduction

A 26-year-old 290-g female Timneh African grey parrot (Psittacus timneh) was presented to the Colorado State University Veterinary Teaching Hospital for CT as part of radiation planning for treatment of a right periocular mass, suspected to be a squamous cell carcinoma.

On initial evaluation, the bird was bright, alert, and responsive and had a body condition score of 2/9. On physical examination, there was severe periocular swelling around the right eye causing the palpebral fissure to be held shut. Thoracic auscultation was performed with a neonatal stethoscope with the diaphragm placed directly over the keel of the sternum at the level of the heart and revealed normal heart sounds and an irregular heart rhythm with a rate of 450 beats/min. Heart rate was determined by counting heartbeats over a 6-second period and multiplying that number by 10. Prior to anesthesia, further diagnostic testing was pursued, including radiography, ECG, and echocardiography. Whole-body radiography revealed hepatomegaly with a normal cardiac silhouette. Echocardiography (2-D and Doppler) performed from a ventromedian approach revealed that cardiac structure and function were within reference limits for African grey parrots.1 Electrocardiography was performed by placing the bird in dorsal recumbency and attaching alligator-clip ECG leads to the bases of both wings and the interdigital spaces of both hind limbs (Supplementary Figure S1).

ECG Interpretation

A 6-lead ECG obtained from the bird revealed an underlying sinus tachycardia with a heart rate of 600 beats/min (Figure 1). The lead II tracing was used for analysis, and ECG measurements were compared with reported reference values for African grey parrots.2 Because of the typically rapid heart rates of birds, paper speed should ideally be at least 100 mm/s to evaluate waveforms accurately and precisely.3 However, because of limitations of the ECG machine that was available, the maximum paper speed was 50 mm/s, meaning that measurements obtained from this bird were less precise, compared with reported reference values.

Figure 1
Figure 1

ECG recordings from a 26-year-old Timneh African grey parrot that was evaluated prior to undergoing CT for radiation planning; an arrhythmia was auscultated during the preanesthetic evaluation. A—Initial 6-lead ECG recording. Sinus tachycardia with an average heart rate of 600 beats/min is present. Notice that so-called long-short R-R cycles are followed by complexes with a different mean electrical axis (arrows). These complexes are preceded by a P wave with an electrical axis and PQ interval consistent with those of preceding complexes, suggesting an Ashman-like phenomenon. In addition, P waves are superimposed on the preceding T waves during periods of the sinus rhythm, consistent with a P-on-T phenomenon previously detected in African grey parrots. Small deflections after the T waves within the long R-R cycle are likely U waves (u). B—Intermittently, the P-P interval slows slightly (brackets) prior to a long R-R interval, which is presumed to be due to sinus arrest. Paper speed = 50 mm/s; 10 mm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 260, 10; 10.2460/javma.20.11.0651

During periods of sinus tachycardia (Figure 1), waveform features were as follows: P-wave duration, 0.02 seconds (reference range, 0.012 to 0.018 seconds); P-wave amplitude, 0.20 to 0.30 mV (reference range, 0.25 to 0.55 mV); PQ-interval duration, 0.040 seconds (reference range, 0.040 to 0.055 seconds); QRS-complex duration, approximately 0.018 seconds (reference range, 0.010 to 0.016 seconds); R-wave amplitude, 0.2 mV (reference range, 0.0 to 0.2 mV); S-wave amplitude, 1.0 mV (reference range, 0.90 to 2.20 mV); QT-interval duration, 0.08 seconds (reference range, 0.048 to 0.070 seconds); and T-wave amplitude, 0.3 mV (reference range, 0.18 to 0.60 mV). The P waves were superimposed on the preceding T waves during periods of sinus rhythm, consistent with a P-on-T phenomenon previously detected in African grey parrots.2 The mean heart rate during sinus rhythm was 600 beats/min. The mean electrical axis was –68° (reference range, –79° to –103°).2,3

The sinus rate was relatively stable with intermittent slight slowing prior to pauses. Pause durations were not multiples of preceding P-P intervals, making sinus arrest more likely than sinoatrial node exit block.4 Also, no P waves were seen prior to the pauses, making second-degree atrioventricular block less likely. During pauses, low-amplitude deflections after T waves likely represented U waves.5 The sinus arrest created a long-short R-R cycle during which a long R-R interval (0.18 seconds) was followed by a short R-R interval (0.10 seconds). Complexes following the short R-R interval had P waves with an inferior axis, PQ intervals of 0.04 seconds, and narrow QRS complexes (duration, approx 0.018 seconds) with a left-shifted mean electrical axis of +77°, consistent with aberrantly conducted sinus-origin beats. A single premature complex with a different morphology was also present after a similar long-short R-R cycle (Figure 2); however, the QRS complex was wide and bizarre (QRS duration, 0.04 seconds; QRS-T duration, 0.08 seconds), and a P wave could not be distinguished from the preceding T wave, suggesting the origin was ventricular rather than supraventricular.

Figure 2
Figure 2

Lead II ECG recording from the bird in Figure 1. A similar rhythm as shown in Figure 1 is seen, except a single premature complex (asterisk) with a different morphology is present with a similar long-short R-R cycle. However, the QRS complex is premature, wide, and bizarre (QRS duration, 0.04 seconds; QRS-T duration, 0.08 seconds), and there is not an obvious P wave in the preceding T wave, suggesting the origin was ventricular. Paper speed = 50 mm/s; 10 mm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 260, 10; 10.2460/javma.20.11.0651

No treatment was recommended at the time, but the patient was premedicated 1 week later with glycopyrrolate (0.01 mg/kg, IM), midazolam (1.0 mg/kg, IM), and butorphanol (2.0 mg/kg, IM) prior to induction of general anesthesia with isoflurane. A 6-lead ECG was obtained while the bird was under general anesthesia (Figure 3) and revealed an underlying sinus tachycardia with an average heart rate of 600 beats/min. The previously noted sinus arrest, rate-dependent aberrancy, and ventricular premature complexes were not seen.

Figure 3
Figure 3

Six-lead ECG recording obtained from the bird in Figure 1 during a recheck examination 1 week later; the recording was obtained after the bird was premedicated with glycopyrrolate, midazolam, and butorphanol and anesthetized with isoflurane. There is sinus tachycardia with an average heart rate of 600 beats/min. The previously noted sinus arrest, rate-dependent aberrancy, and ventricular premature complexes are not seen. Paper speed = 50 mm/s; 10 mm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 260, 10; 10.2460/javma.20.11.0651

Discussion

The arrhythmia seen in this bird was suspected to represent underlying sinus tachycardia with sinus arrest, intermittent Ashman-like aberrant conduction, and rare ventricular premature contractions. Aberrant conduction is defined as abnormal intraventricular conduction of a supraventricular impulse as a result of a functional block in one of the branches of the conduction pathways, early impulse formation, or a change in the duration of the preceding R-R interval.68

Two forms of rate-dependent aberrant conduction are recognized and are distinguished by the phase of the disrupted action potential that results in aberrant intraventricular conduction. Phase 4 aberrant conduction (phase 4 block or bradycardia-dependent block) occurs during long diastolic intervals or long cycle lengths that allow progressive depolarization of the membrane and a more positive (ie, less negative) resting membrane potential. This leads to a decrease in the number of available sodium channels, resulting in a decrease in the rate of rise during phase 0 of the action potential. Therefore, the membrane potential is not sufficient to reach the threshold potential needed to propagate an electrical impulse, resulting in partially depolarized cells and an aberrantly conducted electrical current.6,9 Phase 3 aberrant conduction (phase 3 block or tachycardia-dependent block) occurs when a premature stimulus arrives at tissues that are still refractory. The premature impulse arrives during phase 3 of the action potential, when a portion of the sodium channels remains refractory and the membrane potential is still reduced, resulting in slowed conduction due to incomplete repolarization.9 The latter mechanism was the most likely cause of aberrant conduction in the bird of the present report.

A specific type of tachycardia-dependent aberrancy is the Ashman phenomenon, which refers to aberrant conduction occurring when a short cycle follows a long cycle. The R-R interval preceding a QRS complex directly affects the refractory period of conducting tissues, such that a long R-R interval results in a prolonged refractory period of the bundle branch fibers and a short R-R interval results in a shortened refractory period. When an impulse with a short R-R interval reaches the Purkinje fibers, the fibers are more likely to be in phase 3 of the preceding action potential, resulting in the beat being conducted aberrantly.7,9,10 Although the traditional Ashman phenomenon was described as occurring during atrial fibrillation, the long-short cycles and bizarre QRS complexes with consistent P waves were suggestive of an Ashman-like phenomenon in this bird.

Aberrant intraventricular conduction can be distinguished from ventricular ectopic complexes by examining the coupling interval of the QRS complex and the previous beat, the presence or absence of a pause after the QRS complex, the morphology of the QRS complex, and the tendency of wide QRS complexes to form groups. Ventricular ectopic complexes typically have a fixed coupling interval, whereas supraventricular complexes with aberrant intraventricular conduction have variable coupling intervals. Aberrant intraventricular conduction complexes may be rate dependent and typically are not followed by a pause. Ventricular ectopic beats tend to organize in couplets, triplets, or bigeminy, whereas complexes resulting from aberrant conduction typically do not organize in clusters.8,10,11 In the initial ECG recording for this bird, complexes following long-short R-R cycles were most consistent with aberrant intraventricular conduction. Differential diagnoses for the intermittent premature complexes that were seen include a more aberrantly conducted complex versus a premature ventricular complex. Causes of ventricular ectopy in birds include hypokalemia, thiamine deficiency, vitamin E deficiency, Newcastle disease, avian influenza infection, myocardial infarction due to lead poisoning, atherosclerosis, and digoxin toxicosis. In this bird, given the presence of neoplasia, a paraneoplastic cause could not be ruled out completely.2

In the bird of this report, no definitive cause of the arrhythmia was identified. No antiarrhythmic therapy was instituted because the arrhythmia did not appear to be hemodynamically important. The patient continued to receive radiation under general anesthesia, and no complications were reported.

Supplementary Material

Supplementary materials are posted online at the journal website: avmajournals.avma.org

References

  • 1.

    Pees M, Straub J, Krautwald-Junghanns ME. Echocardiographic examinations of 60 African grey parrots and 30 other psittacine birds. Vet Rec. 2004;155(3):7376.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Nap AMP, Lumeij JT, Stokhof AA. Electrocardiogram of the African grey (Psittacus erithacus) and Amazon (Amazona spp) parrot. Avian Pathol. 1992;21(1):4553.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Lumeij JT, Ritchie BW. Cardiology. In: Ritchie BW, Harrison GJ, Harrison LR, eds. Avian Medicine: Principles and Application. Wingers Publishing Inc; 1994:695722.

    • Search Google Scholar
    • Export Citation
  • 4.

    Santilli R, Moïse NS, Pariaut R, Perego M. Bradyarrhythmias. In: Electrocardiography of the Dog and Cat: Diagnosis of Arrhythmias. 2nd ed. Edra SpA; 2018:239258.

    • Search Google Scholar
    • Export Citation
  • 5.

    Santilli R, Moïse NS, Pariaut R, Perego M. Formation and interpretation of the electrocardiographic waves. In: Electrocardiography of the Dog and Cat: Diagnosis of Arrhythmias. 2nd ed. Edra SpA; 2018:3569.

    • Search Google Scholar
    • Export Citation
  • 6.

    Santilli R, Moïse NS, Pariaut R, Perego M. Aberrant conduction. In: Electrocardiography of the Dog and Cat: Diagnosis of Arrhythmias. 2nd ed. Edra SpA; 2018:286287.

    • Search Google Scholar
    • Export Citation
  • 7.

    Olgin JE, Zipes DP. Specific arrhythmias: diagnosis and treatment. In: Zipes DP, Libby P, Bonow RO, Mann DL, Tomaselli GF, eds. Braunwald’s Heart Disease: a Textbook of Cardiovascular Medicine. 7th ed. Elsevier Saunders; 2005:803863.

    • Search Google Scholar
    • Export Citation
  • 8.

    Schamroth L, Chesler E. Phasic aberrant ventricular conduction. Br Heart J. 1963;25(2):219226. doi:10.1136/hrt.25.2.219

  • 9.

    Issa ZF, Miller JM, Zipes DP. Intraventricular conduction abnormalities. In: Clinical Arrhythmology and Electrophysiology: a Companion to Braunwald’s Heart Disease. 2nd ed. Elsevier Saunders; 2012:194211.

    • Search Google Scholar
    • Export Citation
  • 10.

    Santilli R, Moïse NS, Pariaut R, Perego M. Supraventricular tachycardias. In: Electrocardiography of the Dog and Cat: Diagnosis of Arrhythmias. 2nd ed. Edra SpA; 2018:174180.

    • Search Google Scholar
    • Export Citation
  • 11.

    Sandler IA, Marriott HJL. The differential morphology of anomalous ventricular complexes of RBBB-type in lead V; ventricular ectopy versus aberration. Circulation. 1965;31:551556.

    • PubMed
    • Search Google Scholar
    • Export Citation

Supplementary Materials

  • Figure 1

    ECG recordings from a 26-year-old Timneh African grey parrot that was evaluated prior to undergoing CT for radiation planning; an arrhythmia was auscultated during the preanesthetic evaluation. A—Initial 6-lead ECG recording. Sinus tachycardia with an average heart rate of 600 beats/min is present. Notice that so-called long-short R-R cycles are followed by complexes with a different mean electrical axis (arrows). These complexes are preceded by a P wave with an electrical axis and PQ interval consistent with those of preceding complexes, suggesting an Ashman-like phenomenon. In addition, P waves are superimposed on the preceding T waves during periods of the sinus rhythm, consistent with a P-on-T phenomenon previously detected in African grey parrots. Small deflections after the T waves within the long R-R cycle are likely U waves (u). B—Intermittently, the P-P interval slows slightly (brackets) prior to a long R-R interval, which is presumed to be due to sinus arrest. Paper speed = 50 mm/s; 10 mm = 1 mV.

  • Figure 2

    Lead II ECG recording from the bird in Figure 1. A similar rhythm as shown in Figure 1 is seen, except a single premature complex (asterisk) with a different morphology is present with a similar long-short R-R cycle. However, the QRS complex is premature, wide, and bizarre (QRS duration, 0.04 seconds; QRS-T duration, 0.08 seconds), and there is not an obvious P wave in the preceding T wave, suggesting the origin was ventricular. Paper speed = 50 mm/s; 10 mm = 1 mV.

  • Figure 3

    Six-lead ECG recording obtained from the bird in Figure 1 during a recheck examination 1 week later; the recording was obtained after the bird was premedicated with glycopyrrolate, midazolam, and butorphanol and anesthetized with isoflurane. There is sinus tachycardia with an average heart rate of 600 beats/min. The previously noted sinus arrest, rate-dependent aberrancy, and ventricular premature complexes are not seen. Paper speed = 50 mm/s; 10 mm = 1 mV.

  • 1.

    Pees M, Straub J, Krautwald-Junghanns ME. Echocardiographic examinations of 60 African grey parrots and 30 other psittacine birds. Vet Rec. 2004;155(3):7376.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Nap AMP, Lumeij JT, Stokhof AA. Electrocardiogram of the African grey (Psittacus erithacus) and Amazon (Amazona spp) parrot. Avian Pathol. 1992;21(1):4553.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Lumeij JT, Ritchie BW. Cardiology. In: Ritchie BW, Harrison GJ, Harrison LR, eds. Avian Medicine: Principles and Application. Wingers Publishing Inc; 1994:695722.

    • Search Google Scholar
    • Export Citation
  • 4.

    Santilli R, Moïse NS, Pariaut R, Perego M. Bradyarrhythmias. In: Electrocardiography of the Dog and Cat: Diagnosis of Arrhythmias. 2nd ed. Edra SpA; 2018:239258.

    • Search Google Scholar
    • Export Citation
  • 5.

    Santilli R, Moïse NS, Pariaut R, Perego M. Formation and interpretation of the electrocardiographic waves. In: Electrocardiography of the Dog and Cat: Diagnosis of Arrhythmias. 2nd ed. Edra SpA; 2018:3569.

    • Search Google Scholar
    • Export Citation
  • 6.

    Santilli R, Moïse NS, Pariaut R, Perego M. Aberrant conduction. In: Electrocardiography of the Dog and Cat: Diagnosis of Arrhythmias. 2nd ed. Edra SpA; 2018:286287.

    • Search Google Scholar
    • Export Citation
  • 7.

    Olgin JE, Zipes DP. Specific arrhythmias: diagnosis and treatment. In: Zipes DP, Libby P, Bonow RO, Mann DL, Tomaselli GF, eds. Braunwald’s Heart Disease: a Textbook of Cardiovascular Medicine. 7th ed. Elsevier Saunders; 2005:803863.

    • Search Google Scholar
    • Export Citation
  • 8.

    Schamroth L, Chesler E. Phasic aberrant ventricular conduction. Br Heart J. 1963;25(2):219226. doi:10.1136/hrt.25.2.219

  • 9.

    Issa ZF, Miller JM, Zipes DP. Intraventricular conduction abnormalities. In: Clinical Arrhythmology and Electrophysiology: a Companion to Braunwald’s Heart Disease. 2nd ed. Elsevier Saunders; 2012:194211.

    • Search Google Scholar
    • Export Citation
  • 10.

    Santilli R, Moïse NS, Pariaut R, Perego M. Supraventricular tachycardias. In: Electrocardiography of the Dog and Cat: Diagnosis of Arrhythmias. 2nd ed. Edra SpA; 2018:174180.

    • Search Google Scholar
    • Export Citation
  • 11.

    Sandler IA, Marriott HJL. The differential morphology of anomalous ventricular complexes of RBBB-type in lead V; ventricular ectopy versus aberration. Circulation. 1965;31:551556.

    • PubMed
    • Search Google Scholar
    • Export Citation

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