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Kaiwen Chen Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University, Manhattan, KS

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Matthew Tanner Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University, Manhattan, KS

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Justin D. Thomason Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University, Manhattan, KS

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Introduction

A 9-year-old 10-kg spayed female Pug was presented to the emergency service at the Kansas State University Veterinary Health Center with chief complaints of tachypnea and dyspnea of 3 to 4 days’ duration. On presentation, the dog was quiet, alert, and responsive. Rectal temperature was 38.7 °C; heart rate was 140 beats/min. The dog was panting with a noticeable expiratory push. Stenotic nares, stertorous breathing, and increased referred upper respiratory noise were also noted. There was no heart murmur auscultated on physical examination.

Results of a CBC and serum biochemical profile were unremarkable. Thoracic radiographic findings were consistent with aspiration pneumonia and pectus excavatum. Echocardiography was performed to evaluate for pulmonary arterial hypertension and revealed normal chamber sizes and an absence of pulmonary arterial hypertension. An ECG recording was obtained (Figure 1).

Figure 1
Figure 1

Six-lead ECG tracing from a 9-year-old Pug with preexisting brachycephalic airway syndrome. Suspected left bundle branch block with wide and tall aberrant QRS complexes (asterisks) following a short R-R interval and preceding a relatively prolonged R-R interval is evident. The ECG findings are consistent with atypical atrial flutter with intermittent Ashman phenomenon, Brody effect, or aberrancy. Given the patient’s history, we suspect that the atypical atrial flutter may have been related to chronic inflammation secondary to the dog’s primary respiratory disease. Paper speed = 50 mm/s; 1 cm = 1 mV.

Citation: Journal of the American Veterinary Medical Association 260, 13; 10.2460/javma.21.04.0193

ECG Interpretation

The ECG recording revealed an irregularly irregular rhythm with a calculated mean heart rate of 167 beats/min. There were positive deflections in the inferior leads corresponding to atrial depolarizations, with an atrial heart rate of 428 beats/min. Given the isoelectric line between the atrial waves, these deflections were consistent with the undulating appearance of flutter waves (F waves) suggestive of atypical atrial flutter (AFL). The F waves had variable morphologies and variable F-F intervals. The atrioventricular conduction ratio varied from 2:1 to 4:1, indicating variable second-degree atrioventricular block. Some of the QRS complexes were wide (duration, > 0.1 seconds) with positive deflections in leads II, III, and aVF, suggesting a left bundle branch block morphology. These wide and tall aberrant QRS complexes always followed a short R-R interval and were preceded by a relatively prolonged R-R interval. Therefore, the complexes were consistent with the Ashman phenomenon, the Brody effect, or aberrancy. The final ECG assessment was suspected macroreentrant supraventricular tachycardia, specifically atypical AFL. Additional electrophysiological studies would have been required to achieve a definitive diagnosis. Given the dog’s history of primary airway disease and absence of structural heart disease, the authors suspected that the AFL was related to the dog’s airway disease.

Discussion

Electrical reentry circuits can happen when anatomic or functional blocks and slow conduction areas are present together, along with electrical stimulation. Atrial fibrillation can be classified as a focal microreentrant mechanism; AFL can be classified as a macroreentrant mechanism.1 The pathophysiology of AFL is not fully understood. In people, researchers have shown that chronic obstructive pulmonary disease (COPD) and obstructive sleep apnea are associated with increased risks of AFL, atrial fibrillation, or both.2,3 Patients with COPD who have more symptoms of respiratory distress have a higher risk of developing AFL or atrial fibrillation, and treating these patients with β-adrenoceptor blockers or surgical ablation can decrease the overall mortality rate,4 which makes diagnosing and treating AFL essential. However, no anti-arrhythmia medication was prescribed for the dog described in the present report at the time of evaluation.

In humans, COPD is defined as the presence of airflow limitation associated with an abnormal inflammatory response,5 and similar clinical signs of respiratory distress are observed in a variety of other species. In the dog described in the present report, respiratory distress secondary to pneumonia, pectus excavatum, and brachycephalic airway syndrome, with congenital abnormalities causing airway obstruction, was documented.6 Similar signs are observed in equine patients with recurrent airway obstruction caused by mucus obstructing the bronchioles and alveoli, defined as equine COPD.7

Studies8,9 have shown the close relationship between atrial fibrillation and chronic oxidative damage, acidosis, and systemic inflammation caused by COPD in people. A recent population-based cohort study8 reported that patients with COPD have greater systemic inflammation, as evidenced by higher plasma concentrations of inflammatory mediators such as high-sensitivity C-reactive protein, interleukin-6, and tumor necrosis factor-α, which correlated with a higher risk of developing AFL. Similarly, concentrations of tumor necrosis factor-α, interleukin-10, interleukin-13, and interleukin-17A were significantly higher in dogs with brachycephalic airway syndrome than in healthy dogs, but C-reactive protein, interleukin-1β, and interleukin-6 concentrations did not differ between these groups.6 Among these inflammatory mediators, tumor necrosis factor-α and its associated inflammatory pathways is one of the best characterized, and it has been shown that tumor necrosis factor-α is involved in atrial remodeling, including structural, electrical, and contractility changes, which are all contributing factors to the initiation and maintenance of atrial fibrillation.10 Moreover, high tumor necrosis factor-α concentrations can lead to atrial fibrosis in mice without causing significant changes in cardiac size or function while being arrhythmogenic.11 Fibrosis predisposes to the development of reentrant circuits by promoting conduction block and slow, heterogeneous conduction.12 The conduction abnormalities, in turn, play an important role in creating a unidirectional conduction block, which is necessary for development of atrial fibrillation.13 A transitional atrial fibrillation rhythm may also create a functional line of block and can be followed by stable AFL.14 In addition, an epidemiologic study15 found that a high percentage (47.8%) of brachycephalic dogs have high cardiac troponin I concentrations. Concurrent myocardial damage might contribute to the spontaneous development of AFL.

Medical treatment of AFL secondary to brachycephalic airway syndrome involves controlling the underlying inflammation. Evidence has shown that using low-dose methylprednisolone as a treatment significantly decreases the risk of redeveloping atrial fibrillation in people.16 Similarly, prednisone has been shown to prevent inducible AFL in dogs with experimentally induced sterile pericarditis.17 However, another study18 reported controversial results that NSAIDs other than aspirin could lead to a higher risk of AFL or atrial fibrillation. Owing to the similar pathophysiology and response to treatment between AFL and atrial fibrillation, it might be safe to hypothesize that AFL is also associated with high systemic inflammation caused by COPD. Although the exact cause of AFL still needs further investigation, to the authors’ knowledge, this is the first reported case that documented a potential relationship between brachycephalic airway syndrome in dogs and atypical AFL. However, other causes, such as Marfan syndrome and pectus excavatum, related to atrial fibrillation have also been reported in people.19,20

In conclusion, brachycephalic airway syndrome, which resembles COPD in people, may have led to the suspected atypical AFL in the patient of this report.

Acknowledgments

The authors declare that there were no financial or other conflicts of interest. Kaiwen Chen is sponsored by the China Scholarship Council and US-China Center for Animal Health.

References

  • 1.

    Saoudi N, Cosio F, Waldo A, et al. Classification of atrial flutter and regular atrial tachycardia according to electrophysiologic mechanism and anatomic bases: a statement from a joint expert group from the Working Group of Arrhythmias of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. J Cardiovasc Electrophysiol. 2001;12(7):852866. doi:10.1046/j.1540-8167.2001.00852.x

    • Search Google Scholar
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  • 2.

    Konecny T, Park JY, Somers KR, et al. Relation of chronic obstructive pulmonary disease to atrial and ventricular arrhythmias. Am J Cardiol. 2014;114(2):272277. doi:10.1016/j.amjcard.2014.04.030

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

    Gami AS, Gregg P, Caples SM, et al. Association of atrial fibrillation and obstructive sleep apnea. Circulation. 2004;110(4):364367. doi:10.1161/01.CIR.0000136587.68725.8E

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Goudis CA. Chronic obstructive pulmonary disease and atrial fibrillation: an unknown relationship. J Cardiol. 2017;69(5):699705. doi:10.1016/j.jjcc.2016.12.013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Celli BR, MacNee W, ATS/ERS Task Force. Standards for the diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper. Eur Respir J. 2004;23(6):932946. doi:10.1183/09031936.04.00014304

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Rancan L, Romussi S, Garcia P, et al. Assessment of circulating concentrations of proinflammatory and anti-inflammatory cytokines and nitric oxide in dogs with brachycephalic airway obstruction syndrome. Am J Vet Res. 2013;74(1):155160. doi:10.2460/ajvr.74.1.155

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    López A, Martinson SA. Respiratory system, mediastinum, and pleurae. In: Pathologic Basis of Veterinary Disease. 6th ed. Elsevier; 2017:471–560.e1.doi:10.1016/B978-0-323-35775-3.00009-6

    • Search Google Scholar
    • Export Citation
  • 8.

    Grymonprez M, Vakaet V, Kavousi M, et al. Chronic obstructive pulmonary disease and the development of atrial fibrillation. Int J Cardiol. 2019;276:118124. doi:10.1016/j.ijcard.2018.09.056

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Hayashi T, Fukamizu S, Hojo R, et al. Prevalence and electrophysiological characteristics of typical atrial flutter in patients with atrial fibrillation and chronic obstructive pulmonary disease. EP Europace. 2013;15(12):17771783. doi:10.1093/europace/eut158

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Ren M, Li X, Hao L, Zhong J. Role of tumor necrosis factor alpha in the pathogenesis of atrial fibrillation: a novel potential therapeutic target? Ann Med. 2015;47(4):316324. doi:10.3109/07853890.2015.1042030

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Liew R, Khairunnisa K, Gu Y, et al. Role of tumor necrosis factor-α in the pathogenesis of atrial fibrosis and development of an arrhythmogenic substrate. Circ J. 2013;77(5):11711179. doi:10.1253/circj.cj-12-1155

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Scott L Jr, Li N, Dobrev D. Role of inflammatory signaling in atrial fibrillation. Int J Cardiol. 2019;287:195200. doi:10.1016/j.ijcard.2018.10.020

  • 13.

    Derakhchan K, Li D, Courtemanche M, et al. Method for simultaneous epicardial and endocardial mapping of in vivo canine heart: application to atrial conduction properties and arrhythmia mechanisms. J Cardiovasc Electrophysiol. 2001;12(5):548555. doi:10.1046/j.1540-8167.2001.00548.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Waldo AL, Feld GK. Inter-relationships of atrial fibrillation and atrial flutter. J Am Coll Cardiol. 2008;51(8):779786. doi:10.1016/j.jacc.2007.08.066

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Planellas M, Cuenca R, Tabar M-D, et al. Evaluation of C-reactive protein, Haptoglobin and cardiac troponin 1 levels in brachycephalic dogs with upper airway obstructive syndrome. BMC Vet Res. 2012;8:152. doi:10.1186/1746-6148-8-152

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Dernellis J, Panaretou M. Relationship between C-reactive protein concentrations during glucocorticoid therapy and recurrent atrial fibrillation. Eur Heart J. 2004;25(13):11001107. doi:10.1016/j.ehj.2004.04.025

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Goldstein RN, Ryu K, Khrestian C, van Wagoner DR, Waldo AL. Prednisone prevents inducible atrial flutter in the canine sterile pericarditis model. J Cardiovasc Electrophysiol. 2008;19(1):7481. doi:10.1111/j.1540-8167.2007.00970.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Schmidt M, Christiansen CF, Mehnert F, Schmidt M, et al. Non-steroidal anti-inflammatory drug use and risk of atrial fibrillation or flutter: population based case-control study. BMJ. 2011;343:d3450. doi:10.1136/bmj.d3450

    • Search Google Scholar
    • Export Citation
  • 19.

    Tran NT, Larry Klein J, Paul Mounsey J, et al. Lone atrial fibrillation is associated with pectus excavatum. Heart Rhythm. 2013;10(9):12631269. doi:10.1016/j.hrthm.2013.05.010

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Savolainen A, Kupari M, Toivonen L, Kaitila I, Viitasalo M. Abnormal ambulatory electrocardiographic findings in patients with the Marfan syndrome. J Intern Med. 1997;241(3):221226. doi:10.1046/j.1365-2796.1997.115125000.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Figure 1

    Six-lead ECG tracing from a 9-year-old Pug with preexisting brachycephalic airway syndrome. Suspected left bundle branch block with wide and tall aberrant QRS complexes (asterisks) following a short R-R interval and preceding a relatively prolonged R-R interval is evident. The ECG findings are consistent with atypical atrial flutter with intermittent Ashman phenomenon, Brody effect, or aberrancy. Given the patient’s history, we suspect that the atypical atrial flutter may have been related to chronic inflammation secondary to the dog’s primary respiratory disease. Paper speed = 50 mm/s; 1 cm = 1 mV.

  • 1.

    Saoudi N, Cosio F, Waldo A, et al. Classification of atrial flutter and regular atrial tachycardia according to electrophysiologic mechanism and anatomic bases: a statement from a joint expert group from the Working Group of Arrhythmias of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. J Cardiovasc Electrophysiol. 2001;12(7):852866. doi:10.1046/j.1540-8167.2001.00852.x

    • Search Google Scholar
    • Export Citation
  • 2.

    Konecny T, Park JY, Somers KR, et al. Relation of chronic obstructive pulmonary disease to atrial and ventricular arrhythmias. Am J Cardiol. 2014;114(2):272277. doi:10.1016/j.amjcard.2014.04.030

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

    Gami AS, Gregg P, Caples SM, et al. Association of atrial fibrillation and obstructive sleep apnea. Circulation. 2004;110(4):364367. doi:10.1161/01.CIR.0000136587.68725.8E

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Goudis CA. Chronic obstructive pulmonary disease and atrial fibrillation: an unknown relationship. J Cardiol. 2017;69(5):699705. doi:10.1016/j.jjcc.2016.12.013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Celli BR, MacNee W, ATS/ERS Task Force. Standards for the diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper. Eur Respir J. 2004;23(6):932946. doi:10.1183/09031936.04.00014304

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Rancan L, Romussi S, Garcia P, et al. Assessment of circulating concentrations of proinflammatory and anti-inflammatory cytokines and nitric oxide in dogs with brachycephalic airway obstruction syndrome. Am J Vet Res. 2013;74(1):155160. doi:10.2460/ajvr.74.1.155

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    López A, Martinson SA. Respiratory system, mediastinum, and pleurae. In: Pathologic Basis of Veterinary Disease. 6th ed. Elsevier; 2017:471–560.e1.doi:10.1016/B978-0-323-35775-3.00009-6

    • Search Google Scholar
    • Export Citation
  • 8.

    Grymonprez M, Vakaet V, Kavousi M, et al. Chronic obstructive pulmonary disease and the development of atrial fibrillation. Int J Cardiol. 2019;276:118124. doi:10.1016/j.ijcard.2018.09.056

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Hayashi T, Fukamizu S, Hojo R, et al. Prevalence and electrophysiological characteristics of typical atrial flutter in patients with atrial fibrillation and chronic obstructive pulmonary disease. EP Europace. 2013;15(12):17771783. doi:10.1093/europace/eut158

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Ren M, Li X, Hao L, Zhong J. Role of tumor necrosis factor alpha in the pathogenesis of atrial fibrillation: a novel potential therapeutic target? Ann Med. 2015;47(4):316324. doi:10.3109/07853890.2015.1042030

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Liew R, Khairunnisa K, Gu Y, et al. Role of tumor necrosis factor-α in the pathogenesis of atrial fibrosis and development of an arrhythmogenic substrate. Circ J. 2013;77(5):11711179. doi:10.1253/circj.cj-12-1155

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Scott L Jr, Li N, Dobrev D. Role of inflammatory signaling in atrial fibrillation. Int J Cardiol. 2019;287:195200. doi:10.1016/j.ijcard.2018.10.020

  • 13.

    Derakhchan K, Li D, Courtemanche M, et al. Method for simultaneous epicardial and endocardial mapping of in vivo canine heart: application to atrial conduction properties and arrhythmia mechanisms. J Cardiovasc Electrophysiol. 2001;12(5):548555. doi:10.1046/j.1540-8167.2001.00548.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Waldo AL, Feld GK. Inter-relationships of atrial fibrillation and atrial flutter. J Am Coll Cardiol. 2008;51(8):779786. doi:10.1016/j.jacc.2007.08.066

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Planellas M, Cuenca R, Tabar M-D, et al. Evaluation of C-reactive protein, Haptoglobin and cardiac troponin 1 levels in brachycephalic dogs with upper airway obstructive syndrome. BMC Vet Res. 2012;8:152. doi:10.1186/1746-6148-8-152

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Dernellis J, Panaretou M. Relationship between C-reactive protein concentrations during glucocorticoid therapy and recurrent atrial fibrillation. Eur Heart J. 2004;25(13):11001107. doi:10.1016/j.ehj.2004.04.025

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Goldstein RN, Ryu K, Khrestian C, van Wagoner DR, Waldo AL. Prednisone prevents inducible atrial flutter in the canine sterile pericarditis model. J Cardiovasc Electrophysiol. 2008;19(1):7481. doi:10.1111/j.1540-8167.2007.00970.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Schmidt M, Christiansen CF, Mehnert F, Schmidt M, et al. Non-steroidal anti-inflammatory drug use and risk of atrial fibrillation or flutter: population based case-control study. BMJ. 2011;343:d3450. doi:10.1136/bmj.d3450

    • Search Google Scholar
    • Export Citation
  • 19.

    Tran NT, Larry Klein J, Paul Mounsey J, et al. Lone atrial fibrillation is associated with pectus excavatum. Heart Rhythm. 2013;10(9):12631269. doi:10.1016/j.hrthm.2013.05.010

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Savolainen A, Kupari M, Toivonen L, Kaitila I, Viitasalo M. Abnormal ambulatory electrocardiographic findings in patients with the Marfan syndrome. J Intern Med. 1997;241(3):221226. doi:10.1046/j.1365-2796.1997.115125000.x

    • PubMed
    • Search Google Scholar
    • Export Citation

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