Ablation as targeted perturbation to rewire communication network of persistent atrial fibrillation

PLoS One. 2017 Jul 5;12(7):e0179459. doi: 10.1371/journal.pone.0179459. eCollection 2017.

Abstract

Persistent atrial fibrillation (AF) can be viewed as disintegrated patterns of information transmission by action potential across the communication network consisting of nodes linked by functional connectivity. To test the hypothesis that ablation of persistent AF is associated with improvement in both local and global connectivity within the communication networks, we analyzed multi-electrode basket catheter electrograms of 22 consecutive patients (63.5 ± 9.7 years, 78% male) during persistent AF before and after the focal impulse and rotor modulation-guided ablation. Eight patients (36%) developed recurrence within 6 months after ablation. We defined communication networks of AF by nodes (cardiac tissue adjacent to each electrode) and edges (mutual information between pairs of nodes). To evaluate patient-specific parameters of communication, thresholds of mutual information were applied to preserve 10% to 30% of the strongest edges. There was no significant difference in network parameters between both atria at baseline. Ablation effectively rewired the communication network of persistent AF to improve the overall connectivity. In addition, successful ablation improved local connectivity by increasing the average clustering coefficient, and also improved global connectivity by decreasing the characteristic path length. As a result, successful ablation improved the efficiency and robustness of the communication network by increasing the small-world index. These changes were not observed in patients with AF recurrence. Furthermore, a significant increase in the small-world index after ablation was associated with synchronization of the rhythm by acute AF termination. In conclusion, successful ablation rewires communication networks during persistent AF, making it more robust, efficient, and easier to synchronize. Quantitative analysis of communication networks provides not only a mechanistic insight that AF may be sustained by spatially localized sources and global connectivity, but also patient-specific metrics that could serve as a valid endpoint for therapeutic interventions.

MeSH terms

  • Aged
  • Algorithms
  • Atrial Fibrillation / physiopathology
  • Atrial Fibrillation / surgery*
  • Catheter Ablation / methods*
  • Electrocardiography / methods*
  • Female
  • Heart / physiopathology
  • Heart Atria / physiopathology
  • Heart Atria / surgery
  • Heart Conduction System / physiopathology
  • Heart Conduction System / surgery*
  • Humans
  • Male
  • Middle Aged
  • Models, Cardiovascular
  • Recurrence
  • Treatment Outcome

Grants and funding

This work was supported by grants from the W. W. Smith Charitable Trust (to Ashikaga), the Johns Hopkins University Institute of Clinical and Translational Research (to Ashikaga), the Edward St. John Foundation for AF Research (to Calkins), The Roz and Marvin H Weiner and Family Foundation (to Calkins), The Dr. Francis P. Chiaramonte Foundation (to Calkins), The Marilyn and Christian Poindexter Arrhythmia Research Fund (to Calkins), and The Norbert and Louise Grunwald Cardiac Arrhythmia Research Fund (to Calkins).