Sander Verheule

Associate professor

Dr Sander Verheule has studied Biology at the University of Utrecht, with internships at the Hubrecht Laboratory for Developmental Biology and at the Department of Neurophysiology (VU Amsterdam). As a PhD student in the group of Dr Habo Jongsma (Department of Medical Physiology, Utrecht), he investigated the distribution and electrophysiological behavior of gap junction channels in various regions of the heart, defending his PhD thesis in 1999. From 1999-2003, he worked as an AHA post-doctoral fellow in the group of Dr Jeffrey Olgin and Dr Douglas Zipes at the Krannert Institute of Cardiology in Indianapolis, Indiana. There, his research focussed on the impact of structural remodeling on atrial conduction.

In 2003, Dr Verheule joined the electrophysiology group at the Department of Physiology in Maastricht. In his current research, he investigates the pathophysiological mechanisms underlying atrial fibrillation, and the recognition of these mechanisms in patients. His two main research questions are 1) How do atrial vascular and metabolic remodeling contribute to the progression of atrial fibrillation? and 2) How do changes in atrial tissue structure affect atrial electrical propagation?

 

Department of Physiology
Universiteitssingel 50, 6229 ER Maastricht
PO Box 616, 6200 MD Maastricht
Room number: F3.118
T: +31(0)43 388 10 76

  • 2024
    • Hermans, B., Özgül, O., Wolf, M., Gonçalves Marques, V., van Hunnik, A., Verheule, S., Chaldoupi, S. M., Linz, D., El Haddad, M., Duytschaever, M., Bonizzi, P., Vernooy, K., Knecht, S., Zeemering, S., & Schotten, U. (2024). Selecting repetitive focal and rotational activation patterns with the highest probability of being a source of atrial fibrillation. Journal of Molecular and Cellular Cardiology Plus, 7, Article 100064. https://www.sciencedirect.com/science/article/pii/S2772976124000047
  • 2023
    • Winters, J., Isaacs, A., Zeemering, S., Kawczynski, M., Maesen, B., Maessen, J., Bidar, E., Boukens, B., Hermans, B., van Hunnik, A., Casadei, B., Fabritz, L., Chua, W., Sommerfeld, L., Guasch, E., Mont, L., Batlle, M., Hatem, S., Kirchhof, P., ... Schotten, U. (2023). Heart Failure, Female Sex, and Atrial Fibrillation Are the Main Drivers of Human Atrial Cardiomyopathy: Results From the CATCH ME Consortium. Journal of the American Heart Association, 12(22), Article e031220. https://doi.org/10.1161/JAHA.123.031220
    • Carstensen, H., Nissen, S. D., Saljic, A., Hesselkilde, E. M., van Hunnik, A., Hohl, M., Sattler, S. M., Flogstad, C., Hopster-Iversen, C., Verheule, S., Bohm, M., Schotten, U., Jespersen, T., & Buhl, R. (2023). Long-Term Training Increases Atrial Fibrillation Sustainability in Standardbred Racehorses. Journal of Cardiovascular Translational Research, 16(5), 1205-1219. https://doi.org/10.1007/s12265-023-10378-6
    • Ozgul, O., Hermans, B. JM., van Hunnik, A., Verheule, S., Schotten, U., Bonizzi, P., & Zeemering, S. (2023). High-density and high coverage composite mapping of repetitive atrial activation patterns. Computers in Biology and Medicine, 159(1), Article 106920. https://doi.org/10.1016/j.compbiomed.2023.106920
  • 2022
    • D'Alessandro, E., Winters, J., van Nieuwenhoven, F. A., Schotten, U., & Verheule, S. (2022). The Complex Relation between Atrial Cardiomyopathy and Thrombogenesis. Cells, 11(19), Article 2963. https://doi.org/10.3390/cells11192963
    • Maesen, B., Verheule, S., Zeemering, S., La Meir, M., Nijs, J., Lumeij, S., Lau, D. H., Granier, M., Crijns, H. J., Maessen, J. G., Dhein, S., & Schotten, U. (2022). Endomysial fibrosis, rather than overall connective tissue content, is the main determinant of conduction disturbances in human atrial fibrillation. EP Europace, 24(6), 1015-1024. https://doi.org/10.1093/europace/euac026
    • Kawczynski, M. J., Zeemering, S., Gilbers, M., Isaacs, A., Verheule, S., Zink, M. D., Maesen, B., Bramer, S., Van Gelder, I. C., Crijns, H. J. G. M., Schotten, U., & Bidar, E. (2022). New-onset perioperative atrial fibrillation in cardiac surgery patients: transient trouble or persistent problem?-Authors' reply. EP Europace, 24(6), 1037-1038. Article 317. https://doi.org/10.1093/europace/euab317
    • van der Heijden, C. A. J., Verheule, S., Olsthoorn, J. R., Mihl, C., Poulina, L., van Kuijk, S. M. J., Heuts, S., Maessen, J. G., Bidar, E., & Maesen, B. (2022). Postoperative atrial fibrillation and atrial epicardial fat: Is there a link?IJC Heart and Vasculature, 39, Article 100976. https://doi.org/10.1016/j.ijcha.2022.100976
    • Zink, M. D., Laureanti, R., Hermans, B. J. M., Pison, L., Verheule, S., Philippens, S., Pluymaekers, N., Vroomen, M., Hermans, A., van Hunnik, A., Crijns, H. J. G. M., Vernooy, K., Linz, D., Mainardi, L., Auricchio, A., Zeemering, S., & Schotten, U. (2022). Extended ECG Improves Classification of Paroxysmal and Persistent Atrial Fibrillation Based on P- and f-Waves. Frontiers in physiology, 13, Article 779826. https://doi.org/10.3389/fphys.2022.779826
    • Ramos, K. S., Pool, L., van Schie, M. S., Wijdeveld, L. F. J. M., van der Does, W. F. B., Baks, L., Sultan, H. M. D., van Wijk, S. W., Bogers, A. J. J. C., Verheule, S., de Groot, N. M. S., & Brundel, B. J. J. M. (2022). Degree of Fibrosis in Human Atrial Tissue Is Not the Hallmark Driving AF. Cells, 11(3), Article 427. https://doi.org/10.3390/cells11030427
  • 2021
    • Bidar, E., Zeemering, S., Gilbers, M., Isaacs, A., Verheule, S., Zink, M. D., Maesen, B., Bramer, S., Kawczynski, M., Van Gelder, I. C., Crijns, H. J. G. M., Maessen, J. G., & Schotten, U. (2021). Clinical and electrophysiological predictors of device-detected new-onset atrial fibrillation during 3 years after cardiac surgery. EP Europace, 23(12), 1922-1930. https://doi.org/10.1093/europace/euab136
    • D'Alessandro, E., Scaf, B., van Oerle, R., van Nieuwenhoven, F. A., van Hunnik, A., Verheule, S., Schotten, U., Ten Cate, H., & Spronk, H. M. H. (2021). Thrombin generation by calibrated automated thrombography in goat plasma: Optimization of an assay. Research and practice in thrombosis and haemostasis, 5(8), Article e12620. https://doi.org/10.1002/rth2.12620
    • Verheule, S., & Schotten, U. (2021). Electrophysiological Consequences of Cardiac Fibrosis. Cells, 10(11), Article 3220. https://doi.org/10.3390/cells10113220
    • D'Alessandro, E., Scaf, B., Munts, C., van Hunnik, A., Trevelyan, C. J., Verheule, S., Spronk, H. M. H., Turner, N. A., ten Cate, H., Schotten, U., & van Nieuwenhoven, F. A. (2021). Coagulation Factor Xa Induces Proinflammatory Responses in Cardiac Fibroblasts via Activation of Protease-Activated Receptor-1. Cells, 10(11), Article 2958. https://doi.org/10.3390/cells10112958
    • Gatta, G., Sobota, V., Citerni, C., Diness, J. G., Sorensen, U. S., Jespersen, T., Bentzen, B. H., Zeemering, S., Kuiper, M., Verheule, S., Schotten, U., & van Hunnik, A. (2021). Effective termination of atrial fibrillation by SK channel inhibition is associated with a sudden organization of fibrillatory conduction. EP Europace, 23(11), 1847-1859. https://doi.org/10.1093/europace/euab125
    • Mighiu, A. S., Recalde, A., Ziberna, K., Carnicer, R., Tomek, J., Bub, G., Brewer, A. C., Verheule, S., Shah, A. M., Simon, J. N., & Casadei, B. (2021). Inducibility, but not stability, of atrial fibrillation is increased by NOX2 overexpression in mice. Cardiovascular Research, 117(11), 2354-2364. https://doi.org/10.1093/cvr/cvab019
    • Linz, D., Verheule, S., Isaacs, A., & Schotten, U. (2021). Considerations for the Assessment of Substrates, Genetics and Risk Factors in Patients with Atrial Fibrillation. Arrhythmia & Electrophysiology Review, 10(3), 132-139. https://doi.org/10.15420/aer.2020.51
    • Saljic, A., Fenner, M. F., Winters, J., Flethoj, M., Eggertsen, C. E., Carstensen, H., Nissen, S. D., Hesselkilde, E. M., van Hunnik, A., Schotten, U., Sorensen, U., Jespersen, T., Verheule, S., & Buhl, R. (2021). Increased fibroblast accumulation in the equine heart following persistent atrial fibrillation. IJC Heart and Vasculature, 35, Article 100842. https://doi.org/10.1016/j.ijcha.2021.100842
    • Bosada, F. M., Rivaud, M. R., Uhm, J.-S., Verheule, S., van Duijvenboden, K., Verkerk, A. O., Christoffels, V. M., & Boukens, B. J. (2021). A Variant Noncoding Region Regulates Prrx1 and Predisposes to Atrial Arrhythmias. Circulation Research, 129(3), 420-434. https://doi.org/10.1161/circresaha.121.319146
    • van Hunnik, A., Zeemering, S., Podziemski, P., Kuklik, P., Kuiper, M., Verheule, S., & Schotten, U. (2021). Bi-atrial high-density mapping reveals inhibition of wavefront turning and reduction of complex propagation patterns as main antiarrhythmic mechanisms of vernakalant. EP Europace, 23(7), 1114-1123. https://doi.org/10.1093/europace/euab026
    • Dudink, E. A. M. P., Bidar, E., Jacobs, J., van Hunnik, A., Zeemering, S., Weijs, B., Luermans, J. G. L. M., Maesen, B. A. E., Cheriex, E. C., Maessen, J. G., Hoorntje, J. C. A., Schotten, U., Crijns, H. J. G. M., & Verheule, S. (2021). The relation between the atrial blood supply and the complexity of acute atrial fibrillation. IJC Heart & Vasculature, 34, Article 100794. https://doi.org/10.1016/j.ijcha.2021.100794
    • Gilbers, M. D., Bidar, E., Maesen, B., Zeemering, S., Isaacs, A., Crijns, H., van Gelder, I., Rienstra, M., Verheule, S., Maessen, J., Stoll, M., & Schotten, U. (2021). Reappraisal of Atrial fibrillation: interaction between hyperCoagulability, Electrical remodelling and Vascular destabilisation in the progression of AF (RACE V) Tissue Bank Project: study design. Netherlands Heart Journal, 29(5), 280-287. https://doi.org/10.1007/s12471-021-01538-x
    • Opacic, D., van Hunnik, A., Zeemering, S., Dhalla, A., Belardinelli, L., Schotten, U., & Verheule, S. (2021). Electrophysiological effects of ranolazine in a goat model of lone atrial fibrillation. Heart Rhythm, 18(4), 615-622. https://doi.org/10.1016/j.hrthm.2020.11.021
    • van Rosmalen, F., Maesen, B., van Hunnik, A., Hermans, B. J. M., Bonizzi, P., Bidar, E., Nijs, J., Maessen, J. G., Verheule, S., Delhaas, T., Schotten, U., & Zeemering, S. (2021). Incidence, prevalence, and trajectories of repetitive conduction patterns in human atrial fibrillation. EP Europace, 23(Supplement_1), i123-i132. https://doi.org/10.1093/europace/euaa403
    • Gharaviri, A., Pezzuto, S., Potse, M., Conte, G., Zeemering, S., Sobota, V., Verheule, S., Krause, R., Auricchio, A., & Schotten, U. (2021). Synergistic antiarrhythmic effect of inward rectifier current inhibition and pulmonary vein isolation in a 3D computer model for atrial fibrillation. EP Europace, 23, I161-I168. https://doi.org/10.1093/europace/euaa413
    • Fenner, M. F., Gatta, G., Sattler, S., Kuiper, M., Hesselkilde, E. M., Adler, D. M. T., Smerup, M., Schotten, U., Sorensen, U., Diness, J. G., Jespersen, T., Verheule, S., Van Hunnik, A., & Buhl, R. (2021). Inhibition of Small-Conductance Calcium-Activated Potassium Current (IK,Ca) Leads to Differential Atrial Electrophysiological Effects in a Horse Model of Persistent Atrial Fibrillation. Frontiers in physiology, 12, Article 614483. https://doi.org/10.3389/fphys.2021.614483
    • Sobota, V., Gatta, G., van Hunnik, A., van Tuijn, I., Kuiper, M., Milnes, J., Jespersen, T., Schotten, U., & Verheule, S. (2021). The Acetylcholine-Activated Potassium Current Inhibitor XAF-1407 Terminates Persistent Atrial Fibrillation in Goats. Frontiers in Pharmacology, 11, Article 608410. https://doi.org/10.3389/fphar.2020.608410
    • Gharaviri, A., Pezzuto, S., Potse, M., Verheule, S., Conte, G., Krause, R., Schotten, U., & Auricchio, A. (2021). Left Atrial Appendage Electrical Isolation Reduces Atrial Fibrillation Recurrences A Simulation Study. Circulation-Arrhythmia and Electrophysiology, 14(1), Article e009230. https://doi.org/10.1161/CIRCEP.120.009230
  • 2020
    • Winters, J., von Braunmuhl, M. E., Zeemering, S., Gilbers, M., Ten Brink, T., Scaf, B., Guasch, E., Mont, L., Batlle, M., Sinner, M., Hatem, S., Mansour, M. K., Fabritz, L., Sommerfeld, L. C., Kirchhof, P., Isaacs, A., Stoll, M., Schotten, U., & Verheule, S. (2020). JavaCyte, a novel open-source tool for automated quantification of key hallmarks of cardiac structural remodeling. Scientific Reports, 10(1), Article 20074. https://doi.org/10.1038/s41598-020-76932-3
    • Zeemering, S., van Hunnik, A., van Rosmalen, F., Bonizzi, P., Scaf, B., Delhaas, T., Verheule, S., & Schotten, U. (2020). A Novel Tool for the Identification and Characterization of Repetitive Patterns in High-Density Contact Mapping of Atrial Fibrillation. Frontiers in physiology, 11, Article 570118. https://doi.org/10.3389/fphys.2020.570118
    • Gharaviri, A., Bidar, E., Potse, M., Zeemering, S., Verheule, S., Pezzuto, S., Krause, R., Maessen, J. G., Auricchio, A., & Schotten, U. (2020). Epicardial Fibrosis Explains Increased Endo-Epicardial Dissociation and Epicardial Breakthroughs in Human Atrial Fibrillation. Frontiers in physiology, 11, Article 68. https://doi.org/10.3389/fphys.2020.00068
  • 2019
    • Vroomen, M., Olsthoorn, J. R., Maesen, B., L'Espoir, V., La Meir, M., Das, M., Maessen, J. G., Crijns, H. J. G. M., Verheule, S., & Pison, L. (2019). Quantification of epicardial adipose tissue in patients undergoing hybrid ablation for atrial fibrillation. European Journal of Cardio-Thoracic Surgery, 56(1), 79-86. https://doi.org/10.1093/ejcts/ezy472
  • 2018
    • Gharaviri, A., Verheule, S., Eckstein, J., Potse, M., Krause, R., Auricchio, A., Kuijpers, N. H. L., & Schotten, U. (2018). Effect of Na+-channel blockade on the three-dimensional substrate of atrial fibrillation in a model of endo-epicardial dissociation and transmural conduction. EP Europace, 20(Suppl. 3), iii69-iii76. https://doi.org/10.1093/europace/euy236
    • Podziemski, P., Zeemering, S., Kuklik, P., van Hunnik, A., Maesen, B., Maessen, J., Crijns, H. J., Verheule, S., & Schotten, U. (2018). Rotors Detected by Phase Analysis of Filtered, Epicardial Atrial Fibrillation Electrograms Colocalize With Regions of Conduction Block. Circulation-Arrhythmia and Electrophysiology, 11(10), Article e005858. https://doi.org/10.1161/CIRCEP.117.005858
    • Zhao, J., Schotten, U., Smaill, B., & Verheule, S. (2018). Loss of Side-to-Side Connections Affects the Relative Contributions of the Sodium and Calcium Current to Transverse Propagation Between Strands of Atrial Myocytes. Frontiers in physiology, 9, Article 1212. https://doi.org/10.3389/fphys.2018.01212
    • Manninger, M., Zweiker, D., van Hunnik, A., Alogna, A., Prassl, A. J., Schipke, J., Zeemering, S., Zirngast, B., Schonleitner, P., Schwarzl, M., Herbst, V., Thon-Gutschi, E., Huber, S., Rohrer, U., Ebner, J., Brussee, H., Pieske, B. M., Heinzel, F. R., Verheule, S., ... Scherr, D. (2018). Arterial hypertension drives arrhythmia progression via specific structural remodeling in a porcine model of atrial fibrillation. Heart Rhythm, 15(9), 1328-1336. https://doi.org/10.1016/j.hrthm.2018.05.016
    • van Hunnik, A., Zeemering, S., Podziemski, P., Simons, J., Gatta, G., Hannink, L., Maesen, B., Kuiper, M., Verheule, S., & Schotten, U. (2018). Stationary Atrial Fibrillation Properties in the Goat Do Not Entail Stable or Recurrent Conduction Patterns. Frontiers in physiology, 9, Article 947. https://doi.org/10.3389/fphys.2018.00947
    • Weijs, B., Limantoro, I., Delhaas, T., de Vos, C. B., Blaauw, Y., Houben, R. P. M., Verheule, S., Pisters, R., & Crijns, H. J. G. M. (2018). Cardioversion of persistent atrial fibrillation is associated with a 24-hour relapse gap: Observations from prolonged postcardioversion rhythm monitoring. Clinical Cardiology, 41(3), 366-371. https://doi.org/10.1002/clc.22877
    • van Hunnik, A., Nasrallah, H., Lau, D. H., Kuiper, M., Verheule, S., & Schotten, U. (2018). Vernakalant does not alter early repolarization or contractility in normal and electrically remodelled atria. EP Europace, 20(1), 140-148. https://doi.org/10.1093/europace/eux025
  • 2017
    • Ji, Y., Varkevisser, R., Opacic, D., Bossu, A., Kuiper, M., Beekman, J. D. M., Yang, S., Khan, A. P., Dobrev, D., Voigt, N., Wang, M. Z., Verheule, S., Vos, M. A., & van der Heyden, M. A. G. (2017). The inward rectifier current inhibitor PA-6 terminates atrial fibrillation and does not cause ventricular arrhythmias in goat and dog models. British Journal of Pharmacology, 174(15), 2576-2590. https://doi.org/10.1111/bph.13869
    • Gharaviri, A., Verheule, S., Eckstein, J., Potse, M., Kuklik, P., Kuijpers, N. H. L., & Schotten, U. (2017). How disruption of endo-epicardial electrical connections enhances endo-epicardial conduction during atrial fibrillation. EP Europace, 19(2), 308-318. https://doi.org/10.1093/europace/euv445
    • Spronk, H. M. H., De Jong, A. M., Verheule, S., De Boer, H. C., Maass, A. H., Lau, D. H., Rienstra, M., van Hunnik, A., Kuiper, M., Lumeij, S., Zeemering, S., Linz, D., Kamphuisen, P. W., ten Cate, H., Crijns, H. J., Van Gelder, I. C., van Zonneveld, A. J., & Schotten, U. (2017). Hypercoagulability causes atrial fibrosis and promotes atrial fibrillation. European Heart Journal, 38(1), 38-50. https://doi.org/10.1093/eurheartj/ehw119
  • 2016
    • Linz, D., Hohl, M., Dhein, S., Ruf, S., Reil, J.-C., Kabiri, M., Wohlfart, P., Verheule, S., Boehm, M., Sadowski, T., & Schotten, U. (2016). Cathepsin A mediates susceptibility to atrial tachyarrhythmia and impairment of atrial emptying function in Zucker diabetic fatty rats. Cardiovascular Research, 110(3), 371-380. https://doi.org/10.1093/cvr/cvw071
    • Reilly, S. N., Liu, X., Carnicer, R., Recalde, A., Muszkiewicz, A., Jayaram, R., Carena, M. C., Wijesurendra, R., Stefanini, M., Surdo, N. C., Lomas, O., Ratnatunga, C., Sayeed, R., Krasopoulos, G., Rajakumar, T., Bueno-Orovio, A., Verheule, S., Fulga, T. A., Rodriguez, B., ... Casadei, B. (2016). Up-regulation of miR-31 in human atrial fibrillation begets the arrhythmia by depleting dystrophin and neuronal nitric oxide synthase. Science Translational Medicine, 8(340), Article 340ra74. https://doi.org/10.1126/scitranslmed.aac4296
    • Opacic, D., van Bragt, K. A., Nasrallah, H. M., Schotten, U., & Verheule, S. (2016). Atrial metabolism and tissue perfusion as determinants of electrical and structural remodelling in atrial fibrillation. Cardiovascular Research, 109(4), 527-541. https://doi.org/10.1093/cvr/cvw007
    • van Hunnik, A., Lau, D. H., Zeemering, S., Kuiper, M., Verheule, S., & Schotten, U. (2016). Antiarrhythmic effect of vernakalant in electrically remodeled goat atria is caused by slowing of conduction and prolongation of postrepolarization refractoriness. Heart Rhythm, 13(4), 964-972. https://doi.org/10.1016/j.hrthm.2015.12.009