The autonomic nerves around the vein of Marshall: a postmortem study with clinical implications.
Cardiac autonomic nervous system
atrial fibrillation
cardiovascular cause of death
interstitial fibrosis
vein of Marshall
Journal
APMIS : acta pathologica, microbiologica, et immunologica Scandinavica
ISSN: 1600-0463
Titre abrégé: APMIS
Pays: Denmark
ID NLM: 8803400
Informations de publication
Date de publication:
12 Mar 2024
12 Mar 2024
Historique:
received:
30
03
2023
accepted:
31
01
2024
medline:
12
3
2024
pubmed:
12
3
2024
entrez:
12
3
2024
Statut:
aheadofprint
Résumé
This study aims to analyze the vein of Marshall (VOM) in human autopsy hearts and its correlation with clinical data to elucidate the morphological substrates of atrial fibrillation (AF) and other cardiac diseases. Twenty-three adult autopsy hearts were studied, assessing autonomic nerves by immunohistochemistry with tyrosine hydroxylase (sympathetic nerves), choline acetyltransferase (parasympathetic nerves), growth-associated protein 43 (neural growth), and S100 (general neural marker) antibodies. Interstitial fibrosis was assessed by Masson trichrome staining. Measurements were conducted via morphometric software. The results were correlated with clinical data. Sympathetic innervation was abundant in all VOM-adjacent regions. Subjects with a history of AF, cardiovascular cause of death, and histologically verified myocardial infarction had increased sympathetic innervation and neural growth around the VOM at the mitral isthmus. Interstitial fibrosis increased with age and heart weight was associated with AF and cardiovascular cause of death. This study increases our understanding of the cardiac autonomic innervation in the VOM area in various diseases, offering implications for the development of new therapeutic approaches targeting the autonomic nervous system.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Authors. APMIS published by John Wiley & Sons Ltd on behalf of Scandinavian Societies for Pathology, Medical Microbiology and Immunology.
Références
Corradi D, Callegari S, Gelsomino S, Lorusso R, Macchi E. Morphology and pathophysiology of target anatomical sites for ablation procedures in patients with atrial fibrillation: part II: pulmonary veins, caval veins, ganglionated plexi, and ligament of Marshall. Int J Cardiol. 2013;168:1769-1778.
Makino M, Inoue S, Matsuyama TA, Ogawa G, Sakai T, Kobayashi YI, et al. Diverse myocardial extension and autonomic innervation on ligament of Marshall in humans. J Cardiovasc Electrophysiol. 2006;17:594-599.
Valderrábano M, Peterson LE, Swarup V, Schurmann PA, Makkar A, Doshi RN, et al. Effect of catheter ablation with vein of Marshall ethanol infusion vs catheter ablation alone on persistent atrial fibrillation: the VENUS randomized clinical trial. JAMA. 2020;324:1620-1628.
Lu L, Guo J, Hua Y, Huang K, Magaye R, Cornell J, et al. Cardiac fibrosis in the ageing heart: contributors and mechanisms. Clin Exp Pharmacol Physiol. 2017;44:55-63.
Hassink RJ, Aretz HT, Ruskin J, Keane D. Morphology of atrial myocardium in human pulmonary veins: a postmortem analysis in patients with and without atrial fibrillation. J Am Coll Cardiol. 2003;42:1108-1114.
Horn MA, Trafford AW. Aging and the cardiac collagen matrix: novel mediators of fibrotic remodelling. J Mol Cell Cardiol. 2016;93:175-185.
Báez-Escudero JL, Keida T, Dave AS, Okishige K, Valderrábano M. Ethanol infusion in the vein of marshall leads to parasympathetic denervation of the human left atrium: implications for atrial fibrillation. J Am Coll Cardiol. 2014;63:1892-1901.
Báez-Escudero JL, Morales PF, Dave AS, Sasaridis CM, Kim YH, Okishige K, et al. Ethanol infusion the vein of Marshall facilitates mitral isthmus ablation. Heart Rhythm. 2012;9:1207-1215.
Hindricks G, Potpara T, Dagres N, Arbelo E, Bax JJ, Blomström-Lundqvist C, et al. 2020 ESC guidelines for the diagnosis and management of atrial fibrillation developed in collaboration with the European Association for Cardio-Thoracic Surgery (EACTS). Eur Heart J. 2021;42:373-498.
Michaud K, Basso C, d'Amati G, Giordano C, Kholová I, Preston SD, et al. Diagnosis of myocardial infarction at autopsy: AECVP reappraisal in the light of the current clinical classification. Virchows Arch. 2020;476:179-194.
Basso C, Aguilera B, Banner J, Cohle S, d'Amati G, de Gouveia RH, et al. Guidelines for autopsy investigation of sudden cardiac death: 2017 update from the Association for European Cardiovascular Pathology. Virchows Arch. 2017;471:691-705.
Depes D, Mennander A, Paavonen T, Kholová I. Autonomic nerves in myocardial sleeves around caval veins: potential role in cardiovascular mortality? Cardiovasc Pathol. 2022;59:107426.
Depes D, Mennander A, Vehniäinen R, Paavonen T, Kholová I. Human pulmonary vein myocardial sleeve autonomic neural density and cardiovascular mortality. J Histochem Cytochem. 2022;70:627-642.
Bankhead P, Loughrey MB, Fernández JA, Dombrowski Y, McArt DG, Dunne PD, et al. QuPath: open source software for digital pathology image analysis. Sci Rep. 2017;7:1-7.
Zabówka A, Jakiel M, Bolechała F, Jakiel R, Jasińska KA, Hołda MK. Topography of the oblique vein of the left atrium (vein of Marshall). Kardiol Pol. 2020;78:688-693.
Lin J, Scherlag BJ, Niu G, Lu Z, Patterson E, Liu S, et al. Autonomic elements within the ligament of Marshall and inferior left ganglionated plexus mediate functions of the atrial neural network. J Cardiovasc Electrophysiol. 2009;20:318-324.
Rodríguez-Mañero M, Schurmann P, Valderrábano M. Ligament and vein of Marshall: a therapeutic opportunity in atrial fibrillation. Heart Rhythm. 2016;13:593-601.
Lin J, Scherlag BJ, Lu Z, Zhang Y, Liu S, Patterson E, et al. Inducibility of atrial and ventricular arrhythmias along the ligament of Marshall: role of autonomic factors. J Cardiovasc Electrophysiol. 2008;19:955-962.
Lai Y, Guo Q, Sang C, Gao M, Huang L, Zuo S, et al. Revisiting the characteristics and ablation strategy of biatrial tachycardias: a case series and systematic review. Europace. 2022;25:905-913.
Patterson E, Lazzara R, Szabo B, Liu H, Tang D, Li YH, et al. Sodium-calcium exchange initiated by the Ca2+ transient: an arrhythmia trigger within pulmonary veins. J Am Coll Cardiol. 2006;47:1196-1206.
Chang CM, Wu TJ, Zhou S, Doshi RN, Lee MH, Ohara T, et al. Nerve sprouting and sympathetic hyperinnervation in a canine model of atrial fibrillation produced by prolonged right atrial pacing. Circulation. 2001;103:22-25.
Fu SY, Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol. 1997;14:67-116.
Cao JM, Fishbein MC, Han JB, Lai WW, Lai AC, Wu TJ, et al. Relationship between regional cardiac hyperinnervation and ventricular arrhythmia. Circulation. 2000;101:1960-1969.
Zhou S, Chen LS, Miyauchi Y, Miyauchi M, Kar S, Kangavari S, et al. Mechanisms of cardiac nerve sprouting after myocardial infarction in dogs. Circ Res. 2004;95:76-83.
Fukuda K, Kanazawa H, Aizawa Y, Ardell JL, Shivkumar K. Cardiac innervation and sudden cardiac death. Circ Res. 2015;116:2005-2019.
Liu S, Yu X, Luo D, Qin Z, Wang X, He W, et al. Ablation of the ligament of marshall and left stellate ganglion similarly reduces ventricular arrhythmias during acute myocardial infarction. Circ Arrhythm Electrophysiol. 2018;11:e005945.
Ravelli F, Masè M, Cristoforetti A, Avogaro L, D'Amato E, Tessarolo F, et al. Quantitative assessment of transmural fibrosis profile in the human atrium: evidence for a three-dimensional arrhythmic substrate by slice-to-slice histology. Europace. 2022;25:739-747.
Maesen B, Verheule S, Zeemering S, La Meir M, Nijs J, Lumeij S, et al. Endomysial fibrosis, rather than overall connective tissue content, is the main determinant of conduction disturbances in human atrial fibrillation. Europace. 2022;24:1015-1024.
De Oliveira ÍM, Oliveira BD, Scanavacca MI, Gutierrez PS. Fibrosis, myocardial crossings, disconnections, abrupt turns, and epicardial reflections: do they play an actual role in human permanent atrial fibrillation? A controlled necropsy study. Cardiovasc Pathol. 2013;22:65-69.
Clarke GL, Bhattacherjee A, Tague SE, Hasan W, Smith PG. β-Adrenoceptor blockers increase cardiac sympathetic innervation by inhibiting autoreceptor suppression of axon growth. J Neurosci. 2010;30:12446-12454.
Elia A, Cannavo A, Gambino G, Cimini M, Ferrara N, Kishore R, et al. Aging is associated with cardiac autonomic nerve fiber depletion and reduced cardiac and circulating BDNF levels. J Geriatr Cardiol. 2021;18:549-559.