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Myocardial sleeves of pulmonary veins and atrial fibrillation: a postmortem histopathological study of 100 subjects

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Abstract

Atrial fibrillation (AF) is triggered by ectopic beats originating from extensions of the left atrial myocardium over the pulmonary veins (PVs), so-called myocardial sleeves. A total of 100 hearts (393 PVs) obtained at autopsy were studied. Of these, 50 were from patients with chronic AF and 50 from controls in sinus rhythm. Out of a total of 393 PVs studied, a sleeve was present in 349 PVs (88.8%). The myocardial sleeves frequently harboured senile atrial amyloid and scarring. These two changes were evaluated semi-quantitatively (grade 0–3). Amyloidosis was found in 68% of all hearts and in 55% of all sleeves. It was more frequent in patients with AF (58.5%) than in those without (51.7%), however, without statistical significance (p values 0.948, 0.306, 0.166 and 1). Scarring was present in all 349 sleeves studied. It was significantly more severe in patients with AF (average grade 2.44) than in those without (average grade 2.00) (p values <0.001, <0.1, <0.05 and <0.01). In conclusion, amyloidosis and particularly scarring of the myocardial sleeves of the pulmonary veins, appear to be common in the elderly population as an arrhythmogenic substrate for AF.

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References

  1. Allessie MA, Boyden PA, Camm AJ, Kléber AG, Lab MJ, Legato MJ, Rosen MR, Schwartz PJ, Spooner PM, Van Wagoner DR, Waldo AL (2001) Pathophysiology and prevention of atrial fibrillation. Circulation 103:769–777

    PubMed  CAS  Google Scholar 

  2. Bauer A, McDonald AD, Donahue JK (2004) Pathophysiological findings in a model of persistent atrial fibrillation and severe congestive heart failure. Cardiovasc Res 61:764–770

    Article  PubMed  CAS  Google Scholar 

  3. Boldt A, Wetzel U, Lauschke J, Weigl J, Gummert J, Hindricks G, Kottkamp H, Dhein S (2004) Fibrosis in left atrial tissue of patients with atrial fibrillation with and without underlying mitral valve disease. Heart 90:400–405

    Article  PubMed  CAS  Google Scholar 

  4. Boldt A, Scholl A, Garbade J, Resetar ME, Mohr FW, Gummert JF, Dhein S (2005) ACE-inhibitor treatment attenuates atrial structural remodeling in patients with lone chronic atrial fibrillation. Basic Res Cardiol 100:1–7

    Article  PubMed  CAS  Google Scholar 

  5. Cornwell GG, Murdoch WL, Kyle RA, Westermark P, Pitkänen P (1983) Frequency and distribution of senile cardiovascular amyloid. A clinicopathologic correlation. Am J Med 75:618–623

    Article  PubMed  Google Scholar 

  6. Corradi D, Callegari S, Benussi S, Nascimbene S, Pastori P, Calvi S, Maestri R, Astorri E, Pappone C, Alfieri O (2004) Regional left atrial remodeling in patients with chronic atrial fibrillation undergoing mitral-valve surgery. Virchows Arch 445:498–505

    Article  PubMed  Google Scholar 

  7. Davies MJ, Pomerance A (1972) Pathology of atrial fibrillation in man. Br Heart J 34:520–525

    Article  PubMed  CAS  Google Scholar 

  8. DeGiorgio F, Arena V, DeMercurio D, Pascali VL, Capelli A (2004) Right atrial lipoma with “satellite” atrial fibrillation? Virchows Arch 444:392–394

    Article  PubMed  Google Scholar 

  9. Frustaci A, Chimenti C, Bellocci F, Morgante E, Russo MA, Maseri A (1997) Histological substrate of atrial biopsies in patients with lone atrial fibrillation. Circulation 96:1180–1184

    PubMed  CAS  Google Scholar 

  10. Fuster V, Rydén LE, Asinger RW et al (2001) ACC/AHA/ESC guidelines for the management of patients with atrial fibrillation: executive summary. Circulation 104:2118–2150

    PubMed  CAS  Google Scholar 

  11. Fynn SP, Kalman JM (2004) Pulmonary veins: anatomy, electrophysiology, tachycardia, and fibrillation (review). Pacing Clin Electrophysiol 27:1547–1559

    Article  PubMed  Google Scholar 

  12. Goette A, Juenemann G, Peters B, Klein HU, Roessner A, Huth Ch, Röcken Ch (2002) Determinants and consequences of atrial fibrosis in patients undergoing open heart surgery. Cardiovasc Res 54:390–396

    Article  PubMed  CAS  Google Scholar 

  13. Haїssaguerre M, Jaїs P, Shah DC, Takahashi A, Hocini M, Quiniou G, Garrigue S, Le Mouroux A, Le Métayer P, Clémenty J (1998) Spontaneous initiation of atrial fibrillation by ectopic beats originating in the pulmonary veins. N Engl J Med 339:659–666

    Article  PubMed  Google Scholar 

  14. Haїssaguerre M, Sanders P, Hocini M, Jaїs P, Clémenty J (2004) Pulmonary veins in the substrate for atrial fibrillation. The “venous wave” hypothesis. J Am Coll Cardiol 43:2290–2292

    Article  PubMed  Google Scholar 

  15. Hassink RJ, Aretz HT, Ruskin J, Keane D (2003) Morphology of atrial myocardium in human pulmonary veins. A postmortem analysis in patients with and without atrial fibrillation. J Am Coll Cardiol 42:1108–1114

    Article  PubMed  Google Scholar 

  16. Ho SY, Cabrera JA, Tran VH, Farré J, Anderson RH, Sánchez-Quintana D (2001) Architecture of the pulmonary veins: relevance to radiofrequency ablation. Heart 86:265–270

    Article  PubMed  CAS  Google Scholar 

  17. Hocini M, Sanders P, Jaїs P, Hsu L-F, Takahashi Y, Rotter M, Clémenty J, Haїssaguerre M (2004) Techniques for curative treatment of atrial fibrillation. J Cardiovasc Electrophysiol 15:1467–1471

    Article  PubMed  Google Scholar 

  18. Hodkinson HM, Pomerance A (1977) The clinical significance of senile cardiac amyloidosis: a prospective clinico-pathological study. Q J Med 46:381–387

    PubMed  CAS  Google Scholar 

  19. Hsieh M-H, Tai C-T, Tsai C-F, Yu W-C, Lee S-H, Lin Y-K, Ding Y-A, Chang M-S, Chen S-A (2000) Pulmonary vein electrogram characteristics in patients with focal sources of paroxysmal atrial fibrillation. J Cardiovasc Electrophysiol 11:953–959

    Article  PubMed  CAS  Google Scholar 

  20. Jaїs P, Haїssaguerre M, Shah DC, Chouairi S, Gencel L, Hocini M, Clémenty J (1997) A focal source of atrial fibrillation treated by discrete radiofrequency ablation. Circulation 95:572–576

    PubMed  Google Scholar 

  21. Janse MJ (1997) Why does atrial fibrillation occur? Eur Heart J 18(Suppl. C):C12–C18

    PubMed  Google Scholar 

  22. Kaye GC, Butler MG, D’Ardenne AJ, Edmondson SJ, Camm AJ, Slavin G (1986) Identification of immunoreactive atrial natriuretic peptide in atrial amyloid (letter to the editor). J Clin Pathol 39:581–582

    Article  PubMed  CAS  Google Scholar 

  23. Kholová I, Kautzner J (2003) Anatomic characteristics of extensions of atrial myocardium into the pulmonary veins in subjects with and without atrial fibrillation. Pacing Clin Electrophysiol 26:1348–1355

    Article  PubMed  Google Scholar 

  24. Kholová I, Niessen HWM (2005) Amyloid in the cardiovascular system: a review. J Clin Pathol 58:125–133

    Article  PubMed  Google Scholar 

  25. Kostin S, Klein G, Szalay Z, Hein S, Bauer EP, Schaper J (2002) Structural correlate of atrial fibrillation in human patients. Cardiovasc Res 54:361–379

    Article  PubMed  CAS  Google Scholar 

  26. Lin W-S, Prakash VS, Tai C-T, Hsieh M-H, Tsai C-F, Yu W-C, Lin Y-K, Ding Y-A, Chang M-S, Chen S-A (2000) Pulmonary vein morphology in patients with paroxysmal atrial fibrillation initiated by ectopic beats originating from the pulmonary veins. Implications for catheter ablation. Circulation 101:1274–1281

    PubMed  CAS  Google Scholar 

  27. Lloyd-Jones DM, Wang TJ, Leip EP Larson MG, Levy D, Vasan RS, D’Agostino RB, Massaro JM, Beiser A, Wolf PA, Benjamin EJ (2004) Lifetime risk for development of atrial fibrillation. The Framingham Heart Study. Circulation 110:1042–1046

    Article  PubMed  Google Scholar 

  28. Merlini G, Bellotti V (2003) Molecular mechanisms of amyloidosis. N Engl J Med 349:583–596

    Article  PubMed  CAS  Google Scholar 

  29. Moubarak JB, Rozwadowski JV, Strzalka CT, Buck WR, Tan WS, Kish GF, Kisiel T, Fronc HC, Maloney JD (2000) Pulmonary veins–left atrial junction: anatomic and histological study. Pacing Clin Electrophysiol 23:1836–1838

    PubMed  CAS  Google Scholar 

  30. Nathan H, Eliakim M (1966) The junction between the left atrium and the pulmonary veins. An anatomic study of human hearts. Circulation 34:412–422

    PubMed  CAS  Google Scholar 

  31. Nattel S (2002) New ideas about atrial fibrillation 50 years on. Nature 415:219–226

    Article  PubMed  CAS  Google Scholar 

  32. Pedersen OD, Køber L, Torp-Pedersen C (2004) Atrial fibrillation and atrial cardiomyopathy—two sides of the same coin? Am Heart J 147:953–955

    Article  PubMed  Google Scholar 

  33. Raeuschel F (1954) De arteriarum et venarum structura. Dissertatio inauguralis anatomico-physiologica. Vratislaviae, 1836. In: Purkyně JE, Opera omnia, Tomus 6—dissertation theses of Purkyně’s students. SZN, Praha, pp 165–183

  34. Röcken C, Peters B, Juenemann G, Saeger W, Klein HU, Huth Ch, Roessner A, Goette A (2002) Atrial amyloidosis. An arrhythmogenic substrate for persistent atrial fibrillation. Circulation 106:2091–2097

    Article  PubMed  Google Scholar 

  35. Roux N, Havet E, Mertl P (2004) The myocardial sleeves of the pulmonary veins: potential implications for atrial fibrillation. Surg Radiol Anat 26:285–289

    Article  PubMed  CAS  Google Scholar 

  36. Saito T, Waki K, Becker AE (2000) Left atrial myocardial extension onto pulmonary veins in humans: anatomic observations relevant for atrial arrhythmias. J Cardiovasc Electrophysiol 11:888–894

    Article  PubMed  CAS  Google Scholar 

  37. Scharf C, Sneider M, Case I, Chugh A, Lai SWK, Pelosi F, Knight BP, Kazerooni E, Morady F, Oral H (2003) Anatomy of the pulmonary veins in patients with atrial fibrillation and effects of segmental ostial ablation analyzed by computed tomography. J Cardiovasc Electrophysiol 14:150–155

    Article  PubMed  Google Scholar 

  38. Schubert D, Behl C, Lesley R, Brack A, Dargusch R, Sagara Y, Kimura H (1995) Amyloid peptides are toxic via a common oxidative mechanism. Proc Natl Acad Sci U S A 92:1989–1993

    Article  PubMed  CAS  Google Scholar 

  39. Steiner I (1984) The first description of senile cardiac amyloidosis-I Soyka, 1876, Praha. Cs Patol 20:11–13 (In Czech)

    CAS  Google Scholar 

  40. Steiner I (1987) The prevalence of isolated atrial amyloid. J Pathol 153:395–398

    Article  PubMed  CAS  Google Scholar 

  41. Steiner I (2005) A hitherto unknown priority of Jan Ev Purkyně—myocardial sleeves of the pulmonary veins. Contribution to the pathogenesis of atrial fibrillation. Cas Lek ces 144:709-710 (In Czech)

    CAS  Google Scholar 

  42. Tagawa M, Higuchi K, Chinushi M, Washizuka T, Ushiki T, Ishihara N, Aizawa Y (2001) Myocardium extending from the left atrium onto the pulmonary veins: a comparison between subjects with and without atrial fibrillation. Pacing Clin Electrophysiol 24:1459–1463

    Article  PubMed  CAS  Google Scholar 

  43. Todd DM, Skanes AC, Guiraudon G, Guiraudon C, Krahn AD, Yee R, Klein GJ (2003) Role of the posterior left atrium and pulmonary veins in human lone atrial fibrillation. Electrophysiological and pathological data from patients undergoing atrial fibrillation surgery. Circulation 108:3108–3114

    Article  PubMed  Google Scholar 

  44. Van den Bergh MP, Tjeerdsma G, de Kam PJ, Boomsma F, Crijns HJGM, van Veldhuisen DJ (2002) Longstanding atrial fibrillation causes depletion of atrial natriuretic peptide in patients with advanced congestive heart failure. Eur J Heart Fail 4:255–262

    Article  PubMed  Google Scholar 

  45. Verheule S, Wilson EE, Arora R, Engle SK, Scott LR, Olgin JE (2002) Tissue structure and connexin expression of canine pulmonary veins. Cardiovasc Res 55:727–738

    Article  PubMed  CAS  Google Scholar 

  46. Weiss C, Gocht A, Willems S, Hoffmann M, Risius T, Meinertz T (2002) Impact of the distribution and structure of myocardium in the pulmonary veins for radiofrequency ablation of atrial fibrillation. Pacing Clin Electrophysiol 25:1352–1356

    Article  PubMed  Google Scholar 

  47. Wellens HJJ (2004) Cardiac arrhythmias: the quest for a cure. A historical perspective. J Am Coll Cardiol 44:1155–1163

    PubMed  Google Scholar 

  48. Yoshihara F, Nishikimi T, Sasako Y et al (2002) Plasma atrial natriuretic peptide concentration inversely correlates with left atrial collagen volume fraction in patients with atrial fibrillation. Plasma ANP as a possible biochemical marker to predict the outcome of the maze procedure. J Am Coll Cardiol 39:288–294

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to RNDr. E. Čermáková for statistical evaluation and to Dr. J. Gosney for English edition. This study was supported by the Czech Republic Ministry of Health (Grant IGA 7592-3).

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Authors and Affiliations

  1. Fingerland Department of Pathology, Charles University Faculty of Medicine and Faculty Hospital, Hradec Králové, Czech Republic

    Ivo Steiner, Petra Hájková & Ivana Kholová

  2. First Department of Internal Medicine, Charles University Faculty of Medicine and Faculty Hospital, Hradec Králové, Czech Republic

    Jiří Kvasnička

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  1. Ivo Steiner
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Correspondence to Ivo Steiner.

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Steiner, I., Hájková, P., Kvasnička, J. et al. Myocardial sleeves of pulmonary veins and atrial fibrillation: a postmortem histopathological study of 100 subjects. Virchows Arch 449, 88–95 (2006). https://doi.org/10.1007/s00428-006-0197-2

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  • DOI: https://doi.org/10.1007/s00428-006-0197-2

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