Abstract
Left atrial (LA) functional remodeling as well as LA structural remodeling are associated with incident LA appendage (LAA) thrombus formation. This study aimed to elucidate whether combined assessment of LA functional and structural remodeling can predict LAA dysfunction and recurrent cerebrovascular events in patients with acute ischemic stroke. We performed transthoracic and transesophageal echocardiography in 196 patients within 7 days after acute ischemic stroke. Peak systolic LA strain was evaluated using 2D speckle tracking imaging. We defined the ratio of LA peak systolic strain to LA volume index (LAVI) as the LA remodeling index (LARI). All patients were prospectively followed for recurrent cerebrovascular events. We divided patients into four groups according based on the LARI quartile. LAA dysfunction increased with decreasing LARI. In total, 52 recurrent cerebrovascular events were noted during the median follow-up period of 700 days. Patients with recurrent cerebrovascular events had lower LARI than those without recurrent events (0.50 ± 0.45 vs. 1.10 ± 0.95, P < 0.001). Kaplan–Meier analysis showed that patients with lower LARI were more susceptible to recurrent cerebrovascular events than those with higher LARI. Multivariate Cox proportional hazard regression analysis showed that LARI was an independent predictor of recurrent cerebrovascular events after adjustment for confounding factors. Net reclassification index improved with the addition of LARI to basic predictors. LARI is a novel feasible parameter for LAA dysfunction and can predict recurrent cerebrovascular events in patients with acute ischemic stroke.
Similar content being viewed by others
References
National Institute of Neurological Disorders and Stroke (1990) Special report from National Institute of Neurological Disorders and Stroke. Classification of cerebrovascular diseases III. Stroke 21:637–676
Cooper R, Cutler J, Desvigne-Nickens P, Fortmann SP, Friedman L, Havlik R, Hogelin G, Marler J, McGovern P, Morosco G, Mosca L, Pearson T, Stamler J, Stryer D, Thom T (2000) Trend and disparities in coronary heart disease, stroke, and other cardiovascular diseases in the United States: findings of the national conference on cardiovascular disease prevention. Circulation 102:3137–3147
Benjamin EJ, Wolf PA, D'Agostino RB, Silbershatz H, Kannel WB, Levy D (1998) Impact of atrial fibrillation on the risk of death: the Framingham Heart Study. Circulation 98:946–952
Takada T, Yasaka M, Nagatsuka K, Minematsu K, Yamaguchi T (2001) Blood flow in the left atrial appendage and embolic stroke in non-valvular atrial fibrillation. Eur Neurol 46:148–152
García-Fernández MA, Torrecilla EG, San Román D, Azevedo J, Bueno H, Moreno MM, Delcán JL (1992) Left atrial appendage Doppler flow patterns: implications on thrombus formation. Am Heart J 124:955–961
Kamp O, Verhorst PM, Welling RC, Visser CA (1999) Importance of left atrial appendage flow as a predictor of thromboembolic events in patients with atrial fibrillation. Eur Heart J 20:979–985
Verhorst PM, Kamp O, Visser CA, Verheugt FW (1993) Left atrial appendage flow velocity assessment using transesophageal echocardiography in nonrheumatic atrial fibrillation and systemic embolism. Am J Cardiol 71:192–196
Sparks PB, Mond HG, Vohra JK, Yapanis AG, Grigg LE, Kalman JM (1999) Mechanical remodeling of the left atrium after loss of atrioventricular synchrony: a long-term study in humans. Circulation 100:1714–1721
Sasaki S, Watanabe T, Tamura H, Nishiyama S, Wanezaki M, Sato C, Yamaura G, Ishino M, Arimoto T, Takahashi H, Shishido T, Miyamoto T, Kubota I (2014) Left atrial strain as evaluated by two-dimensional speckle tracking predicts left atrial appendage dysfunction in patients with acute ischemic stroke. BBA Clin 2:40–47
Cameli M, Lunghetti S, Mandoli GE, Righini FM, Lisi M, Curci V, Tommaso CD, Solari M, Nistor D, Gismondi A, Focardi M, Favilli R, Mondillo S (2017) Left atrial strain predicts pro-thrombotic state in patients with non-valvular atrial fibrillation. J Atr Fibrillation 10:1641
Kupczynska K, Michalski BW, Miskowiec D, Kasprzak JD, Wejner-Mik P, Wdowiak-Okrojek K, Lipiec P (2017) Association between left atrial function assessed by speckle-tracking echocardiography and the presence of left atrial appendage thrombus in patients with atrial fibrillation. Anatol J Cardiol 18:15–22
Tamura H, Watanabe T, Nishiyama S, Sasaki S, Arimoto T, Takahashi H, Shishido T, Miyashita T, Miyamoto T, Nitobe J, Hirono O, Kubota I (2011) Increased left atrial volume index predicts a poor prognosis in patients with heart failure. J Card Fail 17:210–216
Hoit BD (2014) Left atrial size and function: role in prognosis. J Am Coll Cardiol 63:493–505
Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, Lancellotti P, Muraru D, Picard MH, Rietzschel ER, Rudski L, Spencer KT, Tsang W, Voigt JU (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 16:233–270
Itoh T, Kimura M, Tomita H, Sasaki S, Owada S, Horiuchi D, Sasaki K, Ishida Y, Kinjo T, Okumura K (2016) Reduced residual conduction gaps and favourable outcome in contact force-guided circumferential pulmonary vein isolation. Europace 18:531–537
Zabalgoitia M, Halperin JL, Pearce LA, Blackshear JL, Asinger PW, Hart RG (1998) Transesophageal echocardiographic correlates of clinical risk of thromboembolism in nonvalvular atrial fibrillation. J Am Coll Cardiol 31:1622–1626
Fatkin D, Kelly RP, Feneley MP (1994) Relationship between left atrial appendage blood flow velocity, spontaneous echocardiographic contrast and thromboembolic risk in vivo. J Am Coll Cardiol 23:961–969
Vianna-Pinton R, Moreno CA, Baxter CM, Lee KS, Tsang TS, Appleton CP (2009) Two-dimensional speckle-tracking echocardiography of the left atrium: feasibility and regional contraction and relaxation differences in normal subjects. J Am Soc Echocardiogr 22:299–305
Matsuo S, Imai E, Horio M, Yasuda Y, Tomita K, Nitta K, Yamagata K, Tomino Y, Yokoyama H, Hishida A, Collaborators developing the Japanese equation for estimated GFR (2009) Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis 53:982–992
Russo C, Jin Z, Liu R, Iwata S, Tugcu A, Yoshita M, Homma S, Elkind MS, Rundek T, Decarli C, Wright CB, Sacco RL, Di Tullio MR (2013) LA volumes and reservoir function are associated with subclinical cerebrovascular disease: the CABL (cardiovascular abnormalities and brain lesions) study. JACC Cardiovasc Imaging 6:313–323
To AC, Flamm SD, Marwick TH, Klein AL (2011) Clinical utility of multimodality LA imaging: assessment of size, function, and structure. JACC Cardiovasc Imaging 4:788–798
Leitman M, Lysyansky P, Sidenko S, Shir V, Peleg E, Binenbaum M, Kaluski E, Krakover R, Vered Z (2004) Two-dimensional strain — a novel software for real-time quantitative echocardiographic assessment of myocardial function. J Am Soc Echocardiogr 17:1021–1029
Leung M, van Rosendael PJ, Abou R, Ajmone Marsan N, Leung DY, Delgado V, Bax JJ (2018) Left atrial function to identify patients with atrial fibrillation at high risk of stroke: new insights from a large registry. Eur Heart J 39:1416–1425
Zhu MR, Wang M, Ma XX, Zheng DY, Zhang YL (2018) The value of left atrial strain and strain rate in predicting left atrial appendage stasis in patients with nonvalvular atrial fibrillation. Cardiol J 25:87–96
Kim D, Shim CY, Hong GR, Kim MH, Seo J (2016) Clinical implications and determinants of left atrial mechanical dysfunction in patients with stroke. Stroke 47:1444–1451
Ciuffo L, Inoue YY, Tao S, Gucuk Ipek E, Balouch M, Lima JAC, Nazarian S, Spragg DD, Marine JE, Berger RD, Calkins H, Ashikaga H (2018) Mechanical dyssynchrony of the left atrium during sinus rhythm is associated with history of stroke in patients with atrial fibrillation. Eur Heart J Cardiovasc Imaging 19:433–441
Benjamin EJ, D'Agostino RB, Belanger AJ, Wolf PA, Levy D (1995) Left atrial size and the risk of stroke and death. The Framingham Heart Study. Circulation 92:835–841
Kizer JR, Bella JN, Palmieri V, Liu JE, Best LG, Lee ET, Roman MJ, Devereux RB (2006) Left atrial diameter as an independent predictor of first clinical cardiovascular events in middle-aged and elderly adults: the Strong Heart Study (SHS). Am Heart J 151:412–418
Tsang TS, Abhayaratna WP, Barnes ME, Miyasaka Y, Gersh BJ, Bailey KR, Cha SS, Seward JB (2006) Prediction of cardiovascular outcomes with left atrial size: is volume superior to area or diameter? J Am Coll Cardiol 47:1018–1023
Sirbu C, Herbots L, D'hooge J, Claus P, Marciniak A, Langeland T, Bijnens B, Rademakers FE, Sutherland GR (2006) Feasibility of strain and strain rate imaging for the assessment of regional left atrial deformation: a study in normal subjects. Eur J Echocardiogr 7:199–208
Morris DA, Belyavskiy E, Aravind-Kumar R, Kropf M, Frydas A, Braunauer K, Marquez E, Krisper M, Lindhorst R, Osmanoglou E, Boldt LH, Blaschke F, Haverkamp W, Tschöpe C, Edelmann F, Pieske B, Pieske-Kraigher E (2018) Potential usefulness and clinical relevance of adding left atrial strain to left atrial volume index in the detection of left ventricular diastolic dysfunction. JACC Cardiovasc Imaging 11:1405–1415
Kuppahally SS, Akoum N, Burgon NS, Badger TJ, Kholmovski EG, Vijayakumar S, Rao SN, Blauer J, Fish EN, Dibella EV, Macleod RS, McGann C, Litwin SE, Marrouche NF (2010) Left atrial strain and strain rate in patients with paroxysmal and persistent atrial fibrillation: relationship to left atrial structural remodeling detected by delayed-enhancement MRI. Circ Cardiovasc Imaging 3:231–239
Allessie M, Ausma J, Schotten U (2002) Electrical, contractile and structural remodeling during atrial fibrillation. Cardiovasc Res 54:230–246
Manolio TA, Kronmal RA, Burke GL, O'Leary DH, Price TR (1996) Short-term predictors of incident stroke in older adults. The Cardiovascular Health Study. Stroke 27:1479–1486
Lodder J, Bamford JM, Sandercock PA, Jones LN, Warlow CP (1990) Are hypertension or cardiac embolism likely causes of lacunar infarction? Stroke 21:375–381
Piccini JP, Daubert JP (2011) Atrial fibrillation and stroke: it’s not necessarily all about the rhythm. Heart Rhythm 8:1424–1425
Chen PS, Chen LS, Fishbein MC, Lin SF, Nattel S (2014) Role of the autonomic nervous system in atrial fibrillation: pathophysiology and therapy. Circ Res 114:1500–1515
Kamel H, Okin PM, Elkind MS, Iadecola C (2016) Atrial Fibrillation and Mechanisms of Stroke: Time for a New Model. Stroke 47:895–900
Acknowledgements
We would like to thank the staff at the Department of Cardiology, Pulmonology, and Nephrology, Yamagata University School of Medicine for their cooperation during this study. We would like to thank Editage (www.editage.jp) for English language editing.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hashimoto, N., Watanabe, T., Tamura, H. et al. Left atrial remodeling index is a feasible predictor of poor prognosis in patients with acute ischemic stroke. Heart Vessels 34, 1936–1943 (2019). https://doi.org/10.1007/s00380-019-01445-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00380-019-01445-7