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Normal reference values for left atrial strains and strain rates in school children assessed using two-dimensional speckle-tracking echocardiography

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Abstract

Left atrium (LA) function is a known predictive marker of heart failure in adults. Few reports of LA function analyses using LA strain (ɛ) and strain rate (SR) measurements in children exist. Thus, this study aimed to determine normal reference values for LA ɛ and SR in healthy school children and to investigate methods of interpreting LA function data based on maturational changes using two-dimensional speckle-tracking echocardiography (2DSTE). We recruited 112 healthy school children (median age 12.0 years; range 6–16 years). LA ɛ and SR were investigated using 2DSTE multi-vendor analysis software (TomTec Imaging Systems, Germany) and compared to Doppler parameters and LA volumes measured by the conventional method. The onset of the P wave was selected as the reference point for the LA ɛ analysis. Normal ranges of LA ɛ [reservoir (ɛRS), conduit (ɛCD), or contractile (ɛCT)] and positive SR (SRPOS), early negative SR (SREN), and late negative SR (SRLN) were obtained using Z-score models via the lambda-mu-sigma method. According to the Z-score curves, all ɛ showed slight falling or continuous flat lines against age, body surface area (BSA), or heart rate (HR); however, ɛ CT showed modestly positive associations with HR. As for SR, the Z-score curves showed falling lines against age and BSA. In contrast, Z-score curves for SREN and SRLN showed rising lines against HR. SREN was independent of E/e′ and was negatively correlated with LA volume indexed against BSA. This study demonstrated the normal reference values for LA ɛ and SR using 2DSTE in school children. The present results recommended that LA ɛ should be evaluated together with changes in LA SR for accurate assessment, considering maturational changes including age, BSA, and HR in school children.

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References

  1. Ghelani SJ, Brown DW, Kuebler JD, Perrin D, Shakti D, Williams DN, Marx GR, Colan SD, Geva T, Harrild DM (2017) Left atrial volumes and strain in healthy children measured by three-dimensional echocardiography: normal values and maturational changes. J Am Soc Echocardiogr 31:187–193

    PubMed  Google Scholar 

  2. Mochizuki A, Yuda S, Oi Y, Kawamukai M, Nishida J, Kouzu H, Muranaka A, Kokubu N, Shimoshige S, Hashimoto A, Tsuchihashi K, Watanabe N, Miura T (2013) Assessment of left atrial deformation and synchrony by three-dimensional speckle-tracking echocardiography: comparative studies in healthy subjects and patients with atrial fibrillation. J Am Soc Echocardiogr 26:165–174

    PubMed  Google Scholar 

  3. 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

    PubMed  Google Scholar 

  4. Brecht A, Oertelt-Prigione S, Seeland U, Rücke M, Hättasch R, Wagelöhner T, Regitz-Zagrosek V, Baumann G, Knebel F, Stangl V (2016) Left atrial function in preclinical diastolic dysfunction: two-dimensional speckle-tracking echocardiography-derived results from the BEFRI trial. J Am Soc Echocardiogr 29:750–758

    PubMed  Google Scholar 

  5. Singh A, Addetia K, Maffessanti F, Mor-Avi V, Lang RM (2017) LA Strain For Categorization of LV diastolic dysfunction. JACC Cardiovasc Imaging 10:735–743

    PubMed  Google Scholar 

  6. Xu TY, Sun JP, Lee AP, Yang XS, Ji L, Zhang Z, Li Y, Yu CM, Wang JG (2015) Left atrial function as assessed by speckle-tracking echocardiography in hypertension. Medicine (Baltimore) 94(6):e526

    Google Scholar 

  7. 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

    PubMed  Google Scholar 

  8. Uetake S, Maruyama M, Mitsuishi T, Takahashi K, Miyauchi Y, Seino Y, Shimizu W (2019) Diastolic wall strain predicts progression from paroxysmal to persistent or permanent atrial fibrillation in structurally normal hearts. J Cardiol 74:339–346

    PubMed  Google Scholar 

  9. Pathan F, D’Elia N, Nolan MT, Marwick TH, Negishi K (2017) Normal ranges of left atrial strain by speckle-tracking echocardiography: a systematic review and meta-analysis. J Am Soc Echocardiogr 30:59–70.e8

    PubMed  Google Scholar 

  10. Mor-Avi V, Lang RM, Badano LP, Belohlavek M, Cardim NM, Derumeaux G, Galderisi M, Marwick T, Nagueh SF, Sengupta PP, Sicari R, Smiseth OA, Smulevitz B, Takeuchi M, Thomas JD, Vannan M, Voigt JU, Zamorano JL (2011) Current and evolving echocardiographic techniques for the quantitative evaluation of cardiac mechanics: ASE/EAE consensus statement on methodology and indications endorsed by the Japanese society of echocardiography. Eur J Echocardiogr 12:167–205

    PubMed  Google Scholar 

  11. Miglioranza MH, Badano LP, Mihăilă S, Peluso D, Cucchini U, Soriani N, Iliceto S, Muraru D (2016) Physiologic determinants of left atrial longitudinal strain: a two-dimensional speckle-tracking and three-dimensional echocardiographic study in healthy volunteers. J Am Soc Echocardiogr 29:1023–1034.e3

    PubMed  Google Scholar 

  12. Sugimoto T, Robinet S, Dulgheru R, Bernard A, Ilardi F, Contu L, Addetia K, Caballero L, Kacharava G, Athanassopoulos GD, Barone D, Baroni M, Cardim N, Hagendorff A, Hristova K, Lopez T, De La Morena G, Popescu BA, Penicka M, Ozyigit T, Rodrigo Carbonero JD, Van De Veire N, Von Bardeleben RS, Vinereanu D, Zamorano JL, Go YY, Marchetta S, Nchimi A, Rosca M, Calin A, Moonen M, Cimino S, Magne J, Cosyns B, Galli E, Donal E, Habib G, Esposito R, Galderisi M, Badano LP, Lang RM, Lancellotti P (2018) Echocardiographic reference ranges for normal left atrial function parameters: results from the EACVI NORRE study. Eur Heart J Cardiovasc Imaging 19:630–638

    PubMed  Google Scholar 

  13. Kutty S, Padiyath A, Li L, Peng Q, Rangamani S, Schuster A, Danford DA (2013) Functional maturation of left and right atrial systolic and diastolic performance in infants, children, and adolescents. J Am Soc Echocardiogr 26:398–409.e2

    PubMed  Google Scholar 

  14. Du Bois D, Du Bois EF (1916) Clinical calorimetry: tenth paper a formula to estimate the approximate surface area if height and weight be known. Arch Intern Med XVII:863–871

    Google Scholar 

  15. Porter TR, Shillcutt SK, Adams MS, Desjardins G, Glas KE, Olson JJ, Troughton RW (2015) Guidelines for the use of echocardiography as a monitor for therapeutic intervention in adults: a report from the American society of echocardiography. J Am Soc Echocardiogr 28:40–56

    PubMed  Google Scholar 

  16. 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. J Am Soc Echocardiogr 28:1–39.e14

    PubMed  Google Scholar 

  17. Lopez L, Colan SD, Frommelt PC, Ensing GJ, Kendall K, Younoszai AK, Lai WW, Geva T (2010) Recommendations for quantification methods during the performance of a pediatric echocardiogram: a report from the Pediatric Measurements Writing Group of the American Society of Echocardiography Pediatric and Congenital Heart Disease Council. J Am Soc Echocardiogr 23:465–495

    PubMed  Google Scholar 

  18. Cole TJ, Green PJ (1992) Smoothing reference centile curves: The LMS method and penalized likelihood. Stat Med 11:1305–1319

    CAS  PubMed  Google Scholar 

  19. Kobayashi T, Fuse S, Sakamoto N, Mikami M, Ogawa S, Hamaoka K, Arakaki Y, Nakamura T, Nagasawa H, Kato T, Jibiki T, Iwashima S, Yamakawa M, Ohkubo T, Shimoyama S, Aso K, Sato S, Saji T, Z Score Project Investigators (2016) A new Z score curve of the coronary arterial internal diameter using the lambda-mu-sigma method in a pediatric population. J Am Soc Echocardiogr 29:794–801.e29

    PubMed  Google Scholar 

  20. Kanda Y (2013) Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Transpl 48:452–458

    CAS  Google Scholar 

  21. Cantinotti M, Scalese M, Giordano R, Franchi E, Assanta N, Molinaro S, Iervasi G, Santoro G, Koestenberger M, Kutty S (2019) Left and right atrial strain in healthy caucasian children by two-dimensional speckle-tracking echocardiography. J Am Soc Echocardiogr 32:165–168.e3

    PubMed  Google Scholar 

  22. Di Salvo G, Drago M, Pacileo G, Rea A, Carrozza M, Santoro G, Bigazzi MC, Caso P, Russo MG, Carminati M, Calabro R (2005) Atrial function after surgical and percutaneous closure of atrial septal defect: A strain rate imaging study. J Am Soc Echocardiogr 18:930–933

    PubMed  Google Scholar 

  23. Shakti D, Friedman KG, Harrild DM, Gauvreau K, Geva T, Colan SD, Brown DW (2018) Left atrial size and function in patients with congenital aortic valve stenosis. Am J Cardiol 122:1541–1545

    PubMed  Google Scholar 

  24. Kang SJ, Ha J, Hwang SJ, Kim HJ (2018) Long term outcomes of left atrial reservoir function in children with a history of Kawasaki disease. J Cardiovasc Ultrasound 26:26–32

    PubMed  PubMed Central  Google Scholar 

  25. Hope KD, Wang Y, Banerjee MM, Montero AE, Pandian NG, Banerjee A (2019) Left atrial mechanics in children: insights from new applications of strain imaging. Int J Cardiovasc Imaging 35:57–65

    PubMed  Google Scholar 

  26. Khoo NS, Smallhorn JF, Kaneko S, Kutty S, Altamirano L, Tham EB (2013) The assessment of atrial function in single ventricle hearts from birth to Fontan: a speckle-tracking study by using strain and strain rate. J Am Soc Echocardiogr 26:756–764

    PubMed  Google Scholar 

  27. Ishizaki U, Nagao M, Shiina Y, Inai K, Mori H, Takahashi T, Sakai S (2019) Global strain and dyssynchrony of the single ventricle predict adverse cardiac events after the Fontan procedure: analysis using feature-tracking cine magnetic resonance imaging. J Cardiol 73:163–170

    PubMed  Google Scholar 

  28. Zhang C, Deng Y, Liu Y, Xu Y, Liu Y, Zhang L, Chen X, Xie M, Ge S (2018) Preclinical cardiovascular changes in children with obesity: a real-time 3-dimensional speckle tracking imaging study. PLoS ONE 13(10):e0205177

    PubMed  PubMed Central  Google Scholar 

  29. D’Ascenzi F, Anselmi F, Focardi M, Mondillo S (2018) Atrial enlargement in the athlete’s heart: assessment of atrial function may help distinguish adaptive from pathologic remodeling. J Am Soc Echocardiogr 31:148–157

    PubMed  Google Scholar 

  30. Genovese D, Singh A, Volpato V, Kruse E, Weinert L, Yamat M, Mor-Avi V, Addetia K, Lang RM (2018) Load dependency of left atrial strain in normal subjects. J Am Soc Echocardiogr 31:1221–1228

    PubMed  PubMed Central  Google Scholar 

  31. Burns AT, La Gerche A, D’hooge J, Macisaac AI, Prior DL (2010) Left ventricular strain and strain rate: characterization of the effect of load in human subjects. Eur J Echocardiogr 11:283–289

    PubMed  Google Scholar 

  32. 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

    PubMed  Google Scholar 

  33. Okamatsu K, Takeuchi M, Nakai H, Nishikage T, Salgo IS, Husson S, Otsuji Y, Lang RM (2009) Effects of aging on left atrial function assessed by two-dimensional speckle tracking echocardiography. J Am Soc Echocardiogr 22:70–75

    PubMed  Google Scholar 

  34. Sakata M, Hayabuchi Y, Inoue M, Onishi T, Kagami S (2013) Left atrial volume change throughout the cardiac cycle in children with congenital heart disease associated with increased pulmonary blood flow: evaluation using a novel left atrium-tracking method. Pediatr Cardiol 34:105–111

    PubMed  Google Scholar 

  35. Rimbaş RC, Mihăilă S, Vinereanu D (2016) Sources of variation in assessing left atrial functions by 2D speckle-tracking echocardiography. Heart Vessels 31:370–381

    PubMed  Google Scholar 

  36. Tanaka S, Noda T, Kawasaki M, Segawa T, Tsugita N, Fuseya T, Kubota T, Iwama M, Nishigaki K, Watanabe S, Minagawa T, Ohashi H, Minatoguchi S (2019) Relationship between electrical conduction and phasic left atrial function: P-wave signal-averaged electrocardiography and time-left atrial volume curve assessments using two-dimensional speckle-tracking echocardiography. Heart Vessels 34:1212–1220

    PubMed  Google Scholar 

  37. de Waal K, Phad N, Boyle A (2018) Left atrium function and deformation in very preterm infants with and without volume load. Echocardiography 35:1818–1826

    PubMed  Google Scholar 

  38. Sabatino J, Di SG, Prota C, Bucciarelli V, Josen M, Paredes J, Borrelli N, Sirico D, Prasad S, Indolfi C, Fraisse A, Daubeney PEF (2019) Left atrial strain to identify diastolic dysfunction in children with cardiomyopathies. J Clin Med 8(8):E1243

    PubMed  Google Scholar 

  39. Cantinotti M, Lopez L (2013) Nomograms for blood flow and tissue Doppler velocities to evaluate diastolic function in children: a critical review. J Am Soc Echocardiogr 26:126–141

    PubMed  Google Scholar 

  40. Cantinotti M, Giordano R, Scalese M, Murzi B, Assanta N, Spadoni I, Crocetti M, Marotta M, Molinaro S, Kutty S, Iervasi G (2016) Nomograms for mitral inflow Doppler and tissue Doppler velocities in Caucasian children. J Cardiol 68:288–299

    PubMed  Google Scholar 

  41. Dallaire F, Slorach C, Hui W, Sarkola T, Friedberg MK, Bradley TJ, Jaeggi E, Dragulescu A, Har RLH, Cherney DZI, Mertens L (2015) Reference values for pulse wave doppler and tissue doppler imaging in pediatric echocardiography. Circ Cardiovasc Imaging 8:1–9

    Google Scholar 

  42. Masutani S, Saiki H, Kurishima C, Kuwata S, Tamura M, Senzaki H (2014) Assessment of ventricular relaxation and stiffness using early diastolic mitral annular and inflow velocities in pediatric patients with heart disease. Heart Vessels 29:825–833

    PubMed  Google Scholar 

  43. Cameli M, Sparla S, Losito M, Righini FM, Menci D, Lisi M, D’Ascenzi F, Focardi M, Favilli R, Pierli C, Fineschi M, Mondillo S (2016) Correlation of left atrial strain and Doppler measurements with invasive measurement of left ventricular end-diastolic pressure in patients stratified for different values of ejection fraction. Echocardiography 33:398–405

    PubMed  Google Scholar 

  44. Takahashi K, Nii M, Takigiku K, Toyono M, Iwashima S, Inoue N, Tanaka N, Matsui K, Shigemitsu S, Yamada M, Kobayashi M, Yazaki K, Itatani K, Shimizu T (2019) Development of suction force during early diastole from the left atrium to the left ventricle in infants, children, and adolescents. Heart Vessels 34:296–306

    PubMed  Google Scholar 

  45. Hayashi S, Yamada H, Bando M, Saijo Y, Nishio S, Hirata Y, Klein AL, Sata M (2015) Optimal analysis of left atrial strain by speckle tracking echocardiography: P-wave versus R-wave trigger. Echocardiography 32:1241–1249

    PubMed  Google Scholar 

  46. Ryan L (2019) Four papers on child growth modelling. Stat Med 38:3505–3506

    PubMed  PubMed Central  Google Scholar 

  47. Martinez-Millana A, Hulst JM, Boon M, Witters P, Fernandez-Llatas C, Asseiceira I, Calvo-Lerma J, Basagoiti I, Traver V, De Boeck K, Ribes-Koninckx C (2018) Optimisation of children z-score calculation based on new statistical techniques. PLoS ONE 13(12):e0208362

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Masashi Mikami, MS, for his statistical support with the Z-score models.

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Authors and Affiliations

  1. Department of Pediatric and Child Health, Nihon University School of Medicine, 30-1 Ohyaguchi-kamicho, Itabashi-ku, Tokyo, 173-8610, Japan

    Shino Jimbo, Nobutaka Noto, Hirotsugu Okuma, Masataka Kato, Akiko Komori, Mamoru Ayusawa & Ichiro Morioka

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  1. Shino Jimbo
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  2. Nobutaka Noto
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  3. Hirotsugu Okuma
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  4. Masataka Kato
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Correspondence to Shino Jimbo.

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Jimbo, S., Noto, N., Okuma, H. et al. Normal reference values for left atrial strains and strain rates in school children assessed using two-dimensional speckle-tracking echocardiography. Heart Vessels 35, 1270–1280 (2020). https://doi.org/10.1007/s00380-020-01594-0

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