Korean Circ J.  2019 Oct;49(10):908-931. 10.4070/kcj.2019.0200.

Two-dimensional Echocardiographic Assessment of Myocardial Strain: Important Echocardiographic Parameter Readily Useful in Clinical Field

• Park JH

• KMID: 2457999
• DOI: http://doi.org/10.4070/kcj.2019.0200

Abstract

Echocardiography is the first and is the most-available imaging modality for many cardiovascular diseases, and echocardiographic parameters can give much important information for diagnosis, treatment, and prognostic evaluations. Left ventricular ejection fraction (LVEF) is the most commonly used echocardiographic parameter for left ventricular (LV) systolic function. Although LVEF is used routinely in daily practice, it is calculated from volumetric change without representing true myocardial properties. Recently, strain echocardiography has been used to objectively measure myocardial deformation. Myocardial strain can give accurate information about intrinsic myocardial function, and it can be used to detect early-stage cardiovascular diseases, monitor myocardial changes with specific therapies, differentiate cardiomyopathies, and predict the prognosis of several cardiovascular diseases. Although strain echocardiography has been applied to measure the right ventricle and left atrium, in addition to analyzing the LV, many cardiologists who are not imaging specialists are unaware of its clinical use and importance. Therefore, this review describes the measurement and clinical utility of 2-dimensional strain analysis in various cardiovascular diseases.

Keyword

Echocardiography, Strain; Prognosis; Diagnosis; Left ventricle; Right ventricle

MeSH Terms

Cardiomyopathies
Cardiovascular Diseases
Diagnosis
Echocardiography*
Heart Atria
Heart Ventricles
Prognosis
Specialization
Stroke Volume

Figure

• 

  Figure 1 Multidimensional strain measurement analysis by 2DSTE in a healthy individual. Arrows denote the direction of movements. Myocardial shortening shows in the longitudinal (A), circumferential (B), and radial directions (C). Myocardial contraction in the longitudinal and circumferential directions during the systolic period represents a negative strain value, and thickening and lengthening in the radial direction shows a positive strain value. 2DSTE = 2-dimensional strain echocardiography.

• 

  Figure 2 A demonstration of 3 different algorithms in a healthy individual. (A) EchoPAC PC software (GE Medical Systems, Milwaukee, WI, USA), (B) VVI (Siemens Medical Solutions, Mountain View, CA, USA), and (C) Tomtec software (Image Arena 4.6; TOMTEC Imaging Systems, Munich, Germany) are the 3 most commonly used algorithms in 2-dimensional speckle tracking echocardiography. Note the vendor differences in the measurement of GLS. GLS = global longitudinal strain; VVI = velocity vector imaging.

• 

  Figure 3 Demonstration of a 2-dimensional strain analysis with GE EchoPAC PC software. After tracing of the endocardial border, the software provides global and regional myocardial strain values automatically in apical 4 chamber (A), apical 2 chamber (B), and apical 3 chamber views (C). The GE EchoPAC algorithm can provide bull's eye maps of regional longitudinal strain values (D).

• 

  Figure 4 Two-dimensional speckle tracking echocardiography can produce bull's eye maps that show specific ischemia patterns in patients with ischemic heart disease of the LAD (A), the LCX (B), and the RCA (C). LAD = left anterior descending coronary artery; LCX = left circumflex coronary artery; RCA = right coronary artery.

• 

  Figure 5 The trend of GLS with treatment of HF in a patient with anthracycline- and trastuzumab-induced cardiotoxicity. GLS was −8.3% at initial presentation (A), improved after 3 months (−13.0%, B), and 6 months of HF management (−17.1%, C) (adapted and modified from Jung MH et al.57) with permission). GLS = global longitudinal strain; HF = heart failure.

• 

  Figure 6 Representative peak longitudinal strain echocardiographic bull's eye maps from patients with various diseases and a healthy person. (A) Healthy. (B) An athlete with compensatory mild left ventricular hypertrophy and a normal strain plot. (C) Cardiac amyloidosis showing severely reduced strain in the basal and midventricular segments with preservation of the apical segments. (D) Hypertensive heart disease with thickened myocardium. (E) Hypertrophic cardiomyopathy involving the whole ventricle. (F) Apical hypertrophic cardiomyopathy, with reduced strain in the apical segments.

• 

  Figure 7 Typical echocardiography features in a patient with cardiac amyloidosis. Thickened left ventricular wall, up to 14 mm on the conventional echocardiographic study (A). In this representative bull's eye map of longitudinal strain by speckle tracking echocardiography (B), the longitudinal strain of the apex is preserved, in contrast to those of the other midventricular or basal segments, suggesting ‘apical sparing’ or a ‘cherry-on-top’ pattern. GLS = global longitudinal strain.

• 

  Figure 8 A demonstration of the 2 different methods used to measure RV strain. RVGLS can be measured from the RVGLStotal (A) or from the RVGLSfree wall (B). RV = right ventricular; RVGLS = right ventricular global longitudinal strain.

• 

  Figure 9 Demonstration of longitudinal strain in the right ventricle of a patient with acute pulmonary embolism before (A) and after treatment (B). Before treatment, midventricular strain (arrows) decreased, as did the RVGLStotal (A). The midventricular strain (arrowheads) and RVGLStotal improved after treatment. RVGLS = right ventricular global longitudinal strain.

• 

  Figure 10 A left atrial strain analysis using 2DSTE in a healthy adult (A) and an illustration of the 3 phases of LA function (B) with an R-R gating analysis. LA = left atrium; PACS = peak atrial contraction strain; PALS = peak atrial longitudinal strain; 2DSTE = 2-dimensional strain echocardiography.

Reference

1. Kümler T, Gislason GH, Køber L, Torp-Pedersen C. Persistence of the prognostic importance of left ventricular systolic function and heart failure after myocardial infarction: 17-year follow-up of the TRACE register. Eur J Heart Fail. 2010; 12:805–811.

2. Joyce E, Hoogslag GE, Leong DP, et al. Association between left ventricular global longitudinal strain and adverse left ventricular dilatation after ST-segment-elevation myocardial infarction. Circ Cardiovasc Imaging. 2014; 7:74–81.

3. Ponikowski P, Voors AA, Anker SD, et al. 2016 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the task force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC)developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J. 2016; 37:2129–2200.

4. Lee JH, Kim MS, Kim EJ, et al. KSHF guidelines for the management of acute heart failure: part I. definition, epidemiology and diagnosis of acute heart failure. Korean Circ J. 2019; 49:1–21.

5. Yancy CW, Jessup M, Bozkurt B, et al. 2016 ACC/AHA/HFSA focused update on new pharmacological therapy for heart failure: an update of the 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology/American Heart Association task force on clinical practice guidelines and the Heart Failure Society of America. J Am Coll Cardiol. 2016; 68:1476–1488.

6. Baumgartner H, Falk V, Bax JJ, et al. 2017 ESC/EACTS guidelines for the management of valvular heart disease. Eur Heart J. 2017; 38:2739–2791.

7. Nishimura RA, Otto CM, Bonow RO, et al. 2017 AHA/ACC focused update of the 2014 AHA/ACC guideline for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association task force on clinical practice guidelines. Circulation. 2017; 135:e1159–95.

8. Lee JY, Sunwoo JS, Kwon KY, et al. Left ventricular ejection fraction predicts poststroke cardiovascular events and mortality in patients without atrial fibrillation and coronary heart disease. Korean Circ J. 2018; 48:1148–1156.

9. Otterstad JE, Froeland G, St John Sutton M, Holme I. Accuracy and reproducibility of biplane two-dimensional echocardiographic measurements of left ventricular dimensions and function. Eur Heart J. 1997; 18:507–513.

10. Smiseth OA, Torp H, Opdahl A, Haugaa KH, Urheim S. Myocardial strain imaging: how useful is it in clinical decision making? Eur Heart J. 2016; 37:1196–1207.

11. Haddad F, Hunt SA, Rosenthal DN, Murphy DJ. Right ventricular function in cardiovascular disease, part I: anatomy, physiology, aging, and functional assessment of the right ventricle. Circulation. 2008; 117:1436–1448.

12. Keramida K, Farmakis D, Bingcang J, et al. Longitudinal changes of right ventricular deformation mechanics during trastuzumab therapy in breast cancer patients. Eur J Heart Fail. 2019; 21:529–535.

13. Negishi K, Negishi T, Haluska BA, Hare JL, Plana JC, Marwick TH. Use of speckle strain to assess left ventricular responses to cardiotoxic chemotherapy and cardioprotection. Eur Heart J Cardiovasc Imaging. 2014; 15:324–331.

14. Phelan D, Thavendiranathan P, Popovic Z, et al. Application of a parametric display of two-dimensional speckle-tracking longitudinal strain to improve the etiologic diagnosis of mild to moderate left ventricular hypertrophy. J Am Soc Echocardiogr. 2014; 27:888–895.

15. Negishi K, Negishi T, Hare JL, Haluska BA, Plana JC, Marwick TH. Independent and incremental value of deformation indices for prediction of trastuzumab-induced cardiotoxicity. J Am Soc Echocardiogr. 2013; 26:493–498.

16. Lang RM, Badano LP, Mor-Avi V, et al. 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. 2015; 28:1–39.e14.

17. Marwick TH. Measurement of strain and strain rate by echocardiography: ready for prime time? J Am Coll Cardiol. 2006; 47:1313–1327.

18. Gorcsan J 3rd, Tanaka H. Echocardiographic assessment of myocardial strain. J Am Coll Cardiol. 2011; 58:1401–1413.

19. Collier P, Phelan D, Klein A. A test in context: myocardial strain measured by speckle-tracking echocardiography. J Am Coll Cardiol. 2017; 69:1043–1056.

20. Farsalinos KE, Daraban AM, Ünlü S, Thomas JD, Badano LP, Voigt JU. Head-to-head comparison of global longitudinal strain measurements among nine different vendors: the EACVI/ASE inter-vendor comparison study. J Am Soc Echocardiogr. 2015; 28:1171–1181.

21. Cho GY, Chan J, Leano R, Strudwick M, Marwick TH. Comparison of two-dimensional speckle and tissue velocity based strain and validation with harmonic phase magnetic resonance imaging. Am J Cardiol. 2006; 97:1661–1666.

22. Sarvari SI, Haugaa KH, Anfinsen OG, et al. Right ventricular mechanical dispersion is related to malignant arrhythmias: a study of patients with arrhythmogenic right ventricular cardiomyopathy and subclinical right ventricular dysfunction. Eur Heart J. 2011; 32:1089–1096.

23. Zamorano JL, Lancellotti P, Rodriguez Muñoz D, et al. 2016 ESC position paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for practice guidelines: the task force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). Eur J Heart Fail. 2017; 19:9–42.

24. Kim H, Chung WB, Cho KI, et al. Diagnosis, treatment, and prevention of cardiovascular toxicity related to anti-cancer treatment in clinical practice: an opinion paper from the working group on cardio-oncology of the Korean Society of Echocardiography. J Cardiovasc Ultrasound. 2018; 26:1–25.

25. Lee JH, Park JH, Park SW, et al. Current awareness and use of the strain echocardiography in routine clinical practices: result of a nationwide survey in Korea. J Cardiovasc Ultrasound. 2017; 25:91–97.

26. Marwick TH, Leano RL, Brown J, et al. Myocardial strain measurement with 2-dimensional speckle-tracking echocardiography: definition of normal range. JACC Cardiovasc Imaging. 2009; 2:80–84.

27. Park JH, Lee JH, Lee SY, et al. Normal 2-dimensional strain values of the left ventricle: a substudy of the normal echocardiographic measurements in Korean population study. J Cardiovasc Ultrasound. 2016; 24:285–293.

28. Yingchoncharoen T, Agarwal S, Popović ZB, Marwick TH. Normal ranges of left ventricular strain: a meta-analysis. J Am Soc Echocardiogr. 2013; 26:185–191.

29. Sugimoto T, Dulgheru R, Bernard A, et al. Echocardiographic reference ranges for normal left ventricular 2D strain: results from the EACVI NORRE study. Eur Heart J Cardiovasc Imaging. 2017; 18:833–840.

30. Takigiku K, Takeuchi M, Izumi C, et al. Normal range of left ventricular 2-dimensional strain: Japanese ultrasound speckle tracking of the left ventricle (JUSTICE) study. Circ J. 2012; 76:2623–2632.

31. Mora V, Roldán I, Romero E, et al. Comprehensive assessment of left ventricular myocardial function by two-dimensional speckle-tracking echocardiography. Cardiovasc Ultrasound. 2018; 16:16.

32. Biering-Sørensen T, Hoffmann S, Mogelvang R, et al. Myocardial strain analysis by 2-dimensional speckle tracking echocardiography improves diagnostics of coronary artery stenosis in stable angina pectoris. Circ Cardiovasc Imaging. 2014; 7:58–65.

33. Sjøli B, Ørn S, Grenne B, Ihlen H, Edvardsen T, Brunvand H. Diagnostic capability and reproducibility of strain by Doppler and by speckle tracking in patients with acute myocardial infarction. JACC Cardiovasc Imaging. 2009; 2:24–33.

34. Bertini M, Mollema SA, Delgado V, et al. Impact of time to reperfusion after acute myocardial infarction on myocardial damage assessed by left ventricular longitudinal strain. Am J Cardiol. 2009; 104:480–485.

35. Kim KH, Na SH, Park JS. Role of quantitative wall motion analysis in patients with acute chest pain at emergency department. J Cardiovasc Ultrasound. 2017; 25:20–27.

36. Park YH, Kang SJ, Song JK, et al. Prognostic value of longitudinal strain after primary reperfusion therapy in patients with anterior-wall acute myocardial infarction. J Am Soc Echocardiogr. 2008; 21:262–267.

37. Lee SH, Lee SR, Rhee KS, Chae JK, Kim WH. Usefulness of myocardial longitudinal strain in prediction of heart failure in patients with successfully reperfused anterior wall ST-segment elevation myocardial infarction. Korean Circ J. 2019; 49:e69.

38. Choi SW, Park JH, Sun BJ, et al. Impaired two-dimensional global longitudinal strain of left ventricle predicts adverse long-term clinical outcomes in patients with acute myocardial infarction. Int J Cardiol. 2015; 196:165–167.

39. Haugaa KH, Grenne BL, Eek CH, et al. Strain echocardiography improves risk prediction of ventricular arrhythmias after myocardial infarction. JACC Cardiovasc Imaging. 2013; 6:841–850.

40. Cramariuc D, Gerdts E, Davidsen ES, Segadal L, Matre K. Myocardial deformation in aortic valve stenosis: relation to left ventricular geometry. Heart. 2010; 96:106–112.

41. Yingchoncharoen T, Gibby C, Rodriguez LL, Grimm RA, Marwick TH. Association of myocardial deformation with outcome in asymptomatic aortic stenosis with normal ejection fraction. Circ Cardiovasc Imaging. 2012; 5:719–725.

42. Lancellotti P, Donal E, Magne J, et al. Risk stratification in asymptomatic moderate to severe aortic stenosis: the importance of the valvular, arterial and ventricular interplay. Heart. 2010; 96:1364–1371.

43. Sato K, Seo Y, Ishizu T, et al. Prognostic value of global longitudinal strain in paradoxical low-flow, low-gradient severe aortic stenosis with preserved ejection fraction. Circ J. 2014; 78:2750–2759.

44. Mascle S, Schnell F, Thebault C, et al. Predictive value of global longitudinal strain in a surgical population of organic mitral regurgitation. J Am Soc Echocardiogr. 2012; 25:766–772.

45. Witkowski TG, Thomas JD, Debonnaire PJ, et al. Global longitudinal strain predicts left ventricular dysfunction after mitral valve repair. Eur Heart J Cardiovasc Imaging. 2013; 14:69–76.

46. Mentias A, Naji P, Gillinov AM, et al. Strain echocardiography and functional capacity in asymptomatic primary mitral regurgitation with preserved ejection fraction. J Am Coll Cardiol. 2016; 68:1974–1986.

47. Park JJ, Park JB, Park JH, Cho GY. Global longitudinal strain to predict mortality in patients with acute heart failure. J Am Coll Cardiol. 2018; 71:1947–1957.

48. Cho GY, Marwick TH, Kim HS, Kim MK, Hong KS, Oh DJ. Global 2-dimensional strain as a new prognosticator in patients with heart failure. J Am Coll Cardiol. 2009; 54:618–624.

49. Shah AM, Claggett B, Sweitzer NK, et al. Prognostic importance of impaired systolic function in heart failure with preserved ejection fraction and the impact of spironolactone. Circulation. 2015; 132:402–414.

50. Nakai H, Takeuchi M, Nishikage T, Lang RM, Otsuji Y. Subclinical left ventricular dysfunction in asymptomatic diabetic patients assessed by two-dimensional speckle tracking echocardiography: correlation with diabetic duration. Eur J Echocardiogr. 2009; 10:926–932.

51. Enomoto M, Ishizu T, Seo Y, et al. Subendocardial systolic dysfunction in asymptomatic normotensive diabetic patients. Circ J. 2015; 79:1749–1755.

52. Ishizu T, Seo Y, Kameda Y, et al. Left ventricular strain and transmural distribution of structural remodeling in hypertensive heart disease. Hypertension. 2014; 63:500–506.

53. Ewer MS, Ewer SM. Cardiotoxicity of anticancer treatments. Nat Rev Cardiol. 2015; 12:620.

54. Ali MT, Yucel E, Bouras S, et al. Myocardial strain is associated with adverse clinical cardiac events in patients treated with anthracyclines. J Am Soc Echocardiogr. 2016; 29:522–527.e3.

55. Thavendiranathan P, Poulin F, Lim KD, Plana JC, Woo A, Marwick TH. Use of myocardial strain imaging by echocardiography for the early detection of cardiotoxicity in patients during and after cancer chemotherapy: a systematic review. J Am Coll Cardiol. 2014; 63:2751–2768.

56. Charbonnel C, Convers-Domart R, Rigaudeau S, et al. Assessment of global longitudinal strain at low-dose anthracycline-based chemotherapy, for the prediction of subsequent cardiotoxicity. Eur Heart J Cardiovasc Imaging. 2017; 18:392–401.

57. Jung MH, Jung JI, Park SM, Youn HJ, Hong KS. A case of reversible but highly vulnerable adriamycin-induced cardiomyopathy: a multi-modality imaging approach. J Cardiovasc Imaging. 2019; 27:156–157.

58. Pelliccia A, Maron BJ, De Luca R, Di Paolo FM, Spataro A, Culasso F. Remodeling of left ventricular hypertrophy in elite athletes after long-term deconditioning. Circulation. 2002; 105:944–949.

59. Caselli S, Montesanti D, Autore C, et al. Patterns of left ventricular longitudinal strain and strain rate in Olympic athletes. J Am Soc Echocardiogr. 2015; 28:245–253.

60. Butz T, van Buuren F, Mellwig KP, et al. Two-dimensional strain analysis of the global and regional myocardial function for the differentiation of pathologic and physiologic left ventricular hypertrophy: a study in athletes and in patients with hypertrophic cardiomyopathy. Int J Cardiovasc Imaging. 2011; 27:91–100.

61. Park JH, Oh JK, Kim KH, et al. Left ventricular longitudinal strain and strain rate values according to sex and classifications of sports in the young university athletes who participated in the 2015 Gwangju Summer Universiade. JACC Cardiovasc Imaging. 2018; 11:1719–1721.

62. Haland TF, Almaas VM, Hasselberg NE, et al. Strain echocardiography is related to fibrosis and ventricular arrhythmias in hypertrophic cardiomyopathy. Eur Heart J Cardiovasc Imaging. 2016; 17:613–621.

63. Yiu KH, Atsma DE, Delgado V, et al. Myocardial structural alteration and systolic dysfunction in preclinical hypertrophic cardiomyopathy mutation carriers. PLoS One. 2012; 7:e36115.

64. Kobayashi T, Popovic Z, Bhonsale A, et al. Association between septal strain rate and histopathology in symptomatic hypertrophic cardiomyopathy patients undergoing septal myectomy. Am Heart J. 2013; 166:503–511.

65. Lee SP, Park JB, Kim HK, Kim YJ, Grogan M, Sohn DW. Contemporary imaging diagnosis of cardiac amyloidosis. J Cardiovasc Imaging. 2019; 27:1–10.

66. Liu D, Hu K, Niemann M, et al. Effect of combined systolic and diastolic functional parameter assessment for differentiation of cardiac amyloidosis from other causes of concentric left ventricular hypertrophy. Circ Cardiovasc Imaging. 2013; 6:1066–1072.

67. Senapati A, Sperry BW, Grodin JL, et al. Prognostic implication of relative regional strain ratio in cardiac amyloidosis. Heart. 2016; 102:748–754.

68. Buss SJ, Emami M, Mereles D, et al. Longitudinal left ventricular function for prediction of survival in systemic light-chain amyloidosis: incremental value compared with clinical and biochemical markers. J Am Coll Cardiol. 2012; 60:1067–1076.

69. Morris DA, Blaschke D, Canaan-Kühl S, et al. Global cardiac alterations detected by speckle-tracking echocardiography in Fabry disease: left ventricular, right ventricular, and left atrial dysfunction are common and linked to worse symptomatic status. Int J Cardiovasc Imaging. 2015; 31:301–313.

70. Lee JH, Park JH. Strain analysis of the right ventricle using two-dimensional echocardiography. J Cardiovasc Imaging. 2018; 26:111–124.

71. Park SJ, Park JH, Lee HS, et al. Impaired RV global longitudinal strain is associated with poor long-term clinical outcomes in patients with acute inferior STEMI. JACC Cardiovasc Imaging. 2015; 8:161–169.

72. Zornoff LA, Skali H, Pfeffer MA, et al. Right ventricular dysfunction and risk of heart failure and mortality after myocardial infarction. J Am Coll Cardiol. 2002; 39:1450–1455.

73. Jamal F, Bergerot C, Argaud L, Loufouat J, Ovize M. Longitudinal strain quantitates regional right ventricular contractile function. Am J Physiol Heart Circ Physiol. 2003; 285:H2842–7.

74. Lu KJ, Chen JX, Profitis K, et al. Right ventricular global longitudinal strain is an independent predictor of right ventricular function: a multimodality study of cardiac magnetic resonance imaging, real time three-dimensional echocardiography and speckle tracking echocardiography. Echocardiography. 2015; 32:966–974.

75. Wang J, Prakasa K, Bomma C, et al. Comparison of novel echocardiographic parameters of right ventricular function with ejection fraction by cardiac magnetic resonance. J Am Soc Echocardiogr. 2007; 20:1058–1064.

76. Vizzardi E, Bonadei I, Sciatti E, et al. Quantitative analysis of right ventricular (RV) function with echocardiography in chronic heart failure with no or mild RV dysfunction: comparison with cardiac magnetic resonance imaging. J Ultrasound Med. 2015; 34:247–255.

77. Freed BH, Tsang W, Bhave NM, et al. Right ventricular strain in pulmonary arterial hypertension: a 2D echocardiography and cardiac magnetic resonance study. Echocardiography. 2015; 32:257–263.

78. Park JH, Negishi K, Kwon DH, Popovic ZB, Grimm RA, Marwick TH. Validation of global longitudinal strain and strain rate as reliable markers of right ventricular dysfunction: comparison with cardiac magnetic resonance and outcome. J Cardiovasc Ultrasound. 2014; 22:113–120.

79. Focardi M, Cameli M, Carbone SF, et al. Traditional and innovative echocardiographic parameters for the analysis of right ventricular performance in comparison with cardiac magnetic resonance. Eur Heart J Cardiovasc Imaging. 2015; 16:47–52.

80. Lemarié J, Huttin O, Girerd N, et al. Usefulness of speckle-tracking imaging for right ventricular assessment after acute myocardial infarction: a magnetic resonance imaging/echocardiographic comparison within the relation between aldosterone and cardiac remodeling after myocardial infarction study. J Am Soc Echocardiogr. 2015; 28:818–827.e4.

81. Park JH, Kusunose K, Kwon DH, et al. Relationship between right ventricular longitudinal strain, invasive hemodynamics, and functional assessment in pulmonary arterial hypertension. Korean Circ J. 2015; 45:398–407.

82. Muraru D, Onciul S, Peluso D, et al. Sex- and method-specific reference values for right ventricular strain by 2-dimensional speckle-tracking echocardiography. Circ Cardiovasc Imaging. 2016; 9:e003866.

83. Park JH, Choi JO, Park SW, et al. Normal references of right ventricular strain values by two-dimensional strain echocardiography according to the age and gender. Int J Cardiovasc Imaging. 2018; 34:177–183.

84. Rimbaş RC, Mihăilă S, Enescu OA, Vinereanu D. A new comprehensive 12-segment approach to right ventricular systolic and diastolic functions by 2D speckle tracking echocardiography in healthy individuals. Echocardiography. 2016; 33:1866–1873.

85. Meris A, Faletra F, Conca C, et al. Timing and magnitude of regional right ventricular function: a speckle tracking-derived strain study of normal subjects and patients with right ventricular dysfunction. J Am Soc Echocardiogr. 2010; 23:823–831.

86. Fine NM, Shah AA, Han IY, et al. Left and right ventricular strain and strain rate measurement in normal adults using velocity vector imaging: an assessment of reference values and intersystem agreement. Int J Cardiovasc Imaging. 2013; 29:571–580.

87. Fine NM, Chen L, Bastiansen PM, et al. Reference values for right ventricular strain in patients without cardiopulmonary disease: a prospective evaluation and meta-analysis. Echocardiography. 2015; 32:787–796.

88. Seo HS, Lee H. Assessment of right ventricular function in pulmonary hypertension with multimodality imaging. J Cardiovasc Imaging. 2018; 26:189–200.

89. Ikeda S, Tsuneto A, Kojima S, et al. Longitudinal strain of right ventricular free wall by 2-dimensional speckle-tracking echocardiography is useful for detecting pulmonary hypertension. Life Sci. 2014; 111:12–17.

90. Fukuda Y, Tanaka H, Sugiyama D, et al. Utility of right ventricular free wall speckle-tracking strain for evaluation of right ventricular performance in patients with pulmonary hypertension. J Am Soc Echocardiogr. 2011; 24:1101–1108.

91. Motoji Y, Tanaka H, Fukuda Y, et al. Efficacy of right ventricular free-wall longitudinal speckle-tracking strain for predicting long-term outcome in patients with pulmonary hypertension. Circ J. 2013; 77:756–763.

92. Fine NM, Chen L, Bastiansen PM, et al. Outcome prediction by quantitative right ventricular function assessment in 575 subjects evaluated for pulmonary hypertension. Circ Cardiovasc Imaging. 2013; 6:711–721.

93. D'Andrea A, Stanziola A, D'Alto M, et al. Right ventricular strain: an independent predictor of survival in idiopathic pulmonary fibrosis. Int J Cardiol. 2016; 222:908–910.

94. Mukherjee M, Chung SE, Ton VK, et al. Unique abnormalities in right ventricular longitudinal strain in systemic sclerosis patients. Circ Cardiovasc Imaging. 2016; 9:e003792.

95. Sugiura E, Dohi K, Onishi K, et al. Reversible right ventricular regional non-uniformity quantified by speckle-tracking strain imaging in patients with acute pulmonary thromboembolism. J Am Soc Echocardiogr. 2009; 22:1353–1359.

96. Lee JH, Park JH, Park KI, et al. A comparison of different techniques of two-dimensional speckle-tracking strain measurements of right ventricular systolic function in patients with acute pulmonary embolism. J Cardiovasc Ultrasound. 2014; 22:65–71.

97. Lee K, Kwon O, Lee EJ, et al. Prognostic value of echocardiographic parameters for right ventricular function in patients with acute non-massive pulmonary embolism. Heart Vessels. 2019; 34:1187–1195.

98. Vitarelli A, Barillà F, Capotosto L, et al. Right ventricular function in acute pulmonary embolism: a combined assessment by three-dimensional and speckle-tracking echocardiography. J Am Soc Echocardiogr. 2014; 27:329–338.

99. Holman WL, Kormos RL, Naftel DC, et al. Predictors of death and transplant in patients with a mechanical circulatory support device: a multi-institutional study. J Heart Lung Transplant. 2009; 28:44–50.

100. Argiriou M, Kolokotron SM, Sakellaridis T, et al. Right heart failure post left ventricular assist device implantation. J Thorac Dis. 2014; 6:Suppl 1. S52–S59.

101. Grant AD, Smedira NG, Starling RC, Marwick TH. Independent and incremental role of quantitative right ventricular evaluation for the prediction of right ventricular failure after left ventricular assist device implantation. J Am Coll Cardiol. 2012; 60:521–528.

102. Cameli M, Lisi M, Righini FM, et al. Right ventricular longitudinal strain correlates well with right ventricular stroke work index in patients with advanced heart failure referred for heart transplantation. J Card Fail. 2012; 18:208–215.

103. Lisi M, Cameli M, Righini FM, et al. RV longitudinal deformation correlates with myocardial fibrosis in patients with end-stage heart failure. JACC Cardiovasc Imaging. 2015; 8:514–522.

104. Morris DA, Krisper M, Nakatani S, et al. Normal range and usefulness of right ventricular systolic strain to detect subtle right ventricular systolic abnormalities in patients with heart failure: a multicentre study. Eur Heart J Cardiovasc Imaging. 2017; 18:212–223.

105. Park JH, Park JJ, Park JB, Cho GY. Prognostic value of biventricular strain in risk stratifying in patients with acute heart failure. J Am Heart Assoc. 2018; 7:e009331.

106. Teske AJ, Cox MG, Te Riele AS, et al. Early detection of regional functional abnormalities in asymptomatic ARVD/C gene carriers. J Am Soc Echocardiogr. 2012; 25:997–1006.

107. Aneq MA, Engvall J, Brudin L, Nylander E. Evaluation of right and left ventricular function using speckle tracking echocardiography in patients with arrhythmogenic right ventricular cardiomyopathy and their first degree relatives. Cardiovasc Ultrasound. 2012; 10:37.

108. Vitarelli A, Cortes Morichetti M, Capotosto L, et al. Utility of strain echocardiography at rest and after stress testing in arrhythmogenic right ventricular dysplasia. Am J Cardiol. 2013; 111:1344–1350.

109. D'Andrea A, Caso P, Bossone E, et al. Right ventricular myocardial involvement in either physiological or pathological left ventricular hypertrophy: an ultrasound speckle-tracking two-dimensional strain analysis. Eur J Echocardiogr. 2010; 11:492–500.

110. D'Andrea A, Limongelli G, Baldini L, et al. Exercise speckle-tracking strain imaging demonstrates impaired right ventricular contractile reserve in hypertrophic cardiomyopathy. Int J Cardiol. 2017; 227:209–216.

111. Okamatsu K, Takeuchi M, Nakai H, et al. Effects of aging on left atrial function assessed by two-dimensional speckle tracking echocardiography. J Am Soc Echocardiogr. 2009; 22:70–75.

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

113. Donal E, Lip GY, Galderisi M, et al. EACVI/EHRA expert consensus document on the role of multi-modality imaging for the evaluation of patients with atrial fibrillation. Eur Heart J Cardiovasc Imaging. 2016; 17:355–383.

114. Schneider C, Malisius R, Krause K, et al. Strain rate imaging for functional quantification of the left atrium: atrial deformation predicts the maintenance of sinus rhythm after catheter ablation of atrial fibrillation. Eur Heart J. 2008; 29:1397–1409.

115. Providência R, Trigo J, Paiva L, Barra S. The role of echocardiography in thromboembolic risk assessment of patients with nonvalvular atrial fibrillation. J Am Soc Echocardiogr. 2013; 26:801–812.

116. Kojima T, Kawasaki M, Tanaka R, et al. Left atrial global and regional function in patients with paroxysmal atrial fibrillation has already been impaired before enlargement of left atrium: velocity vector imaging echocardiography study. Eur Heart J Cardiovasc Imaging. 2012; 13:227–234.

117. Yoon YE, Oh IY, Kim SA, et al. Echocardiographic predictors of progression to persistent or permanent atrial fibrillation in patients with paroxysmal atrial fibrillation (E6P study). J Am Soc Echocardiogr. 2015; 28:709–717.

118. Obokata M, Negishi K, Kurosawa K, et al. Left atrial strain provides incremental value for embolism risk stratification over CHA₂DS₂-VASc score and indicates prognostic impact in patients with atrial fibrillation. J Am Soc Echocardiogr. 2014; 27:709–716.e4.

119. Aung SM, Güler A, Güler Y, Huraibat A, Karabay CY, Akdemir I. Left atrial strain in heart failure with preserved ejection fraction. Herz. 2017; 42:194–199.

120. Santos AB, Roca GQ, Claggett B, et al. Prognostic relevance of left atrial dysfunction in heart failure with preserved ejection fraction. Circ Heart Fail. 2016; 9:e002763.

121. Ersbøll M, Andersen MJ, Valeur N, et al. The prognostic value of left atrial peak reservoir strain in acute myocardial infarction is dependent on left ventricular longitudinal function and left atrial size. Circ Cardiovasc Imaging. 2013; 6:26–33.

122. Debonnaire P, Leong DP, Witkowski TG, et al. Left atrial function by two-dimensional speckle-tracking echocardiography in patients with severe organic mitral regurgitation: association with guidelines-based surgical indication and postoperative (long-term) survival. J Am Soc Echocardiogr. 2013; 26:1053–1062.

123. Yang LT, Liu YW, Shih JY, et al. Predictive value of left atrial deformation on prognosis in severe primary mitral regurgitation. J Am Soc Echocardiogr. 2015; 28:1309–1317.e4.

124. Galli E, Fournet M, Chabanne C, et al. Prognostic value of left atrial reservoir function in patients with severe aortic stenosis: a 2D speckle-tracking echocardiographic study. Eur Heart J Cardiovasc Imaging. 2016; 17:533–541.