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Early left atrial dysfunction in idiopathic pulmonary fibrosis patients without chronic right heart failure

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Abstract

No data are actually available regarding the left atrial (LA) functional assessment by two-dimensional speckle tracking echocardiography (2D-STE) in early-stage idiopathic pulmonary fibrosis (IPF). The primary end-point of our study was to assess whether global LA peak strain (GLAPS), measured by 2D-STE analysis, may detect early alterations in LA function in IPF patients without right heart failure (RHF). Between September 2017 and January 2019, 50 consecutive IPF patients (73.8 ± 6.8 years, 36 males) without chronic RHF and 30 controls matched by age, sex and cardiovascular risk factors, were enrolled in an observational retrospective case–control study. All patients underwent a complete echocardiographic study implemented with 2D-STE analysis. GLAPS, left ventricular (LV) global longitudinal strain (GLS), right atrial (RA) reservoir strain (GSA+) and right ventricular (RV)-GLS were obtained in each patient. LVFP were significantly increased in IPF patients in comparison to controls (average E/e′ ratio 14.4 ± 3.0 vs 9.6 ± 1.5, p < 0.0001), while LV-GLS was slightly reduced in IPF patients compared to controls (19.4 ± 3.6% vs 21.0 ± 2.2%, p = 0.03).Moreover, GLAPS was significantly impaired in IPF patients in comparison to controls (18.4 ± 3.7% vs 28.4 ± 5.6%, p < 0.0001).Finally, the two groups of patients did not show any statistically significant difference in both RA-GSA + (23.9 ± 3.7% vs 24.5 ± 4.0%, p = 0.49) and RV-GLS (− 22.6 ± 3.3% vs − 23.5 ± 3.0%, p = 0.22). Notably, LV-GLS was strongly inversely correlated both with RV/LV basal diameter ratio and TRV in IPF patients (r = − 0.87 and − 0.82, respectively) but not in controls (r = − 0.29 and − 0.27, respectively). This finding highlights a likely process of ventricular interdependence in non-advanced IPF, with consequent LV diastolic dysfunction and secondary impairment in LV-GLS and GLAPS. Early LA reservoir dysfunction in IPF patients may be secondary to LV diastolic dysfunction induced by ventricular interdependence and may develop before RV diastolic and systolic dysfunction.

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Abbreviations

2D:

Two-dimensional

2D-STE:

Two-dimensional speckle tracking echocardiography

6MWT:

Six-minute walking test

AF:

Atrial fibrillation

BSA:

Body surface area

CAD:

Coronary artery disease

CI:

Confidence interval

CVD:

Cardiovascular disease

DLCO:

Diffusing capacity of the lungs for carbon monoxide

ECG:

Electrocardiogram

GLAPS:

Global left atrial peak strain

GLS:

Global longitudinal strain

GSA+:

Positive global atrial strain

GSA−:

Negative global atrial strain

GSR+:

Positive global strain rate

GSRE:

Global early-diastolic strain rate

GSRL:

Global late-diastolic strain rate

HF:

Heart failure

HR:

Heart rate

HRCT:

High-resolution computed tomography

ICC:

Intraclass correlation coefficient

ILD:

Interstitial lung disease

IPF:

Idiopathic pulmonary fibrosis

LA:

Left atrial

LV:

Left ventricular

LVFP:

Left ventricular filling pressure

MDRD:

Modification of diet in renal disease

PH:

Pulmonary hypertension

PW:

Pulsed-wave

RHF:

Right heart failure

ROI:

Region of interest

RV:

Right ventricular

SPSS:

Statistical package for social science

SR:

Strain rate

STE:

Speckle tracking echocardiography

TDI:

Tissue Doppler imaging

TGSA:

Total global atrial strain

TLC:

Total lung capacity

TTE:

Transthoracic echocardiography

References

  1. van Cleemput J, Sonaglioni A, Wuyts WA, Bengus M, Stauffer JL, Harari S (2019) idiopathic pulmonary fibrosis for cardiologists: differential diagnosis, cardiovascular comorbidities, and patient management. Adv Ther 36(2):298–317

    Article  PubMed  Google Scholar 

  2. Raghu G, Remy-Jardin M, Myers JL et al (2018) Diagnosis of idiopathic pulmonary fibrosis. An official ATS/ERS/JRS/ALAT clinical practice guideline. Am J Respir Crit Care Med 198(5):e44–68

    Article  PubMed  Google Scholar 

  3. Ley B, Collard HR, King TE Jr (2011) Clinical course and prediction of survival in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 183(4):431–440

    Article  PubMed  Google Scholar 

  4. Nalysnyk L, Cid-Ruzafa J, Rotella P, Esser D (2012) Incidence and prevalence of idiopathic pulmonary fibrosis: review of the literature. Eur Respir Rev 21(126):355–361

    Article  PubMed  Google Scholar 

  5. Hutchinson J, Fogarty A, Hubbard R, McKeever T (2015) Global incidence and mortality of idiopathic pulmonary fibrosis: a systematic review. Eur Respir J 46(3):795–806

    Article  PubMed  Google Scholar 

  6. Harari S, Madotto F, Caminati A, Conti S, Cesana G (2016) Epidemiology of idiopathicpulmonary fibrosis in Northern Italy. PLoS ONE 11(2):e0147072

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Dalleywater W, Powell HA, Hubbard RB, Navaratnam V (2015) Risk factors for cardiovascular disease in people with idiopathic pulmonary fibrosis: a population-based study. Chest 147(1):150–156

    Article  PubMed  Google Scholar 

  8. Suzuki A, Kondoh Y (2017) The clinical impact of major comorbidities on idiopathic pulmonary fibrosis. Respir Investig 55(2):94–103

    Article  PubMed  Google Scholar 

  9. King TE Jr, Albera C, Bradford WZ et al (2014) All-cause mortality rate in patients with idiopathic pulmonary fibrosis Implications for the design and execution of clinical trials. Am J Respir Crit Care Med 189(7):825–831

    Article  PubMed  Google Scholar 

  10. King CS, Nathan SD (2017) Idiopathic pulmonary fibrosis: effects and optimal management of comorbidities. Lancet Respir Med 5(1):72–84

    Article  PubMed  Google Scholar 

  11. Caminati A, Lonati C, Cassandro R et al (2019) Comorbidities in idiopathic pulmonary fibrosis: an underestimated issue. Eur Respir Rev 28(153):190044. https://doi.org/10.1183/16000617.0044-2019

    Article  PubMed  Google Scholar 

  12. Ponikowski P, Voors AA, Anker SD et al (2016) 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 37(27):2129–2200

    Article  PubMed  Google Scholar 

  13. Dandel M, Hetzer R (2009) Echocardiographic strain and strain rate imaging—clinical applications. Int J Cardiol 132(1):11–24

    Article  PubMed  Google Scholar 

  14. Carerj S, La Carrubba S, Antonini-Canterin F et al (2010) The incremental prognostic value of echocardiography in asymptomatic stage a heart failure. J Am Soc Echocardiogr 23(10):1025–1034

    Article  PubMed  Google Scholar 

  15. Gunasekaran P, Panaich S, Briasoulis A, Cardozo S, Afonso L (2017) Incremental value of two dimensional speckle tracking echocardiography in the functional assessment and characterization of subclinical left ventricular dysfunction. Curr Cardiol Rev 13(1):32–40

    Article  PubMed  PubMed Central  Google Scholar 

  16. 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(3):299–305

    Article  PubMed  Google Scholar 

  17. Cameli M, Lisi M, Focardi M et al (2012) Left atrial deformation analysis by speckle tracking echocardiography for prediction of cardiovascular outcomes. Am J Cardiol 110(2):264–269

    Article  PubMed  Google Scholar 

  18. Kuppahally SS, Akoum N, Burgon NS et al (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(3):231–239

    Article  PubMed  Google Scholar 

  19. D'Andrea A, Stanziola A, Di Palma E et al (2016) Right ventricular structure and function in idiopathic pulmonary fibrosis with or without pulmonary hypertension. Echocardiography 33(1):57–65

    Article  PubMed  Google Scholar 

  20. D'Andrea A, Stanziola AA, Saggar R et al (2019) Right ventricular functional reserve in early-stage idiopathic pulmonary fibrosis: an exercise two-dimensional speckle tracking doppler echocardiography study. Chest 155(2):297–306. https://doi.org/10.1016/j.chest.2018.11.015

    Article  PubMed  Google Scholar 

  21. Alageel S, Gulliford MC (2019) Health checks and cardiovascular risk factor values over six years’ follow-up: matched cohort study using electronic health records in England. PLoS Med 16(7):e1002863. https://doi.org/10.1371/journal.pmed.1002863

    Article  PubMed  PubMed Central  Google Scholar 

  22. Harari S, Cereda F, Pane F (2019) Lung cryobiopsy for the diagnosis of interstitial lung diseases: a series contribution to a debated procedure. Medicina (Kaunas) 55(9):E606. https://doi.org/10.3390/medicina55090606

    Article  Google Scholar 

  23. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D (1999) A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of diet in renal disease study group. Ann Intern Med 130(6):461–470

    Article  CAS  PubMed  Google Scholar 

  24. Lang RM, Badano LP, Mor-Avi V et al (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):1–39

    Article  PubMed  Google Scholar 

  25. Nagueh SF, Smiseth OA, Appleton CP et al (2016) Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 29(4):277–314

    Article  PubMed  Google Scholar 

  26. Rudski LG, Lai WW, Afilalo J et al (2010) Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr 23(7):685–713

    Article  PubMed  Google Scholar 

  27. Miglioranza MH, Badano LP, Mihăilă S et al (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(11):1023–1034

    Article  PubMed  Google Scholar 

  28. 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(1):59–70

    Article  PubMed  Google Scholar 

  29. Sugimoto T, Dulgheru R, Bernard A et al (2017) Echocardiographic reference ranges for normal left ventricular 2D strain: results from the EACVI NORRE study. Eur Heart J Cardiovasc Imaging 18(8):833–840. https://doi.org/10.1093/ehjci/jex140

    Article  PubMed  Google Scholar 

  30. Nathan SD, Noble PW, Tuder RM (2007) Idiopathic pulmonary fibrosis and pulmonary hypertension: connecting the dots. Am J Respir Crit Care Med 175(9):875–880

    Article  PubMed  Google Scholar 

  31. Lettieri CJ, Nathan SD, Barnett SD, Ahmad S, Shorr AF (2006) Prevalence and outcomes of pulmonary arterial hypertension in advanced idiopathic pulmonary fibrosis. Chest 129(3):746–752

    Article  PubMed  Google Scholar 

  32. Kizer JR, Zisman DA, Blumenthal NP et al (2004) Association between pulmonary fibrosis and coronary artery disease. Arch Intern Med 164(5):551–556

    Article  PubMed  Google Scholar 

  33. Nathan SD, Basavaraj A, Reichner C et al (2010) Prevalence and impact of coronary artery disease in idiopathic pulmonary fibrosis. Respir Med 104(7):1035–1041

    Article  PubMed  Google Scholar 

  34. Kowalewski M, Urban M, Mroczko B, Szmitkowski M (2002) Proinflammatory cytokines (IL-6, TNF-alpha) and cardiac troponin I (cTnI) in serum of young people with ventricular arrhythmias. Pol Arch Med Wewn 108(1):647–651

    CAS  PubMed  Google Scholar 

  35. Shibata Y, Watanabe T, Osaka D et al (2011) Impairment of pulmonary function is an independent risk factor for atrial fibrillation: the Takahata study. Int J Med Sci 8(7):514–522

    Article  PubMed  PubMed Central  Google Scholar 

  36. Hubbard RB, Smith C, Le Jeune I, Gribbin J, Fogarty AW (2008) The association between idiopathic pulmonary fibrosis and vascular disease: a population-based study. Am J Respir Crit Care Med 178(12):1257–1261

    Article  PubMed  Google Scholar 

  37. Agrawal A, Verma I, Shah V, Agarwal A, Sikachi RR (2016) Cardiac manifestations of idiopathic pulmonary fibrosis. Intract Rare Dis Res 5(2):70–75. https://doi.org/10.5582/irdr.2016.01023

    Article  Google Scholar 

  38. Ancona R, Comenale Pinto S, Caso P et al (2014) Left atrium by echocardiography in clinical practice: from conventional methods to new echocardiographic techniques. Sci World J 2014:451042. https://doi.org/10.1155/2014/451042

    Article  Google Scholar 

  39. Rimbaş RC, Dulgheru RE, Vinereanu D (2015) Methodological gaps in left atrial function assessment by 2D speckle tracking echocardiography (Article in English, Portuguese). Arq Bras Cardiol 105(6):625–636. https://doi.org/10.5935/abc.20150144

    Article  PubMed  PubMed Central  Google Scholar 

  40. Her AY, Choi EY, Shim CY et al (2012) Prediction of left atrial fibrosis with speckle tracking echocardiography in mitral valve disease: a comparative study with histopathology. Korean Circ J 42(5):311–318

    Article  PubMed  PubMed Central  Google Scholar 

  41. Longobardo L, Todaro MC, Zito C et al (2014) Role of imaging in assessment of atrial fibrosis in patients with atrial fibrillation: state-of-the-art review. Eur Heart J Cardiovasc Imaging 15(1):1–5

    Article  PubMed  Google Scholar 

  42. Tops LF, Delgado V, Bertini M et al (2011) Left atrial strain predicts reverse remodeling after catheter ablation for atrial fibrillation. J Am Coll Cardiol 57(3):324–331

    Article  PubMed  Google Scholar 

  43. Vieira MJ, Teixeira R, Gonçalves L, Gersh BJ (2014) Left atrial mechanics: echocardiographic assessment and clinical implications. J Am Soc Echocardiogr 27(5):463–478

    Article  PubMed  Google Scholar 

  44. Lazar JM, Flores AR, Grandis DJ, Orie JE, Schulman DS (1993) Effects of chronic right ventricular pressure overload on left ventricular diastolic function. Am J Cardiol 72(15):1179–1182

    Article  CAS  PubMed  Google Scholar 

  45. Santamore WP, Dell'Italia LJ (1998) Ventricular interdependence: significant left ventricular contributions to right ventricular systolic function. Prog Cardiovasc Dis 40(4):289–308

    Article  CAS  PubMed  Google Scholar 

  46. Morris-Thurgood JA, Frenneaux MP (2000) Diastolic ventricular interaction and ventricular diastolic filling. Heart Fail Rev 5(4):307–323

    Article  CAS  PubMed  Google Scholar 

  47. Satoh H, Kurishima K, Ishikawa H, Ohtsuka M (2006) Increased levels of KL-6 and subsequent mortality in patients with interstitial lung diseases. J Intern Med 260(5):429–434

    Article  CAS  PubMed  Google Scholar 

  48. Kinder BW, Brown KK, McCormack FX et al (2009) Serum surfactant protein-a is a strong predictor of early mortality in idiopathic pulmonary fibrosis. Chest 135(6):1557–1563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Barlo NP, van Moorsel CH, Ruven HJ, Zanen P, van den Bosch JM, Grutters JC (2009) Surfactant protein-D predicts survival in patients with idiopathic pulmonary fibrosis. Sarcoidosis Vasc Diffuse Lung Dis 26(2):155–161

    CAS  PubMed  Google Scholar 

  50. Rosas IO, Richards TJ, Konishi K et al (2008) (2008) MMP1 and MMP7 as potential peripheral blood biomarkers in idiopathic pulmonary fibrosis. PLoS Med 5(4):e93

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Galiè N, Humbert M, Vachiery JL et al (2015) 2015 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: the Joint Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS): Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC), International Society for Heart and Lung Transplantation (ISHLT). Eur Respir J 46(4):903–975

    Article  PubMed  CAS  Google Scholar 

  52. Voigt JU, Pedrizzetti G, Lysyansky P et al (2015) Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging. Eur Heart J Cardiovasc Imaging 16(1):1–11

    Article  CAS  PubMed  Google Scholar 

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Acknowledgement

This work has been supported by Italian Ministry of Health Ricerca Corrente—IRCCS MultiMedica.

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Correspondence to Antonella Caminati.

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Antonella Caminati reports personal fees from Roche and Boehringer Ingelheim, outside the submitted work. Sergio Harari reports grants and personal fees from Roche, Actelion and Boehringer Ingelheim, outside the submitted work. All other authors declares no conflict of interest.

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All procedures performed in the present study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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10554_2020_1887_MOESM1_ESM.jpg

Supplementary file1 Supplemental Table Intra- and interobserver variability analysis of the main conventional and functional echocardiographic parameters, measured in a subgroup of 20 patients. ICC, intraclass correlation coefficient. GLAPS, global left atrial peak strain. LAVi, left atrial volume indexed. LV, left ventricular. LVEDVi, left ventricular end-diastolic volume indexed. LVEF, left ventricular ejection fraction. LVMi, left ventricular mass indexed. RV, right ventricular. TRV, tricuspid regurgitation peak velocity (JPG 1466 kb)

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Sonaglioni, A., Caminati, A., Lipsi, R. et al. Early left atrial dysfunction in idiopathic pulmonary fibrosis patients without chronic right heart failure. Int J Cardiovasc Imaging 36, 1711–1723 (2020). https://doi.org/10.1007/s10554-020-01887-5

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