Internal and Emergency Medicine

, Volume 14, Issue 8, pp 1279–1285 | Cite as

Focus on echocardiographic right ventricular strain analysis in cystic fibrosis adults without cardiovascular risk factors: a case–control study

  • Edoardo SciattiEmail author
  • Enrico Vizzardi
  • Ivano Bonadei
  • Francesca Valentini
  • Elisa Menotti
  • Francesco Prati
  • Lucia Dallapellegrina
  • Marialma Berlendis
  • Piercarlo Poli
  • Rita Padoan
  • Marco Metra


Strain echocardiography is able to detect subclinical ventricular systolic and diastolic dysfunction. Prolonged survival to cystic fibrosis favors heart and vessel involvement. The purpose of the present study was to compare clinically stable adult patients affected by cystic fibrosis without overt pulmonary hypertension with controls to evaluate right ventricular (RV) systolic and diastolic function by means of strain and tissue Doppler imaging (TDI), respectively. 22 adults affected by cystic fibrosis and 24 healthy volunteers matched for age and sex were enrolled. None had known cardiovascular risk factors or overt pulmonary hypertension. All people underwent blood pressure measurement and transthoracic echocardiography. Cystic fibrosis patients showed higher sPAP [median 25 (IQR 21–30) vs 22 (22–22) mmHg; p = 0.02] and more frequent RV diastolic dysfunction (p < 0.001). Among cases, some RV systolic parameters were significantly altered than controls, such as TAPSE [20 (18–24) vs. 23 (21–28) mm; p = 0.001], FAC [34 (26–44) vs. 49 (48–50)%; p < 0.001], midwall tissue strain [− 25.0 (− 31.3 to − 22.8) vs. − 30.5 (− 31.8 to − 29.3)%; p = 0.03], apical tissue strain [− 22 (− 29.3 to − 19.0) vs. − 30.5 (− 32.8 to − 28.3)%; p = 0.001] and 2D strain [− 22.0 (− 25.1 to − 19.0) vs. − 29.5 (− 31.8 to − 27.3)%; p < 0.001]. Finally, 2D strain correlated with spirometric FEV1 (ρ = − 0.463, p = 0.03) and nearly with FEF25–75% (ρ = − 0.393, p = 0.07). Our study confirmed a RV subclinical systo-diastolic dysfunction in clinically stable patients affected by cystic fibrosis without overt pulmonary hypertension nor cardiovascular risk factors. This may be due to systemic inflammation and temporary recurrent pulmonary hypertension. We retain that RV 2D strain and TDI echocardiography could become an important tool in the follow-up of these patients.


Cystic fibrosis Strain Right ventricle Echocardiography Speckle tracking 



The authors are grateful to “Lega Italiana Fibrosi Cistica-onlus Lombardia” for its interest in helping these patients.

Author contributions

EV, ES, MB, RP wrote the paper; ES analyzed data; ES, IB, FV, EM, FP, LD, PP collected data; MB, RP, MM revised the paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Statements on human and animal rights

This was a prospective single-center case-control study in compliance with the Declaration of Helsinki and approved by the local ethical committee.

Informed consent

Every patient gave his/her informed consent.


  1. 1.
    Cystic Fibrosis Foundation Patient Registry (2017) Annual data report. Cystic Fibrosis Foundation, Bethesda, MDGoogle Scholar
  2. 2.
    Ionescu AA, Nixon LS, Evans WD et al (2002) Bone density, body composition and inflammatory status in cystic fibrosis. Am J Respir Crit Care Med 162:789–794CrossRefGoogle Scholar
  3. 3.
    MacNee W, Maclay J, McAllister D (2008) Cardiovascular injury and repair in chronic obstructive pulmonary disease. Proc Am Thorac Soc 5:824–833CrossRefGoogle Scholar
  4. 4.
    Wiglesworth FW (1946) Fibrocystic disease of pancreas. Am J Med Sci 212(3):351–365CrossRefGoogle Scholar
  5. 5.
    Royce SW (1951) Cor pulmonale in infancy and early childhood; report on 34 patients, with special reference to the occurrence of pulmonary heart disease in cystic fibrosis of the pancreas. Pediatrics 8(2):255–274PubMedGoogle Scholar
  6. 6.
    Florea VG, Florea ND, Sharma R et al (2000) Right ventricular dysfunction in adult severe cystic fibrosis. Chest 118(4):1063–1068CrossRefGoogle Scholar
  7. 7.
    Rovedder PM, Ziegler B, Pinotti AF, Menna Barreto SS, Dalcin Pde T (2008) Prevalence of pulmonary hypertension evaluated by Doppler echocardiography in a population of adolescent and adult patients with cystic fibrosis. J Bras Pneumol 34(2):83–90CrossRefGoogle Scholar
  8. 8.
    Ionescu AA, Ionescu AA, Payne N, Obieta-Fresnedo I, Fraser AG, Shale DJ (2001) Subclinical right ventricular dysfunction in cystic fibrosis. A study using tissue Doppler echocardiography. Am J Respir Crit Care Med 163(5):1212–1218CrossRefGoogle Scholar
  9. 9.
    Baño-Rodrigo A, Salcedo-Posadas A, Villa-Asensi JR, Tamariz-Martel A, Lopez-Neyra A, Blanco-Iglesias E (2012) Right ventricular dysfunction in adolescents with mild cystic fibrosis. J Cyst Fibros 11(4):274–280CrossRefGoogle Scholar
  10. 10.
    Giacchi V, Rotolo N, Amato B, Di Dio G, Betta P, La Rosa M, Leonardi S, Sciacca P (2015) Heart involvement in children and adults with cystic fibrosis: correlation with pulmonary indexes and inflammation markers. Heart Lung Circ 24(10):1002–1010CrossRefGoogle Scholar
  11. 11.
    Koelling TM, Dec GW, Ginns LC, Semigran MJ (2003) Left ventricular diastolic function in patients with advanced cystic fibrosis. Chest 123(5):1488–1494CrossRefGoogle Scholar
  12. 12.
    Koestenberger M, Ravekes W (2013) Tricuspid annular peak systolic velocity (s') in pediatric patients with mild cystic fibrosis. Pediatr Cardiol 34(2):483CrossRefGoogle Scholar
  13. 13.
    Labombarda F, Pellissier A, Ellafi M, Creveuil C, Ribault V, Laurans M, Guillot M, Bergot E, Grollier G, Milliez P, Zalcman G, Saloux E (2011) Myocardial strain assessment in cystic fibrosis. J Am Soc Echocardiogr 24(9):1037–1045CrossRefGoogle Scholar
  14. 14.
    Sellers ZM, McGlocklin L, Brasch A (2015) Strain rate echocardiography uncovers subclinical left ventricular dysfunction in cystic fibrosis. J Cyst Fibros 14(5):654–660CrossRefGoogle Scholar
  15. 15.
    Ozcelik N, Shell R, Holtzlander M, Cua C (2013) Decreased right ventricular function in healthy pediatric cystic fibrosis patients versus non-cystic fibrosis patients. Pediatr Cardiol 34(1):159–164CrossRefGoogle Scholar
  16. 16.
    Eising JB, van der Ent CK, Teske AJ, Vanderschuren MM, Uiterwaal CSPM, Meijboom FJ (2018) Young patients with cystic fibrosis demonstrate subtle alterations of the cardiovascular system. J Cyst Fibros 1:643–649CrossRefGoogle Scholar
  17. 17.
    Pellegrino R, Viegi G, Brusasco V, Crapo RO, Burgos F, Casaburi R, Coates A, van der Grinten CP, Gustafsson P, Hankinson J, Jensen R, Johnson DC, MacIntyre N, McKay R, Miller MR, Navajas D, Pedersen OF, Wanger J (2005) Interpretative strategies for lung function tests. Eur Respir J 26(5):948–968CrossRefGoogle Scholar
  18. 18.
    Zapletal A, Paul T, Samánek M (1977) Significance of contemporary methods of lung function testing for the detection of airway obstruction in children and adolescents (author's transl). Z Erkr Atmungsorgane 149(3):343–371PubMedGoogle Scholar
  19. 19.
    Nagueh SF, Appleton CP, Gillebert TC et al (2009) Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr 22(2):107–133CrossRefGoogle Scholar
  20. 20.
    Lang RM, Bierig M, Devereux RB et al (2005) Recommendations for chamber quantification: a report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18(12):1440–1463CrossRefGoogle Scholar
  21. 21.
    Rudski LG, Lai WW, Afilalo J, Hua L 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 (quiz 786–788) CrossRefGoogle Scholar
  22. 22.
    Vogel M, Cheung MM, Li J, Kristiansen SB, Schmidt MR, White PA, Sorensen K, Redington AN (2003) Noninvasive assessment of LV force-frequency relationships using tissue Doppler-derived isovolumic acceleration: validation in an animal model. Circulation 107(12):1647–1652CrossRefGoogle Scholar
  23. 23.
    Voigt JU, Pedrizzetti G, Lysyansky P, Marwick TH, Houle H, Baumann R, Pedri S, Ito Y, Abe Y, Metz S, Song JH, Hamilton J, Sengupta PP, Kolias TJ, d'Hooge J, Aurigemma GP, Thomas JD, Badano LP (2015) Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging. J Am Soc Echocardiogr 28:183–193CrossRefGoogle Scholar
  24. 24.
    Labombarda F, Saloux E, Brourd J, Bergot E, Milliez P (2016) Heart involvement in cystic fibrosis: a specific cystic fibrosis-related myocardial changes? Respir Med 118:31–38CrossRefGoogle Scholar
  25. 25.
    Orabona R, Sciatti E, Vizzardi E, Bonadei I, Prefumo F, Valcamonico A, Metra M, Frusca T (2018) Ultrasound evaluation of left ventricular and aortic fibrosis after pre-eclampsia. Ultrasound Obstet Gynecol 52:648–653CrossRefGoogle Scholar
  26. 26.
    Iles L, Pfluger H, Phrommintikul A, Cherayath J, Aksit P, Gupta SN, Kaye DM, Taylor AJ (2008) Evaluation of diffuse myocardial fibrosis in heart failure with cardiac magnetic resonance contrast-enhanced T1 mapping. J Am Coll Cardiol. 52:1574–1580CrossRefGoogle Scholar
  27. 27.
    Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Bauersachs J, Engelhardt S (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456:980–984CrossRefGoogle Scholar
  28. 28.
    de Boer RA, Daniels LB, Maisel AS, Januzzi JL Jr (2015) State of the art: newer biomarkers in heart failure. Eur J Heart Fail 17:559–569CrossRefGoogle Scholar
  29. 29.
    Schelbert EB, Fonarow GC, Bonow RO, Butler J, Gheorghiade M (2014) Therapeutic targets in heart failure: refocusing on the myocardial interstitium. J Am Coll Cardiol 63:2188–2198CrossRefGoogle Scholar
  30. 30.
    Gorter TM, van Veldhuisen DJ, Bauersachs J, Borlaug BA, Celutkiene J, Coats AJS, Crespo-Leiro MG, Guazzi M, Harjola VP, Heymans S, Hill L, Lainscak M, Lam CSP, Lund LH, Lyon AR, Mebazaa A, Mueller C, Paulus WJ, Pieske B, Piepoli MF, Ruschitzka F, Rutten FH, Seferovic PM, Solomon SD, Shah SJ, Triposkiadis F, Wachter R, Tschöpe C, de Boer RA (2018) Right heart dysfunction and failure in heart failure with preserved ejection fraction: mechanisms and management. Position statement on behalf of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail 20:16–37CrossRefGoogle Scholar
  31. 31.
    Gargani L, Pignone A, Agoston G et al (2013) Clinical and echocardiographic correlations of exercise-induced pulmonary hypertension in systemic sclerosis: a multicenter study. Am Heart J 165(2):200–207CrossRefGoogle Scholar

Copyright information

© Società Italiana di Medicina Interna (SIMI) 2019

Authors and Affiliations

  • Edoardo Sciatti
    • 1
    Email author
  • Enrico Vizzardi
    • 1
  • Ivano Bonadei
    • 1
  • Francesca Valentini
    • 1
  • Elisa Menotti
    • 1
  • Francesco Prati
    • 1
  • Lucia Dallapellegrina
    • 1
  • Marialma Berlendis
    • 2
  • Piercarlo Poli
    • 3
  • Rita Padoan
    • 3
  • Marco Metra
    • 1
  1. 1.Section of Cardiovascular Diseases, Department of Medical and Surgical Specialties, Radiological Sciences and Public HealthUniversity of BresciaBresciaItaly
  2. 2.Pulmonology UnitASST Spedali Civili of BresciaBresciaItaly
  3. 3.Pediatric Department, Cystic Fibrosis CenterUniversity of Brescia, ASST Spedali Civili of BresciaBresciaItaly

Personalised recommendations