Pediatric Cardiology

, Volume 39, Issue 4, pp 695–704 | Cite as

Respiratory Training Late After Fontan Intervention: Impact on Cardiorespiratory Performance

  • Lamia Ait Ali
  • Alessandro Pingitore
  • Paolo Piaggi
  • Fabio Brucini
  • Mirko Passera
  • Marco Marotta
  • Alessandra Cadoni
  • Claudio Passino
  • Giosuè Catapano
  • Pierluigi Festa
Original Article


Fontan palliation allows patients with “single ventricle” circulation to reach adulthood with an acceptable quality of life, although exercise tolerance is significantly reduced. To assess whether controlled respiratory training (CRT) increases cardiorespiratory performance. 16 Adolescent Fontan patients (age 17. 5 ± 3.8 years) were enrolled. Patients were divided into CRT group (n = 10) and control group (C group, n = 6). Maximal cardiopulmonary test (CPT) was repeated at the end of CRT in the CRT group and after an average time of 3 months in the C group. In the CRT group a CPT endurance was also performed before and after CRT. In the CRT group there was a significant improvement in cardiovascular and respiratory response to exercise after CRT. Actually, after accounting for baseline values, the CRT group had decreased breathing respiratory reserve (− 15, 95% CI −22.3 to − 8.0, p = 0.001) and increased RR peak (+ 4.8, 95% CI 0.7–8.9, p = 0.03), VE peak (+ 13.7, 95% CI 5.6–21.7, p = 0.004), VO2 of predicted (+ 8.5, 95% CI 0.1–17.0, p = 0.05), VO2 peak (+ 4.3, 95% CI 0.3 to 8.2, p = 0.04), and VO2 workslope (+ 1.7, 95% CI 0.3–3.1, p = 0.02) as compared to the control group. Moreover, exercise endurance time increased from 8.45 to 17.7 min (p = 0.01). CRT improves cardiorespiratory performance in post-Fontan patients leading to a better aerobic capacity.


Congenital heart disease Fontan circulation Controlled respiratory training Ergospirometry 



We gratefully thank Ms Elaine Laws for her precious help in the English editing of this manuscript.

Compliance with Ethical Standards

Conflict of interest

All the authors have not to declare conflict of interest.

Research involving Human Participants and/or Animals

The research protocol was approved by the local ethics-committee review board (Prot 0015-17 2014 P).

Informed Consent

All patients or legal guardians gave informed consent, and authorized physicians to use their clinical data in accordance with Italian law.


  1. 1.
    Hoffman JI, Kaplan S, Liberthson RR (2004) Prevalence of congenital heart disease. Am Heart J 147:425–439. CrossRefPubMedGoogle Scholar
  2. 2.
    Fontan F, Baudet E (1971) Surgical repair of tricuspid atresia. Thorax 26:240–248CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Kukreja M, Bryant AS, Cleveland DC, Dabal R, Hingorani N, Kirklin JK (2015) Health-related quality of life in adult survivors after the Fontan operation. Semin Thorac Cardiovasc Surg 27:299. CrossRefPubMedGoogle Scholar
  4. 4.
    Gewillig M (2005) The Fontan circulation. Heart 91:839–846. CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Sutherland N, Jones B, d’Udekem Y (2015) Should we recommend exercise after the Fontan procedure? Heart Lung Circ 24:753–768. CrossRefPubMedGoogle Scholar
  6. 6.
    Opotowsky AR, Landzberg MJ, Earing MG, Wu FM, Triedman JK, Casey A, Ericson DA, Systrom D, Paridon SM, Rhodes J (2014) Abnormal spirometry after the Fontan procedure is common and associated with impaired aerobic capacity. Am J Physiol Heart Circ Physiol 307:H110–H117. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Sengupta P (2012) Health impacts of yoga and pranayama: a state-of-the-art review. Int J Prev Med 3:444–458PubMedPubMedCentralGoogle Scholar
  8. 8.
    Bernardi L, Passino C, Spadacini G, Bonfichi M, Arcaini L, Malcovati L, Bandinelli G, Schneider A, Keyl C, Feil P (2007) Reduced hypoxic ventilatory response with preserved blood oxygenation in yoga trainees and Himalayan Buddhist monks at altitude: evidence of a different adaptive strategy? Eur J Appl Physiol 99:511–518. CrossRefPubMedGoogle Scholar
  9. 9.
    Brown RP, Gerbarg PL (2009) Yoga breathing, meditation, and longevity. Ann NY Acad Sci 1172:54–62. CrossRefPubMedGoogle Scholar
  10. 10.
    Paul-Labrador M, Polk D, Dwyer JH, Velasquez I, Nidich S, Rainforth M, Schneider R, Merz CNB (2006) Effects of a randomized controlled trial of transcendental meditation on components of the metabolic syndrome in subjects with coronary heart disease. Arch Int Med 166:1218–1224. CrossRefGoogle Scholar
  11. 11.
    Bernardi L, Spadacini G, Bellwon J, Hajric R, Roskamm H, Frey AW (1998) Effect of breathing rate on oxygen saturation and exercise performance in chronic heart failure. Lancet 351:1308–1311. CrossRefPubMedGoogle Scholar
  12. 12.
    Fernandes M, Cukier A, Feltrim MIZ (2011) Efficacy of diaphragmatic breathing in patients with chronic obstructive pulmonary disease. Chron Respir Dis 8:237–244. CrossRefPubMedGoogle Scholar
  13. 13.
    Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J, ATS/ERS Task Force (2005) Standardisation of spirometry. Eur Respir J 26:319–338. CrossRefPubMedGoogle Scholar
  14. 14.
    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 26:948–968. CrossRefPubMedGoogle Scholar
  15. 15.
    Macintyre N, Crapo RO, Viegi G, Johnson DC, van der Grinten CP, Brusasco V, Burgos F, Casaburi R, Coates A, Enright P, Gustafsson P, Hankinson J, Jensen R, McKay R, Miller MR, Navajas D, Pedersen OF, Pellegrino R, Wanger J (2005) Standardization of the single-breath determination of carbon monoxide uptake in the lung. Eur Respir J 26:720–735. CrossRefPubMedGoogle Scholar
  16. 16.
    Campbell SC (1982) A comparison of the maximum voluntary ventilation with the forced expiratory volume in one second: an assessment of subject cooperation. J Occup Med 24:531–533PubMedGoogle Scholar
  17. 17.
    American Thoracic Society, American College of Chest Physicians (2003) ATS/ACCP statement on cardiopulmonary exercise testing. Am J Respir Crit Care Med 167: 211–277. CrossRefGoogle Scholar
  18. 18.
    Hill K, Jenkins SC, Philippe DL, Cecins N, Shepherd KL, Green DJ, Hillman DR, Eastwood PR (2006) High-intensity inspiratory muscle training in COPD. Eur Respir J 27:1119–1128. CrossRefPubMedGoogle Scholar
  19. 19.
    Shei RJ, Paris HL, Wilhite DP, Chapman RF, Mickleborough TD (2016) The role of inspiratory muscle training in the management of asthma and exercise-induced bronchoconstriction. Phys Sportsmed 26:1–8. Google Scholar
  20. 20.
    Geddes EL, O’Brien K, Reid WD, Brooks D, Crowe J (2008) Inspiratory muscle training in adults with chronic obstructive pulmonary disease: an update of a systematic review. Respir Med 102:1715–1729. CrossRefPubMedGoogle Scholar
  21. 21.
    Laoutaris I, Dritsas A, Brown MD, Manginas A, Alivizatos PA, Cokkinos DV (2004) Inspiratory muscle training using an incremental endurance test alleviates dyspnea and improves functional status in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil 11:489–496CrossRefPubMedGoogle Scholar
  22. 22.
    Zeren M, Demir R, Yigit Z, Gurses HN (2016) Effects of inspiratory muscle training on pulmonary function, respiratory muscle strength and functional capacity in patients with atrial fibrillation: a randomized controlled trial. Clin Rehabil 30:1165–1174. CrossRefPubMedGoogle Scholar
  23. 23.
    Jung JH, Kim NS (2016) Relative activity of respiratory muscles during prescribed inspiratory muscle training in healthy people. J Phys Ther Sci 28:1046–1049. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Silva IS, Fregonezi GA, Dias FA, Ribeiro CT, Guerra RO, Ferreira GM (2013) Inspiratory muscle training for asthma. Cochrane Database Syst Rev 8:CD003792. Google Scholar
  25. 25.
    Zhu E, Petrof BJ, Gea J, Comtois N, Grassino AE (1997) Diaphragm muscle fiber injury after inspiratory resistive breathing. Am J Respir Crit Care Med 155:1110–1116. CrossRefPubMedGoogle Scholar
  26. 26.
    Anzueto A, Andrade FH, Maxwell LC, Levine SM, Lawrence RA, Gibbons WJ, Jenkinson SG (1992) Resistive breathing activates the glutathione redox cycle and impairs performance of rat diaphragm. J Appl Physiol 72:529–534CrossRefPubMedGoogle Scholar
  27. 27.
    Penny D, Hayek Z, Redington A (1991) The effects of positive and negative extrathoracic pressure ventilation on pulmonary blood flow after the total cavopulmonary shunt procedure. Int J Cardiol 30:128–130CrossRefPubMedGoogle Scholar
  28. 28.
    Shekerdemian LS, Bush A, Shore DF, Lincoln C, Redington AN (1997) Cardiopulmonary interactions after Fontan operations augmentation of cardiac output using negative pressure ventilation. Circulation 96:3934–3942. CrossRefPubMedGoogle Scholar
  29. 29.
    Penny DJ, Redington AN (1991) Doppler echocardiography evaluation of pulmonary blood flow after the Fontan operation: the role of the lungs. Br Heart J 66:372–374CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    La Gerche A, Gewilling M (2010) What limits cardiac performance during exercise in normal subjects and in healthy Fontan patients?. Int J Pediatr. PubMedPubMedCentralGoogle Scholar
  31. 31.
    Gewilling M, Brown SC, Eyskens B, Heying R, Ganame J, Budts W, La Gerche A, Gorenflo M (2010) The Fontan circulation: who controls cardiac output? Interact Cardiovasc Thorac Surg 10:428–433. CrossRefGoogle Scholar
  32. 32.
    Gewillig M, Brown SC (2016) The Fontan circulation after 45 years: update in physiology. Heart 102:1081–1086. CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Redington AN (2014) Low cardiac output due to acute right ventricular dysfunction and cardiopulmonary interactions in congenital heart disease. Pulm Circ 4:191–199. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Robbers-Visser D, Jan Ten Harkel D, Kapusta L, Strengers JL, Dalinghaus M, Meijboom FJ, Pattynama PM, Bogers AJ, Helbing WA (2008) Usefulness of cardiac magnetic resonance imaging combined with low-dose dobutamine stress to detect an abnormal ventricular stress response in children and young adults after Fontan operation at young age. Am J Cardiol 101:1657–1662. CrossRefPubMedGoogle Scholar
  35. 35.
    Robbers-Visser D, Helderman F, Strengers JL, van Osch-Gevers L, Kapusta L, Pattynama PM, Bogers AJ, Krams R, Helbing WA (2008) Pulmonary artery size and function after Fontan operation at a young age. J Magn Reson Imaging 28:1101–1107. CrossRefPubMedGoogle Scholar
  36. 36.
    Giardini A, Balducci A, Specchia S, Gargiulo G, Bonvicini M, Picchio FM (2008) Effect of sildenafil on haemodynamic response to exercise and exercise capacity in Fontan patients. Eur Heart J 29:1681–1687. CrossRefPubMedGoogle Scholar
  37. 37.
    Shafer KM, Garcia JA, Babb TG, Fixler DE, Ayers CR, Levine BD (2012) The importance of the muscle and ventilatory blood pumps during exercise in patients without a subpulmonary ventricle (Fontan operation). J Am Coll Cardiol 60:2115–2121. CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Dua JS, Cooper AR, Fox KR, Stuart AG (2010) Exercise training in adults with congenital heart disease: feasibility and benefits. Int J Cardiol 138:196–205. CrossRefPubMedGoogle Scholar
  39. 39.
    Longmuir PE, Tyrrell PN, Corey M, Faulkner G, Russell JL, McCrindle BW (2013) Home-based rehabilitation enhances daily physical activity and motor skill in children who have undergone the fontan procedure. Pediatric Cardiol 34:1130–1151. CrossRefGoogle Scholar
  40. 40.
    Minamisawa S, Nakazawa M, Momma K, Imai Y, Satomi G (2001) Effect of aerobic training on exercise performance in patients after the Fontan operation. Am J Cardiol 88:695–698. CrossRefPubMedGoogle Scholar
  41. 41.
    Moalla W, Elloumi M, Chamari K, Dupont G, Maingourd Y, Tabka Z, Ahmaidi S (2012) Training effects on peripheral muscle oxygenation and performance in children with congenital heart diseases. Appl Physiol Nutr Metab 37:621–630. CrossRefPubMedGoogle Scholar
  42. 42.
    Ruttenberg HD, Adams TD, Orsmond GS, Conlee RK, Fisher AG (1983) Effects of exercise training on aerobic fitness in children after open heart surgery. Pediatr Cardiol 4:19–24. CrossRefPubMedGoogle Scholar
  43. 43.
    Opocher F, Varnier M, Sanders SP, Tosoni A, Zaccaria M, Stellin G, Milanesi O (2005) Effects of aerobic exercise training in children after the Fontan operation. Am J Cardiol 95:150–152. CrossRefPubMedGoogle Scholar
  44. 44.
    Pike NA, Evangelista LS, Doering LV, Eastwood JA, Lewis AB, Child JS (2012) Quality of life, health status, and depression: comparison between adolescents and adults after the Fontan procedure with healthy counterparts. J Cardiovasc Nurs 27:539. CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Ray US, Pathak A, Tomer OS (2011) Hatha yoga practices: energy expenditure, respiratory changes and intensity of exercise. Evid Based Complement Alternat Med 2011:241294. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Lamia Ait Ali
    • 1
    • 2
  • Alessandro Pingitore
    • 1
  • Paolo Piaggi
    • 5
  • Fabio Brucini
    • 1
  • Mirko Passera
    • 1
  • Marco Marotta
    • 2
  • Alessandra Cadoni
    • 3
  • Claudio Passino
    • 2
    • 4
  • Giosuè Catapano
    • 2
  • Pierluigi Festa
    • 2
  1. 1.Clinical Physiology InstituteCNRPisaItaly
  2. 2.Fondazione G. Monasterio, Regione ToscanaPisaItaly
  3. 3.Pediatric CardiologyBrotzu HospitalCagliariItaly
  4. 4.Institute of Life SciencesScuola Superiore Sant’AnnaPisaItaly
  5. 5.National Institute of Diabetes and Digestive and Kidney DiseaseNational Institutes of HealthPhoenixUSA

Personalised recommendations