Advertisement

Left ventricular adaptation to high altitude: speckle tracking echocardiography in lowlanders, healthy highlanders and highlanders with chronic mountain sickness

  • Chantal Dedobbeleer
  • Alia Hadefi
  • Aurelien Pichon
  • Francisco Villafuerte
  • Robert Naeije
  • Philippe Unger
Original Paper

Abstract

Hypoxic exposure depresses myocardial contractility in vitro, but has been associated with indices of increased cardiac performance in intact animals and in humans, possibly related to sympathetic nervous system activation. We explored left ventricular (LV) function using speckle tracking echocardiography and sympathetic tone by spectral analysis of heart rate variability (HRV) in recently acclimatized lowlanders versus adapted or maladapted highlanders at high altitude. Twenty-six recently acclimatized lowlanders, 14 healthy highlanders and 12 highlanders with chronic mountain sickness (CMS) were studied. Control measurements at sea level were also obtained in the lowlanders. Altitude exposure in the lowlanders was associated with slightly increased blood pressure, decreased LV volumes and decreased longitudinal strain with a trend to increased prevalence of post-systolic shortening (p = 0.06), whereas the low frequency/high frequency (LF/HF) ratio increased (1.62 ± 0.81 vs. 5.08 ± 4.13, p < 0.05) indicating sympathetic activation. Highlanders had a similarly raised LF/HF ratio, but no alteration in LV deformation. Highlanders with CMS had no change in LV deformation, no significant increase in LF/HF, but decreased global HRV still suggestive of increased sympathetic tone, and lower mitral E/A ratio compared to healthy highlanders. Short-term altitude exposure in lowlanders alters indices of LV systolic function and increases sympathetic nervous system tone. Life-long altitude exposure in highlanders is associated with similar sympathetic hyperactivity, but preserved parameters of LV function, whereas diastolic function may be altered in those with CMS. Altered LV systolic function in recently acclimatized lowlanders may be explained by combined effects of hypoxia and changes in loading conditions.

Keywords

Hypoxia Altitude Left ventricular strain Myocardial deformation Chronic mountain sickness 

Notes

Acknowledgments

The authors wish to thank the expedition team, V. Faoro and P. Jespers for their helpful contribution and the Instituto de Investigaciones de la Altura Universidad Peruana Cayetano Heredia for the Cerro de Pasco Facilities.

Conflict of interest

None.

References

  1. 1.
    Hajjar RJ, Gwathmey JK (1990) Direct evidence of changes in myofilament responsiveness to Ca2+ during hypoxia and reoxygenation in myocardium. Am J Physiol 259:H784–H795PubMedGoogle Scholar
  2. 2.
    Silverman HS, Wei S, Haigney MC, Ocampo CJ, Stern MD (1997) Myocyte adaptation to chronic hypoxia and development of tolerance to subsequent acute severe hypoxia. Circ Res 80:699–707CrossRefPubMedGoogle Scholar
  3. 3.
    Tucker CE, James WE, Berry MA, Johnstone CJ, Grover RF (1976) Depressed myocardial function in the goat at high altitude. J Appl Physiol 41:356–361PubMedGoogle Scholar
  4. 4.
    Suarez J, Alexander JK, Houston CS (1987) Enhanced left ventricular systolic performance at high altitude during Operation Everest II. Am J Cardiol 60:137–142CrossRefPubMedGoogle Scholar
  5. 5.
    Allemann Y, Rotter M, Hutter D, Lipp E, Sartori C, Scherrer U, Seiler C (2004) Impact of acute hypoxic pulmonary hypertension on LV diastolic function in healthy mountaineers at high altitude. Am J Physiol Heart Circ Physiol 286:H856–H862CrossRefPubMedGoogle Scholar
  6. 6.
    Huez S, Faoro V, Guénard H, Martinot JB, Naeije R (2009) Echocardiographic and tissue Doppler imaging of cardiac adaptation to high altitude in native highlanders versus acclimatized lowlanders. Am J Cardiol 103:1605–1609CrossRefPubMedGoogle Scholar
  7. 7.
    Naeije R (2010) Physiological adaptation of the cardiovascular system to high altitude. Prog Cardiovasc Dis 52:456–466CrossRefPubMedGoogle Scholar
  8. 8.
    Dedobbeleer C, Hadefi A, Naeije R, Unger P (2013) Left ventricular adaptation to acute hypoxia: a speckle tracking imaging study. J Am Soc Echocardiogr 26:736–745CrossRefPubMedGoogle Scholar
  9. 9.
    Mor-Avi V, Lang RM, Badano LP et al (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. J Am Soc Echocardiogr 24:277–313CrossRefPubMedGoogle Scholar
  10. 10.
    Leon-Velarde F, Maggiorini M, Reeves JT et al (2005) Consensus statement on chronic and subacute high altitude diseases. High Alt Med Biol 6:147–157CrossRefPubMedGoogle Scholar
  11. 11.
    Keyl C, Schneider A, Gamboa A et al (2003) Autonomic cardiovascular function in high-altitude Andean natives with chronic mountain sickness. J Appl Physiol 94:213–219CrossRefPubMedGoogle Scholar
  12. 12.
    Roach RC, Bärtsch P, Hackett PH, Oelz O (1993) The Lake Louise acute mountain sickness scoring system. In: Sutton JR, Houston CS, Coates G (eds) Hypoxia and Mountain Medicine. Queen City, Burlington, pp 327–330Google Scholar
  13. 13.
    Groepenhoff H, Overbeek MJ, Mulè M et al (2012) Exercice pathophysiology in patients with chronic mountain sickness. Chest 2012(142):877–884CrossRefGoogle Scholar
  14. 14.
    Lang RM, Bierig M, Devereux RB et al (2005) Chamber Quantification Writing Group. 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. American Society of Echocardiography’s Guidelines and Standards Committee; European Association of Echocardiography. J Am Soc Echocardiogr 18:1440–1463CrossRefPubMedGoogle Scholar
  15. 15.
    Atlas G, Berger J, Dhar S (2010) Afterload assessment with or without central venous pressure: a preliminary clinical comparison. Cardiovasc Eng 10:246–252CrossRefPubMedGoogle Scholar
  16. 16.
    Tei C, Ling LH, Hodge DO, Bailey KR et al (1995) New index of combined systolic and diastolic myocardial performance: a simple and reproducible measure of cardiac function–a study in normals and dilated cardiomyopathy. J Cardiol 26:357–366PubMedGoogle Scholar
  17. 17.
    Jurcut R, Giusca S, La Gerche A, Vasile S, Ginghina C, Voigt JU (2010) The echocardiographic assessment of the right ventricle: what to do in 2010? Eur J Echocardiogr 11:81–96CrossRefPubMedGoogle Scholar
  18. 18.
    Kircher BJ, Himelman RB, Schiller NB (1990) Noninvasive estimation of right atrial pressure from the inspiratory collapse of the inferior vena cava. Am J Cardiol 66:493–936CrossRefPubMedGoogle Scholar
  19. 19.
    Chemla D, Castelain V, Provencher S, Humbert M, Simonneau G, Hervé P (2009) Evaluation of various empirical formulas for estimating mean pulmonary artery pressure by using systolic pulmonary artery pressure in adults. Chest 135:760–768CrossRefPubMedGoogle Scholar
  20. 20.
    Abbas AE, Fortuin FD, Schiller NB, Appleton CP, Moreno CA, Lester SJ (2003) A simple method for noninvasive estimation of pulmonary vascular resistance. J Am Coll Cardiol 41:1021–1027CrossRefPubMedGoogle Scholar
  21. 21.
    Borg AN, Harrison JL, Argyle RA, Ray SG (2008) Left ventricular torsion in primary chronic mitral regurgitation. Heart 94:597–603CrossRefPubMedGoogle Scholar
  22. 22.
    Burns AT, La Gerche A, MacIsaac AI, Prior DL (2008) Augmentation of left ventricular torsion with exercise is attenuated with age. J Am Soc Echocardiogr 21:315–320CrossRefPubMedGoogle Scholar
  23. 23.
    Maliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84:482–492CrossRefGoogle Scholar
  24. 24.
    Pagani M, Mazzuero G, Ferrari A et al (1991) Sympathovagal interaction during mental stress: a study employing spectral analysis of heart rate variability in healthy controls and in patients with a prior myocardial infarction. Circulation (suppl II):11-43-11-51Google Scholar
  25. 25.
    Larsen PD, Tzeng YC, Sin PY, Galletly DC (2010) Respiratory sinus arrhythmia in conscious humans during spontaneous respiration. Respir Physiol Neurobiol 174:111–118CrossRefPubMedGoogle Scholar
  26. 26.
    Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Eur Heart J 17:354–381CrossRefGoogle Scholar
  27. 27.
    Winer BJ, Brown DR, Michels KM (1991) Statistical principles in experimental design, 3rd edn. Mc Grall-Hill, New York, pp 220–283Google Scholar
  28. 28.
    Sawka MN, Young AJ, Rock PB et al (1996) Altitude acclimatization and blood volume: effects of exogenous erythrocyte volume expansion. J Appl Physiol 81:636–642PubMedGoogle Scholar
  29. 29.
    Hainsworth R, Drinkhill MJ, Rivera-Chira M (2007) The autonomic nervous system at high altitude. Clin Auton Res 17:13–19CrossRefPubMedCentralPubMedGoogle Scholar
  30. 30.
    Tamisier R, Anand A, Nieto LM, Cunnington D, Weiss JW (2005) Arterial pressure and muscle sympathetic nerve activity are increased after two hours of sustained but not cyclic hypoxia in healthy humans. J Appl Physiol 98:343–349CrossRefPubMedGoogle Scholar
  31. 31.
    Cikes M, Sutherland GR, Anderson LJ, Bijnens BH (2010) The role of echocardiographic deformation imaging in hypertrophic myopathies. Nat Rev Cardiol 7:384–396CrossRefPubMedGoogle Scholar
  32. 32.
    Huez S, Retailleau K, Unger P et al (2005) Right and left ventricular adaptation to hypoxia: a tissue Doppler imaging study. Am J Physiol Heart Circ Physiol 289:H1391–H1398CrossRefPubMedGoogle Scholar
  33. 33.
    Frøbert O, Moesgaard J, Toft E, Poulsen SH, Søgaard P (2004) Influence of oxygen tension on myocardial performance. Evaluation by tissue Doppler imaging. Cardiovasc Ultrasound 2(2):22CrossRefPubMedCentralPubMedGoogle Scholar
  34. 34.
    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 11:283–289CrossRefPubMedGoogle Scholar
  35. 35.
    A’roch R, Gustafsson U, Johansson G, Poelaert J, Haney M (2012) Left ventricular strain and peak systolic velocity: responses to controlled changes in load and contractility, explored in a porcine model. Cardiovasc Ultrasound 28(10):22CrossRefGoogle Scholar
  36. 36.
    Ishizu T, Seo Y, Baba M et al (2011) Impaired subendocardial wall thickening and post-systolic shortening are signs of critical myocardial ischemia in patients with flow-limiting coronary stenosis. Circ J 75:1934–1941CrossRefPubMedGoogle Scholar
  37. 37.
    Voigt JU, Lindenmeier G, Exner B et al (2003) Incidence and characteristics of segmental postsystolic longitudinal shortening in normal, acutely ischemic, and scarred myocardium. J Am Soc Echocardiogr 16:415–423CrossRefPubMedGoogle Scholar
  38. 38.
    Boussuges A, Molenat F, Burnet H et al (2000) Operation Everest III (Comex ‘97): modifications of cardiac function secondary to altitude-induced hypoxia. An echocardiographic and Doppler study. Am J Respir Crit Care Med 161:264–270CrossRefPubMedGoogle Scholar
  39. 39.
    Kjaergaard J, Snyder EM, Hassager C, Olson TP, Oh JK, Johnson BD (2006) The effect of 18 h of simulated high altitude on left ventricular function. Eur J Appl Physiol 98:411–418CrossRefPubMedGoogle Scholar
  40. 40.
    Naeije R, Dedobbeleer C (2013) Pulmonary hypertension and the right ventricle in hypoxia. Exp Physiol 98:1247–1256CrossRefPubMedGoogle Scholar
  41. 41.
    Leon-Velarde F, Villafuerte FC, Richalet JP (2010) Chronic mountain sickness and the heart. Prog Cardiovasc Dis 52:540–549CrossRefPubMedGoogle Scholar
  42. 42.
    Reeves JT, Leon-Velarde F (2004) Chronic mountain sickness: recent studies of the relationship between hemoglobin concentration and oxygen transport. High Alt Med Biol 5:147–155CrossRefPubMedGoogle Scholar
  43. 43.
    Ge RL, Mo VY, Januzzi JL et al (2011) B-type natriuretic peptide, vascular endothelial growth factor, endothelin-1, and nitric oxide synthase in chronic mountain sickness. Am J Physiol Heart Circ Physiol 300:H1427–H1433CrossRefPubMedGoogle Scholar
  44. 44.
    Rimoldi SF, Rexhaj E, Pratali L et al (2012) Systemic vascular dysfunction in patients with chronic mountain sickness. Chest 141:139–146CrossRefPubMedGoogle Scholar
  45. 45.
    Rivera-Ch M, León-Velarde F, Huicho L (2007) Treatment of chronic mountain sickness: critical reappraisal of an old problem. Respir Physiol Neurobiol 158:251–265CrossRefPubMedGoogle Scholar
  46. 46.
    Maignan M, Rivera-Ch M, Privat C, León-Velarde F, Richalet JP, Pham I (2009) Pulmonary pressure and cardiac function in chronic mountain sickness patients. Chest 135:499–504CrossRefPubMedGoogle Scholar
  47. 47.
    Klein AL, Burstow DJ, Tajik AJ, Zachariah PK, Bailey KR, Seward JB (1994) Effects of age on left ventricular dimensions and filling dynamics in 117 normal persons. Mayo Clin Proc 69:212–224CrossRefPubMedGoogle Scholar
  48. 48.
    Naeije R, Vanderpool R (2013) Pulmonary hypertension and chronic mountain sickness. High Alt Med Biol 14:117–125CrossRefPubMedGoogle Scholar
  49. 49.
    Zghal F, Bougteb H, Réant P, Lafitte S, Roudaut R (2011) Assessing global and regional left ventricular myocardial function in elderly patients using the bidimensional strain method. Echocardiography 28:978–982CrossRefPubMedGoogle Scholar
  50. 50.
    Reckefuss N, Butz T, Horstkotte D, Faber L (2011) Evaluation of longitudinal and radial left ventricular function by two-dimensional speckle-tracking echocardiography in a large cohort of normal probands. Int J Cardiovasc Imaging 27:515–526CrossRefPubMedGoogle Scholar
  51. 51.
    Stembridge M, Ainslie PN, Hughes MG et al (2014) Ventricular structure, function, and mechanics at high altitude: chronic remodeling in Sherpa vs. short-term lowlander adaptation. J Appl Physiol 117:334–343CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Chantal Dedobbeleer
    • 1
  • Alia Hadefi
    • 1
  • Aurelien Pichon
    • 2
  • Francisco Villafuerte
    • 3
  • Robert Naeije
    • 4
    • 1
  • Philippe Unger
    • 5
  1. 1.Department of Cardiology, Erasme University HospitalUniversité libre de BruxellesBrusselsBelgium
  2. 2.Cellular and Functional Responses to Hypoxia LaboratoryLaboratory of Excellence Gr-ExBobignyFrance
  3. 3.Laboratorio de Fisiología Comparada, Facultad de Ciencias y FilosofíaUniversidad Peruana Cayetano HerediaLimaPeru
  4. 4.Department of Pathophysiology, Erasme University HospitalUniversité libre de BruxellesBrusselsBelgium
  5. 5.Department of Cardiology, Centre Hospitalier Universitaire Saint PierreUniversité libre de BruxellesBrusselsBelgium

Personalised recommendations