Skip to main content
Log in

Myocardial blood flow and its transit time, oxygen utilization, and efficiency of highly endurance-trained human heart

  • Original Contribution
  • Published:
Basic Research in Cardiology Aims and scope Submit manuscript

Abstract

Highly endurance-trained athlete’s heart represents the most extreme form of cardiac adaptation to physical stress, but its circulatory alterations remain obscure. In the present study, myocardial blood flow (MBF), blood mean transit time (MTT), oxygen extraction fraction (OEF) and consumption (MVO2), and efficiency of cardiac work were quantified in highly trained male endurance athletes and control subjects at rest and during supine cycling exercise using [15O]-labeled radiotracers and positron emission tomography. Heart rate and MBF were lower in athletes both at rest and during exercise. OEF increased in response to exercise in both groups, but was higher in athletes (70 ± 21 vs. 63 ± 11 % at rest and 86 ± 13 vs. 73 ± 10 % during exercise). MTT was longer and vascular resistance higher in athletes both at rest and during exercise, but arterial content of 2,3-diphosphoglycerate (oxygen affinity) was unchanged. MVO2 per gram of myocardium trended (p = 0.08) lower in athletes both at rest and during exercise, while myocardial efficiency of work and MVO2 per beat were not different between groups. Arterial levels of free fatty acids were ~twofold higher in athletes likely leading to higher myocardial fatty acid oxidation and hence oxygen cost, which may have blunted the bradycardia-induced decrease in MVO2. Finally, the observed group differences in MBF, OEF, MTT and vascular resistance remained significant also after they were controlled for differences in MVO2. In conclusion, in highly endurance-trained human heart, increased myocardial blood transition time enables higher oxygen extraction levels with a lower myocardial blood flow and higher vascular resistance. These physiological adaptations to exercise training occur independently of the level of oxygen consumption and together with training-induced bradycardia may serve as mechanisms to increase functional reserve of the human heart.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Baumgartner H, Hung J, Bermejo J, Chambers JB, Evangelista A, Griffin BP, Iung B, Otto CM, Pellikka PA, Quinones M (2009) Echocardiographic assessment of valve stenosis: EAE/ASE recommendations for clinical practice. J Am Soc Echocardiogr 22:1–23. doi:10.1016/j.echo.2008.11.029

    Article  PubMed  Google Scholar 

  2. Binak K, Harmanci N, Sirmaci N, Ataman N, Ogan H (1967) Oxygen extraction rate of the myocardium at rest and on exercise in various conditions. Br Heart J 29:422–427. doi:10.1136/hrt.29.3.422

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Bing RJ, Siegel A, Vitale A, Balboni F, Sparks E, Taeschler M, Klapper M, Edwards S (1953) Metabolic studies on the human heart in vivo. I. Studies on carbohydrate metabolism of the human heart. Am J Med 15:284–296. doi:10.1016/0002-9343(53)90082-5

    Article  CAS  PubMed  Google Scholar 

  4. Breuer HW, Skyschally A, Schulz R, Martin C, Wehr M, Heusch G (1993) Heart rate variability and circulating catecholamine concentrations during steady state exercise in healthy volunteers. Br Heart J 70:144–149. doi:10.1136/hrt.70.2.144

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Camici PG, Olivotto I, Rimoldi OE (2012) The coronary circulation and blood flow in left ventricular hypertrophy. J Mol Cell Cardiol 52:857–864. doi:10.1016/j.yjmcc.2011.08.028

    Article  CAS  PubMed  Google Scholar 

  6. Duncker DJ, Bache RJ (2008) Regulation of coronary blood flow during exercise. Physiol Rev 88:1009–1086. doi:10.1152/physrev.00045.2006

    Article  CAS  PubMed  Google Scholar 

  7. Ferguson S, Gledhill N, Jamnik VK, Wiebe C, Payne N (2001) Cardiac performance in endurance-trained and moderately active young women. Med Sci Sports Exerc 33:1114–1119. doi:10.1097/00005768-200107000-00008

    Article  CAS  PubMed  Google Scholar 

  8. Gertz EW, Wisneski JA, Neese R, Houser A, Korte R, Bristow JD (1980) Myocardial lactate extraction: multi-determined metabolic function. Circulation 61:256–261. doi:10.1161/01.CIR.61.2.256

    Article  CAS  PubMed  Google Scholar 

  9. Gledhill N, Cox D, Jamnik R (1994) Endurance athletes’ stroke volume does not plateau: major advantage is diastolic function. Med Sci Sports Exerc 26:1116–1121. doi:10.1249/00005768-199409000-00008

    Article  CAS  PubMed  Google Scholar 

  10. Grubbstrom J, Berglund B, Kaijser L (1991) Myocardial blood flow and lactate metabolism at rest and during exercise with reduced arterial oxygen content. Acta Physiol Scand 142:467–474. doi:10.1111/j.1748-1716.1991.tb09181.x

    Article  CAS  PubMed  Google Scholar 

  11. Haskell WL, Sims C, Myll J, Bortz WM, St Goar FG, Alderman EL (1993) Coronary artery size and dilating capacity in ultradistance runners. Circulation 87:1076–1082. doi:10.1161/01.CIR.87.4.1076

    Article  CAS  PubMed  Google Scholar 

  12. Heinonen I, Nesterov SV, Liukko K, Kemppainen J, Nagren K, Luotolahti M, Virsu P, Oikonen V, Nuutila P, Kujala UM, Kainulainen H, Boushel R, Knuuti J, Kalliokoski KK (2008) Myocardial blood flow and adenosine A2A receptor density in endurance athletes and untrained men. J Physiol 586:5193–5202. doi:10.1113/jphysiol.2008.158113

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Heiss HW, Barmeyer J, Wink K, Hell G, Cerny FJ, Keul J, Reindell H (1976) Studies on the regulation of myocardial blood flow in man. I.: training effects on blood flow and metabolism of the healthy heart at rest and during standardized heavy exercise. Basic Res Cardiol 71:658–675. doi:10.1007/BF01906411

    Article  CAS  PubMed  Google Scholar 

  14. Heusch G (2012) Reprint of: the paradox of alpha-adrenergic coronary vasoconstriction revisited. J Mol Cell Cardiol 52:832–839. doi:10.1016/j.yjmcc.2011.12.010

    Article  CAS  PubMed  Google Scholar 

  15. Heusch G, Baumgart D, Camici P, Chilian W, Gregorini L, Hess O, Indolfi C, Rimoldi O (2000) Alpha-adrenergic coronary vasoconstriction and myocardial ischemia in humans. Circulation 101:689–694. doi:10.1161/01.CIR.101.6.689

    Article  CAS  PubMed  Google Scholar 

  16. Holtz J, Mayer E, Bassenge E (1977) Demonstration of alpha-adrenergic coronary control in different layers of canine myocardium by regional myocardial sympathectomy. Pflugers Arch 372:187–194. doi:10.1007/BF00585335

    Article  CAS  PubMed  Google Scholar 

  17. Huang SC, Barrio JR, Yu DC, Chen B, Grafton S, Melega WP, Hoffman JM, Satyamurthy N, Mazziotta JC, Phelps ME (1991) Modelling approach for separating blood time-activity curves in positron emission tomographic studies. Phys Med Biol 36:749–761. doi:10.1088/0031-9155/36/6/004

    Article  CAS  PubMed  Google Scholar 

  18. Iellamo F, Legramante JM, Pigozzi F, Spataro A, Norbiato G, Lucini D, Pagani M (2002) Conversion from vagal to sympathetic predominance with strenuous training in high-performance world class athletes. Circulation 105:2719–2724. doi:10.1161/01.CIR.0000018124.01299.AE

    Article  PubMed  Google Scholar 

  19. Iida H, Jones T, Miura S (1993) Modeling approach to eliminate the need to separate arterial plasma in oxygen-15 inhalation positron emission tomography. J Nucl Med 34:1333–1340

    CAS  PubMed  Google Scholar 

  20. Iida H, Rhodes CG, Araujo LI, Yamamoto Y, de Silva R, Maseri A, Jones T (1996) Noninvasive quantification of regional myocardial metabolic rate for oxygen by use of 15O2 inhalation and positron emission tomography. Theory, error analysis, and application in humans. Circulation 94:792–807. doi:10.1161/01.CIR.94.4.808

    Article  CAS  PubMed  Google Scholar 

  21. Iida H, Rhodes CG, de Silva R, Araujo LI, Bloomfield PM, Lammertsma AA, Jones T (1992) Use of the left ventricular time-activity curve as a noninvasive input function in dynamic oxygen-15-water positron emission tomography. J Nucl Med 33:1669–1677

    CAS  PubMed  Google Scholar 

  22. Kaijser L, Grubbstrom J, Berglund B (1993) Myocardial lactate release during prolonged exercise under hypoxaemia. Acta Physiol Scand 149:427–433. doi:10.1111/j.1748-1716.1993.tb09639.x

    Article  CAS  PubMed  Google Scholar 

  23. Kaijser L, Pernow J, Berglund B, Grubbstrom J, Lundberg JM (1994) Neuropeptide Y release from human heart is enhanced during prolonged exercise in hypoxia. J Appl Physiol 76:1346–1349

    Article  CAS  PubMed  Google Scholar 

  24. Kalsner S (1985) Cholinergic mechanisms in human coronary artery preparations: implications of species differences. J Physiol 358:509–526

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Kitamura K, Jorgensen CR, Gobel FL, Taylor HL, Wang Y (1972) Hemodynamic correlates of myocardial oxygen consumption during upright exercise. J Appl Physiol 32:516–522. doi:10.1016/0002-9149(70)90485-6

    CAS  PubMed  Google Scholar 

  26. Knaapen P, Germans T, Knuuti J, Paulus WJ, Dijkmans PA, Allaart CP, Lammertsma AA, Visser FC (2007) Myocardial energetics and efficiency: current status of the noninvasive approach. Circulation 115:918–927. doi:10.1161/CIRCULATIONAHA.106.660639

    Article  PubMed  Google Scholar 

  27. Kudomi N, Hayashi T, Watabe H, Teramoto N, Piao R, Ose T, Koshino K, Ohta Y, Iida H (2009) A physiologic model for recirculation water correction in CMRO2 assessment with 15O2 inhalation PET. J Cereb Blood Flow Metab 29:355–364. doi:10.1038/jcbfm.2008.132

    Article  PubMed  Google Scholar 

  28. Laaksonen MS, Heinonen I, Luotolahti M, Knuuti J, Kalliokoski KK (2014) VO2peak, myocardial hypertrophy, and myocardial blood flow in endurance-trained men. Med Sci Sports Exerc (in press)

  29. Laaksonen MS, Kalliokoski KK, Luotolahti M, Kemppainen J, Teras M, Kyrolainen H, Nuutila P, Knuuti J (2007) Myocardial perfusion during exercise in endurance-trained and untrained humans. Am J Physiol Regul Integr Comp Physiol 293:R837–R843. doi:10.1152/ajpregu.00771.2006

    Article  CAS  PubMed  Google Scholar 

  30. Laine H, Katoh C, Luotolahti M, Yki-Jarvinen H, Kantola I, Jula A, Takala TO, Ruotsalainen U, Iida H, Haaparanta M, Nuutila P, Knuuti J (1999) Myocardial oxygen consumption is unchanged but efficiency is reduced in patients with essential hypertension and left ventricular hypertrophy. Circulation 100:2425–2430. doi:10.1161/01.CIR.100.24.2425

    Article  CAS  PubMed  Google Scholar 

  31. Laughlin MH, Bowles DK, Duncker DJ (2012) The coronary circulation in exercise training. Am J Physiol Heart Circ Physiol 302:H10–H23. doi:10.1152/ajpheart.00574.2011

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Levine BD (2008) VO2max: what do we know, and what do we still need to know? J Physiol 586:25–34. doi:10.1113/jphysiol.2007.147629

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Levine BD, Lane LD, Buckey JC, Friedman DB, Blomqvist CG (1991) Left ventricular pressure-volume and Frank-Starling relations in endurance athletes. Implications for orthostatic tolerance and exercise performance. Circulation 84:1016–1023. doi:10.1161/01.CIR.84.3.1016

    Article  CAS  PubMed  Google Scholar 

  34. Maron BJ, Pelliccia A (2006) The heart of trained athletes: cardiac remodeling and the risks of sports, including sudden death. Circulation 114:1633–1644. doi:10.1161/CIRCULATIONAHA.106.613562

    Article  PubMed  Google Scholar 

  35. Mjos OD (1971) Effect of free fatty acids on myocardial function and oxygen consumption in intact dogs. J Clin Invest 50:1386–1389. doi:10.1172/JCI106621

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Neri Serneri GG, Boddi M, Modesti PA, Cecioni I, Coppo M, Padeletti L, Michelucci A, Colella A, Galanti G (2001) Increased cardiac sympathetic activity and insulin-like growth factor-I formation are associated with physiological hypertrophy in athletes. Circ Res 89:977–982. doi:10.1161/hh2301.100982

    Article  CAS  PubMed  Google Scholar 

  37. Opie LH, Knuuti J (2009) The adrenergic-fatty acid load in heart failure. J Am Coll Cardiol 54:1637–1646. doi:10.1016/j.jacc.2009.07.024

    Article  CAS  PubMed  Google Scholar 

  38. Pluim BM, Chin JC, de Roos A, Doornbos J, Siebelink HM, van der Laarse A, Vliegen HW, Lamerichs RM, Bruschke AV, van der Wall EE (1996) Cardiac anatomy, function and metabolism in elite cyclists assessed by magnetic resonance imaging and spectroscopy. Eur Heart J 17:1271–1278. doi:10.1093/oxfordjournals.eurheartj.a015046

    Article  CAS  PubMed  Google Scholar 

  39. Pluim BM, Lamb HJ, Kayser HW, Leujes F, Beyerbacht HP, Zwinderman AH, van der Laarse A, Vliegen HW, de Roos A, van der Wall EE (1998) Functional and metabolic evaluation of the athlete’s heart by magnetic resonance imaging and dobutamine stress magnetic resonance spectroscopy. Circulation 97:666–672. doi:10.1161/01.CIR.97.7.666

    Article  CAS  PubMed  Google Scholar 

  40. Pluim BM, Zwinderman AH, van der Laarse A, van der Wall EE (2000) The athlete’s heart. A meta-analysis of cardiac structure and function. Circulation 101:336–344. doi:10.1161/01.CIR.101.3.336

    Article  CAS  PubMed  Google Scholar 

  41. Radvan J, Choudhury L, Sheridan DJ, Camici PG (1997) Comparison of coronary vasodilator reserve in elite rowing athletes versus hypertrophic cardiomyopathy. Am J Cardiol 80:1621–1623. doi:10.1016/S0002-9149(97)00778-9

    Article  CAS  PubMed  Google Scholar 

  42. Sahn DJ, DeMaria A, Kisslo J, Weyman A (1978) Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58:1072–1083. doi:10.1161/01.CIR.58.6.1072

    Article  CAS  PubMed  Google Scholar 

  43. Saltin B (1985) Hemodynamic adaptations to exercise. Am J Cardiol 55:42D–47D. doi:10.1016/0002-9149(85)91054-9

    Article  CAS  PubMed  Google Scholar 

  44. Simonsen S, Kjekshus JK (1978) The effect of free fatty acids on myocardial oxygen consumption during atrial pacing and catecholamine infusion in man. Circulation 58:484–491. doi:10.1161/01.CIR.58.3.484

    Article  CAS  PubMed  Google Scholar 

  45. Stone HL (1980) Coronary flow, myocardial oxygen consumption, and exercise training in dogs. J Appl Physiol 49:759–768

    CAS  PubMed  Google Scholar 

  46. Stone HL (1983) Control of the coronary circulation during exercise. Annu Rev Physiol 45:213–227. doi:10.1146/annurev.ph.45.030183.001241

    Article  CAS  PubMed  Google Scholar 

  47. Takala TO, Nuutila P, Katoh C, Luotolahti M, Bergman J, Maki M, Oikonen V, Ruotsalainen U, Gronroos T, Haaparanta M, Kapanen J, Knuuti J (1999) Myocardial blood flow, oxygen consumption, and fatty acid uptake in endurance athletes during insulin stimulation. Am J Physiol 277:E585–E590

    CAS  PubMed  Google Scholar 

  48. 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. Circulation 93:1043–1065. doi:10.1161/01.CIR.93.5.1043

    Article  Google Scholar 

  49. Tuunanen H, Engblom E, Naum A, Nagren K, Hesse B, Airaksinen KE, Nuutila P, Iozzo P, Ukkonen H, Opie LH, Knuuti J (2006) Free fatty acid depletion acutely decreases cardiac work and efficiency in cardiomyopathic heart failure. Circulation 114:2130–2137. doi:10.1161/CIRCULATIONAHA.106.645184

    Article  CAS  PubMed  Google Scholar 

  50. von Restorff RW, Holtz J, Bassenge E (1977) Exercise induced augmentation of myocardial oxygen extraction in spite of normal coronary dilatory capacity in dogs. Pflugers Arch 372:181–185. doi:10.1007/BF00585334

    Article  Google Scholar 

  51. Wisneski JA, Gertz EW, Neese RA, Gruenke LD, Morris DL, Craig JC (1985) Metabolic fate of extracted glucose in normal human myocardium. J Clin Invest 76:1819–1827. doi:10.1172/JCI112174

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Yamamoto Y, de Silva R, Rhodes CG, Iida H, Lammertsma AA, Jones T, Maseri A (1996) Noninvasive quantification of regional myocardial metabolic rate of oxygen by 15O2 inhalation and positron emission tomography. Experimental validation. Circulation 94:808–816. doi:10.1161/01.CIR.94.4.808

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The study was conducted within the Centre of Excellence in Molecular Imaging in Cardiovascular and Metabolic Research—supported by the Academy of Finland, University of Turku, Turku University Hospital and Åbo Akademi University. The authors want to thank the personnel of Turku PET Centre for their excellent assistance. The study was financially supported by the Ministry of Education of the State of Finland (Grants 74/627/2006, 58/627/2007, and 45/627/2008), the Academy of Finland (Grants 108539, 214329 and 251572, and Centre of Excellence funding), the Finnish Cardiovascular Foundation, the Finnish Cultural Foundation and its South-Western Fund, the Finnish Sport Research Foundation, and the Hospital District of Southwest Finland.

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ilkka Heinonen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Heinonen, I., Kudomi, N., Kemppainen, J. et al. Myocardial blood flow and its transit time, oxygen utilization, and efficiency of highly endurance-trained human heart. Basic Res Cardiol 109, 413 (2014). https://doi.org/10.1007/s00395-014-0413-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00395-014-0413-1

Keywords

Navigation