Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Delayed parasympathetic reactivation and sympathetic withdrawal following maximal cardiopulmonary exercise testing (CPET) in hypoxia

Abstract

Purpose

This study investigated the effects of acute hypoxic exposure on post-exercise cardiac autonomic modulation following maximal cardiopulmonary exercise testing (CPET).

Methods

Thirteen healthy men performed CPET and recovery in normoxia (N) and normobaric hypoxia (H) (FiO2 = 13.4%, ≈ 3500 m). Post-exercise cardiac autonomic modulation was assessed during recovery (300 s) through the analysis of fast-phase and slow-phase heart rate recovery (HRR) and heart rate variability (HRV) indices.

Results

Both short-term, T30 (mean difference (MD) 60.0 s, 95% CI 18.2–101.8, p = 0.009, ES 1.01), and long-term, HRRt (MD 21.7 s, 95% CI 4.1–39.3, p = 0.020, ES 0.64), time constants of HRR were higher in H. Fast-phase (30 and 60 s) and slow-phase (300 s) HRR indices were reduced in H either when expressed in bpm or in percentage of HRpeak (p < 0.05). Chronotropic reserve recovery was lower in H than in N at 30 s (MD − 3.77%, 95% CI − 7.06 to − 0.49, p = 0.028, ES − 0.80) and at 60 s (MD − 7.23%, 95% CI − 11.45 to − 3.01, p = 0.003, ES − 0.81), but not at 300 s (p = 0.436). Concurrently, Ln-RMSSD was reduced in H at 60 and 90 s (p < 0.01) but not at other time points during recovery (p > 0.05).

Conclusions

Affected fast-phase, slow-phase HRR and HRV indices suggested delayed parasympathetic reactivation and sympathetic withdrawal after maximal exercise in hypoxia. However, a similar cardiac autonomic recovery was re-established within 5 min after exercise cessation. These findings have several implications in cardiac autonomic recovery interpretation and in HR assessment in response to high-intensity hypoxic exercise.

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

Fig. 1

Abbreviations

ANOVA:

Analysis of variance

ANS:

Autonomic nervous system

CPET:

Cardiopulmonary exercise testing

CRR:

Chronotropic reserve recovery

EPOCt:

Excess of post-exercise oxygen consumption time constant

EPOCMAG :

Excess of post-exercise oxygen consumption magnitude

LF:

Low-frequency spectral power

Ln:

Natural logarithm transformation

HF:

High-frequency spectral power

HR:

Heart rate

HRR:

Heart rate recovery

HRRt:

Long-term time constant of heart rate recovery

HRV:

Heart rate variability

RMSSD:

Root mean square of successive differences of R–R intervals

T30:

Short-term time constant of heart rate recovery

TP:

Total spectral power

References

  1. Achten J, Jeukendrup AE (2003) Heart rate monitoring. Sport Med 33:517–538

  2. Al Haddad H, Laursen PB, Chollet D et al (2010) Effect of cold or thermoneutral water immersion on post-exercise heart rate recovery and heart rate variability indices. Auton Neurosci 156:111–116. https://doi.org/10.1016/j.autneu.2010.03.017

  3. Al Haddad H, Mendez-Villanueva A, Bourdon PC, Buchheit M (2012) Effect of acute hypoxia on post-exercise parasympathetic reactivation in healthy men. Front Physiol 3:289

  4. Albouaini K, Egred M, Alahmar A, Wright DJ (2007) Cardiopulmonary exercise testing and its application. Postgrad Med J 83:675–682. https://doi.org/10.1136/hrt.2007.121558

  5. Amann M, Kayser B (2009) Nervous system function during exercise in hypoxia. High Alt Med Biol 10:149–164. https://doi.org/10.1089/ham.2008.1105

  6. Barak OF, Ovcin ZB, Jakovljevic DG et al (2011) Heart rate recovery after submaximal exercise in four different recovery protocols in male athletes and non-athletes. J Sports Sci Med 10:369–375

  7. Bellenger CR, Fuller JT, Thomson RL et al (2016) Monitoring athletic training status through autonomic heart rate regulation: a systematic review and meta-analysis. Sport Med 46:1461–1486. https://doi.org/10.1007/s40279-016-0484-2

  8. Borg E, Borg G (2002) A comparison of AME and CR100 for scaling perceived exertion. Acta Psychol (Amst) 109:157–175. https://doi.org/10.1016/S0001-6918(01)00055-5

  9. Borresen J, Lambert MI (2008) Autonomic control of heart rate during and after exercise: measurements and implications for monitoring training status. Sports Med 38:633–646

  10. Bourdillon N, Saugy J, Schmitt L et al (2017) Acute and chronic changes in baroreflex sensitivity in hypobaric vs. normobaric hypoxia. Eur J Appl Physiol 117:2401–2407. https://doi.org/10.1007/s00421-017-3726-6

  11. Brocherie F, Girard O, Faiss R, Millet GP (2017) Effects of repeated-sprint training in hypoxia on sea-level performance: a meta-analysis. Sport Med 47:1651–1660. https://doi.org/10.1007/s40279-017-0685-3

  12. Buchheit M, Richard R, Doutreleau S et al (2004) Effect of acute hypoxia on heart rate variability at rest and during exercise. Int J Sports Med 25:264–269

  13. Buchheit M, Laursen PB, Ahmaidi S (2007a) Parasympathetic reactivation after repeated sprint exercise. AJP Hear Circ Physiol 293:H133–H141. https://doi.org/10.1152/ajpheart.00062.2007

  14. Buchheit M, Papelier Y, Laursen PB, Ahmaidi S (2007b) Noninvasive assessment of cardiac parasympathetic function: postexercise heart rate recovery or heart rate variability? AJP Hear Circ Physiol 293:H8–H10. https://doi.org/10.1152/ajpheart.00335.2007

  15. Buchheit M, Al Haddad H, Laursen PB, Ahmaidi S (2009a) Effect of body posture on postexercise parasympathetic reactivation in men. Exp Physiol 94:795–804. https://doi.org/10.1113/expphysiol.2009.048041

  16. Buchheit M, Peiffer JJ, Abbiss CR, Laursen PB (2009b) Effect of cold water immersion on postexercise parasympathetic reactivation. Am J Physiol Circ Physiol 296:H421–H427. https://doi.org/10.1152/ajpheart.01017.2008

  17. Calbet JAL, Boushel R, Rådegran G et al (2003) Determinants of maximal oxygen uptake in severe acute hypoxia. Am J Physiol Regul Integr Comp Physiol 284:R291–R303. https://doi.org/10.1152/ajpregu.00155.2002

  18. Calbet JAL, Robach P, Lundby C (2009) The exercising heart at altitude. Cell Mol Life Sci 66:3601–3613. https://doi.org/10.1007/s00018-009-0148-6

  19. Chapman RF, Karlsen T, Resaland GK et al (2014) Defining the “dose” of altitude training: how high to live for optimal sea level performance enhancement. J Appl Physiol 116:595–603. https://doi.org/10.1152/japplphysiol.00634.2013

  20. Clark SA, Bourdon PC, Schmidt W et al (2007) The effect of acute simulated moderate altitude on power, performance and pacing strategies in well-trained cyclists. Eur J Appl Physiol 102:45–55. https://doi.org/10.1007/s00421-007-0554-0

  21. Cottin F, Médigue C, Leprêtre P-M et al (2004) Heart rate variability during exercise performed below and above ventilatory threshold. Med Sci Sports Exerc 36:594–600

  22. Cunha FA, Midgley AW, Gonçalves T et al (2015) Parasympathetic reactivation after maximal CPET depends on exercise modality and resting vagal activity in healthy men. Springerplus 4:100. https://doi.org/10.1186/s40064-015-0882-1

  23. Danieli A, Lusa L, Potočnik N et al (2014) Resting heart rate variability and heart rate recovery after submaximal exercise. Clin Auton Res 24:53–61

  24. de Oliveira Ottone V, de Castro Magalhães F, de Paula F et al (2014) The effect of different water immersion temperatures on post-exercise parasympathetic reactivation. PLoS One 9:e113730. https://doi.org/10.1371/journal.pone.0113730

  25. Dinenno FA (2016) Skeletal muscle vasodilation during systemic hypoxia in humans. J Appl Physiol 120:216–225. https://doi.org/10.1152/japplphysiol.00256.2015

  26. do Nascimento Salvador PC, de Aguiar RA, Teixeira AS et al (2016) Are the oxygen uptake and heart rate off-kinetics influenced by the intensity of prior exercise? Respir Physiol Neurobiol 230:60–67. https://doi.org/10.1016/j.resp.2016.05.007

  27. Duffin J (2007) Measuring the ventilatory response to hypoxia. J Physiol 584:285–293. https://doi.org/10.1113/jphysiol.2007.138883

  28. Esco MR, Olson MS, Williford HN et al (2010) The relationship between resting heart rate variability and heart rate recovery. Clin Auton Res 20:33–38. https://doi.org/10.1007/s10286-009-0033-2

  29. Faiss R, Girard O, Millet GP (2013) Advancing hypoxic training in team sports: from intermittent hypoxic training to repeated sprint training in hypoxia. Br J Sports Med 47:i45–i50. https://doi.org/10.1136/bjsports-2013-092741

  30. Favret F, Richalet J-P (2007) Exercise and hypoxia: the role of the autonomic nervous system. Respir Physiol Neurobiol 158:280–286. https://doi.org/10.1016/j.resp.2007.04.001

  31. Fisher JP (2015) Cardiac autonomic regulation during hypoxic exercise. Am J Physiol Hear Circ Physiol 308:H1474–H1475. https://doi.org/10.1152/ajpheart.00311.2015

  32. Gaston A-F, Durand F, Roca E et al (2016) Exercise-induced hypoxaemia developed at sea-level influences responses to exercise at moderate altitude. PLoS One 11:e0161819. https://doi.org/10.1371/journal.pone.0161819

  33. Giles D, Kelly J, Draper N (2016) Alterations in autonomic cardiac modulation in response to normobaric hypoxia. Eur J Sport Sci 16:1023–1031

  34. Girard O, Malatesta D, Millet GP (2017) Walking in hypoxia: an efficient treatment to lessen mechanical constraints and improve health in obese individuals? Front Physiol 8:73. https://doi.org/10.3389/fphys.2017.00073

  35. Goldberger JJ, Le FK, Lahiri M et al (2006) Assessment of parasympathetic reactivation after exercise. AJP Hear Circ Physiol 290:H2446–H2452. https://doi.org/10.1152/ajpheart.01118.2005

  36. Goodwin ML, Harris JE, Herna¡ndez A, Gladden LB (2007) Blood lactate measurements and analysis during exercise: a guide for clinicians. J Diabetes Sci Technol 1:558–569

  37. Grataloup O, Busso T, Castells J et al (2007) Evidence of decrease in peak heart rate in acute hypoxia: effect of exercise-induced arterial hypoxemia. Int J Sports Med 28:181–185. https://doi.org/10.1055/s-2006-924216

  38. Hainsworth R, Drinkhill MJ, Rivera-Chira M (2007) The autonomic nervous system at high altitude. Clin Auton Res 17:13–19. https://doi.org/10.1007/s10286-006-0395-7

  39. Hopkins WG, Marshall SW, Batterham AM, Hanin J (2009) Progressive statistics for studies in sports medicine and exercise science. Med Sci Sport Exerc 41:3–13. https://doi.org/10.1249/MSS.0b013e31818cb278

  40. Imai K, Sato H, Hori M et al (1994) Vagally mediated heart rate recovery after exercise is accelerated in athletes but blunted in patients with chronic heart failure. J Am Coll Cardiol 24:1529–1535

  41. Iwasaki K, Ogawa Y, Aoki K et al (2006) Cardiovascular regulation response to hypoxia during stepwise decreases from 21 to 15% inhaled oxygen. Aviat Space Environ Med 77:1015–1019

  42. Kuipers H, Verstappen FT, Keizer HA, Geurten P, Van Kranenburg G (1985) Variability of aerobic performance in the laboratory and its physiologic correlates. Int J Sports Med 6(04):197–201

  43. Lizamore CA, Hamlin MJ (2017) The use of simulated altitude techniques for beneficial cardiovascular health outcomes in nonathletic, sedentary, and clinical populations: a literature review. High Alt Med Biol ham. https://doi.org/10.1089/ham.2017.0050

  44. Lundby C, Saltin B, van Hall G (2000) The “lactate paradox”, evidence for a transient change in the course of acclimatization to severe hypoxia in lowlanders. Acta Physiol Scand 170:265–269. https://doi.org/10.1046/j.1365-201x.2000.00785.x

  45. Malik M (1996) Heart rate variability. Ann Noninvasive Electrocardiol 1:151–181

  46. Mann TN, Webster C, Lamberts RP, Lambert MI (2014) Effect of exercise intensity on post-exercise oxygen consumption and heart rate recovery. Eur J Appl Physiol 114:1809–1820. https://doi.org/10.1007/s00421-014-2907-9

  47. Michael S, Jay O, Halaki M et al (2016) Submaximal exercise intensity modulates acute post-exercise heart rate variability. Eur J Appl Physiol 116:697–706

  48. Michael S, Graham KS, Davis GM (2017a) Cardiac autonomic responses during exercise and post-exercise recovery using heart rate variability and systolic time intervals—a review. Front Physiol 8:301. https://doi.org/10.3389/fphys.2017.00301

  49. Michael S, Jay O, Graham KS, Davis GM (2017b) Longer exercise duration delays post-exercise recovery of cardiac parasympathetic but not sympathetic indices. Eur J Appl Physiol 117:1897–1906. https://doi.org/10.1007/s00421-017-3673-2

  50. Michael S, Jay O, Graham KS, Davis GM (2018) Influence of exercise modality on cardiac parasympathetic and sympathetic indices during post-exercise recovery. J Sci Med Sport. https://doi.org/10.1016/J.JSAMS.2018.01.015

  51. Millet GP, Roels B, Schmitt L et al (2010) Combining hypoxic methods for peak performance. Sport Med 40:1–25. https://doi.org/10.2165/11317920-000000000-00000

  52. Millet GP, Debevec T, Brocherie F et al (2016) Therapeutic use of exercising in hypoxia: promises and limitations. Front Physiol 7:224. https://doi.org/10.3389/fphys.2016.00224

  53. Molina GE, Fontana KE, Porto LGG, Junqueira LF (2016) Post-exercise heart-rate recovery correlates to resting heart-rate variability in healthy men. Clin Auton Res 26:415–421

  54. Mollard P, Woorons X, Letournel M et al (2007a) Role of maximal heart rate and arterial O2 saturation on the decrement of VO2max in moderate acute hypoxia in trained and untrained men. Int J Sports Med 28:186–192. https://doi.org/10.1055/s-2006-924215

  55. Mollard P, Woorons X, Letournel M et al (2007b) Determinants of maximal oxygen uptake in moderate acute hypoxia in endurance athletes. Eur J Appl Physiol 100:663–673. https://doi.org/10.1007/s00421-007-0457-0

  56. Nobrega ACL, O’Leary D, Silva BM et al (2014) Neural regulation of cardiovascular response to exercise: role of central command and peripheral afferents. Biomed Res Int 2014:1–20. https://doi.org/10.1155/2014/478965

  57. Ofner M, Wonisch M, Frei M et al (2014) Influence of acute normobaric hypoxia on physiological variables and lactate turn point determination in trained men. J Sports Sci Med 13:774–781

  58. Oliveira ALMB, Rohan P, de A, Gonçalves TR, et al (2017) Effects of hypoxia on heart rate variability in healthy individuals: a systematic review. Int J Cardiovasc Sci 30:251–261. https://doi.org/10.5935/2359-4802.20170035

  59. Pecanha T, Bartels R, Brito LC et al (2017) Methods of assessment of the post-exercise cardiac autonomic recovery: a methodological review. Int J Cardiol 227:795–802

  60. Peçanha T, de Brito LC, Fecchio RY et al (2016) Metaboreflex activation delays heart rate recovery after aerobic exercise in never-treated hypertensive men. J Physiol 594:6211–6223. https://doi.org/10.1113/JP272851

  61. Perini R, Veicsteinas A (2003) Heart rate variability and autonomic activity at rest and during exercise in various physiological conditions. Eur J Appl Physiol 90:317–325

  62. Qiu S, Cai X, Sun Z et al (2017) Heart rate recovery and risk of cardiovascular events and all-cause mortality: a meta-analysis of prospective cohort studies. J Am Heart Assoc 6:e005505. https://doi.org/10.1161/JAHA.117.005505

  63. Robergs RA, Dwyer D, Astorino T (2010) Recommendations for improved data processing from expired gas analysis indirect calorimetry. Sports Med 40(2):95–111

  64. Romero SA, Minson CT, Halliwill JR (2017) The cardiovascular system after exercise. J Appl Physiol 122:925–932. https://doi.org/10.1152/japplphysiol.00802.2016

  65. Schmitt L, Hellard P, Millet GP et al (2006) Heart rate variability and performance at two different altitudes in well-trained swimmers. Int J Sports Med 27:226–231

  66. Seiler S, Haugen O, Kuffel E (2007) Autonomic recovery after exercise in trained athletes: Intensity and duration effects. Med Sci Sports Exerc 39:1366–1373. https://doi.org/10.1249/mss.0b013e318060f17d

  67. Siebenmann C, Rasmussen P, Sørensen H et al (2015) Hypoxia increases exercise heart rate despite combined inhibition of β-adrenergic and muscarinic receptors. Am J Physiol Hear Circ Physiol 308:H1540–H1546. https://doi.org/10.1152/ajpheart.00861.2014

  68. Somers VK, Mark AL, Zavala DC, Abboud FM (1989) Influence of ventilation and hypocapnia on sympathetic nerve responses to hypoxia in normal humans. J Appl Physiol 67(5):2095–100

  69. Task Force of the European Society of C (1996) Heart rate variability standards of measurement, physiological interpretation, and clinical use. Eur Hear J 17:354–381

  70. Terziotti P, Schena F, Gulli G, Cevese A (2001) Post-exercise recovery of autonomic cardiovascular control: a study by spectrum and cross-spectrum analysis in humans. Eur J Appl Physiol 84:187–194. https://doi.org/10.1007/s004210170003

  71. Thayer JF, Ahs F, Fredrikson M et al (2012) A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev 36:747–756. https://doi.org/10.1016/j.neubiorev.2011.11.009

  72. van Hall G (2007) Counterpoint: the lactate paradox does not occur during exercise at high altitude. J Appl Physiol 102:2399–2401. https://doi.org/10.1152/japplphysiol.00039a.2007

  73. Ward SA, Grocott MPW, Levett DZH (2017) Exercise testing, supplemental oxygen, and hypoxia. Ann Am Thorac Soc 14:S140–S148. https://doi.org/10.1513/AnnalsATS.201701-043OT

  74. Wehrlin JP, Hallén J (2006) Linear decrease in VO2max and performance with increasing altitude in endurance athletes. Eur J Appl Physiol 96:404–412. https://doi.org/10.1007/s00421-005-0081-9

  75. West JB (2007) Point: the lactate paradox does/does not occur during exercise at high altitude. J Appl Physiol 102:2398–2399. https://doi.org/10.1152/japplphysiol.00039.2007

  76. Yamamoto Y, Hoshikawa Y, Miyashita M (1996) Effects of acute exposure to simulated altitude on heart rate variability during exercise. J Appl Physiol 81:1223–1229

  77. Zupet P, Princi T, Finderle Z (2009) Effect of hypobaric hypoxia on heart rate variability during exercise: a pilot field study. Eur J Appl Physiol 107:345–350

Download references

Acknowledgements

The authors would like to thank the subjects for their time and enthusiasm. The research was supported by the Ministry for Higher education, Research Innovation (France) and Tomsk Polytechnic University Competitiveness Enhancement Program Grant (Project No. ВИУ-ИСГТ-108/2017 - TPU CEP-HSTI-108/2017).

Author information

AF, AS, SS, LB, LM and BP participated in study conception and design. AF, AS and SS participated in data acquisition. AF, FSt, GB and AZ participated in data analysis. AF and LM were responsible for data interpretation. AF, AS, SS, GB, AZ, LM and BP contributed to the draft of the paper. AF, AS, SS, GB, AZ, FSc, LM and BP critically reviewed the manuscript. All authors approved the final version of the manuscript.

Correspondence to Alessandro Fornasiero.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by I. Mark Olfert.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 27 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fornasiero, A., Savoldelli, A., Skafidas, S. et al. Delayed parasympathetic reactivation and sympathetic withdrawal following maximal cardiopulmonary exercise testing (CPET) in hypoxia. Eur J Appl Physiol 118, 2189–2201 (2018). https://doi.org/10.1007/s00421-018-3945-5

Download citation

Keywords

  • Heart rate recovery
  • Hypoxia
  • Post-exercise recovery
  • Hypoxic exercise
  • Cardiac autonomic activity