European Journal of Applied Physiology

, Volume 97, Issue 5, pp 607–612 | Cite as

Influence of different respiratory maneuvers on exercise-induced cardiac vagal inhibition

  • Ricardo Brandão Oliveira
  • Lauro Casqueiro Vianna
  • Djalma Rabelo Ricardo
  • Marcos Bezerra de Almeida
  • Claudio Gil S. Araújo
Original Article


Physical exercise inhibits cardiac vagal activity. To study the relationship between heart rate (HR) and respiratory pattern, we applied the 4-s exercise test (4sET) and measured cardiac vagal index (CVI) in 30 healthy subjects who served as their own controls, using the standard plus three additional variations, essentially respiratory, of the original protocol: (a) a maximum inspiratory apnea of 16 s, of which 8 s were in the pre-exercise phase (4sETinsp); (b) free respiratory pattern (4sETunc); and (c) maximum expiratory apnea of 12 s (4sETexp). The respective results were expressed by the following CVIs: CVIinsp, CVIunc and CVIexp. CVI was determined in a continuous digital ECG recording through a specific ratio of two RR interval durations. The results [(mean ± SEM)] for the four different maneuvers were as follows: CVI (1.56 ± 0.05), CVIinsp (1.55 ± 0.05), CVIunc (1.63 ± 0.05) and CVIexp (1.37 ± 0.02). ANOVA-Bonferroni significant differences were only found between CVIexp and CVIinsp (P = 0.009), CVIunc (P < 0.001) and CVI (P = 0.003). Dividing our sample in terciles according to CVI values, those with lower CVI, showed an attenuation of biphasic HR response after a 15 s maximum inspiratory apnea. We conclude that cardiac vagal reflex seems to be influencing the biphasic HR response modulation after a 12 s inspiratory apnea as described in the original protocol of 4sET, and this appears to be the option that best discriminates the cardiac vagal reflex, with less variability in the maneuvers when subjects are divided in terciles.


Autonomic nervous system 4-s Exercise test Heart rate Apnea 


  1. American Thoracic Society (ATS) (1995) Standardization of spirometry, 1994 update. Am J Respir Crit Care Med 152:1107–1136Google Scholar
  2. Araújo CGS, Nobrega AC, Castro CL (1992) Heart rate responses to deep breathing and 4-seconds of exercise before and after pharmacological blockade with atropine and propranolol. Clin Auton Res 2:35–40PubMedCrossRefGoogle Scholar
  3. Araújo CGS, Ricardo DR, Almeida MB (2003) Intra and interdays reliability of the 4-second exercise test. Rev Bras Med Esporte 9:299–303CrossRefGoogle Scholar
  4. Bernardi L, Porta C, Gabutti A, Spicuzza L, Sleight P (2001) Modulatory effects of respiration. Auton Neurosci 90:47–56PubMedCrossRefGoogle Scholar
  5. Clynes M (1960) Respiratory sinus arrhythmia: laws derived from computer simulation. J Appl Physiol 15:863–874PubMedGoogle Scholar
  6. Cole CR, Blackstone EH, Pashkow FJ, Snader CE, Lauer MS (1999) Heart-rate recovery immediately after exercise as a predictor of mortality. N Engl J Med 341:1351–1357PubMedCrossRefGoogle Scholar
  7. Davidson NS, Goldner S, McCloskey DI (1976) Respiratory modulation of barareceptor and chemoreceptor reflexes affecting heart rate and cardiac vagal efferent nerve activity. J Physiol 259:523–530PubMedGoogle Scholar
  8. Eckberg DL (2003). The human respiratory gate. J Physiol 548:339–352PubMedGoogle Scholar
  9. Eckberg DL, Kifle YT, Roberts VL (1980) Phase relationship between normal human respiration and baroreflex responsiveness. J Physiol 304:489–502PubMedGoogle Scholar
  10. Freyschuss U, Melcher A (1976). Respiratory sinus arrhythmia in man: relation to cardiovascular pressures. Scand J Clin Lab Invest 36:221–229PubMedCrossRefGoogle Scholar
  11. Haymet BT, McCloskey DI (1975) Baroreceptor and chemoreceptor influences on heart rate during the respiratory cycle in the dog. J Physiol 245:699–712PubMedGoogle Scholar
  12. Joels N, Samueloff M (1956) The activity of the medullary centres in diffusion respiration. J Physiol 133: 360–372PubMedGoogle Scholar
  13. Katona PG, Poitras JW, Barnett GO, Terry BS (1970) Cardiac vagal efferent activity and heart period in the carotid sinus reflex. Am J Physiol 218:1030–1037PubMedGoogle Scholar
  14. Kitney RI, Fulton T, McDonald AH, Linkens DA (1985) Transient interactions between blood pressure, respiration and heart rate in man. J Biomed Eng 7:217–224PubMedCrossRefGoogle Scholar
  15. Kleiger RE, Miller JP, Bigger JT Jr, Moss AJ (1987) Decreased heart rate variability and its association with increased mortality after acute myocardial infarction. Am J Cardiol 59:256–262PubMedCrossRefGoogle Scholar
  16. Knopfli BH, Bar-Or O (1999) Vagal activity and airway response to ipratropium bromide before and after exercise in ambient and cold conditions in healthy cross-country runners. Clin J Sport Med 9:170–176PubMedCrossRefGoogle Scholar
  17. Knopfli BH, Bar-Or O, Araújo CGS (2005) Effect of ipratropium bromide on EIB in children depends on vagal activity. Med Sci Sports Exerc 37:354–359PubMedCrossRefGoogle Scholar
  18. La Rovere MT, Bigger JT Jr, Marcus FI, Mortara A, Schwartz PJ (1998) Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators. Lancet 351:478–484PubMedCrossRefGoogle Scholar
  19. La Rovere MT, Bersano C, Gnemmi M, Specchia G, Schwartz PJ (2002) Exercise-induced increase in baroreflex sensitivity predicts improved prognosis after myocardial infarction. Circulation 106:945–949PubMedCrossRefGoogle Scholar
  20. Lazzoli JK, Silva Soares PP, Nobrega AC, Araújo CGS (2003) Electrocardiographic criteria for vagotonia-validation with pharmacological parasympathetic blockade in healthy subjects. Int J Cardiol 87:231–236PubMedCrossRefGoogle Scholar
  21. Levy MN, DeGeest H, Zieske H (1966) Effects of respiratory center activity on the heart. Circ Res 18:67–78PubMedGoogle Scholar
  22. Mehlsen J, Pagh K, Nielsen JS, Sestoft L, Nielsen SL (1987) Heart rate response to breathing: dependency upon breathing pattern. Clin Physiol 7:115–124PubMedCrossRefGoogle Scholar
  23. Melcher A (1980) Carotid baroreflex heart rate control during the active and the assisted breathing cycle in man. Acta Physiol Scand 108:165–171PubMedCrossRefGoogle Scholar
  24. Nobrega AC, Williamson JW, Araújo CGS, Friedman DB (1994) Heart rate and blood pressure responses at the onset of dynamic exercise: effect of Valsalva manoeuvre. Eur J Appl Physiol Occup Physiol 68:336–340PubMedCrossRefGoogle Scholar
  25. Ricardo DR, de Almeida MB, Franklin BA, Araújo CGS (2005) Initial and final exercise heart rate transients: influence of gender, aerobic fitness, and clinical status. Chest 127:318–327PubMedCrossRefGoogle Scholar
  26. Slonim NB, Hamilton LH (1987) Respiratory physiology, 5th edn. Mosby, Saint Louis, MO, pp 26–38Google Scholar
  27. Soares PP, Nobrega AC, Araújo CGS (1994) Initial heart rate transient at dynamic exercise performed in apnea. Influence of the variation rate of previous lung volume. Arq Bras Cardiol 63:287–292PubMedGoogle Scholar
  28. Yasuma F, Hayano J (2004) Respiratory sinus arrhythmia: why does the heartbeat synchronize with respiratory rhythm? Chest 125:683–690PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Ricardo Brandão Oliveira
    • 1
  • Lauro Casqueiro Vianna
    • 1
  • Djalma Rabelo Ricardo
    • 2
  • Marcos Bezerra de Almeida
    • 3
  • Claudio Gil S. Araújo
    • 1
    • 4
  1. 1.Universidade Gama FilhoRio de JaneiroBrazil
  2. 2.SUPREMAJuiz de ForaBrazil
  3. 3.UNIABEURio de JaneiroBrazil
  4. 4.CLINIMEX, Clínica de Medicina do ExercícioRio de JaneiroBrazil

Personalised recommendations