Minute-Ventilation Variability during Cardiopulmonary Exercise Test is Higher in Sedentary Men Than in Athletes

Renata Rodrigues Teixeira de Castro Sabrina Pedrosa Lima Allan Robson Kluser Sales Antonio Claudio Lucas da Nóbrega About the authors

Abstract

Background:

The occurrence of minute-ventilation oscillations during exercise, named periodic breathing, exhibits important prognostic information in heart failure. Considering that exercise training could influence the fluctuation of ventilatory components during exercise, we hypothesized that ventilatory variability during exercise would be greater in sedentary men than athletes.

Objective:

To compare time-domain variability of ventilatory components of sedentary healthy men and athletes during a progressive maximal exercise test, evaluating their relationship to other variables usually obtained during a cardiopulmonary exercise test.

Methods:

Analysis of time-domain variability (SD/n and RMSSD/n) of minute-ventilation (Ve), respiratory rate (RR) and tidal volume (Vt) during a maximal cardiopulmonary exercise test of 9 athletes and 9 sedentary men was performed. Data was compared by two-tailed Student T test and Pearson´s correlations test.

Results:

Sedentary men exhibited greater Vt (SD/n: 1.6 ± 0.3 vs. 0.9 ± 0.3 mL/breaths; p < 0.001) and Ve (SD/n: 97.5 ± 23.1 vs. 71.6 ± 4.8 mL/min x breaths; p = 0.038) variabilities than athletes. VE/VCO2 correlated to Vt variability (RMSSD/n) in both groups.

Conclusions:

Time-domain variability of Vt and Ve during exercise is greater in sedentary than athletes, with a positive relationship between VE/VCO2 pointing to a possible influence of ventilation-perfusion ratio on ventilatory variability during exercise in healthy volunteers.

Keywords:
Breathing; Respiratory Function Tests; Sedentary Lifestyle; Athletes; Pulmonary Ventilation; Exercise

Resumo

Fundamento:

A ocorrência de oscilações de variabilidade ventilatória durante o exercício, denominada respiração periódica, apresenta importantes informações prognósticas na insuficiência cardíaca. Considerando que o treinamento físico poderia influenciar a flutuação dos componentes ventilatórios durante o exercício, nós hipotetizamos que a variabilidade ventilatória durante o exercício seria maior nos homens sedentários do que nos atletas.

Objetivo:

Comparar a variabilidade temporal das componentes ventilatórias de homens sedentários saudáveis e atletas durante um teste de esforço máximo progressivo, avaliando sua relação com outras variáveis normalmente obtidas durante um teste de exercício cardiopulmonar.

Métodos:

Foi realizada uma análise da variabilidade temporal (SD/n e RMSSD/n) da ventilação por minuto (Ve), da frequência respiratória (RR) e do volume corrente (Vt) durante um teste de exercício cardiopulmonar máximo em 9 atletas e 9 homens sedentários. Os dados foram comparados pelo teste T de Student bicaudal e pelo teste de correlação de Pearson.

Resultados:

Os homens sedentários apresentaram maior variabilidade Vt (SD/n: 1,6 ± 0,3 vs 0,9 ± 0,3 mL/respirações, p < 0,001) e Ve (SD/n: 97,5 ± 23,1 vs. 71,6 ± 4,8 mL/min x respirações; p = 0,038) do que os atletas. VE/VCO2 correlacionou-se à variabilidade de Vt (RMSSD/n) em ambos os grupos.

Conclusões:

A variabilidade temporal de Vt e Ve durante o exercício é maior em sedentários do que em atletas, com uma relação positiva entre VE/VCO2 apontando para uma possível influência da relação ventilação-perfusão na variabilidade ventilatória durante o exercício em voluntários saudáveis

Palavras-chave:
Respiração; Testes de Função Respiratória; Estilo de Vida Sedentário; Atletas; Ventilação Pulmonar; Exercício

Introduction

During a progressively increasing work rate exercise test, ventilation is expected to exhibit a curvilinear behavior when plotted against time, as work rate is increased above anaerobic threshold.11 Wasserman K, Hansen JE, Sue DY, Stringer WW, Whipp BJ. Principles of exercise testing and interpretation: including pathophysiology and clinical applications. Philadelphia: Lippincott Williams and Wilkins; 2005. Some heart failure patients' ventilation versus time plot does not comply with this physiological pattern and exhibits oscillations, with sequenced ups and downs in their ventilation versus time graphics during a cardiopulmonary exercise test. The presence of abnormal ventilatory oscillations in exercise test, named periodic breathing, is a powerful predictor of adverse outcome which prevalence varies from 25 to 31% of heart failure patients, depending on the criteria used to define it22 Ingle L, Isted A, Witte KK, Cleland JG, Clark AL. Impact of different diagnostic criteria on the prevalence and prognostic significance of exertional oscillatory ventilation in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil. 2009;16(4):451-6. and regardless of the presence of other classic prognostic parameters.33 Leite JJ, Mansur AJ, de Freitas HF, Chizola PR, Bocchi EA, Terra-Filho M, et al. Periodic breathing during incremental exercise predicts mortality in patients with chronic heart failure evaluated for cardiac transplantation. J Am Coll Cardiol. 2003;41(12):2175-81.,44 Sun XG, Hansen JE, Beshai JF, Wasserman K. Oscillatory breathing and exercise gas exchange abnormalities prognosticate early mortality and morbidity in heart failure. J Am Coll Cardiol. 2010;55(17):1814-23.

Recently, the prognostic value of oscillatory ventilation has been described in patients with heart failure with preserved ejection fraction55 Shafiq A, Brawner CA, Aldred HA, Lewis B, Williams CT, Tita C, et al. Prognostic value of cardiopulmonary exercise testing in heart failure with preserved ejection fraction. The Henry Ford HospITal CardioPulmonary EXercise Testing (FIT-CPX) project. Am Heart J. 2016;174:167-72.,66 Guazzi M, Myers J, Peberdy MA, Bensimhon D, Chase P, Arena R. Exercise oscillatory breathing in diastolic heart failure: prevalence and prognostic insights. Eur Heart J. 2008;29(22):2751-9. and its occurrence has been described in apparently healthy people.77 Guazzi M, Arena R, Pellegrino M, Bandera F, Generati G, Labate V, et al. Prevalence and characterization of exercise oscillatory ventilation in apparently healthy individuals at variable risk for cardiovascular disease: a subanalysis of the EURO-EX trial. Eur J Prev Cardiol. 2016;23(3):328-34. Despite the prognostic value of this ventilatory parameter, there is still disagreement about the criteria that should be used to detect this phenomenon.22 Ingle L, Isted A, Witte KK, Cleland JG, Clark AL. Impact of different diagnostic criteria on the prevalence and prognostic significance of exertional oscillatory ventilation in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil. 2009;16(4):451-6.,88 Cornelis J, Beckers P, Vanroy C, Volckaerts T, Vrints C, Vissers D. An overview of the applied definitions and diagnostic methods to assess exercise oscillatory ventilation--a systematic review. Int J Cardiol. 2015;190:161-9. Noteworthy, many variables that indicate prognosis in cardiopulmonary exercise tests are analyzed in a dichotomized approach. This means that a cut-off point categorize patients regarding their risk. Although this is convenient, there may be loss of important information.99 Myers J, Arena R, Cahalin LP, Labate V, Guazzi M. Cardiopulmonary exercise testing in heart failure. Curr Probl Cardiol. 2015;40(8):322-72. In fact, we have previously shown that some patients' ventilation versus time plot exhibits modest oscillations that although are not normal neither comply to any established criteria of periodic breathing.1010 Castro RR, Antunes-Correa LM, Ueno LM, Rondon MU, Negrao CE, Nobrega AC. Reversal of periodic breathing after aerobic training in heart failure. Eur Respir J. 2010;35(6):1409-11. Thus there is a grey area of ventilation variability pattern that is usually neglected by a binary approach. This is probably indicating that periodic breathing is the abnormal extreme of a more insidious process characterized by the inability to keep minute ventilation varying around an accepted set point. Thus, a method capable of quantifying the ventilation variability may not only add to the understanding of ventilatory patterns during exercise, but also to analyze prognosis in a leveled approach that could be more detailed than a binary one.

Time-domain variability techniques are used in cardiology for the analysis of heart rate variability. We have previously replicated this technique to analyze ventilatory variability in heart failure patients during a maximal exercise test.1010 Castro RR, Antunes-Correa LM, Ueno LM, Rondon MU, Negrao CE, Nobrega AC. Reversal of periodic breathing after aerobic training in heart failure. Eur Respir J. 2010;35(6):1409-11.,1111 Castro RR, Antunes-Correa LM, Ueno LM, Rondon MU, Negrao CE, Nobrega AC. Ventilation variability inversely correlates to ejection fraction in heart failure. Eur Respir J. 2010;36(6):1482-3.

Exercise training confers adaptations capable of modifying not only resting ventilatory parameters, but also their acute responses to a single exercise section.1212 Dempsey JA, Johnson BD, Saupe KW. Adaptations and limitations in the pulmonary system during exercise. Chest. 1990;97(3 Suppl):81S-7S. The adaptability of ventilatory variability to physical training is still unknown, but we have previously reported the reversal of periodic breathing, and reduction of ventilatory variability, after 14 weeks of cardiac rehabilitation in a patient with heart failure.1010 Castro RR, Antunes-Correa LM, Ueno LM, Rondon MU, Negrao CE, Nobrega AC. Reversal of periodic breathing after aerobic training in heart failure. Eur Respir J. 2010;35(6):1409-11.

Considering that exercise training could influence the fluctuation of ventilation during a progressive exercise test, we hypothesized that time-domain ventilatory variability during exercise would be greater in sedentary men than in athletes. Thus, the present study was designed to compare time-domain minute-ventilation variability of sedentary healthy men and athletes during a progressive maximal exercise test.

Methods

Volunteers

Eighteen male volunteers (9 sedentary and 9 athletes) were invited to participate in the study. All of them were considered healthy after clinical history and physical examination. None of them was a smoker or had been in regular use of any medication. Sedentary men were not involved in any regular physical activity during the last three months and have never been considered as athletes before. Athletes were professional soccer players from the same soccer team, playing first division in Rio de Janeiro, Brazil.

Study protocol

All volunteers provided written informed consent to participate in the study after full explanation of the procedures and their potential risks. The investigation conformed to the principles outlined in the Declaration of Helsinki and have been approved by the Institutional Research Ethics Committee on Human Research.

All volunteers performed a maximal cardiopulmonary treadmill (Trackmaster 30x30, USA) exercise test following an individualized ramp protocol up to exhaustion. All tests achieved at least three of the following criteria to be considered maximum:1313 Poole DC, Wilkerson DP, Jones AM. Validity of criteria for establishing maximal O2 uptake during ramp exercise tests. Eur J Appl Physiol. 2008;102(4):403-10. achievement of oxygen consumption (VO2) plateau; perceived exertion (modified BORG scale) = 10; achievement of maximal predicted heart rate (220-age); respiratory exchange ratio ≥ 1,10.

Cardiopulmonary exercise tests were performed with gas exchange and ventilatory variables being analyzed breath-by-breath using a calibrated computer-based exercise system (Ultima CardiO2 System, Medical Graphics Corporation, USA). The O2 and CO2 analyzers were calibrated before each test using a reference gas (12% O2; 5% CO2; nitrogen balance). The pneumotachograph used was also calibrated, with a 3L syringe using different flow profiles. During each cardiopulmonary exercise test, a 12-lead electrocardiogram was continuously recorded (Cardioperfect, Welch Allin, USA) and heart rate automatically derived. Carbon dioxide production (CO2), VO2, tidal volume (Vt) and respiratory rate (RR), were registered breath-by-breath. Minute ventilation (VE), O2 and CO2 ventilatory equivalents (VE/VO2 and VE/VCO2) were automatically calculated (Breeze Software 6.4.1, Medical Graphics, USA). All breath-by-breath results were exported to an Excel spreadsheet (Microsoft Corporation, USA), where standard deviation (SD) and root mean square successive difference (RMSSD) of VE during exercise test were calculated for each patient. Considering that the number of observations has a direct influence on variability measurement, results (SD and RMSSD) were normalized to the number of respiratory cycles during the test, reducing the probability that a greater number of observations registered in longer tests would be the sole responsible for greater variability (SD/n and RMSSD/n, respectively).1414 Castro R, Antunes-Correa LM, Ueno LM, Rondon MU, Negrão CE, Nóbrega AC. Ventilation variability inversely correlates to ejection fraction in heart failure. Eur Respir J. 2010;36(6):1482-3.

Statistical analysis

Statistical analysis was performed using the software Statistica 7.0 (Statsoft Inc, USA). Variables from the cardiopulmonary exercise tests showed normal distribution when analyzed by the Shapiro Wilk's test. Exercise variables in both groups were compared by paired two-tailed Student T test. Significance was set at p < 0.05. Results are presented as mean ± standard deviation.

A sample size of twelve individuals (6 in each group) would be needed to provide an 80% power with a 2-sided alpha of 0.05 to detect a difference of 10 ± 5 ml/min x breaths in SD/n ventilation variability between the two groups. Considering that ventilatory variability is a new variable, and that there are no published data to guide us regarding expected values, we have decided to increase sample in 50% and that is why the presented study included 18 individuals. After finishing the study, the calculated power of ventilatory variability is 100%.

Results

The demographic and anthropometric characteristics of both groups are described in table 1. All tests achieved the oxygen consumption plateau and a respiratory quotient greater than 1.10, and thus were considered maximum testes. Peak cardiopulmonary exercise data of both groups are shown in table 2.

Table 1
Demographic and anthropometric data of volunteers (n = 18)
Table 2
Peak exercise data during graded maximal cardiopulmonary exercise test performed by athletes and sedentary men in a treadmill

Sedentary men exhibited higher time-domain variability of minute-ventilation than athletes during cardiopulmonary exercise test, as showed in figure 1.

Figure 1
Minute-ventilation variability (SD/n and RMSSD/n) of athletes (green bars) and sedentary men (blue bars) during a graded maximal exercise test. * p < 0.05 vs. sedentary.

Discussion

The analysis of minute-ventilation curve during exercise has gained interest since the first reports of exercise oscillatory ventilation.1515 Ribeiro JP, Knutzen A, Rocco MB, Hartley LH, Colucci WS. Periodic breathing during exercise in severe heart failure. Reversal with milrinone or cardiac transplantation. Chest. 1987;92(3):555-6.,1616 Kremser CB, O'Toole MF, Leff AR. Oscillatory hyperventilation in severe congestive heart failure secondary to idiopathic dilated cardiomyopathy or to ischemic cardiomyopathy. Am J Cardiol. 1987;59(8):900-5. Although a lot of progress has been done regarding the prognosis value of this phenomenon since then,44 Sun XG, Hansen JE, Beshai JF, Wasserman K. Oscillatory breathing and exercise gas exchange abnormalities prognosticate early mortality and morbidity in heart failure. J Am Coll Cardiol. 2010;55(17):1814-23.,66 Guazzi M, Myers J, Peberdy MA, Bensimhon D, Chase P, Arena R. Exercise oscillatory breathing in diastolic heart failure: prevalence and prognostic insights. Eur Heart J. 2008;29(22):2751-9.,1717 Corra U, Giordano A, Bosimini E, Mezzani A, Piepoli M, Coats AJ, et al. Oscillatory ventilation during exercise in patients with chronic heart failure: clinical correlates and prognostic implications. Chest. 2002;121(5):1572-80. there was almost no progress in the quantification of this phenomenon.1818 Olson TP, Johnson BD. Quantifying oscillatory ventilation during exercise in patients with heart failure. Respir Physiol Neurobiol. 2014;190:25-32. There are currently two major diagnostic definitions of exercise oscillatory ventilation.33 Leite JJ, Mansur AJ, de Freitas HF, Chizola PR, Bocchi EA, Terra-Filho M, et al. Periodic breathing during incremental exercise predicts mortality in patients with chronic heart failure evaluated for cardiac transplantation. J Am Coll Cardiol. 2003;41(12):2175-81.,1717 Corra U, Giordano A, Bosimini E, Mezzani A, Piepoli M, Coats AJ, et al. Oscillatory ventilation during exercise in patients with chronic heart failure: clinical correlates and prognostic implications. Chest. 2002;121(5):1572-80. Both definitions require the visualization of the ventilatory pattern during exercise to determine the presence or absence of exercise oscillatory ventilation, in a dichotomized way. We have previously shown that applying time-domain variability techniques can be easily performed and may help quantifying exercise ventilatory oscillations. Olson and Johnson1818 Olson TP, Johnson BD. Quantifying oscillatory ventilation during exercise in patients with heart failure. Respir Physiol Neurobiol. 2014;190:25-32. have also proposed a software application to quantify measures of exercise oscillatory ventilation in heart failure patients.

Considering that most ventilatory parameters exhibit some adaptation to physical training, it is conceivable to hypothesize that ventilatory variability would also be affected by chronic exposure to physical exercise. The present study compared ventilatory variability throughout exercise in athletes and sedentary men and concluded that untrained volunteers exhibited greater minute-ventilation variability than soccer athletes.

It is important to note that all volunteers were healthy and without any cardiovascular or respiratory disease. Therefore, some mechanisms involved in Cheyne-Stokes respiration and periodic breathing, such as hypocapnia, and pulmonary blood flow fluctuations,1919 Yajima T, Koike A, Sugimoto K, Miyahara Y, Marumo F, Hiroe M. Mechanism of periodic breathing in patients with cardiovascular disease. Chest. 1994;106(1):142-6. which are considered key mechanisms of periodic breathing in heart failure, would probably not be useful in understanding physiological ventilatory variability during exercise in healthy subjects. Increased central and peripheral chemosensitivity2020 Lorenzi-Filho G, Genta PR, Figueiredo AC, Inoue D. Cheyne-Stokes respiration in patients with congestive heart failure: causes and consequences. Clinics (Sao Paulo). 2005;60(4):333-44. is also involved with Cheyne-Stokes respiration. Ohyabu et al showed that ventilatory sensitivity during hypoxia was attenuated in long-distance runners and sprinters compared to non-athletes.2121 Ohyabu Y, Usami A, Ohyabu I, Ishida Y, Miyagawa C, Arai T, et al. Ventilatory and heart rate chemosensitivity in track-and-field athletes. Eur J Appl Physiol Occup Physiol. 1990;59(6):460-4. In fact, endurance training reduces the ventilatory response to a given level of work due to an attenuated chemosensitivity.2222 McConnell AK, Semple ES. Ventilatory sensitivity to carbon dioxide: the influence of exercise and athleticism. Med Sci Sports Exerc. 1996;28(6):685-91.,2323 Katayama K, Sato Y, Morotome Y, Shima N, Ishida K, Mori S, et al. Ventilatory chemosensitive adaptations to intermittent hypoxic exposure with endurance training and detraining. J Appl Physiol (1985). 1999;86(6):1805-11. So, it is possible that reduced chemosensitivity would explain the findings of the present study.

Although there was no statistical difference regarding weight or body mass index between groups, volunteers in the sedentary group exhibited near significantly higher weight and BMI. One could hypothesize that this slight and non-significant difference could have influenced the different breathing patterns found in the study. In fact, in morbid obese individuals, excessive body weight can induce chest wall restriction2424 Piper AJ. Obesity hypoventilation syndrome--the big and the breathless. Sleep Med Rev. 2011;15(2):79-89. and loosing body weight may improve lung function.2525 Xavier MA, Ceneviva R, Terra Filho J, Sankarankutty AK. Pulmonary function and quality of life in patients with morbid obesity six months after bariatric surgery. Acta Cir Bras. 2010;25(5):407-15. Nevertheless, although there was some overweight volunteers in both groups, there was not a single obese volunteer in this study. We could not found any study that compared ventilatory parameters in overweight and not overweight individuals during exercise. Regarding rest breathing patterns, it seems that body mass only influences lung function when obese individuals are in supine position. Our volunteers were non-obese and all tests were performed in the upright position. Thus, it seems unlikely that the slight and non significant difference in BMI between groups would have influenced the ventilatory variability results of the present study.

The analysis of table 2 shows maximal VO2 that is not as high as expected for professional soccer players. There are several possible explanations for this finding. First of all, data was collected in the beginning of the season, just after holydays. So, athletes were not in their best shape. It is also important to note that there is clear VO2max variation profiles between soccer players accordingly to their playing position and style.2626 Da Silva CD, Bloomfield J, Marins JC. A review of stature, body mass and maximal oxygen uptake profiles of u17, u20 and first division players in brazilian soccer. J Sports Sci Med. 2008;7(3):309-19. We have included athletes from all playing positions, from the same team, in the athlete group. So, there were differences between their VO2max. Finally, players in Brazil appear to be shorter in stature, similar in body mass and have a lower overall aerobic capacity when compared to their European equivalents.2626 Da Silva CD, Bloomfield J, Marins JC. A review of stature, body mass and maximal oxygen uptake profiles of u17, u20 and first division players in brazilian soccer. J Sports Sci Med. 2008;7(3):309-19.

Study limitations

Some operational and technical aspects could have influenced the results of the present study. Subjects were not submitted to rest pulmonary function tests before entering the study. Considering none of them had any past history of pulmonary disease or smoking, the absence of rest pulmonary function tests, although desirable, does not seem to be a major issue influencing the present results.

The use of different interfaces to breath analysis may influence the depth and rate of breathing.2727 Askanazi J, Silverberg PA, Foster RJ, Hyman AI, Milic-Emili J, Kinney JM. Effects of respiratory apparatus on breathing pattern. J Appl Physiol Respir Environ Exerc Physiol. 1980;48(4):577-80. Although this effect appears to be restricted to lower levels of exercise,2828 Paek D, McCool FD. Breathing patterns during varied activities. J Appl Physiol (1985). 1992;73(3):887-93. it seems reasonable not to interchangeably compare ventilatory variability results recorded using mask, mouthpiece or canopy. All breath-by-breath data in this study was collected throughout a face mask. Thus, the selected interface could not have influenced the different results when both groups were compared.

This is a cross-sectional study where trained and untrained men were compared. A study that evaluates the effects of physical training would rather have a longitudinal than the present design. Nevertheless, the only difference between both studied groups was their peak VO2, which was higher in athletes, as expected. Thus, although athletes were not longitudinally evaluated, it seems that the different exercise responses in both groups could be directly attributable to physical training.

Conclusions

The presence of periodic breathing is a powerful predictor of adverse outcome in heart failure.22 Ingle L, Isted A, Witte KK, Cleland JG, Clark AL. Impact of different diagnostic criteria on the prevalence and prognostic significance of exertional oscillatory ventilation in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil. 2009;16(4):451-6. This is an extreme presentation of a ventilatory variation that although unseen by our eyes can be mathematically calculated. The present study adds information regarding the quantification of exercise minute-ventilation variability, and points to the direction that this is a trainable exercise variable. The exact mechanisms that influence ventilatory variability during exercise remain to be studied.

  • Sources of Funding
    There were no external funding sources for this study.

  • Study Association
    This study is not associated with any thesis or dissertation work.

References

  • 1
    Wasserman K, Hansen JE, Sue DY, Stringer WW, Whipp BJ. Principles of exercise testing and interpretation: including pathophysiology and clinical applications. Philadelphia: Lippincott Williams and Wilkins; 2005.
  • 2
    Ingle L, Isted A, Witte KK, Cleland JG, Clark AL. Impact of different diagnostic criteria on the prevalence and prognostic significance of exertional oscillatory ventilation in patients with chronic heart failure. Eur J Cardiovasc Prev Rehabil. 2009;16(4):451-6.
  • 3
    Leite JJ, Mansur AJ, de Freitas HF, Chizola PR, Bocchi EA, Terra-Filho M, et al. Periodic breathing during incremental exercise predicts mortality in patients with chronic heart failure evaluated for cardiac transplantation. J Am Coll Cardiol. 2003;41(12):2175-81.
  • 4
    Sun XG, Hansen JE, Beshai JF, Wasserman K. Oscillatory breathing and exercise gas exchange abnormalities prognosticate early mortality and morbidity in heart failure. J Am Coll Cardiol. 2010;55(17):1814-23.
  • 5
    Shafiq A, Brawner CA, Aldred HA, Lewis B, Williams CT, Tita C, et al. Prognostic value of cardiopulmonary exercise testing in heart failure with preserved ejection fraction. The Henry Ford HospITal CardioPulmonary EXercise Testing (FIT-CPX) project. Am Heart J. 2016;174:167-72.
  • 6
    Guazzi M, Myers J, Peberdy MA, Bensimhon D, Chase P, Arena R. Exercise oscillatory breathing in diastolic heart failure: prevalence and prognostic insights. Eur Heart J. 2008;29(22):2751-9.
  • 7
    Guazzi M, Arena R, Pellegrino M, Bandera F, Generati G, Labate V, et al. Prevalence and characterization of exercise oscillatory ventilation in apparently healthy individuals at variable risk for cardiovascular disease: a subanalysis of the EURO-EX trial. Eur J Prev Cardiol. 2016;23(3):328-34.
  • 8
    Cornelis J, Beckers P, Vanroy C, Volckaerts T, Vrints C, Vissers D. An overview of the applied definitions and diagnostic methods to assess exercise oscillatory ventilation--a systematic review. Int J Cardiol. 2015;190:161-9.
  • 9
    Myers J, Arena R, Cahalin LP, Labate V, Guazzi M. Cardiopulmonary exercise testing in heart failure. Curr Probl Cardiol. 2015;40(8):322-72.
  • 10
    Castro RR, Antunes-Correa LM, Ueno LM, Rondon MU, Negrao CE, Nobrega AC. Reversal of periodic breathing after aerobic training in heart failure. Eur Respir J. 2010;35(6):1409-11.
  • 11
    Castro RR, Antunes-Correa LM, Ueno LM, Rondon MU, Negrao CE, Nobrega AC. Ventilation variability inversely correlates to ejection fraction in heart failure. Eur Respir J. 2010;36(6):1482-3.
  • 12
    Dempsey JA, Johnson BD, Saupe KW. Adaptations and limitations in the pulmonary system during exercise. Chest. 1990;97(3 Suppl):81S-7S.
  • 13
    Poole DC, Wilkerson DP, Jones AM. Validity of criteria for establishing maximal O2 uptake during ramp exercise tests. Eur J Appl Physiol. 2008;102(4):403-10.
  • 14
    Castro R, Antunes-Correa LM, Ueno LM, Rondon MU, Negrão CE, Nóbrega AC. Ventilation variability inversely correlates to ejection fraction in heart failure. Eur Respir J. 2010;36(6):1482-3.
  • 15
    Ribeiro JP, Knutzen A, Rocco MB, Hartley LH, Colucci WS. Periodic breathing during exercise in severe heart failure. Reversal with milrinone or cardiac transplantation. Chest. 1987;92(3):555-6.
  • 16
    Kremser CB, O'Toole MF, Leff AR. Oscillatory hyperventilation in severe congestive heart failure secondary to idiopathic dilated cardiomyopathy or to ischemic cardiomyopathy. Am J Cardiol. 1987;59(8):900-5.
  • 17
    Corra U, Giordano A, Bosimini E, Mezzani A, Piepoli M, Coats AJ, et al. Oscillatory ventilation during exercise in patients with chronic heart failure: clinical correlates and prognostic implications. Chest. 2002;121(5):1572-80.
  • 18
    Olson TP, Johnson BD. Quantifying oscillatory ventilation during exercise in patients with heart failure. Respir Physiol Neurobiol. 2014;190:25-32.
  • 19
    Yajima T, Koike A, Sugimoto K, Miyahara Y, Marumo F, Hiroe M. Mechanism of periodic breathing in patients with cardiovascular disease. Chest. 1994;106(1):142-6.
  • 20
    Lorenzi-Filho G, Genta PR, Figueiredo AC, Inoue D. Cheyne-Stokes respiration in patients with congestive heart failure: causes and consequences. Clinics (Sao Paulo). 2005;60(4):333-44.
  • 21
    Ohyabu Y, Usami A, Ohyabu I, Ishida Y, Miyagawa C, Arai T, et al. Ventilatory and heart rate chemosensitivity in track-and-field athletes. Eur J Appl Physiol Occup Physiol. 1990;59(6):460-4.
  • 22
    McConnell AK, Semple ES. Ventilatory sensitivity to carbon dioxide: the influence of exercise and athleticism. Med Sci Sports Exerc. 1996;28(6):685-91.
  • 23
    Katayama K, Sato Y, Morotome Y, Shima N, Ishida K, Mori S, et al. Ventilatory chemosensitive adaptations to intermittent hypoxic exposure with endurance training and detraining. J Appl Physiol (1985). 1999;86(6):1805-11.
  • 24
    Piper AJ. Obesity hypoventilation syndrome--the big and the breathless. Sleep Med Rev. 2011;15(2):79-89.
  • 25
    Xavier MA, Ceneviva R, Terra Filho J, Sankarankutty AK. Pulmonary function and quality of life in patients with morbid obesity six months after bariatric surgery. Acta Cir Bras. 2010;25(5):407-15.
  • 26
    Da Silva CD, Bloomfield J, Marins JC. A review of stature, body mass and maximal oxygen uptake profiles of u17, u20 and first division players in brazilian soccer. J Sports Sci Med. 2008;7(3):309-19.
  • 27
    Askanazi J, Silverberg PA, Foster RJ, Hyman AI, Milic-Emili J, Kinney JM. Effects of respiratory apparatus on breathing pattern. J Appl Physiol Respir Environ Exerc Physiol. 1980;48(4):577-80.
  • 28
    Paek D, McCool FD. Breathing patterns during varied activities. J Appl Physiol (1985). 1992;73(3):887-93.

Publication Dates

  • Publication in this collection
    Sept 2017

History

  • Received
    12 Oct 2016
  • Reviewed
    30 Jan 2017
  • Accepted
    29 Mar 2017
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