Cardiorespiratory optimal point: a submaximal variable of the cardiopulmonary exercise testing

Abstracts

FUNDAMENTO: No Teste Cardiopulmonar de Exercício (TCPE) máximo são analisadas diversas variáveis ventilatórias, incluindo o equivalente ventilatório de oxigênio (VE/VO2). O valor mínimo do VE/VO2 reflete a melhor integração entre os sistemas respiratório e cardiovascular, podendo ser denominado Ponto Ótimo Cardiorrespiratório (POC). OBJETIVO: Determinar o comportamento do POC em função do gênero e da idade em adultos saudáveis e verificar a associação com outras variáveis do TCPE. MÉTODOS: De 2.237 indivíduos, foram selecionados 624 (62% homens e 48 ± 12 anos de idade), não atletas, saudáveis, submetidos ao TCPE máximo. O POC ou VE/VO2 mínimo foi obtido a partir da análise da ventilação e do consumo de oxigênio em cada minuto do TCPE. Foi verificada a relação entre idade e POC para os dois gêneros, assim como as associações com: VO2máx, VO2 no limiar anaeróbico (VO2LA), eficiência da inclinação de consumo de oxigênio (OUES) e com VE máxima. Comparou-se ainda a intensidade do esforço (MET) no POC, LA e VO2máx. RESULTADOS: O POC aumenta com a idade, sendo 23,2 ± 4,48 e 25,0 ± 5,14, respectivamente, em homens e mulheres (p < 0,001). Há associações moderadas e inversas com VO2máx (r = -0,47; p < 0,001), com VO2LA (r = -0,42; p < 0,001) e com o OUES (r = -0,34; p < 0,001). O POC ocorreu, em média, a (44% do VO2máx) e antes do LA (67% do VO2máx) (p < 0,001). CONCLUSÃO: POC, uma variável submáxima, aumenta com a idade e é discretamente mais alto em mulheres. Sendo modestamente associado a outras medidas ventilatórias, parece haver uma contribuição independente na interpretação da resposta cardiorrespiratória ao TCPE.

Exercício; teste cardiopulmonar de exercício; espirometria; consumo de oxigênio; relação ventilação-perfusão

^IFaculdade de Ciências Médicas e da Saúde de Juiz de Fora - SUPREMA- Juiz de Fora, MG

^IIHospital e Maternidade Therezinha de Jesus- Juiz de Fora, MG

^IIIPrograma de pós-graduação em Ciências do Exercício e do Esporte - PPGCEE - Universidade Gama Filho- Rio de Janeiro, RJ

^IVClínica de Medicina do Exercício (CLINIMEX)- Rio de Janeiro, RJ, Brazil

Mailing Address

ABSTRACT

BACKGROUND: At the maximal Cardiopulmonary Exercise Testing (CPET), several ventilatory variables are analyzed, including the ventilatory equivalent for oxygen (VE/VO2). The minimum VE/VO2 value reflects the best integration between the respiratory and cardiovascular systems and may be called "Cardiorespiratory Optimal Point (COP)".

OBJECTIVE: To determine the behavior of the COP according to gender and age in healthy adults and verify its association with other CPET variables.

METHODS: Of 2,237 individuals, 624 were selected (62% men and 48 ± 12 years), non- athletes, healthy, who were submitted to maximal CPET. COP or minimum VE/VO2 was obtained from the analysis of ventilation and oxygen consumption in every minute of CPET. We investigated the association between age and COP for both genders, as well as associations with: VO₂max, VO2 at anaerobic threshold (VO2AT), oxygen uptake efficiency slope (OUES) and with maximum VE. We also compared the intensity of exertion (MET) at the COP, AT and VO₂max.

RESULTS: COP increases with age, being 23.2 ± 4.48 and 25.0 ± 5.14, respectively, in men and women = (p < 0.001). There are moderate and inverse associations with VO₂max (r = -0.47; p < 0.001), with VO2AT (r = -0.42; p < 0.001) and with OUES (r = -0.34; p < 0.001). COP occurred, on average, at 44% do VO₂max and before AT (67% of VO₂max) (p < 0.001).

CONCLUSION: COP, a submaximal variable, increases with age and is slightly higher in women. Being modestly associated with other ventilation measures, there seems to be an independent contribution to the interpretation of the cardiorespiratory response to CPET.

Keywords: Respiratory function tests; exercise; oxygen consumption; spirometry; ventilation-perfusion ratio.

Introduction

During a maximum Cardiopulmonary Exercise Testing (CPET), different ventilatory data are obtained with clinical, diagnostic and/or prognostic implications¹, such as maximum oxygen consumption (VO₂max) - an objective measure of cardiorespiratory function^2,3 - the maximum oxygen pulse, both absolute and relative to body weight^4,5, the anaerobic threshold (AT)⁶, the ventilatory equivalent for carbon dioxide (VE/VCO2)⁷ and the curve generated by the oxygen uptake efficiency slope (OUES)⁸. However, there are several limitations with the measurement of these variables, such as low reproducibility ⁹, different manners of calculation or identification¹⁰, and the fact that to obtain most of these, it is necessary to perform a truly maximum test^11,12, which usually depends the motivations of the evaluator and the evaluated.

The typical behavior of the ventilatory equivalents in an incremental exercise has a U-shape, characterized by suboptimal levels of efficiency at rest and very intensive efforts and improved efficiency at submaximal levels of exercise. Among the ventilatory measures obtained during an incremental exercise, the minimum value of the ventilatory equivalent for oxygen (VE/VO2 minimum), i.e., the lowest value of this variable at any given minute of CPET performed in a ramp protocol, remains to be better explored. In theory, the moment at which VE/VO2 minimum occurs represents the best association or integration between the respiratory and cardiovascular systems or ventilation-perfusion, which may be called Cardiorespiratory Optimal Point (COP). In practice, the COP corresponds to the moment during the incremental exercise in which there is less ventilation (VE) for a liter of oxygen to be consumed (VO2).

An important characteristic of COP is that - unlike most of other ventilatory indices or variables obtained or calculated at CPET - in order to obtain it, it is not necessary to perform a maximum effort. Hypothetically, the COP is much less dependent on the evaluator and, most likely, on the choice of protocol or the incremental effort ratio, thus being easier to measure, with greater accuracy. Thus, it seems appropriate to investigate the behavior of the COP in a large sample of healthy individuals, providing objective conditions for the clinical and physiological interpretation of this variable. Therefore, the aim of this study was to determine the COP related to gender and age for adults with no cardiopulmonary diseases. In addition, the associations between COP and other ventilatory variables commonly obtained in a maximum CPET were also determined.

Methods

Sample

We retrospectively analyzed data from 2,237 medical and functional evaluations performed at a private clinic specialized in Exercise Medicine between 2006 and March 2012, and identified 624 adults (62% men) non-athletes, aged 48 ± 12 years (mean ± standard deviation), who concomitantly met the following inclusion criteria: 1) no history of cardiorespiratory disease or mitral valve prolapse, 2) no regular use of cardiorespiratory medication, 3) absence of obesity (body mass index < 30 kg/m²), 4) present a result of FEV1/FVC > 70% of the value measured¹³ at resting spirometry, 5) absence of electrocardiographic alterations suggestive of significant myocardial ischemia at the CPET, 6) no locomotor limitation that could affect performance at the CPET, 7) performing the CPET on a lower-limb cycle ergometer and 8) having completed a truly maximum CPET, i.e., one that was not stopped early due to heart rate and/or blood pressure thresholds.

Protocol

The evaluation consisted of a clinical examination, comprising detailed history and physical examination. Data on anthropometrics, spirometry and electrocardiogram at rest were obtained prior to the performance of the maximum CPET. Subjects voluntarily submitted to the assessment, typically done at their own request and by indication of their attending physicians. All subjects read and signed a specific informed consent form, before the performance of the procedures, formally authorizing the use of data in scientific research, whereas preserving individual privacy. The consent form and retrospective analysis of data were previously approved by the institutional ethics committee in research, according to Resolution 196/96 of the National Health Council and the Declaration of Helsinki.

Resting Spirometry

At least three maneuvers were carried out to determine the flow-volume curve using a periodically calibrated pneumotachograph (Cardiovit AT-10, Schiller, Switzerland), using the protocol specified in the guidelines of the American Thoracic Society and European Respiratory Society¹⁴.

Maximum Cardiopulmonary Exercise Testing (CPET)

All subjects were submitted to a maximum CPET in a lower-limb cycle ergometer (Cateye EC-1600, Cateye, Japan or Inbrasport CG-04, Inbrasport, Brazil), following an individualized ramp protocol targeting a duration between 8 and 12 minutes. The load in watts was increased gradually until the patient reached exhaustion, represented by the incapacity to continue to ride at the previously established cycling frequency. Subjects were strongly encouraged by verbal stimuli to reach the maximum effort during the CPET, and this only stopped when individuals reached the maximum voluntary exhaustion. As mentioned in the inclusion criteria, the CPETs were only considered in the analysis when they were not interrupted by clinical reasons, such as exaggerated BP response and/or the occurrence of an incompetent chronotropic response, or even due to electrocardiographic, hemodynamic and ventilatory alterations¹⁵.

Analysis of Exhaled Gases

During the CPET, the exhaled gases were collected by a Prevent pneumotachograph (MedGraphics, USA) coupled to a mouthpiece, with concomitant nasal occlusion, and quantified by a VO2000 metabolic analyzer (MedGraphics, USA), calibrated periodically by a 2-L syringe and gases of known concentration. The metabolic analyzer enabled the quantification of pulmonary ventilation and partial fractions of oxygen and carbon dioxide, expressed and analyzed every 10 s. Following a standardization pattern¹⁶, VO2 values were reported every minute during the CPET, through the mean of six readings obtained during this period. Thus, the value of the largest mean obtained referring to a given minute was considered the VO₂max.

Determination of Anaerobic Threshold (AT)

The AT was determined based on the graphical inspection of data on VO2 and VE, at which point there was a decrease in the linearity of VE, whereas VO2 continued to increase linearly with the work load¹⁷.

Determination of Oxygen Uptake Efficiency Slope (OUES)

OUES was determined by linear regression related to the log transformation of VE and VO2 obtained every minute of CPET using the following equation (VO2 = a log VE + b). In this equation, the constant 'a' represents the regression coefficient (called OUES), and 'b' represents the intercept^8,18.

Determination of COP

COP, a dimensionless result, was obtained by identifying the lowest value of the ratio between the data ventilation (VE) and oxygen uptake (VO2) obtained at every minute during the maximum CPET, regardless of when it occurred.

Statistical Analysis

Initially, the normality (Kolmogorov-Smirnov) and homogeneity of data distribution were tested, validating the use of parametric statistics. To describe the sample, the central tendency and variability of the data were expressed as mean ± standard deviation (2.5 and 97.5 percentiles), while for the data used in inferential statistics, the results were presented as mean ± standard error of mean. An analysis of variance for repeated measures was used to compare the values of exercise intensity in MET in three occasions: COP, AT and VO2max. Pearson's correlation was used to test the association between COP and other ventilatory variables. The influence of age on the COP, separately by gender, was analyzed by linear regression. Statistical calculations were performed using SPSS (IBM, USA), release 17 and Prism release 5.01 (GraphPad, USA), considering a significance level of 5%.

Results

The demographic characteristics, as well as the results of resting spirometry and CPET regarding gender are shown in Table 1.

The associations between COP and VO₂max as well as with OUES and the VO₂AT were significant, but only moderate, whereas the correlation coefficient between the COP and maximum VE was weak (Table 2).

In all tested subjects, the COP always occurred before AT, being identified at 4.1 ± 0.05 metabolic equivalents (MET) (44% of VO₂max), quite lower than the value of AT 6.4 ± 0.09 MET (67% of VO₂max), and maximum effort 9.7 ± 0.12 MET (p < 0.001) (Figure 1).

COP increases progressively with age in both men and women, with no difference between the regression slope (p = 0.76); however, women have a slightly higher COP, two points for the same age, with a difference in the intercept of the linear regression (p = 0.001) (Figure 2). The linear regression equations that explain the association between COP and age for each gender are shown in Table 3. Figure 3 shows the behavior of the COP related to age range and gender, and for its use in clinical practice, we present in Table 4 the COP percentiles by age range and gender.

Discussion

Our study makes an original contribution to the body of knowledge, being the first to address the behavior of the COP during CPET in a large and carefully selected cohort, determining the regression equations of this variable related to age for healthy adults of both genders. Our sample selection was carried out with a stringent control to include only distinctly healthy individuals, where several criteria had to be met simultaneously, including specifically, to have never been diagnosed or treated for cardiovascular and/or respiratory diseases and obesity and not having any musculoskeletal abnormalities that could impair the performance at the CPET on a lower-limb cycle ergometer.

We also suggest in our study that the COP can be directly related to a probably optimal point of cardiorespiratory and metabolic integration, reflecting a more efficient and less expensive use of inspired VE, which is particularly important when one knows that there is a considerable energy expenditure to maintain a high pulmonary ventilation, which can reach up to 15% of the observed VO₂max¹⁹. Particularly, this variable has some advantages when compared to others obtained during a CPET, such as VO₂max, the oxygen pulse curve and AT, which are often addressed in other studies related to ergospirometry and presented as good prognostic indicators^3,6. However, we must emphasize that to obtain VO₂max and other such indices it is necessary to perform a truly maximum effort^1,12 and that the determination of AT time can be influenced by the protocol used, the choice of method of detection¹⁰ and the experience and knowledge of the evaluator²⁰. As for the determination of the COP, it is not necessary to perform a truly maximum exercise considering that this variable has always been identified at relatively low levels of exercise intensity and well before the AT, and that its determination does not depend on the evaluator's interpretation, as it is easily obtained by identifying the lowest numerical ratio between the VE and VO2 values for each minute of the CPET, thus being a dimensionless ratio, simple to express and compare.

There are other ventilatory indices in the CPET that tend to express the association between the respiratory and cardiovascular systems. In 1996, Baba et al.⁸ proposed an index associated to the cardiorespiratory functional reserve, related to an equation that determines the oxygen uptake efficiency slope (OUES), using the ventilatory equivalent for oxygen (VE/VO2). This variable has a strong association with VO₂max (r = 0.94, p < 0.001) in pediatric (r = 0.78, p < 0.001) and adult patients; however, these authors took into consideration several points of the VE/VO2 curve^18,21 and adjusted it as if it had a linear behavior, a fact that does not reflect the physiological behavior of this variable. Furthermore, the calculation of the equation for OUES determination is mathematically more complex and less practical than the identification of only one value, such as with the COP proposed by our study.

Our results demonstrate that the COP has a modest association with VO₂max (-0.47, p < 0.001) and a low association with maximum VE (-0.14, p < 0.001), as well as OUES (-0.34, p < 0.001), thus suggesting that it is a possible independent variable with potential complementary contribution to the interpretation of cardiorespiratory integration during the CPET. Another equally important aspect is that the COP (Figure 1) occurs between approximately 30% and 50% of the VO₂max, i.e., at a relatively low intensity effort, being considerably less intense than the AT in a CPET performed using an individualized ramp protocol, which can be useful when thinking about the evaluation of patients with severe coronary artery disease or even in patients with advanced heart failure. In our results of healthy individuals, the COP occurred on average at 4.1 MET, compatible with the concept of cardiorespiratory optimal point, considering that most situations of everyday movements and physical activities, exercises and sports are performed between 2 and 6 MET²², rather than at truly maximum effort.

The aging process results in several structural and physiological alterations, such as muscle strength decrease²³, loss of flexibility²⁴ and VO₂max reduction²⁵, so we might expect that this would occur with the COP. Regarding the ventilatory variables, it is known that, over the years, there is also a reduction in respiratory muscle strength²⁶ and some ventilatory indicators, such as forced expiratory volume in one second (FEV1)²⁷ and forced vital capacity (FVC )²⁸, as well as a less effective response to the increase in PaCO2 at rest²⁹.

More specifically, in our study we observed that with increasing age, there is an increase in the COP value, a fact that can probably be explained by changes that occur in the respiratory system^28,30. Evidence has shown a reduction in alveolar surface, increase in the alveolar dead space, conditions that are associated with pulmonary hyperinflation and a reduction in the alveolar-capillary diffusion capacity^30,31, in addition to a lower VE²⁹, which, together with the stiffening of blood vessels³² contributes to a worst ratio or increase in the V/Q^28,30-32. In younger individuals, the pulmonary capillary recruitment probably occurs with greater efficiency, allowing an expansion of the so-called West zone III to the region of zones I and II, maintaining a more appropriate V/Q ratio³³. It should be noted that the increased ventilation in exercise is not only related to the CO2 concentration, but also with afferent stimuli from the mechanoreceptors^34,35. Evidence of that is data from Araujo and Monteiro³⁶ indicating that there are substantial differences in the VE and also in VE/VO2, with probably different afferent stimuli, when an individual walks or runs for the same velocity on the treadmill.

The behavior of COP seems to be slightly different according to gender, while there is a similar increase in the COP with age for men and women. Over the years, one can consider that there is a worsening in VE³¹ and a reduction in VO₂max²⁵, i.e. variables directly involved in the calculation of the COP; it seems, however, that the decline in ventilation is less significant or numerically important than the reduction in VO2, thereby explaining the higher COP values in older individuals.

Regarding gender, the slightly higher COP values found in women are probably related to the fact that they have lower values of VO₂max³⁷ and ventilation, when compared to men, remembering that, as with the equations^26,38,39 that predict ventilatory variables at resting spirometry, body size is taken into account and typically women are smaller than men.

Notwithstanding all the methodological steps involved in this study, we can point out some possible limitations to greater clinical application and external validity of our data, such as the characterization of the COP for CPET performed only in lower-limb cycle ergometer. However, this may also represent a strong point, as, by avoiding gait transitions when walking and running, which are normally observed in treadmill protocols, perhaps it was possible to better characterize the physiological behavior of the COP. Another potential limitation is the fact that it has not been objectively tested whether the COP values were distinct between individuals habitually active and sedentary, in spite of some evidence demonstrating differences in certain variables obtained at the CPET⁴⁰. However, the modest association with the VO₂max and the VO₂AT suggests that there should be a marked overlap in COP values between active and sedentary individuals. Perhaps the most appropriate way to study the influence of the regular pattern of physical exercise on the COP is to evaluate the behavior of this variable before and after participating in an exercise program. Further studies will compare different ergometers that might produce different assessments and therefore, other results. Another important aspect is to test the potential clinical and epidemiological contribution of COP, either by measuring its response to interventions such as exercise programs, or by its prognostic impact on mortality.

Conclusion

In conclusion, this study proposes the analysis of a new submaximal variable in a CPET, which is easy to obtain, shows observer-independent quantification, is physiologically plausible and well-grounded, able to add relevant clinical information. The value of COP increases with age and is slightly higher in women, with associations being modest with other ventilation measures, suggesting an independent and potential contribution in the interpretation of the cardiorespiratory response at the CPET. The study also contributes by showing a comprehensive database of healthy individuals of both genders within a broad age spectrum, which will allow the analysis and interpretation of results obtained from patients suffering from cardiopulmonary diseases.

Potential Conflict of Interest

The author Claudio Gil Soares de Araújo declares to have conflict of interest with INBRAMED and MICROMED for cession of some of the equipments used in the study.

Sources of Funding

This study was partially funded by CNPq e FAPERJ.

Study Association

This article is part of the doctoral dissertation of Plinio Santos Ramos at the Graduate Program in Exercise and Sport Sciences of Gama Filho University.

References

• ¹
  Meneghelo RS, Araújo CGS, Stein R, Mastrocolla LE, Albuquerque PF, Serra SM, et al.; Sociedade Brasileira de Cardiologia. III Diretrizes da Sociedade Brasileira de Cardiologia sobre teste ergométrico. Arq Bras Cardiol. 2010;95(5 supl.1):1-26.
• ²
  Sharma S, Elliott P, Whyte G, Jones S, Mahon N, Whipp B, et al. Utility of cardiopulmonary exercise in the assessment of clinical determinants of functional capacity in hypertrophic cardiomyopathy. Am J Cardiol. 2000;86(2):162-8.
• ³
  Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med. 2002;346(11):793-801.
• ⁴
  Oliveira RB, Myers J, Araujo CG. Long-term stability of the oxygen pulse curve during maximal exercise. Clinics. 2011;66(2):203-9.
• ⁵
  Perim RR, Signorelli GR, Araujo CG. Stability of relative oxygen pulse curve during repeated maximal cardiopulmonary testing in professional soccer players. Braz J Med Biol Res. 2011;44(7):700-6.
• ⁶
  Whipp BJ, Ward SA. The physiological basis of the 'anaerobic threshold' and implications for clinical cardiopulmonary exercise testing. Anaesthesia. 2011;66(11):1048-9.
• ⁷
  Poggio R, Arazi HC, Giorgi M, Miriuka SG. Prediction of severe cardiovascular events by VE/VCO2 slope versus peak VO2 in systolic heart failure: a meta-analysis of the published literature. Am Heart J. 2010;160(6):1004-14.
• ⁸
  Baba R, Nagashima M, Goto M, Nagano Y, Yokota M, Tauchi N, et al. Oxygen uptake efficiency slope: a new index of cardiorespiratory functional reserve derived from the relation between oxygen uptake and minute ventilation during incremental exercise. J Am Coll Cardiol. 1996;28(6):1567-72.
• ⁹
  Yeh MP, Gardner RM, Adams TD, Yanowitz FG, Crapo RO. "Anaerobic threshold": problems of determination and validation. J Appl Physiol. 1983;55(4):1178-86.
• ¹⁰
  Neder JA, Stein R. A simplified strategy for the estimation of the exercise ventilatory thresholds. Med Sci Sports Exerc. 2006;38(5):1007-13.
• ¹¹
  Araujo CG, Pinto VL. Maximal heart rate in exercise tests on treadmill and in a cycloergometer of lower limbs. Arq Bras Cardiol. 2005;85(1):45-50.
• ¹²
  Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, et al. Clinician's Guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation. 2010;122(2):191-225.
• ¹³
  Nathell L, Nathell M, Malmberg P, Larsson K. COPD diagnosis related to different guidelines and spirometry techniques. Respir Res. 2007;8:89.
• ¹⁴
  Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26(2):319-38.
• ¹⁵
  Ramos PS, Araujo CG. Normotensive individuals with exaggerated exercise blood pressure response have increased cardiac vagal tone. Arq Bras Cardiol. 2010;95(1):85-90.
• ¹⁶
  Araújo CGS. Analisando os gases expirados no Teste Cardiopulmonar de Exercício Máximo: uma proposta de padronização do intervalo amostral. Rev DERC. 2010;49:6-8.
• ¹⁷
  Araújo CGS. Respostas cardiorespiratórias a um exercicio submáximo prolongado. Arq Bras Cardiol. 1983;41(1):37-45.
• ¹⁸
  Baba R. The oxygen uptake efficiency slope and its value in the assessment of cardiorespiratory functional reserve. Congest Heart Fail. 2000;6(5):256-8.
• ¹⁹
  Dempsey JA, Harms CA, Ainsworth DM. Respiratory muscle perfusion and energetics during exercise. Med Sci Sports Exerc. 1996;28(9):1123-8.
• ²⁰
  Hopker JG, Jobson SA, Pandit JJ. Controversies in the physiological basis of the 'anaerobic threshold' and their implications for clinical cardiopulmonary exercise testing. Anaesthesia. 2011;66(2):111-23.
• ²¹
  Hollenberg M, Tager IB. Oxygen uptake efficiency slope: an index of exercise performance and cardiopulmonary reserve requiring only submaximal exercise. J Am Coll Cardiol. 2000;36(1):194-201.
• ²²
  Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, Franklin BA, et al. Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Circulation. 2007;116(9):1081-93.
• ²³
  Vianna LC, Oliveira RB, Araujo CG. Age-related decline in handgrip strength differs according to gender. J Strength Cond Res. 2007;21(4):1310-4.
• ²⁴
  Araujo CG. Flexibility assessment: normative values for flexitest from 5 to 91 years of age. Arq Bras Cardiol. 2008;90(4):257-63.
• ²⁵
  Betik AC, Hepple RT. Determinants of VO2 max decline with aging: an integrated perspective. Appl Physiol Nutr Metab. 2008;33(1):130-40.
• ²⁶
  Neder JA, Andreoni S, Castelo-Filho A, Nery LE. Reference values for lung function tests. I. Static volumes. Braz J Med Biol Res. 1999;32(6):703-17.
• ²⁷
  Ware JH, Dockery DW, Louis TA, Xu XP, Ferris BG Jr, Speizer FE. Longitudinal and cross-sectional estimates of pulmonary function decline in never-smoking adults. Am J Epidemiol. 1990;132(4):685-700.
• ²⁸
  Sharma G, Goodwin J. Effect of aging on respiratory system physiology and immunology. Clin Interv Aging. 2006;1(3):253-60.
• ²⁹
  Peterson DD, Pack AI, Silage DA, Fishman AP. Effects of aging on ventilatory and occlusion pressure responses to hypoxia and hypercapnia. Am Rev Respir Dis. 1981;124(4):387-91.
• ³⁰
  Oyarzun GM. Pulmonary function in aging. Rev Med Chil. 2009;137(3):411-8.
• ³¹
  Janssens JP, Pache JC, Nicod LP. Physiological changes in respiratory function associated with ageing. Eur Respir J. 1999;13(1):197-205.
• ³²
  Greaney JL, Farquhar WB. Why do veins stiffen with advancing age? J Appl Physiol. 2011;110(1):11-2.
• ³³
  West JB. Regional differences in gas exchange in the lung of erect man. J Appl Physiol. 1962;17:893-8.
• ³⁴
  McCloskey DI, Mitchell JH. Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol. 1972;224(1):173-86.
• ³⁵
  Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Group III and IV muscle afferents contribute to ventilatory and cardiovascular response to rhythmic exercise in humans. J Appl Physiol. 2010;109(4):966-76.
• ³⁶
  Monteiro WD, Araujo CG. Cardiorespiratory and perceptual responses to walking and running at the same speed. Arq Bras Cardiol. 2009;93(4):418-25, 410-7.
• ³⁷
  Ogawa T, Spina RJ, Martin WH 3^rd, Kohrt WM, Schechtman KB, Holloszy JO, et al. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation. 1992;86(2):494-503.
• ³⁸
  Evans JA, Whitelaw WA. The assessment of maximal respiratory mouth pressures in adults. Respir Care. 2009;54(10):1348-59.
• ³⁹
  Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC. Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J. 1993;16:5-40.
• ⁴⁰
  Herdy AH, Uhlendorf D. Reference values for cardiopulmonary exercise testing for sedentary and active men and women. Arq Bras Cardiol. 2011;96(1):54-9.

Cardiorespiratory optimal point: a submaximal variable of the cardiopulmonary exercise testing

Plínio Santos Ramos^I,II,III; Djalma Rabelo Ricardo^I,II,III; Claudio Gil Soares de Araújo^III,IV

Publication Dates

• Publication in this collection
  02 Oct 2012
• Date of issue
  Nov 2012

History

• Received
  08 May 2012
• Accepted
  21 June 2012
• Reviewed
  19 June 2012