Eur J Appl Physiol (2001) 85: 333338 DOI 10.

1007/s004210100441

O R I GI N A L A R T IC L E

A.M. Edwards N.V. Challis J.H. Chapman D.B. Claxton M.L. Fysh

The test-retest reliability of gas exchange kinetics in humans using a pseudo random binary sequence exercise test
Accepted: 17 March 2001 / Published online: 8 June 2001 Springer-Verlag 2001

Abstract The purpose of this study was to compare the _ O2 ) kinetics test-retest reliability of oxygen uptake (V _ CO2 ) kinetics using a with carbon dioxide output (V pseudo random binary sequence (PRBS) exercise test. A reliable test of gas exchange kinetics would have the potential of being applied as a sports tness test. Ten healthy male subjects agreed to participate in the study and all subjects completed two identical PRBS exercise tests (test 1 and test 2), separated by a 30 min period of inactivity. Three consecutive 300 s PRBS cycles were completed in each test with 20 s exercise intensity changes between 25 and 85 W using an electrically braked cycle ergometer. Fourier analysis was computed for frequencies 3.3, 6.7 and 10 mHz. Statistical analysis by two-way ANOVA with repeated measures did not reveal signicant dierences between test 1 and test 2 for _ O2 kinetics or V _ CO2 kinetics. Static gain of V _ O2 either V for test 1 [9.11 (SD 0.59) mlmin1W1] and test 2 [9.23 (SD 0.64) mlmin1W1] did not dier signicantly _ CO2 between tests. The 95% limits of agreement for V kinetics displayed increased variability in comparison to _ O2 kinetics at each frequency of amplitude ratio and V phase shift. Systematic bias ranged between 0% and 4%, _ CO2 kinetics phase except at frequency 10 mHz of V
A.M. Edwards (&) Physical Education and Sport, School of Education, Reading University, Bulmershe Court, Reading, Berks, RG6 1HY, UK E-mail: a.m.edwards@reading.ac.uk Tel.: +44-0118-9875123 Fax: +44-0118-9318863 N.V. Challis School of Science and Mathematics, Sheeld Hallam University, Sheeld, UK J.H. Chapman D.B. Claxton M.L. Fysh Centre for Sport and Exercise Science, School of Sport and Leisure Management, Sheeld Hallam University, Sheeld, UK

_ O2 kinetics shift which showed a 10% bias for slower V in test 2. It is possible that the increased variability of _ O2 kinetics might be _ CO2 kinetics compared to V V _ CO2 attributable to a lower signal to noise ratio in V kinetics, variations in ventilation or the storage mecha_ O2 kinetics nisms of CO2. The lower variability of V _ compared with V CO2 kinetics suggests that the PRBS _ O2 kinetics has the greater potential for further test of V development as an indicator of aerobic tness. Keywords Pseudo random binary sequence Oxygen uptake Carbon dioxide output kinetics Test-retest reliability

Introduction
_ O2 ) and carbon dioxide output Oxygen uptake (V _ (V CO2 ) kinetics have previously been shown to be faster in individuals possessing higher levels of aerobic tness (Ebfeld et al. 1987; Zhang et al. 1991). This suggests that a reliable test of gas exchange kinetics would have the potential of being applied as a sports tness test. A pseudo random binary sequence (PRBS) exercise test has previously been shown to dierentiate between _ O2 kinetics of elite endurance runners and elite the V sprinters (Edwards et al. 1999a), but not between the _ CO2 kinetics (Edwards et al. 1999b). However, an V earlier study (Fukuoka et al. 1997) investigating the effect of a combination of sprint and strength training on _ O2 and V _ CO2 kinetics observed that V _ O2 kinetics were V unaected by training over a 9 month period, while _ CO2 kinetics were signicantly slowed after 6 and V 9 months (P<0.05). That study used a sinusoidal form of exercise protocol, ranging from 30 W to 60% of the individual maximal oxygen uptake. Although gas exchange kinetics were assessed using a dierent protocol, the ndings of Fukuoka et al. (1997) suggest that, in _ CO2 contrast to the ndings of Edwards et al. (1999b) V kinetics might prove a more sensitive assessment _ O2 kinetics. of training and/or tness levels than V

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However, it is possible that, as the protocol used in study by Fukuoka et al. (1997) elicited elevated plasma lactate concentrations, the results obtained were not exclusively those of phase II gas exchange kinetics. The aim of this study was to evaluate the test-retest _ O2 and V _ CO2 kinetics resulting from reliability of V PRBS testing. Bland and Altman (1986) advocated the use of the 95% limits of agreement method to assess the extent of the reliability between the test and retest results obtained during the performance of identical protocols. Atkinson and Nevill (1998) also suggested that for a new subject from the population studied, it would be expected (with 95% probability) that the dierence between any two tests should lie within the limits of agreement. This method has now been widely applied to examine the reproducibility of sport specic tests (Lamb et al. 1999; Nicholas et al. 2000; Wilkinson et al. 1999). Currently, there is limited knowledge concerning the reproducibility of replicate estimates of gas exchange kinetics. Berry and Moritani (1985) reported the repro_ O2 kinetics ducibility of replicate measurements of V made during two identical step tests. They described the results of their study as satisfactory evidence for the _ O2 kinetics. From a review of reproducibility of V the literature, it appears that no studies have reported on _ CO2 kinetics in response to the test-retest reliability of V low intensity dynamic exercise.

Methods
Subjects Ten healthy male subjects agreed to participate in this study [mean age 25 (SD 3.89) years, body mass 79.88 (SD 13.27) kg, height 183.7 (SD 4.5) cm]. All subjects participated regularly in physical activity and provided their informed consent prior to any test in accordance with the Research Degree Committee regulations of Sheeld Hallam University. Tests 1 and 2 were carried out on the same day and test 2 was completed after a 30 min period of inactivity. The PRBS exercise test In a PRBS test, exercise intensity is switched between two levels over a predened period of time according to the output of a computer algorithm known as a shift register with feedback (Bennett et al. 1981; Kerlin 1974). Several identical sequences can be placed in series over the duration of the exercise test and consequently considerable test data can be gained from the response to identical cycles of the PRBS. In truly random signals, the exercise intensity transitions from high to low or low to high could occur at any time. In a PRBS, the changes in exercise intensity must occur at specic times and are, therefore, controlled by a computer system (Hampton 1965). The externally controlled changes in exercise intensity allows the test to appear random to the subject who cannot predict where these changes will occur and consequently cannot prepare for them. The PRBS protocol chosen for this study was based on the 300 s model utilised by Homann et al. (1992, 1994a) and is the same as used in previous work from this research group (Edwards et al. 1999a, b). All exercise tests were performed on an electrically braked cycle ergometer (550 ERG, Bosch, Berlin, Germany) at a constant pedalling frequency of 1 Hz. The ergometer was linked to

Fig. 1 Breath-by-breath oxygen uptake, carbon dioxide output and work rate (25 W and 85 W) during pseudo random binary sequence exercise in a single subject an exercise intensity control system and the alternating exercise intensities were automatically adjusted by computer (First Breath Software, version 2.0, 1992, Ontario, Canada,). The base unit of the 300 s PRBS comprises 20 s blocks of exercise intensity changes alternating between 25 and 85 W. Three successive repetitions of the 300 s PRBS pattern were performed and the protocol started with a 360 s period at the lower intensity of 25 W which acted as a warmup and concluded with 360 s at 85 W to check for non-linearity in _ O2 and the system. The full test procedure and breath-by-breath V _ CO2 responses of a single subject are shown in Fig. 1. V Measurement of gas exchange kinetics _ O2 and V _ CO2 were measured breath-by-breath using a The V computerised system (Marquette Electronics Inc, Milwaukee, Wis.) incorporating a mass spectrometer (Marquette MGA 1100) and a volume turbine (Alpha Technologies VMM-110). The calibration of the mass spectrometer was checked immediately before and after each test with standard calibration gases. A 3 l syringe was used to calibrate the volume turbine using ow rates similar to subject

335 ventilation. The required tolerance for calibration was 1%. Gas volumes were corrected to standard temperature pressure dry. An algorithm (Beaver et al. 1981) was used to calculate gas exchange at the alveolar level with corrections for changes in lung volume and lung gas composition. In order to reduce the inuence of nonphysiological noise, a computer software (First Breath Software version 2.0, 1992) lter was used to eliminate outlying data. System linearity A criterion for system linearity was set such that there should be no _ O2 between min 3 and 6 of constant insignicant increase in V tensity exercise at the higher intensity following the PRBS cycles. A signicant increase would indicate the presence of a slow component which would aect system linearity (Barstow 1994; Whipp and Ward 1990). Static gain was calculated in order to determine whether the selected PRBS protocol was set at appropriate exercise intensities for aerobic exercise. Static gain was derived from the steady-state _ O2 values at 25 W and 85 W prior to and following the PRBS V cycles. Data analysis of gas exchange kinetics All breath-by-breath data from the three PRBS cycles was linearly interpolated at 1 s intervals and averaged to yield a single 300 s data set per subject. Fourier transform was then performed on the input and output signals for comparison at individual harmonic frequencies. The Fourier technique is a standard method of analysis for multifrequent tests, such as the PRBS. Step tests have typically been used to analyse gas exchange kinetics in the time domain (Hughson and Morrissey 1982; Phillips et al. 1995; Whipp et al. 1982) whereas sinusoidal or multifrequent changes in exercise intensity have been used to analyse gas exchange kinetics in the frequency domain (Homann et al. 1992, 1994a, b; Kowalchuk and Hughson 1990; Kusenbach et al. 1999). Fourier analysis yielded estimates of the response to a sinusoidal exercise intensity at each harmonic frequency. From the Fourier analysis, amplitude ratios (millilitres per minute per watt) and phase shift angle (degrees) were calculated (Jenkins and Watts 1968). The amplitude ratio indicated the magnitude of the response made by the subject, while the phase shift angle described the delay in the response. It is known (Homann et al. 1992, 1994a, b) that the system controlling gas exchange kinetics during PRBS tests is at least quasi-linear over a range of frequencies at least down to periods of 100 s. Consequently, Fourier transform was computed for frequencies 3.3, 6.7 and 10 mHz. Beyond this point, it was unlikely that the subject response will be discernible from non-physiological breath-by-breath noise (Homann et al. 1992). Statistical analysis A two-way analysis of variance (ANOVA) with repeated measures was used to investigate whether dierences existed between test 1 and test 2. Limits of agreement (95%) were applied to the breath-bybreath data generated from the PRBS exercise test. An example of individual dierences between test 1 and test 2 have been plotted _ O2 kinetics at frequency 6.7 mHz against the mean dierence of V of the phase shift. Upper and lower limits of agreement of 1.96 SD were set, within which 95% of the dierences between tests should occur (Fig. 2). _ O2 kinetics and Measurement error has been calculated for V _ CO2 kinetics and has been expressed as a percentage (Atkinson V and Nevill 1998) by applying the calculation: 100(1.96SD di/ grand mean), where SD di represents standard deviation of the dierences between test 1 and test 2 and grand mean represents (mean of test 1+mean of test 2)/2. This method enables the

Fig. 2 An example of the individual dierences plotted for the 95% limits of agreement. Upper and lower limits are displayed at SD1.96 researcher to quickly assess measurement error between comparable tests or harmonic frequencies as a percentage. Systematic bias was assessed as a percentage from the average dierence between tests/the mean of test 1 and test 2100.

Results
System linearity The criterion for system linearity was met by all subjects _ O2 during the 360 s at 85 W did (n=10). Steady-state V not change and consequently no slow components were _ O2 responses. observed in the V _ O2 in test 1 Static gain was calculated for V [9.11 (SD 0.59) mlmin1W1] and test 2 [9.23 (SD 0.64) mlmin1W1) and did not change signicantly between test 1 and test 2. _ O2 kinetics V A two way ANOVA with repeated measures did not reveal signicant dierences between test 1 and test 2 of _ O2 _ O2 kinetics. The limits of agreement results for V V kinetics are shown in Table 1. Systematic bias ranged between 0% and 1% for the _ O2 kinetics and between 1% and amplitude ratio of V 4% for phase shift. A trend for a positive or negative systematic bias was not evident between tests 1 and 2 for _ O2 kinetics. V Measurement error between tests 1 and 2 for the amplitude ratio ranged from 22% to 35% and between 18% and 29% for phase shift. _ O2 An example of the 95% limits of agreement for V kinetics is displayed graphically for frequency 6.7 mHz of phase shift (Fig. 2). _ CO2 kinetics V No signicant dierence was observed between _ CO2 kinetics in tests 1 and 2 using a two-way the V

336 Table 1 The mean values, systematic bias, measurement error and limits of agreement for amplitude ratio and phase shift of oxygen uptake kinetics Frequency (mHz) 3.3 Amplitude: mean values (mlmin1W1) test 1 Amplitude: mean values (mlmin1W1) test 2 Amplitude: systematic bias (%) 95% Limits of agreement Measurement error (%) Phase shift: mean values () test 1 Phase shift: mean values () test 2 Phase shift: systematic bias (%) 95% Limits of agreement () Measurement error (%) 7.57 (SD 0.89) 7.68 (SD 1.04) 1 1.57 to 1.79 22 38.99 (SD 3.75) 37.31 (SD 6.44) 4 13 to 9.64 29 6.7 5.83 (SD 0.77) 5.79 (SD 0.87) 0 2.06 to 1.99 34 67.54 (SD 5.81) 70.5 (SD7.96) 4 10 to 15.93 18 10 4.17 (SD 0.65) 4.2 (SD 1.06) 0 1.47 to 1.52 35 94.31 (SD 15.46) 93.11 (SD 9.56) 1 26.69 to 24.29 27

ANOVA) with repeated measures. The limits of agree_ CO2 kinetics are shown in Table 2. ment results for V _ CO2 kinetics showed inThe limits of agreement for V _ O2 kinetics at creased variability when compared to V each frequency of both amplitude ratio and phase shift. _ CO2 The systematic bias for the amplitude ratio of V kinetics ranged between 2% and 4% compared with 0% _ O2 kinetics. The systematic bias for the and 1% of V _ CO2 kinetics was identical to that of V _ O2 phase shift of V kinetics at frequencies 3.3 and 6.7 mHz, but was higher _ CO2 kinetics 10% and V _ O2 kiat frequency 10 mHz (V netics 1%). The measurement error (percentage) was consistently _ CO2 kinetics when compared with V _ O2 kihigher for V netics at all frequencies of both amplitude ratio and phase shift (Tables 1, 2).

Discussion
The results of this study showed that the PRBS exercise _ O2 kinetics test produces a more reliable estimate of V _ than V CO2 kinetics. The relatively large variability be_ CO2 kinetics tests, as evidenced tween tests 1 and 2 of V by wider limits of agreement and measurement error _ CO2 kinetics are unlikely (Tables 1, 2), suggested that V to detect physiological dierences between groups or

detect change following a period of training. This nding _ O2 kinetics dierensupports previous work in which V _ CO2 kinetics did tiated between elite sprinters while V not (Edwards et al. 1999b). _ O2 and V _ CO2 The calculation of systematic bias for V kinetics did not show a positive or negative trend be_ CO2 kitween tests, however, a 10% bias for slower V netics was detected in test 2 at frequency 10 mHz of the phase shift. A consistent systematic bias between tests could indicate that a learning eect had occurred or that fatigue had inuenced the results, however, the 10% bias observed was most likely to have been a feature of the _ CO2 kinetics assessed in response to high variability in V such relatively low intensity exercise. _ CO2 kinetics The higher variability observed in V might be attributable to dierences in the signal to noise _ O2 kinetics and V _ CO2 kinetics, greater ratio between V _ _ O2 , variations in ventilation in V CO2 compared with V or a change in CO2 storage during the test period. At the workrates used in the PRBS test, CO2 production is lower than O2 uptake and this is reected in _ CO2 kinetics compared the lower amplitude ratios for V _ with V O2 kinetics (Tables 1, 2). A consequence of the reduced amplitude of the CO2 response is that the signal to noise ratio will be lower, thus reducing the condence _ CO2 kinetic measures and increasing the test in the V retest variability.

Table 2 The mean values, systematic bias, measurement error and limits of agreement for amplitude ratio and phase shift of carbon dioxide output kinetics Frequency (mHz) 3.3 Amplitude: mean values (mlmin1W1) test 1 Amplitude: mean values (mlmin1W1) test 2 Amplitude: systematic bias (%) 95% Limits of agreement Measurement error (%) Phase shift: mean values () test 1 Phase shift: mean values () test 2 Phase shift: systematic bias (%) 95% Limits of agreement () Measurement error (%) 5.34 (SD 1.6) 5.21 (SD 1.88) 2 3.01 to 2.85 57 50.48 (SD 11.82) 48.48 (SD 20.66) 4 35.45 to 31.38 66 6.7 4.05 (SD 0.93) 3.91 (SD 1.18) 4 2.55 to 2.25 59 81.28 (SD 13.39) 85.12 (SD 22.99) 4 29.48 to 37.16 39 10 2.45 (SD 1.52) 2.41 (SD 1.13) 2 2.72 to 2.65 108 116.13 (SD 61.45) 128.67 (SD 36.68) 10 95.77 to 120.86 87

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_ CO2 has previously been shown Breath-by-breath V to exhibit lower variability in the steady state of exercise _ O2 (di Prampero and Lafortuna 1989). This than V suggests that variations in ventilation were unlikely to have accounted for the dierences seen in the present study. It is possible, however, that the variability of _ CO2 and V _ O2 might be dependent on breath-by-breath V the type of exercise protocol employed. At the onset of exercise, the CO2 production at the lung increases relatively slowly compared to the O2 consumed (Diamond et al. 1977; Linnarsson 1974; Whipp and Mahler 1980). This is attributable to the relatively high solubility of CO2 in tissues compared to O2 (Whipp and Ward 1990). Storage of CO2 increases during the 1st min of exercise (Zhang et al. 1991) and the presence of sizeable intervening stores of CO2 is likely to _ CO2 from CO2 production (Whipp and dissociate V Ward 1990). Therefore, while a proportion of CO2 production is being stored during low intensity exercise, _ CO2 kinetics measured at the mouth might not the V directly reect CO2 kinetics at the muscle. In response to beginning exercise, it is known that _ CO2 kinetics are characterised by _ O2 kinetics and V V _ O2 three phases (Whipp et al. 1982). Although both V _ and V CO2 follow three distinct phases, much slower _ CO2 response dynamics have been demonstrated for V _ O2 (t1/2  30 s) (Diamond et al. 1977; (t1/2  45 s) than V Linnarsson 1974; Whipp and Mahler 1980) suggesting the presence of intervening mechanisms. It is possible that the dierences in reliability observed in this study _ CO2 and V _ O2 were a result of the inuence of between V a greater tissue capacitance for CO2 than O2 causing a _ CO2 dynamics. delay in V A number of studies (Hughson and Morrissey 1982; _ CO2 Whipp et al. 1982) have shown that the kinetics of V _ and V O2 are dependent on the exercise transitions _ O2 kinetics are faster than studied. From rest to work, V _ CO2 kinetics, however, when exercise proceeds from V _ O2 light to moderate or heavy exercise intensities, V _ CO2 kinetics are either kinetics become slower while V unchanged or become faster (Hughson and Morrissey 1982). Thus the pattern changes such that less CO2 is stored at higher exercise intensities. However, the variability of CO2 storage over the test sessions is unclear and further work will be required to investigate the stability of CO2 storage in response to dynamically alternating exercise intensities. The closer agreement between test 1 and test 2 of _ O2 kinetics, in comparison to V _ CO2 kinetics, supV _ O2 ported previous work which identied that a test of V kinetics could distinguish between groups of athletes (Edwards et al. 1999a; Fukuoka et al. 1995). An individual's dynamic O2 response to exercise depends on various factors such as exercise intensity (Casaburi et al. 1989; Jones and Reeves 1968), state of tness (Hagberg et al. 1978; Hickson et al. 1978) and age (Chillibeck et al. 1996). A quicker response would reect a more eective aerobic system with less reliance on anaerobic energy contribution at the onset of exercise. In terms of an

athlete's performance, this would have the benecial eect of enabling athletes to have more energy available for a competitive event and would also be of benet to athletes requiring a change of pace during a race, as they would avoid incurring premature fatigue. A number of physiological tests exist which have the potential to describe aerobic tness however, the direct measurement of maximal capacity has more traditionally been expected to provide a better estimation of aerobic tness than submaximal evaluation. Tests of maximal capacity do, however, present greater cardiorespiratory stress than submaximal tests and could be inconvenient for elite athletes undergoing training, or in studies of the wider population, due to the potential risk from undiagnosed heart disease. A suitable submaximal test, such as the PRBS exercise test that can describe aerobic tness, would provide an attractive alternative. _ O2 kinetics in In conclusion, the lower variability of V _ comparison with V CO2 kinetics indicated that, as a single session laboratory PRBS exercise test, measure_ O2 kinetics has greater potential for development of V _ CO2 kinetics. Single session laboratory tests ment than V have often been reported to uctuate (Hughson and Inman 1986) and although these test-retest results of _ O2 kinetics were in closer agreement than for V _ CO2 V kinetics, the relatively high variability of both measurements suggested that the test might be limited to the comparisons among groups rather than assessment of an individual's tness. Condence in laboratory tests might be enhanced by repeated tests as a greater averaged test response would minimise the inuence of nonphysiological breath-by-breath noise (Lamarra et al. 1987). However, the further development of the PRBS exercise test depends on it being suciently reliable in describing aerobic tness with a minimal imposition on _ O2 kinetics the subjects. According to this criterion, V measured by this particular PRBS exercise test has greater potential as an exercise test for group compari_ CO2 kinetics. sons than V

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