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TECHNOLOGY, COMPUTING, AND SIMULATION

The Accuracy of the Oxygen Washout Technique for Functional Residual Capacity Assessment During Spontaneous Breathing

Hermann Heinze, MD^*, Bernhard Schaaf, MD, Jochen Grefer, MD^*, Karl Klotz, MD^*, and Wolfgang Eichler, MD^*

From the Departments of *Anesthesiology and Medicine III, University of Luebeck, Luebeck, Germany.

Address correspondence and reprint requests to Hermann Heinze, MD, Department of Anesthesiology, University of Luebeck, Ratzeburger Allee 160, 23538 Luebeck, Germany. Address e-mail to Hermannheinze{at}ngi.de.

	Abstract

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BACKGROUND: Measurement of functional residual capacity (FRC) is of considerable interest for monitoring patients with lung injury. The lack of instruments has impeded routine bedside FRC measurement. Recently, a simple automated method for FRC assessment by O₂ washout has been introduced. We designed this study to evaluate the accuracy of FRC measurement using the O₂ washout technique.

METHODS: The LUFU system (Draeger, Luebeck, Germany) estimates FRC by O₂ washout, a variant of multiple breath nitrogen washout. This technique uses a sidestream O₂-analyzer to calculate FRC from end-inspired and end-expired O₂ concentrations during fast changes of Fio₂. We measured FRC in 23 healthy, spontaneously breathing volunteers in the sitting position using three techniques: 1) helium dilution (FRC-He), 2) body plethysmography (FRC-bp), 3) oxygen washout (FRC-O₂).

RESULTS: FRC-O₂ (mean 4.1 ± 1.1 L, range 2.4–6.9 L) corresponds with FRC-He (mean 4.0 ± 1.0 L, range 2.4–6.2 L; bias of FRC-O₂: –0.2 ± 0.4 L) and FRC-bp (mean 4.2 ± 1.0 L, range 2.8–6.1 L; bias of FRC-O₂: 0.1 ± 0.6 L).

CONCLUSIONS: The bias and precision of the O₂ washout technique using the LUFU system were clinically acceptable when compared with FRC-He and FRC-bp for FRC assessment in spontaneously breathing volunteers.

	Introduction

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Acute lung injury (ALI) or acute respiratory distress syndrome (ARDS) causes alveolar collapse, resulting in a reduction of functional residual capacity (FRC) (1–4). Furthermore, by using lung-protective strategies with low tidal volume ventilation to prevent alveolar over-distension and secondary ventilator-induced lung injury, derecruitment and a reduction of FRC is possible (5). Several techniques for maintaining FRC in mechanically ventilated patients have been advocated, i.e., adequate positive end-expiratory pressure (PEEP), recruitment maneuvers, and prone positioning. To guide such therapies, an accurate noninvasive method of measuring FRC would be helpful (5,6).

There are three general techniques that have been used to assess FRC. Body plethysmography has been used in anesthetized patients (7), but is too cumbersome for the intensive care setting. The helium dilution method is a rebreathing technique, which requires a gas-tight closed circuit, including the respirator, in order to reach equilibrium of the tracer gas. As intensive care unit ventilators usually do not use rebreathing systems, they are not practical for FRC measurement with this technique (8). The washin/washout of a tracer gas (e.g., sulfur hexafluoride, nitrogen, or O₂) can be analyzed in a multiple breath procedure to determine FRC. The problem with any tracer gas is the need of a sensitive gas analyzer, which is fast enough to allow breath-by-breath computation of inspired or expired tracer gas mass by multiplication of gas concentration by inspired and expired flow (9–13).

A simple automated method for evaluating FRC using O₂ washout has been introduced into clinical practice (14). Because the response time of O₂ sensors is not fast enough to follow the timecourse of the concentration during transition from inspiration to expiration and vice versa, the device was equipped with a mainstream analyzer for O₂ and CO₂. The system estimated FRC assuming that the course of O₂ and CO₂ concentrations are mirror images of each other, thus the dead-space measured with O₂ is nearly identical to that measured with CO₂. The technique showed high accuracy when compared with the helium dilution technique and body plethysmography and, furthermore, increments by change of body position and induction of general anesthesia could be reliably detected (14). However, methodological difficulties using the CO₂ waveform for FRC measurement may lead to gross systematic errors of up to 20% (15).

We used an advancement of O₂ washout technique using a sidestream O₂ analyzer. This is possible by using a physical/mathematical model that calculates the flow-dependent delay time of the sidestream O₂ analyzer. Therefore, a mainstream CO₂ analyzer is no longer required to separate inspiration and expiration.

The aim of our study was to evaluate the accuracy of FRC measurements with the improved O₂ washout technique using a sidestream O₂ analyzer in vivo. Toward that end, we compared the new O₂ washout technique with the helium dilution technique and with body plethysmographic determination of FRC during spontaneous breathing in volunteers.

	METHODS

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After receiving approval by the local ethics committee and written informed patient consent, we examined FRC in 23 clinically healthy, spontaneously breathing volunteers using three techniques, i.e., O₂ washout (FRC-O₂), body plethysmography (FRC-bp), and helium dilution (FRC-He). Demographic data are presented in Table 1. After termination of one measurement, the next one was started immediately. All three measurements together lasted approximately 20 min. The sequence of measurements was randomized by drawing lots. For all three techniques, the volunteers were in the same sitting position and a nose clip and a mouthpiece were used. The ventilator was set to the spontaneous breathing mode with no level of continuous positive airway pressure (CPAP).

FRC Evaluation by O₂ Washout (FRC-O₂)
The FRC estimation by O₂ washout with the LUFU system (Draeger Medical, Luebeck, Germany) is a variant of the multiple breath nitrogen washout method. Measurements of ventilatory pressures and flow were performed using an intensive care ventilator (EVITA XL®, Draeger Medical, Luebeck, Germany). Oxygen was measured using a fast paramagnetic sensor (Pm1111E, Servomex Group, Crowborough, England) in the sidestream connected with a sampling line at the Y-piece of a standard respiratory tubing system. The response time T_10–90 of the sensor to a step change of O₂ concentration is about 200 ms. Sample flow was adjusted to 200 mL/min.

FRC Determination
When FRC is determined by an O₂ washin or washout, the mass balance is described by the following equation:

C_et,0 and C_et,N are the end-tidal concentrations (fractions) of O₂ before and at the end of the maneuver, M_insp and M_exp are the inspired and expired amounts of O₂ and T is the duration of a breath. The term represents the steady-state difference between inspired and expired fluxes of O₂, i.e., O₂ consumption. However, because other factors like e.g., measurement errors also contribute to this difference, the parameter serves mainly as a quantity that balances this steady-state difference, irrespective of the physiological or technical factors causing it. V_lung is the change of the lung volume during the measurement; V the accumulated difference between inspired and expired volumes. Because the influence of an RQ different from 1.0 needs to be corrected independently (16), the difference between V and V_lung is only given by the alterations of the O₂ content of the blood, VO₂, caused to the changed Fio₂. Equation (1) can therefore be rewritten to:

In the above formula, we have neglected the small influence of the expired CO₂ concentration and the humidity of the gas on the end-tidal concentrations, because they contribute only to the factors proportional to V and VO₂, respectively. Consideration of these small corrections had otherwise made the formulas unduly complicated.

Delay Correction
Sidestream analyzers exhibit a significant delay of about 1 s. In addition, the delay changes during measurements due to changing of gas viscosity and cyclically alternating ventilatory pressures. The method used in the LUFU system for calculation of the variable delay time is based on a physical/mathematical model of the entire pneumatic circuit of the O₂ analyzer (17). The components of this model are the sampling tube from the Y-piece to the water trap, the volume of the water trap, the tubing integral to the gas analyzer, and the characteristics of the gas pump. The gas concentration is sampled at a constant frequency with a fixed time interval dt. Therefore the delay can be expressed in terms of the number N of samples. When the pressure at the Y-piece is zero, the gas flows at a constant speed U_0.. With L = length of the tube and N₀ = delay at zero pressure we get:

During respiration or ventilation, the pressure gradient across the tube alternates. Therefore the speed U is not constant but is different for each sample "i." Because the distance L the gas sample has to travel is unchanged, the Eq. (2) has to be modified to:

From that follows after elimination of L and dt:

The actual delay in terms of samples N is calculated by summation of the normalized speeds U_i/U₀ until this sum equals N₀. The issue is therefore the determination of the normalized speed for each sample. Because the speed U of the gas flow is proportional to the pressure gradient P and inversely proportional to the mean gas viscosity , the normalized speed is given by:

The parameters of this model are the pressure in the water trap at zero ventilation pressure, the volume of the water trap, the sample flow at zero ventilation pressure, and the characteristics of the gas pump. With this model, the gas flow through the various components of the instrument is calculated continuously. From that follows the transit time of gas from the Y-piece to the sensor. The finite response time of the O₂ sensor is corrected using a standard procedure to reconstruct the ingoing signal out of the dampened outgoing signal. The flow signals measured by the ventilator are further corrected for the influence of the gas composition on the flow reading. Thus, synchrony between flow and gas concentration measurements can be restored (17). This allows the determination of volumetric gas fluxes as needed for FRC measurement.

Inequality of Inspired and Expired Volumes
During measurement, the flow of O₂ from the lungs to the blood will change transiently, even during constant O₂ consumption. This leads to concurrent transient changes of the difference between inspired and expired lung volumes. However, the difference between inspired and expired volumes can also change for other reasons not related to a changed O₂ content of the blood. Intermittent large volume breaths, e.g. during partial ventilatory support, can lead to a change of the lung volume that persists until the end of the measurement. As the two factors require different mathematical considerations, they need to be corrected independently. Unfortunately, the only information that is available for this correction is the accumulated difference between inspired and expired volumes, V.

This volume difference consists of two components. One is the change of lung volume during the measurement, V_lung; the other is the change of the O₂ content of the blood, VO₂. However, only the sum of both is measurable:

The change of lung volume can only be assessed after VO₂ is known. Because VO₂ can be estimated only after the completion of the measurement, it seems preferable to perform the calculations in two steps. In the first step, VO₂ is ignored and V_lung is approximated by the measured total V. In the second step, the result is corrected for the neglected parameter VO₂ by:

The LUFU system starts the analysis automatically by detecting a step change of inspired O₂ fraction of 10% O₂ or more. All data needed for the FRC determination, i.e., inspired and expired volumes, mean inspiratory and expiratory O₂ concentrations, and end-expiratory O₂ concentration are continuously analyzed and displayed online. After each breath, the current estimate of the FRC using the acquired data is displayed. Analysis is terminated automatically when the accumulated net ventilated volume, sum of tidal volume minus serial dead-space (calculated using the Bohr formula), is more than eight times the calculated FRC.

During the experiment, the O₂ washin period was started by changing the inspired O₂ fraction abruptly from 0.21 to 0.8. After automatic termination of the measurement, a washout period of O₂ was started immediately by changing Fio₂ again to 0.21. During the whole period, there was no disconnection of the ventilator.

FRC Evaluation by Body Plethysmography (FRC-bp)
The FRC-bp measurements were made with an automated pressure/flow plethysmograph (Bodyscope-S, Ganshorn Medizin Electronic, Niederlauer, Germany). FRC-bp was calculated using standard equations for plethysmography (18).

FRC Evaluation by Helium Dilution Technique (FRC-He)
An automated pulmonary function testing system (CO-Diffusion, Ganshorn Medizin Electronic, Niederlauer, Germany) was used. FRC-He was calculated using standard equations (19).

Statistical Analysis
Before beginning of the study, a power analysis based on Eichler et al. ’s study data (14) was performed. We calculated that 22 volunteers were needed to detect a difference of 25%, a threshold we considered clinically relevant, between each technique at a test power of 80% with a two-tailed Type I error of 0.05.

If not stated otherwise all values are presented as mean ± sd. Agreement between pairs of measurements (FRC-O₂ versus FRC-bp or FRC-He, respectively and FRC-bp versus FRC-He) were analyzed according to the methods described by Bland and Altman (20). A probability value of <0.05 was considered as significant (21).

We calculated the mean value of one washin and one washout procedure (FRC-O₂).

	RESULTS

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Mean FRC values were as follows: FRC-O₂ (4.1 ± 1.1 L, range 2.4 –6.9 L); FRC-He (4.0 ± 1.0 L, range 2.4 –6.2 L); FRC-bp (4.2 ± 1.0 L, range 2.8 –6.1 L). The Bland-Altman transformation revealed a bias of FRC-O₂ of –0.2 ± 0.4 L corresponding to about 5% of FRC-He with a doubled standard deviation (2 sd) of 0.9 L (22.5%) (Fig. 1) and a bias between FRC-bp and FRC-O of 0.1 ± 0.6 L, corresponding to about 2.6% of FRC-bp with a 2 SD of 1.1 L (26.2%) (Fig. 2). Bias between FRC-bp and FRC-He was –0.3 ± 0.5 L or, expressed in percentage, about 6.6% of FRC-He, with a precision (2 sd) of 1.0 L (25%) (Fig. 3).

View larger version (10K): [in this window] [in a new window]   Figure 1. Absolute differences versus mean values for functional residual capacity (FRC) measurement by the helium indicator method (FRC-He) and oxygen washout method (FRC-O2) in spontanously breathing volunteers. The traced line corresponds to the mean of the differences between FRC-He and FRC-O2 (–0.2 L), the dashed lines are equivalent to double standard deviations (–1.0; +0.8).

View larger version (11K): [in this window] [in a new window]   Figure 2. Absolute differences versus mean values for functional residual capacity (FRC) measurement by bodyplethysmography (FRC-bp) and oxygen washout method (FRC-O2) in spontanously breathing volunteers. The traced line corresponds to the mean of the differences between FRC-bp and FRC-O2 (0.1), the dashed lines are equivalent to double standard deviations (–1.0; +1.2).

View larger version (12K): [in this window] [in a new window]   Figure 3. Absolute differences versus mean values for functional residual capacity (FRC) measurement by the helium indicator method (FRC-He) and bodyplethysmography (FRC-bp) in spontanously breathing volunteers. The traced line corresponds to the mean of the differences between FRC-He and FRC-bp (–0.3), the dashed lines are equivalent to double standard deviations (–1.3; +0.8).

	DISCUSSION

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These data indicate that the FRC assessment by O₂ washout provides clinically acceptable accuracy when compared with FRC evaluation using helium dilution or body plethysmography during spontaneous breathing in healthy volunteers. The FRC-O₂ technique showed low bias values compared with standard methods for measuring FRC during spontaneous breathing, but the large limits of agreement reflect a low precision.

The O₂ washout method is based on the multiple breath nitrogen washout technique. The method as proposed here requires neither a nitrogen analyzer nor special tracer gas analyzers nor gas delivery valves, e.g., like the SF₆ method (10,12,13). The technique was first described by Fretschner et al. (15) and an improved variant was introduced into clinical practice by Eichler et al. (14). The basic concept behind their methods is that the waveforms of expired O₂ and CO₂ are nearly mirror images of each other. Therefore, the time course of expired O₂ can be estimated from the minimum and maximum O₂ fraction and the time course of expired CO₂. These methods have several drawbacks. Although the O₂ and CO₂ waveforms are nearly inversely congruent under steady-state conditions, this congruency may get lost during the first breaths of the washin or washout maneuver. In addition, the reconstruction can be performed only during expiration, but assumptions must be made on the inspiratory waveform. Although the concentration of O₂ at the ventilator outlet may change in a stepwise manner, the tubing system and humidifiers act as an additional compartment that also has to be washed in or out. This leads to large systematic errors as described by Fretschner et al. (15). Because the response time of commercially available O₂ sensors is not fast enough to determine the amount of inspired and expired O₂, Eichler et al. had to combine it with a "rapid" CO₂ analyzer (14).

In this study we used a simplified technique with a sidestream O₂ analyzer. In addition, pressures and flow were measured with the ventilator’s built-in analyzers. If integrated in future ventilators the device could work fully automatically. This could help in guiding therapy, although further studies are needed to establish the clinical utility of FRC measurement.

Determination of FRC is not a routine monitoring tool in critically ill patients, but has mainly been used in research situations, either by tracer gas dilution in a closed system, e.g., helium, or by multiple breath washout technique. One problem with rebreathing methods is that intensive care unit ventilators usually do not use rebreathing systems, and therefore have to be modified substantially (8). The multiple breath nitrogen washout method has been used in mechanically ventilated patients (22). The accuracy of FRC determination with nitrogen using sidestream gas analysis critically depends on methodological sophistication because of synchronization of gas flow and concentration measurements. This may gain special importance during spontaneous breathing or partial ventilatory support due to the dynamic pulmonary status or the constantly changing breathing pattern. Zinserling et al. (23) described a technique using corrections for gas viscosity, sampling delay time, and re-inspired nitrogen during partial ventilatory support. Their results suggest a good repeatability in patients, and good accuracy in a lung model. But the main problem with nitrogen washout for routine clinical use is that it requires either a mass spectrometer or a Raman scattering technique for direct analysis. Olegard et al. (24) circumvented this problem by using the end-tidal and inspiratory O₂ and CO₂ concentration output signals from a standard sidestream gas monitor and flow measurements from the ventilator. In patients in whom no gases other than O₂, CO₂, and nitrogen are present, nitrogen can be calculated as the residual by measuring O₂ and CO₂. Their method can be used with a step change as small as 10% in inspiratory O₂ concentrations, an issue very important for patients with ALI or ARDS with high Fio₂ (24). Olegard et al. (24) showed high accuracy in a lung model and high repeatability in ventilated patients with their device, but it has not been used during partial ventilatory support or spontaneous breathing.

One basic assumption of any method that requires a Fio₂ change, is that O₂ is regarded as an insoluble gas, i.e., the amount of O₂ stored in the blood does not change significantly during measurement. Lundin (25) determined the rate at which nitrogen is eliminated from the blood and the tissue during O₂ breathing. He found that the body compartment with the shortest time-constant has a volume slightly more than that of the blood, and that it is washed out with a half-life of about 2 minutes. From these data and the solubility of O₂, Weismann et al. (17) estimated that under typical conditions, the body stores for O₂ lead to a systematic overestimation of the FRC by 180 mL. This needs to be corrected. Additional corrections, e.g., by Spo₂ measurement, may be required for patients with a low O₂ saturation.

The methods of both Zinserling et al. and Olegard et al. have shown high accuracy only in a lung model and good repeatability during duplicate measurements in patients, but have not been compared with other methods for FRC assessment (23,24). The O₂ washout method using the LUFU System has proven to measure FRC reliably under laboratory conditions with a lung simulator. By changing compliance, tidal volumes, and ventilation modes, worst case scenarios were simulated. The accuracy was <5% with tidal volumes more than 400 mL. With tidal volumes of 300 mL, the accuracy may reach up to 10%. Reproducibility is unaffected by a change of tidal volume and amounts to 2%–3%. The asymmetry, i.e., the difference between consecutive washins and washouts, was of the same magnitude (17).

In addition, we compared the O₂ washout method with standard methods for FRC estimation during spontaneous breathing in volunteers. As expected, the O₂ washout technique seemed to slightly underestimate the FRC compared to FRC-bp. Body plethysmography determines the total intrathoracic air volume, including even air behind collapsed airways, which does not participate in ventilation and is therefore expected to result in higher FRC values than gas dilution techniques even in healthy subjects (8,26). This can also be seen by comparing FRC-bp and FRC-He, where FRC-bp showed higher values.

Compared to the method described by Eichler et al. (14), we could show a further improvement of accuracy by the new O₂ washout technique. In their study, the bias between FRC-He and FRC-O₂ was 0.53 L, corresponding to about 16% of mean FRC-He. The data presented here show a bias of –0.2 L, corresponding to about 3.8% of mean FRC-He. The bias between FRC-bp and FRC-O₂ in our study was slightly higher than in the publication by Eichler et al. (14) (0.1 L (2.6%) and 0.03 L (1%), respectively). But this difference is well within the range of demanded measurement errors of 5% (8).

Although the FRC-O₂ method showed low bias values when compared with standard methods for measuring FRC during spontaneous breathing, the large limits of agreement reflect a low precision. This limits the clinical usefulness when considering absolute FRC values. But during spontaneous breathing, absolute values of FRC may differ significantly. This can be seen in the precision of FRC-He when compared with FRC-bp. The derived limits of agreement of 1.0 L, representing approximately 25% of the mean FRC-He value, show low precision using these standard techniques. But more important than absolute values may be the reproducibility to consider changes over time. Future work should study if consecutive measurements in volunteers or patients reveal the same good results as in a lung model. Weismann et al. reported a variability of consecutive measurements of about 2.5% (17).

There are limitations to this study. Patients with ALI or ARDS are those expected to benefit most from a measurement of FRC. But these patients are not ventilated with a mouthpiece but with a tube or a CPAP-mask. In addition, they are lying down, have different PEEP levels and, especially during the weaning process with partial ventilatory support, changing breathing patterns. Of course our data cannot be applied to this patient group. But, as a first step to introduce the further developed FRC-O₂-measurement with the sidestream analyzer into clinical routine, it was the aim of this study to compare it with standard measurements of FRC in spontaneous breathing. Therefore we had to use the same modalities as FRC-BP or FRC-He, i.e., using a mouthpiece and placing the volunteers in a sitting position. Because of this we could not use different CPAP or PEEP levels. The next step would be to study the accuracy and reproducibility of FRC-O₂ in patients with ALI and ARDS.

The algorithm of the LUFU system was designed to compensate for fluctuating tidal volumes, which are present during spontaneous breathing as well as during assisted ventilation. Whether the results are as good under clinical conditions in patients with ALI or ARDS as in a lung model (17) should be investigated in further studies.

We used a large O₂-step from Fio₂ 0.21–0.8. This may not be possible in patients who require high Fio₂ values to maintain adequate arterial oxygenation. This large change was chosen in order to generate a great change of viscosity of the sample gas, thereby introducing a significant change of the sample delay. We hypothesized that if the LUFU system would measure FRC under these conditions with high accuracy compared to standard measurements, the results should be better, or at least equal, using smaller step changes of Fio₂. Further studies are needed to confirm that hypothesis.

Another drawback of any O₂ or nitrogen washin/ washout is the requirement for stable circulatory conditions. Any change of cardiac output immediately before or after the measurement may change the O₂ content of the venous blood significantly. This can lead to gross errors. Olegard et al. (24) measured O₂ consumption and CO₂ production using indirect calorimetry. Because our method does not correct the measured FRC for a change of O₂ consumption, measurement should not be performed immediately after e.g., a recruitment maneuver, as well as during any change of hemodynamic therapy that could alter the hemodynamic status. To further improve the FRC-O₂ measurement, this should be addressed in future studies.

In conclusion, we have shown that FRC assessment by O₂ washout using the LUFU system provides clinically acceptable accuracy when compared with standard methods for FRC evaluation, i.e., helium-dilution and body plethysmography, in spontaneously breathing volunteers.

	ACKNOWLEDGMENTS

 
The authors thank Draeger Medical, Luebeck, Germany for providing the LUFU system and Dr. Dieter Weismann from Draeger Medical for his technical support. The authors also acknowledge the help of the institutional statistician Michael Hueppe, PhD.

	Footnotes

 
Accepted for publication September 27, 2006.

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