Research ArticleOriginal Research

The Effect of Alveolar Dead Space on the Measurement of End-Expiratory Lung Volume by Modified Nitrogen Wash-Out/Wash-In in Lavage-Induced Lung Injury

Rui Tang, Yingzi Huang, Qiuhua Chen, Xia Hui, Yang Li, Qing Yu, Hongjie Zhao, Yi Yang and Haibo Qiu
Respiratory Care December 2012, 57 (12) 2074-2081; DOI: https://doi.org/10.4187/respcare.01800

Abstract

BACKGROUND: The accuracy of end-expiratory lung volume measurement by the modified nitrogen wash-out/wash-in method (EELV-N2) depends on the precise determination of carbon dioxide elimination (V̇CO2), which is affected by alveolar dead space (VD-alv). The purpose of this study was to investigate the influence of VD-alv on EELV-N2.

METHODS: Six piglets with lavage-induced acute lung injury were mechanically ventilated in a decremental PEEP trial that was reduced from 20 to 4 cm H2O in steps of 4 cm H2O every 10 min. EELV was measured by the modified EELV-N2 method and computed tomography scan (EELV-CT), volumetric capnography, blood gas measurements, and hemodynamic data were recorded at each PEEP level. The data were divided into higher and lower PEEP groups.

RESULTS: During the decremental PEEP trial, EELV-N2 exhibited a high correlation (r2 = 0.86, P < .001) with EELV-CT, with a bias of −48.6 ± 150.7 mL (1 ± 18%). In the higher PEEP group, EELV-N2 was not correlated with EELV-CT, with a bias of –168.1 ± 171.5 mL (−14 ± 14%). However, in the lower PEEP group, EELV-N2 exhibited a high correlation (r2 = 0.86, P < .001) with EELV-CT, with a bias of 11.2 ± 97.2 mL (6 ± 17%). The measurement bias was negatively correlated with VD-alv (r2 = 0.44, P = .04) and V̇CO2 (r2 = 0.47, P = .03) in the higher PEEP group.

CONCLUSIONS: In this surfactant-depleted model, EELV measurement by the modified EELV-N2 method reveals a systematic underestimation at high PEEP levels that is partly due to an increase in VD-alv.

Introduction

Determination of end-expiratory lung volume (EELV) can help to monitor severity of acute lung injury1; to assess respiratory mechanics, such as specific lung compliance,2 lung strain,3,4 and alveolar recruitment5–7; to guide lung-protective ventilation8–10; and to identify patients who profit from recruitment maneuver after endotracheal suctioning.11

Despite its critical role in the management of critically ill patients, EELV measurement is not without difficulties, especially in ventilated patients. Quantitative analysis of pulmonary computed tomography (CT) at end-expiration is the gold standard for EELV measurement.12 However, the repeated measurements of EELV by pulmonary CT are obviously impractical because of radiation exposure, arduous analysis process, and the unavailability of the CT scan at the bedside. Recently, multiple breath wash-out methods, such as the modified nitrogen wash-out/wash-in technique (EELV-N2),13 have enabled EELV determination in ventilated patients without the need to interrupt mechanical ventilation. Previous studies demonstrated that the EELV-N2 method is highly accurate in patients with acute respiratory failure,13,14 ventilated pediatric patients,15 and in an animal model of unilateral pleural effusion.16

Although the EELV-N2 technique is now commercially available and can be performed easily, a potential problem in using this method is alveolar dead space (VD-alv), which can affect the accuracy. According to the algorithm of the method, the volume of nitrogen wash-out/wash-in is not measured directly but is calculated by determining oxygen consumption (V̇O2), carbon dioxide elimination (V̇CO2), and inspiratory and end-tidal concentrations of oxygen and carbon dioxide (PETCO2).13 Alveolar tidal volume (VT-alv) is an important variable to calculate the volume of nitrogen in this method, and is computed according to the Bohr formula: VT-alv=V˙CO2/PETCO2

Previous studies showed that an increase in VD-alv that is induced by PEEP leads to impaired V̇CO2 in both healthy and injured lungs,17–19 which can cause an underestimation of VT-alv and EELV. Furthermore, in order to solve the synchronization problems about gas flow and concentration measurements, PETCO2 is used to calculate VT-alv. However, PETCO2 is higher than the alveolar partial pressure of CO2 in acute lung injury, as the phase III slope for volumetric capnography is not always a plateau, but can be positive.20–22 Thus, VT-alv may be underestimated when calculated using PETCO2 instead of alveolar CO2 concentration, which can potentially lead to errors in EELV measurements.

In light of the above reasons, the purposes of this study were to evaluate the effect of VD-alv on the accuracy of measuring EELV-N2 in lavage-induced lung injury, and to determine whether an increase in VD-alv at high PEEP induces an underestimation of EELV.

QUICK LOOK

Current knowledge

The accuracy of end-expiratory lung volume measurement by modified nitrogen wash-out/wash-in requires precise measurement of carbon dioxide production (V̇CO2). While V̇CO2 measurement is straightforward, the accuracy can be affected by alveolar dead space.

What this paper contributes to our knowledge

In a surfactant-depleted porcine model of acute respiratory distress, the accuracy of end-expiratory lung volume (EELV) measurements is affected by an increase in alveolar dead space caused by excessive PEEP. EELV measurements underestimate actual volumes at high PEEP.

Methods

Animal Preparation

This study was conducted at Southeast University School of Medicine, Nanjing, China, after approval by the institutional animal ethics committee. Six healthy piglets (2 male, 4 female) weighing 33.3 ± 1.6 kg were pre-medicated with intramuscular midazolam (0.3 mg/kg) and ketamine (10 mg/kg). The animals were subsequently anesthetized by a continuous infusion of pentobarbital (10–20 mg/kg/h), fentanyl (3–6 μg/kg/h), and pancuronium (0.5 mg/kg/h).

The animals were tracheotomized and mechanically ventilated in the supine position via an 8-mm inner diameter endotracheal tube (Mallinckrodt/Covidien, Mansfield, Massachusetts) using a constant flow volume controlled mode (Engström CareStation, Datex, GE Healthcare, Madison, Wisconsin). Throughout the experiment the animals were ventilated with a VT of 6 mL/kg, a respiratory rate of 30 breaths/min, an inspiratory/expiratory ratio of 1:2, and an FIO2 of 0.5.

Lung Lavage Procedure

Lung injury was induced by surfactant depletion after lung lavage with warmed normal saline (30 mL/kg at 37–39°C). Lung lavages were performed every 5 min until PaO2 was below 150 mm Hg on pure oxygen and PEEP of 0 cm H2O. The injury was then allowed to stabilize over the following 60 min on baseline ventilator settings.

Protocol

After stabilization of the lung injury, the animals were transferred to the CT scan room. A 2-min recruitment maneuver was performed in the pressure control mode with a PEEP of 20 cm H2O, a peak inspiratory pressure of 50 cm H2O, respiratory rate of 20 breaths/min, inspiratory/expiratory ratio of 1:1, and FIO2 of 1.0. Thereafter the ventilator was changed back to the previous settings, and PEEP was reduced in 4 cm H2O steps, from 20 cm H2O to 4 cm H2O. Each PEEP level was maintained for 10 min before data acquisition. At the end of the study, all experimental animals were euthanized by an intravenous overdose of potassium chloride solution.

Hemodynamic Monitoring and Blood Gas Measurements

Central venous and pulmonary artery pressures were measured using a 7.5 French pulmonary artery catheter (Arrow, Teleflex Medical, Reading Pennsylvania) that was advanced via the left internal jugular vein. The right femoral artery was cannulated with a 4 French, 8-cm catheter (PiCCO, Pulsion Medical Systems, Feldkirchen, Germany). For hemodynamic monitoring, an electrocardiogram monitor (PM-9000 Express, Mindray, Shenzhen, China) and a hemodynamic monitor (PiCCO plus, Pulsion Medical Systems, Feldkirchen, Germany) were used. Cardiac output was measured by the hemodynamic monitor system as the average of 3 repeat injections of 10 mL iced normal saline into the right atrial port of the pulmonary artery catheter. Arterial and mixed venous blood gases were measured using a blood gas analyzer (Critical Care Xpress, Nova Biomedical, Waltham, Massachusetts). The venous admixture was calculated using the formula (capillary oxygen content – arterial oxygen content)/(capillary oxygen content – mixed venous oxygen content). After establishing intravenous access, a continuous infusion of normal saline was delivered at a rate of 5 mL/kg/h. Body temperature (rectal) was maintained at 36–38°C with an electric blanket.

EELV-N2 Method

EELV-N2 was determined twice via the technique available on the Engström CareStation ventilator, E-COVX, which is an automated procedure with an FIO2 step change of 0.1, as described previously by Olegård et al.13 Air flow was measured with a flow sensor (Pedi-lite+, GE Healthcare, Madison, Wisconsin) with an accuracy of 6% or 4 mL and a dead space of 2.5 mL. At each time point, EELV was taken as the mean of the the wash-out and wash-in values. The absence of a circuit leak was confirmed by a lack of an obvious reduction in airway pressure during a 10-second end-inspiration pause.

EELV-CT Method

At each PEEP level, whole-lung CT scans were performed during end-expiratory breath-holding (Somatom Sensation 64, Siemens, Forchheim, Germany), using a 512 × 512 matrix, 120 KV, 120 mAs, an exposure time of 0.33 second per rotation, a pitch of 1.2, and a collimation of 0.6 mm. The images were reconstructed with 5-mm slice thickness, using a body reconstruction filter (Siemens notation, B80f). The voxel volume ranged from 0.44 × 0.44 × 5 mm to 0.60 × 0.60 × 5 mm (0.97 – 1.8 mm3). The CT number characterizing each voxel was expressed in Hounsfield units (HU).

To analyze the images, commercially available software was used (Pulmo Option, Syngo, Siemens). All of the images were assessed at a window width of 1,600 HU and a window center of –600 HU, and only the lung parenchyma was selected as a region of interest, by excluding the chest wall, mediastinum, large vessels, and airways, by manual segmentation. The voxels of each CT slice were distributed into 10 compartments, ranging from –1,000 to 100 HU, with an interval of 100 HU. For each compartment of a known number of voxels, the lung, gas, and tissue volumes were calculated as follows1:

  • Lung volume = number of voxels × volume of the voxel

  • Gas volume = (mean CT/–1,000) × lung volume

where the volume of gas = 0 if the compartment considered had a CT number above 0, and

  • Tissue volume = lung volume – gas volume

The total volume of lung, gas (EELV-CT), and tissue was computed by summing the value of each volume of all slices. Different aerated lung regions were divided into 4 functional compartments, according to the following standard definition, based on HU23:

  • Non-aerated: 100 to –100 HU

  • Poorly aerated: −100 to –500 HU

  • Normally aerated: −500 to –900 HU

  • Hyperinflated −900 to –1,000 HU

Volumetric Capnography Analysis

Volumetric capnography was recorded using Ventrak 1550/Capnogard 1265 and Aplus Software (Novametrix, Wallingford, Connecticut). Air flow and airway opening pressure were measured using fixed-orifice differential pressure flow sensors (model 7222, Novametrix, Wallingford, Connecticut, with a dead space of 8 mL). CO2 was measured using an infrared mainstream sensor (Capnostat, Philips Respironics, Murrysville, Pennsylvania, with a response time < 75 ms, an accuracy of ± 5% at values between 41–100 mm Hg, and ± 2 mm Hg below 40 mm Hg, a resolution of 1 mm Hg, and a dead space of the airway adapter of 5 mL). All 3 sensors (including the Pedi-lite+) were placed at the airway opening. The sensors were calibrated according to the manufacturer's instructions.

Physiologic dead space was calculated using the Enghoff modification of the Bohr formula.24 Anatomical dead space was determined using the Fowler method.25 VD-alv was computed by subtracting the anatomical dead space from the physiologic dead space. VD-alv/VT-alv was then obtained by dividing VD-alv by VT-alv (VT-alv = VT – anatomical dead space). V̇CO2 (the CO2 volume exhaled per minute) and PETCO2 were measured with the ventilator.

Statistical Analysis

Data are presented as mean ± SD unless specified otherwise. The EELV-N2 and EELV-CT values were compared with the Bland-Altman technique,26 using a linear regression model. The data were divided into the higher and lower PEEP group according to PEEP above or below and equal to PEEP at the lowest VD-alv/VT-alv. The reason for the division was that VD-alv/VT-alv was useful for detecting lung collapse and for establishing open-lung PEEP in lavage-induced lung injury.27 The difference between the higher and lower PEEP groups was compared using the Student t test or Mann-Whitney U test. Statistical comparisons of the data over time were conducted using a repeated-measures analysis of variance, followed by Bonferroni correction for multiple comparisons. The correlations between 2 variables were determined by a linear regression analysis or a Spearman correlation analysis. Differences with P < .05 were considered statistically significant. Statistics software (SPSS 16.0, SPSS, Chicago, Illinois) was used.

Results

During the decremental PEEP process, EELV-N2 was strongly correlated with the EELV-CT (r2 = 0.86, P < .001). A Bland-Altman plot of the data revealed a bias of −48.6 ± 150.7 mL (1 ± 18%) (Fig. 1).

Fig. 1.
Fig. 1.

Comparison of end-expiratory lung volume (EELV) measured by the modified nitrogen wash-out/wash-in method (EELV-N2) and by computed tomography (CT) scan (EELV-CT) during the decremental PEEP protocol. A: EELV-N2 was correlated with EELV-CT (r2 = 0.86, P < .001). B: A Bland-Altman plot of the EELV-N2 levels and EELV-CT (average difference –48.6 ± 150.7 mL, limits of agreement –344.0 to 246.8 mL).

The lowest VD-alv/VT-alv value was at a PEEP of 13 ± 2 cm H2O. In the higher PEEP group, EELV-N2 was not correlated with the EELV-CT, with a bias of −168.1 ± 171.5 mL (−14 ± 14%) (Fig. 2). However, in the lower PEEP group, EELV-N2 maintained a high correlation (r2 = 0.86, P < .001) with EELV-CT, with a bias of 11.2 ± 97.2 mL (6 ± 17%) (Fig. 3).

Fig. 2.
Fig. 2.

Comparison of end-expiratory lung volume (EELV) measured by the modified nitrogen wash-out/wash-in method (EELV-N2) and by computed tomography (CT) scan (EELV-CT) in the higher PEEP group. A: EELV-N2 was not correlated with EELV-CT. B: A Bland-Altman plot of the EELV-N2 and EELV-CT (average difference –168.1 ± 171.5 mL, limits of agreement –504.2 to 168.0 mL).

Fig. 3.
Fig. 3.

Comparison of end-expiratory lung volume (EELV) measured by the modified nitrogen wash-out/wash-in method (EELV-N2) and computed tomography (CT) scan (EELV-CT) in the lower PEEP group. A: EELV-N2 was correlated with EELV-CT (r2 = 0.86, P < .001). B: A Bland-Altman plot of the EELV-N2 and EELV-CT (average difference 11.2 ± 97.2 mL, limits of agreement –179.4 to 201.8 mL).

The volumes of hyperinflated, normally, poorly and non-aerated lung regions and venous admixture were significantly different between the higher and lower PEEP groups. VD-alv, VD-alv/VT-alv, and PETCO2 did not differ between the 2 groups (Table 1). However, VD-alv was correlated with the hyperinflated lung region in the higher PEEP group (r2 = 0.47, P = .03), whereas VD-alv was correlated with venous admixture (Rho = 0.83, P < .001) and the non-aerated lung region (Rho = 0.81, P < .001) in the lower PEEP group. V̇CO2 was negatively correlated with VD-alv in the higher PEEP group (r2 = 0.42, P = .04), whereas V̇CO2 was negatively correlated with VD-alv (Rho = –0.81, P < .001) and venous admixture (Rho = –0.53, P = .02) in the lower PEEP group.

View this table:
Table 1.

Dead-Space Variables, Lung Morphology, and Venous Admixture in the Higher and Lower PEEP Groups

During the decremental PEEP process, EELV-N2 and EELV-CT values were progressively reduced. Compared with the PEEP levels ranging from 16 to 8 cm H2O, there was a decreasing trend in V̇CO2 and an increasing trend in VD-alv at PEEP of 20 cm H2O and 4 cm H2O. The measurement bias changed from the minor overestimation to systematic underestimation along with the increase of lung volume (Table 2). The measurement bias was negatively correlated with VD-alv (r2 = 0.44, P = .04), hyperinflated lung region (r2 = 0.72, P = .002), and carbon dioxide elimination (r2 = 0.47, P = .03) in the higher PEEP group (Fig. 4). These relationships were not observed in the lower PEEP group.

View this table:
Table 2.

EELV Measurement, Alveolar Dead Space, Carbon Dioxide Elimination, and Measurement Bias at Each PEEP Level

Fig. 4.
Fig. 4.

Correlations between measurement bias, alveolar dead space, hyperinflated lung region, and carbon dioxide elimination at high PEEP levels. A: Measurement bias was negatively correlated with alveolar dead space (r2 = 0.44, P = .04). B: Measurement bias was negatively correlated with hyperinflated lung region (r2 = 0.72, P = .002). C: Measurement bias was correlated with carbon dioxide elimination (r2 = 0.47, P = .03). Measurement bias = EELV-N2 – EELV-CT.

Mean arterial pressure, mean pulmonary arterial pressure, and cardiac output were stable during the decremental PEEP process. However, mean arterial pressure and cardiac output were decreased at PEEP of 20 cm H2O, although it did not reach statistical significance (Table 3).

View this table:
Table 3.

Hemodynamic Data at Each PEEP Level

Discussion

This study demonstrates that EELV can be accurately measured using the modified nitrogen wash-out/wash-in method in a swine model of acute lung injury, especially at low PEEP levels. However, an increase in VD-alv partly induces an underestimation of EELV at high PEEP levels.

The saline lavage model that was used in this study is characterized by increased VD-alv, which is clearly affected by PEEP.27 Thus, this model was suitable for our evaluation of the influence of VD-alv on EELV-N2 measurements. In general, the modified EELV-N2 method revealed an average lung volume underestimation of –48.6 ± 150.7 mL (1 ± 18%), compared with EELV-CT. The high variation in accuracy was due to the minor overestimation at low lung volumes and the obvious underestimation at high lung volumes. However, the accuracy of the modified method was as high as 1%, and the average measurement bias was only about 50 mL. In fact, the respiratory pattern of the small VT and high respiratory rate adopted in our study, which conformed to lung-protective ventilation in acute lung injury, was unfavorable to this method, due to a possible insufficient wash-out/wash-in time. Despite the aforementioned disadvantages, the modified EELV-N2 method provides acceptable accuracy for measuring EELV in acute lung injury.

As a multiple breath wash-out method, the volume that is measured by the modified EELV-N2 method is in fact “accessible pulmonary gas volume.”12 However, the difference between the traditional nitrogen wash-out/wash-in method28,29 and the modified method lies in how the volume of nitrogen is measured. In the modified method, nitrogen is not measured using a mass spectrometer technique, but is calculated by determining V̇O2 and V̇CO2. As a result, lung volume, as determined by the modified method, is not only accessible but also should take part in gas exchange. Previous studies showed that increased VD-alv caused by PEEP impaired V̇CO2 in both healthy and injured lungs,17–19 and this may have led to an underestimation of EELV by the modified method. Our results demonstrate that in the higher PEEP group, EELV-N2 is systemically lower than the EELV-CT and is no longer correlated with EELV-CT. The accuracy of the measurements was lowered to –14%. Thus, the underestimated measurement values at high PEEP levels merit attention. However, in the lower PEEP group, EELV-N2 maintained a significant linear relationship with EELV-CT, and the accuracy of the measurement was sufficient for clinic use. In fact, in previous studies that demonstrated a high accuracy of EELV measurements using the modified method, the PEEP level did not exceed 10 cm H2O.14–16

The CO2 elimination by the lung is influenced by cardiac output, effective alveolar surface area, and alveolar ventilation.17,30 Because of the mechanical heterogeneity of the acutely injured lung, VD-alv was significantly increased in the higher PEEP group, which was induced by hyperinflated lung region. Hence, the reduction of V̇CO2 at high PEEP levels was partially due to an increased VD-alv and hyperinflated lung region. Furthermore, the measurement bias was correlated with VD-alv, hyperinflated lung region, and V̇CO2 in the higher PEEP group. Thus, VD-alv played a role in the underestimation of EELV at high PEEP levels. In a recent study that assessed lung volume changes induced by PEEP in patients with ARDS, EELV was measured using the modified EELV-N2 method.7 Four of the 30 patients who were ventilated with the highest PEEP level used in the study (> 16 cm H2O) were excluded from the analysis due to a measurement error that the researchers attributed to a possible circuit leak. However, we propose another explanation for this error, namely, an increase in VD-alv that was caused by high PEEP.

There were significant differences between the higher and lower PEEP groups, including hyperinflated, normally, poorly and non-aerated lung regions. However, VD-alv and VD-alv/VT-alv did not differ between the 2 groups because the venous admixture had a substantial influence on the calculation of VD-alv, as VD-alv was calculated according to the Enghoff modification of the Bohr equation.31 Thus, VD-alv in the lower PEEP group was highly correlated with the venous admixture and was more suitably interpreted as “shunt dead space,”32 which is not a reflection of the true VD-alv (the ventilated alveoli without perfusion). Hence, the reduction in V̇CO2 was partially due to higher VD-alv caused by hyperinflated lung region at higher PEEP levels, and was primarily due to higher VD-alv caused by alveolar collapse and venous admixture at lower PEEP levels. Accordingly, EELV measured by the modified method was accurate at low PEEP levels but not valid at high PEEP levels. Thus, when VD-alv is calculated according to the Enghoff modification of the Bohr equation, the increased VD-alv has a differential effect on EELV measurements, with the modified EELV-N2 method between the higher and lower PEEP groups.

Limitations

There are several potential limitations to this study. First, the respiratory pattern of small VT and fast respiratory rate that we used may have lowered the measurement accuracy, as each wash-out/wash-in time may not have been sufficient. However, the respiratory pattern was not changed during the study protocol, and the underestimation of EELV was not found in the lower PEEP group. Accordingly, high respiratory rate is not the reason for the EELV measurement error at high PEEP levels. Second, the volume control mode that we used differed from partial ventilatory support, as variable VT during spontaneous breathing may lower the accuracy of the modified method. Third, the surfactant-depletion model that was used in this study may not adequately represent the complex set of conditions that exists in actual patients. Therefore, caution should be applied when interpreting our results. Fourth, the sample size was small, thereby limiting the power of the statistical analysis.

Conclusions

In this surfactant-depleted model, the modified EELV-N2 method can be used to measure EELV with acceptable accuracy, particularly at low PEEP levels. However, partly due to high VD-alv, EELV is underestimated at high PEEP levels. Thus, clinicians should be cautious of the potential EELV measurement errors at high PEEP levels.

Footnotes

  • Correspondence: Haibo Qiu MD PhD, Department of Critical Care Medicine, Zhong-Da Hospital, Southeast University School of Medicine, Nanjing 210009, China. E-mail: haiboq2000{at}yahoo.com.cn.

  • This study was funded by project of the National Key Clinical Specialty Construction (2100299) and Jiangsu Key Medical Discipline (889-KJXW11.3). The authors have disclosed no conflicts of interest.

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