J Appl Physiol 104: 224-229, 2008.
First published November 8, 2007; doi:10.1152/japplphysiol.00582.2007
8750-7587/08 $8.00
Single-breath test in lateral decubitus reflects function of single lungs grafted for interstitial lung disease
Alain Van Muylem,1
Pierre Alain Gevenois,2
Elizabeth Kallinger,3
Alexander A. Bankier,4
Christiane Knoop,1
Geert Verleden,5 and
Marc Estenne1
Departments of 1Chest Medicine and 2Radiology, Erasme University Hospital, Brussels, Belgium; the 3Department of Radiology, Medical University of Vienna, Vienna, Austria; 4Radiology, Beth Israel Deaconess Medical Center, Boston, Massachusetts; and 5Department of Chest Medicine, Gasthuisberg Hospital, Leuven, Belgium
Submitted 31 May 2007
; accepted in final form 29 October 2007
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ABSTRACT
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After single-lung transplantation (SLT) for emphysema, heterogeneity of ventilation distribution in the graft can be assessed by measuring the slope of the alveolar plateau, computed from a single-breath test, performed in lateral decubitus with this lung in the nondependent position. We tested the validity of this technique in patients with SLT for interstitial lung diseases (ILD). Twelve patients with SLT for ILD, 12 nontransplanted patients with ILD, and 10 healthy control subjects performed single-breath washouts in right and left lateral decubitus; nitrogen slope (SN2) and the difference between SF6 and He slopes (SSF6-SHe) were measured between 75 and 100% of expired volume. In 10 transplant recipients, the volume of each lung was measured in both postures by computerized tomography. Slopes were unaffected by posture in normal control subjects and patients with ILD. On the other hand, SN2 and SSF6-SHe in transplant recipients were smaller with the graft in the nondependent than in the dependent position (0.366 ± 0.445 vs. 1.035 ± 0.498 for SN2; 0.094 ± 0.201 vs. 0.218 ± 0.277 for SSF6-SHe). Values of SN2 and SSF6-SHe obtained in the former position were similar to those obtained in normal controls, while values obtained in the latter position were similar to those obtained in nontransplanted patients with ILD. Computerized tomography studies with the graft in the nondependent position indicated that this lung contributed 82% of the volume expired below functional residual capacity. We conclude that, in patients with SLT for ILD, the slope of the alveolar plateau obtained with the graft in the nondependent position reflects heterogeneity of ventilation distribution in this lung.
lung transplantation; pulmonary fibrosis; distribution of ventilation
PREVIOUS STUDIES AFTER BILATERAL or heart-lung transplantation have shown that the heterogeneity of ventilation distribution in the allograft is increased by infection (9) and by acute and chronic rejection (2, 5, 8–10, 12). For example, the slope of the alveolar plateau for nitrogen or helium obtained during a single-breath washout test increases in the early stages of bronchiolitis obliterans, which is considered a manifestation of chronic allograft rejection and is characterized by gradual obliteration of the small airways (3). Based on these studies, measuring the slope of the alveolar plateau has been advocated as a noninvasive tool for the early detection of this complication in recipients of bilateral grafts (2, 5, 10, 12).
When performed in the seated posture in patients with single-lung transplantation, the single-breath test cannot be used to assess the distribution of ventilation in the allograft, because both the native and the transplanted lungs contribute to the slope of the alveolar plateau. However, our laboratory recently showed in patients with single-lung transplantation for emphysema that this limitation can be overcome by performing the test in lateral decubitus (11). When the patient was in lateral decubitus with the graft in the nondependent position, this lung contributed all of the volume expired in the last part of the washout. Consequently, the slope of the alveolar plateau for nitrogen measured over this volume range reflected primarily the heterogeneity of ventilation distribution in the graft.
The predominant volume contribution of the graft resulted from the fact that, due to the combined effects of emphysema and gravity, expiratory flow from the native lung decreased markedly at low lung volumes, such that this lung stopped emptying before the graft. However, this effect of posture, and hence the information provided by measuring the slope of the alveolar plateau with the graft in the nondependent position, may be different in patients with single-lung transplantation for interstitial lung diseases (ILD) who have no airflow obstruction in the native lung. So, in these patients, the slope of the washout curve measured in lateral decubitus may be less effective in distinguishing the graft from the native lung and hence may not be a valid surrogate marker of ventilation distribution in the graft.
The aim of the present study was, therefore, to assess the effect of posture on the slope of the alveolar plateau in recipients of single grafts for ILD. We obtained single-breath washouts in right and left lateral decubitus in 12 transplant recipients, 10 normal controls, and 12 nontransplanted patients with ILD. In each posture, we computed the slope of the alveolar plateau for nitrogen and the difference between SF6 (SSF6) and He slopes (SHe). The great value of this index is that it provides an estimate of the heterogeneity of ventilation distribution within small lung areas and hence may reflect more specifically inhomogeneities arising in the graft. In addition to the washouts, we measured the volumes of the graft and the native lung at different levels over the vital capacity (VC) range using computerized tomography (CT) in 10 transplant recipients.
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METHODS
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Patients.
Twelve patients participated in the study after giving written informed consent to the protocol, as approved by the Human Studies Committee of the institution. Data obtained in the transplant recipients were compared with data obtained in 10 normal subjects and 12 nontransplanted patients with a variety of ILD. The group of healthy controls was the same as that used in our laboratory's previous study (11) and was matched for age and sex with the donors. At the time of studies, all transplant recipients were clinically stable and free of acute infection and rejection.
Single-breath washouts.
Single-breath tests were performed in right and left lateral decubitus. The subjects were connected to a double bag-in-box system through a non-rebreathing valve with a 20-ml instrumental dead space. They inhaled a gas mixture containing 90% O2, 5% He, and 5% SF6 from functional residual capacity (FRC) to 1 liter above FRC, and then expired at a constant flow of 
0.20 l/s to residual volume (RV) (7). To account for differences in dilution and expired volume in the two postures, gas concentration was expressed as a percentage of mean expired concentration (i.e., the surface area of the concentration vs. expired volume curve divided by total expired volume), and volume was expressed as a percentage of total expired volume (Fig. 1), yielding slope values that were without units. The slope of the alveolar plateau for N2, He, and SF6 was computed between 75 and 100% of the expired volume, and the difference between SF6 and He slopes (SSF6-SHe) was calculated. Single-breath tests were always performed in duplicate by the same investigator (A. Van Muylem), who was blinded to the side of transplantation, and slope values were calculated as the average of two measurements.
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Fig. 1. Representative washout curves obtained during a single-breath test performed in right (R) and left (L) lateral decubitus in 1 nontransplanted patient with interstitial lung disease (ILD; A), 1 single-lung transplant (Tx) recipient (B), and 1 control subject (C). In the Tx recipient, the graft was in the dependent position in the L lateral decubitus and in the nondependent position in the R lateral decubitus. The portion of the washout curve used to compute N2 slope (SN2) (between 75 and 100% of expired volume) is shown on each curve (continuous thick lines).
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CT scans.
Thin-section CT scans were performed in 10 patients on the same day as the single-breath tests. Scans were not obtained in the healthy control subjects and the nontransplanted patients with ILD, because the relative contributions of the dependent and nondependent lungs to the exhaled volume were not expected to be different in right vs. left lateral decubitus; we, therefore, considered it ethically unjustified to expose these subjects to radiation. Acquisitions were made with the patients in right and left lateral decubitus on a Sensation 64 scanner (Siemens, Medical Solution, Forchheim, Germany) using the multidetector spiral mode (5-mm slice thickness, acquisition 64 x 0.6 mm, pitch 1.4, 120 kV, 124 effective mAs, 0.37 s rotation time). Acquisitions were performed at total lung capacity (TLC), 1 liter above FRC, FRC, and RV; when the patient was on the side with the graft in the nondependent position, one additional acquisition was made between FRC and RV. To attain this volume and the volume corresponding to FRC + 1 liter, the patient was connected to a spirometer. At each volume, acquisitions were obtained from the lung apex to the lung base, and images were reconstructed every 5 mm. Lung volumes were measured using the 3dwk-L3LungCAD software (KMS Kallinger Medical Software, Vienna, Austria). This software automatically delineates the lung contours and segments lung parenchyma in each section. Lung volume was then calculated using values for lung area, section thickness, and contour interval.
Simulation.
A simulation was performed to assess the combined effects of heterogeneity of ventilation to volume ratios between the transplanted and native lungs (
V/V0, or specific ventilation) and changes in their relative contribution to the volume expired during the washout; because these variables are expected to be affected by posture, the simulation was done for the two postures used in the study. V/V0 was computed using CT data, which provided both V0 (the FRC of each lung) and V (the increase in the volume of each lung during the 1-liter inspiration from FRC). Values of V/V0 were used to compute N2 concentration in each lung at the end of the 1-liter inspiration. We also used CT data to calculate the contribution of each lung to the volume expired on going from 1 liter above FRC to RV. Values of N2 concentration and volume contribution were then used to compute a washout curve, and the slope of the last 25% of the curve was calculated. These simulations were done assuming that 1) ventilation was homogeneously distributed in each lung, and 2) changes in volume derived from CT data obtained in static conditions could be used to estimate the dynamic changes in volume occurring during the washout.
Statistics.
Comparisons were made using paired and unpaired t-tests and two-way ANOVA for repeated measurements, when appropriate. The level of statistical significance was taken as P < 0.05. Data are presented as means ± SD throughout the text, Table 3, and Figures 2–4, unless otherwise stated.
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Fig. 4. Top: average values (±SE) for the volumes of the native lung and the graft (Tx) measured by computerized tomography in 10 single-lung Tx recipients for ILD who were in lateral decubitus with the graft in the dependent position (Y-axis). Scans were obtained at total lung capacity (TLC), functional residual capacity (FRC) + 1 liter, FRC, and residual volume (RV). P values refer to differences between the volume of the Tx and native lungs. For the sake of clarity, error bars are not shown for total lung volume (X-axis); they are twice as great as those shown for individual lung volumes (Y-axis). Bottom: same as above but data obtained with the graft in the nondependent position are displayed (Y-axis). One additional acquisition was made between FRC and RV.
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RESULTS
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Patients.
All subjects performed the single-breath tests satisfactorily within 15 min. Details of the 12 transplant recipients studied are given in Table 1. Six patients had been transplanted for usual interstitial pneumonia, two for chronic extrinsic allergic alveolitis, one for scleroderma-related pulmonary fibrosis, one for chemotherapy-induced pulmonary fibrosis, one for sarcoidosis, and one for silicosis. There were 10 men and 2 women who were 55 ± 13 yr of age and had 8 left and 4 right transplants; the median time interval between transplantation and study was 461 days (range, 105–4,178). For the group as a whole, forced expiratory volume in 1 s (FEV1) averaged 71.7 ± 19.9% of predicted value and 92.7 ± 7.3% of best postoperative value; eight patients were in bronchiolitis obliterans syndrome (BOS) stage 0 (defined as FEV1 > 90% and mid-expiratory flow rate > 75% of best postoperative value), and four patients were in BOS stage 0-p (i.e., potential BOS, defined as FEV1 between 81 and 90%, and/or mid-expiratory flow rate 
75% of best postoperative value) (4). All patients had patent anastomoses and no malacia at endoscopy. The group of 12 nontransplanted patients with ILD included 4 men and 8 women, who were 61 ± 9 yr of age; VC and TLC averaged 56 ± 19% and 55 ± 12% of predicted, respectively (Table 2). One patient had chronic hypersensitivity pneumonitis, one patient had sarcoidosis, two patients had nonspecific interstitial pneumonia, and five patients had usual interstitial pneumonia. ILD was chemotherapy induced in one patient and related to collagen vascular diseases in two patients. The group of healthy controls consisted of five men and five women who were 37.4 ± 14.3 yr of age.
N2 single-breath washouts.
Figure 1 shows typical single-breath washout curves obtained in right and left lateral decubitus in a nontransplanted patient with ILD (patient 7), a patient with a left transplant (patient 2), and a control subject. As expected, the two washout curves were superimposed in the nontransplanted patient and the control subject. On the other hand, in the transplant recipient, SN2 measured between 75 and 100% of the expired volume was much steeper when the test was performed with the graft in the dependent than in the nondependent position. Figure 2 shows individual values for SN2 in the three groups. Values found with the graft in the dependent position (1.035 ± 0.498) were similar to those found in the patients with ILD (0.749 ± 0.285). In contrast, they were significantly greater than those found in the transplanted patients with the graft in the nondependent position (0.366 ± 0.445) and in the control subjects (0.205 ± 0.198). Values found in these two groups were not significantly different.
SSF6-He single-breath washouts.
Figure 3 shows individual values for SSF6-SHe in the three groups. Values found with the graft in the dependent position (0.218 ± 0.277) and in the patients with ILD (0.160 ± 0.136) were not significantly different; in contrast, they were significantly greater than those found with the graft in the nondependent position (0.094 ± 0.201) and in the control subjects (0.002 ± 0.038). Values of SSF6-SHe found with the graft in the nondependent position and in the normal controls were not significantly different.
Figures 2 and 3 show that patient 9 was an outlier. In contrast to the other patients, he showed a greater SN2 with the graft in the nondependent than in dependent position; in addition, SN2 and SSF6-SHe in the nondependent position were much greater in this patient than in others. At the time of study, patient 9 had no clinical sign suggesting acute infection or rejection, and his inspiratory and expiratory CT scans did not show any parenchymal abnormality other than fibrosis in the native lung. Although he was in BOS 0-p, he had stable spirometric values, and, as of September 2007 (19 mo after data collection), he had not progressed to BOS 1 or greater. There was no difference in SN2 and SSF6-SHe between the eight patients who were in BOS stage 0 and the four patients who were in BOS stage 0-p.
CT scans.
Table 3 and Fig. 4 summarize results of the CT studies in the 10 transplant recipients. Figure 4 shows that, in both postures, the volume of the native lung tended to be smaller than that of the graft; the difference was significant at all volumes, except FRC and RV with the graft in the dependent position (Fig. 4A). The volume of the graft was significantly greater in the nondependent than in the dependent position at FRC + 1 liter (P < 0.015) and FRC (P < 0.001), and a similar difference was observed for the native lung at FRC (P = 0.009) and RV (P < 0.028); however, the effect of posture on lung volume was quantitatively larger for the graft than for the native lung. Figure 4 also shows that, in each posture, the volume of both lungs decreased progressively on going from TLC to RV (P < 0.001), with this change being much greater for the graft than for the native lung. With the graft in the dependent position, VC averaged 0.74 ± 0.44 liter for the native lung and 2.01 ± 0.52 liters for the graft (P < 0.001); with the graft in the nondependent position, corresponding values were 0.75 ± 0.47 and 2.03 ± 0.50 liters, respectively (P < 0.001).
With the graft in the dependent position (Fig. 4A), the volume change between FRC and RV (which corresponded to the last 25% of expired volume used to compute SN2 in this position) was not significantly different for the two lungs (0.30 ± 0.14 liter for the native lung and 0.21 ± 0.06 liter for the graft; P = 0.16) (Table 3). On the other hand, with the graft in the nondependent position, the volume expired between the level corresponding roughly to the middle of the expiratory reserve volume and RV (which corresponded to the last 25% of expired volume used to compute SN2 in this position) was much greater (P < 0.001) for the graft (0.54 ± 0.09) than for the native lung (0.08 ± 0.06) (Table 3).
Simulation.
When the graft was dependent, N2 concentrations at the end of the 1-liter inspiration were 46% in the graft and 62% in the native lung; with the graft nondependent, corresponding values were 59 and 57%, respectively. The slope of the terminal portion of SN2 was 0.098 with the graft in the dependent position and 0.006 with the graft in the nondependent position. These values were thus much smaller than those found in the transplanted patients (see above). This suggests that, whatever the posture studied, only a small fraction of SN2 could be accounted for by the combined effects of heterogeneity of ventilation-to-volume ratios between the transplanted and native lungs and changes in their relative contribution to the expired volume.
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DISCUSSION
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Monitoring the function of the graft in patients with single-lung transplantation for ILD may be clinically relevant, as unilateral grafting is the most frequent procedure performed for this disease category. The Registry of the International Society for Heart and Lung Transplantation indicates that 65% of the 2,992 procedures performed between 1995 and 2005 were unilateral (6). In this study, we investigated a group of patients who had been operated on for a variety of ILD, were clinically stable, and had spirometric values comparable to those reported in previous studies (e.g., a FEV1 of 70% predicted) (1). They were compared with a group of nontransplanted patients with a similar variety of ILD and to a group of healthy controls matched with the donors.
The study demonstrates that, in all but one transplanted patient, the terminal portion of SN2 decreased when the graft was shifted from the dependent to the nondependent position. In the former, values of SN2 were similar to those obtained in the nontransplanted patients with ILD, whereas, in the latter, they were similar to those obtained in the normal controls. This effect of posture was observed irrespective of the time elapsed since surgery, the side of the transplant, and the type of ILD affecting the native lung. In addition, it was qualitatively similar to that seen in patients with single-lung transplantation for emphysema. So, despite a totally different physiology, patients with single-lung transplantation for ILD and emphysema (11) showed a decrease in SN2 when the graft is shifted from the dependent to the nondependent position.
The slope of the alveolar plateau is influenced by both convection-dependent interregional inhomogeneities (i.e., inhomogeneities between lungs, or between regions located in one lung) and diffusion-dependent intraregional inhomogeneities (i.e., inhomogeneities arising in one lung region). So, the decrease in SN2 observed when the graft was shifted from the dependent to the nondependent position might be accounted for by two distinct mechanisms. First, it may reflect the effect of convection-dependent inhomogeneities between lungs. As expiration proceeded, the relative contribution of the graft to the volume expired progressively decreased when this lung was dependent, but it progressively increased when the graft was nondependent (Fig. 4 and Table 3). This difference, and the fact that the graft and the native lung had different V/V0 in the two postures (and hence different N2 concentrations), might explain the effect of posture on SN2. When the graft was dependent, a greater proportion of the volume exhaled in the last part of the washout came from the native lung, which had a higher N2 concentration, and the converse was true when the graft was nondependent.
To assess the potential contribution of this mechanism, we used CT data obtained in each posture to compute the V/V0 of the transplanted and native lungs and their relative contribution to the expired volume. The washout curves simulated with these data (assuming that ventilation was homogeneously distributed in each lung) had a positive slope in both postures, and the slope was smaller with the graft in the nondependent than in the dependent position. This is qualitatively similar to the effect of posture observed in the patients, but the slopes generated by the simulation were at least one order of magnitude smaller than those seen in the patients, which suggests that the impact of this mechanism on SN2 is likely to be small.
Alternatively, the smaller SN2 found with the graft in the nondependent position may indicate that the terminal portion of the slope in this posture reflected primarily the heterogeneity of ventilation distribution in the graft (i.e., the effect of posture would reflect differences in intralung inhomogeneities between the graft and the native lung). The graft, which is expected to have more homogeneous distribution of ventilation than the native lung, indeed contributed most of the volume exhaled in the last part of expiration (Fig. 4 and Table 3). To investigate this mechanism, we analyzed the difference between SSF6 and SHe. The great value of SSF6-SHe is that it provides an estimate of the heterogeneity of ventilation distribution within small lung areas where molecular diffusion becomes preponderant. Because SSF6 and SHe are similarly affected by convection-dependent inhomogeneities between large lung regions (located in one lung or in two lungs), this component is canceled when SSF6-SHe is computed (7, 8). The response of SSF6-SHe to changes in posture was qualitatively similar to that of SN2: both indexes were smaller with the graft in the nondependent than in the dependent position, and both had values close to those of healthy subjects in the former position. This observation, together with the results of the simulation, strongly suggests that 1) the terminal portion SN2 measured in lateral decubitus included a component generated by intralung inhomogeneities, and 2) SN2 was smaller when measured with the graft in the nondependent position, because it reflected, at least in part, the more homogeneous distribution of ventilation in this lung.
Consistent with this analysis, the increase in SN2 that may occur as BOS develops may be due to either a progressive increase in the contribution of the native lung to the volume expired toward the end the washout (for example, due to an increase in the closing volume of the graft), and/or to an increase in the heterogeneity of ventilation distribution in the graft. It should be emphasized, however, that this cross-sectional study did not validate the measurement of SN2 in lateral decubitus as a surrogate biomarker of BOS in patients with single-lung transplantation for ILD. Longitudinal studies in these patients are now needed to specifically assess this question and establish that, as in recipients of bilateral grafts (2, 5, 10, 12), this measurement is useful for the early detection of BOS.
The present study has several limitations. First, the severity of the disease affecting the lungs in the nontransplanted patients was not matched with the severity of the disease affecting the native lung in the transplanted patients. This matching was not possible because there is no means to assess specifically the function of the native lung. We, therefore, decided to include patients with a degree of ventilatory impairment comparable to that usually seen in patients with ILD awaiting lung transplantation (VC and TLC 55% of predicted) (1). Second, we have no definite explanation for the different response of SN2 to postural changes observed in patient 9, who showed an increase in slope when the graft was shifted from the dependent to the nondependent position. The fact that both SN2 and SSF6-SHe measured in the latter were greater in this patient than in the others is consistent with an altered distribution of ventilation in the graft. The patient only showed a modest alteration in lung function, corresponding to the BOS 0-p stage, but changes in slope very often precede changes in spirometry (2, 5, 10, 12). It should be stressed, however, that the three other patients who were in BOS 0-p responded to postural changes in the same way as patients who were in BOS 0.
In conclusion, the present studies showed that, in patients with single-lung transplantation for ILD, the function of the graft may be assessed by measuring the slope of the terminal portion of the single-breath washout obtained with this lung in the nondependent position.
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GRANTS
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This work was supported in part by a grant (1.5050.02F) from the Fonds National de la Recherche Scientifique (Belgium).
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FOOTNOTES
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Address for reprint requests and other correspondence: M. Estenne, Chest Service, Erasme Univ. Hospital, 808, Route de Lennik, B-1070 Brussels, Belgium (e-mail: mestenne{at}ulb.ac.be)
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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REFERENCES
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- Van Muylem A, Antoine M, Yernault JC, Paiva M, Estenne M. Inert gas single-breath washout after heart-lung transplantation. Am J Respir Crit Care Med 152: 947–952, 1995.[Abstract]
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Copyright © 2008 by the American Physiological Society.
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ABSTRACT
METHODS
), 12 single-lung Tx recipients for ILD (
and 
for patient 9), and 10 healthy control subjects (
). In the Tx recipients, each point is the mean of 2 consecutive measurements obtained in lateral decubitus with the graft in the dependent (Tx dep) and nondependent (Tx non-dep) position. In the control subjects and the patients with ILD, each point is the mean of 2 measurements obtained in the R and L lateral decubitus (data were unaffected by posture). Because N2 concentration was expressed as a percentage of mean expired concentration and volume was expressed as a percentage of total expired volume, values for SN2 are without units. Means ± SD are shown for each group.