Journal of Applied Physiology AJP: Lung Cellular and Molecular Physiology
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J Appl Physiol 100: 834-838, 2006. First published November 23, 2005; doi:10.1152/japplphysiol.01307.2005
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Single-breath test in lateral decubitus reflects function of single lungs grafted for emphysema

Alain Van Muylem,1 Pietro Scillia,2 Christiane Knoop,1 Manuel Paiva,3 and Marc Estenne1

Departments of 1Chest Medicine and 2Radiology, Erasme University Hospital, and 3Biomedical Physics Laboratory, Université Libre de Bruxelles, Brussels, Belgium

Submitted 12 October 2005 ; accepted in final form 23 November 2005


   ABSTRACT
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METHODS
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The slope of alveolar plateau for nitrogen derived from the single-breath test is useful to assess the function of bilateral lung grafts, but this technique is not applicable to patients with single-lung grafts due to the confounding influence of the native lung. We tested the hypothesis that the nitrogen slope measured in lateral decubitus with the graft in nondependent position may primarily reflect the distribution of ventilation in this lung. Fifteen patients with single-lung transplantation for emphysema, 10 healthy controls, and 7 patients with advanced emphysema performed single-breath washouts in right and left lateral decubitus; nitrogen slope was measured between 75 and 100% of expired volume. In 10 transplant recipients, the volume of each lung was measured in the two postures by computerized tomography. Nitrogen slope was unaffected by posture in normal controls and emphysema patients. On the other hand, nitrogen slope in transplant recipients was invariably smaller, with the graft in nondependent vs. in dependent position. Values of nitrogen slope with the graft in nondependent position were similar to those obtained in normal controls but significantly smaller than those obtained in emphysema patients. Computerized tomography studies in this position indicated that the volume expired below functional residual capacity was exclusively contributed by the graft. We conclude that, in patients with single-lung transplantation for emphysema, 1) measuring nitrogen slope in lateral decubitus allows to distinguish between the graft and the native lung, and 2) nitrogen slope obtained with the graft in nondependent position reflects ventilation distribution in this lung.

lung transplantation; ventilation distribution; bronchiolitis obliterans

PREVIOUS STUDIES HAVE SHOWN that indexes of ventilation distribution, e.g., the slope of the alveolar plateau for nitrogen or helium obtained during a single-breath washout test, may be useful for the detection of allograft dysfunction after bilateral or heart-lung transplantation (7, 21, 25, 26). This technique, however, cannot be applied to patients with single-lung transplantation due to the confounding influence of the native lung. We reasoned that this limitation could be overcome by performing the washout test in lateral decubitus with the graft in nondependent position. In an early study that used single-breath washouts in lateral decubitus, Anthonisen et al. (1) showed that, as lung volume decreased, the nondependent lung contributed an increasing fraction of the expired volume, whereas the fraction contributed by the dependent lung decreased. This phenomenon may be amplified when the dependent lung is emphysematous, due to the marked reduction in expiratory flow at low lung volumes.

On this basis, we hypothesized that, in patients undergoing single-lung transplantation for emphysema, the terminal portion of the nitrogen slope obtained in lateral decubitus with the graft in nondependent position could reflect primarily the distribution of ventilation in this lung. To test this hypothesis, we performed a feasibility study in which single-breath washout tests were obtained in right and left lateral decubitus in 15 patients with single-lung transplantation for emphysema, 10 normal controls, and 7 patients with advanced emphysema. In addition, we measured the volumes of the graft and the native lung at different levels over the vital capacity range using computerized tomography (CT) in 10 transplant recipients. Some of the results of these studies have been previously reported in abstract form (27).


   METHODS
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Patients.   Between January 1990 and the end of the study in July 2005, 28 single-lung transplantations for emphysema were performed at our institution. Nine patients were alive at the start of the study in January 2004, and seven patients were transplanted during the study period. One patient who had undergone an upper lobe lobectomy of the native lung for posttransplant lymphoma and was not in a clinically stable state was excluded. Fifteen patients thus participated in the study after written informed consent to the protocol was received, which was approved by the Human Studies Committee of the institution. Data obtained in the transplant recipients were compared with data obtained in 10 normal subjects matched for age and sex with the donors and 7 patients with advanced emphysema. At the time of studies, all transplant recipients were clinically stable and free of acute infection and rejection.

Techniques.   Single-breath tests were performed in right and then in left lateral decubitus. The subjects were connected to a double bag-in-box system through a nonrebreathing valve with a 20-ml instrumental dead space. They inhaled a gas mixture containing 100% O2 from functional residual capacity (FRC) to 1 liter above FRC and then expired at a constant flow of ~0.20 l/s (24). To account for differences in dilution and expired volume in the two postures, N2 concentration was expressed as a percentage of mean expired concentration, and volume was expressed as a percentage of total expired volume (Fig. 1), yielding slope values that are without units. The slope of the alveolar plateau was calculated over two different volume ranges by a linear regression analysis performed between 50 and 75% and between 75 and 100% of the expired volume. Single-breath tests were always performed in duplicate by the same investigator who was blinded to the side of the transplantation, and slope values were calculated as the average of two measurements.


Figure 1
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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 patient with emphysema (A), 1 single-lung transplant (Tx) recipient (B), and 1 control subject (C). In the transplant recipient, graft was in dependent position in left lateral decubitus (L) and in nondependent position in right lateral decubitus (R). In each panel, thick lines indicate the portion of the washout curve that was used to compute the slope of the alveolar plateau for N2 (SN2) (between 75 and 100% of expired volume).

 
Thin-section CT scans were performed in 10 patients on the same day as the single-breath tests. 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 mA·s, 0.37 -s rotation time). Acquisitions were performed from the lung apex to the lung base at total lung capacity (TLC), at 1 liter above FRC, at FRC, and at residual volume (RV); when the patient was on the side with the graft in 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. The Pulmo CT option from Siemens (14) was used to trace the lung contours on each scan and measure lung area; lung volume was then calculated using values of lung area and slice interval (6).

Comparisons were made using paired and unpaired t-tests, and two-way ANOVAs for repeated measurements, when appropriate. The level of statistical significance was taken as P < 0.05. Data are presented as means ± SD throughout, unless otherwise stated.


   RESULTS
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All subjects performed the single-breath tests satisfactorily, within ~15 min. Details of the 15 transplant recipients studied are given in Table 1. There were eight men and seven women with eight right and seven left transplants; the median time interval between transplantation and study was 710 days (range of 107–4,706 days). For the group as a whole, the forced expiratory volume in 1 s (FEV1) averaged 58.5 ± 9.6% of predicted and 87.2 ± 11.4% of the best postoperative value; 12 patients were in bronchiolitis obliterans syndrome (BOS) stage 0 (FEV1 between 100 and 81% of the best postoperative value), and 3 patients (patients 2, 5, 10) were in BOS stage 1 (FEV1 between 80 and 66% of the best postoperative value) (8, 9). One patient (patient 7) who had a malacia treated by a stent placed in the middle and lower bronchus on the side of the transplant could not be classified using the BOS scoring system (9). The other patients had patent anastomoses and no malacia at endoscopy. The group of healthy controls consisted of five men and five women who were 37.4 ± 14.3 y of age; the group of emphysema patients included four men and three women who were 55 ± 8 y of age and had a mean FEV1 of 19.8 ± 4.3% of predicted.


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  		Table 1. Characteristics of study population

 
Figure 1 shows typical single-breath washout curves obtained in right and left lateral decubitus in a patient with emphysema, a patient with a left transplant, and a control subject. As expected, the two washout curves were superimposed in the emphysema patient and the control subject. On the other hand, in the transplant recipient, the slope of the alveolar plateau for N2 (SN2) measured between 75 and 100% of the expired volume was much steeper when the test was performed with the graft in dependent vs. in nondependent position. Figure 2 shows that this difference was observed in all of the subjects studied. The values found with the graft in dependent position (0.67 ± 0.26) were similar to those found in the emphysema patients (0.55 ± 0.24; P = 0.36), but they were significantly greater than those found with the graft in nondependent position (0.10 ± 0.25; P < 0.001) and in the control subjects (0.21 ± 0.20; P < 0.001). The values found with the graft in nondependent position and in the normal controls were similar (P = 0.29). There was no difference in SN2 between the 12 patients in BOS stage 0 and the 3 patients in BOS stage 1.


Figure 2
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  		Fig. 2. Individual values for SN2 measured between 75 and 100% of the expired volume in 7 emphysema patients ({triangleup}), 15 single-lung transplant recipients for emphysema (bullet), and 10 healthy controls ({circ}). In the transplant recipients, each point is the mean of 2 consecutive measurements obtained in lateral decubitus with the graft in dependent (Tx dep) and nondependent (Tx non-dep) position. In the control subjects and the emphysema patients, each point is the mean of 2 measurements obtained in right and in left 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. Values for each group are means ± SD.

 
When the graft was in dependent position, values of SN2 measured between 50 and 75% and between 75 and 100% of the expired volume were similar (0.67 ± 0.26 between 50 and 75% vs. 0.62 ± 0.51 between 75 and 100%; P = 0.67); on the other hand, when the graft was in nondependent position, values measured between 50 and 75% (0.34 ± 0.30) were significantly greater than those measured between 75 and 100% (0.10 ± 0.25) (P < 0.003).

Table 2 and Fig. 3 summarize results of the CT studies in the 10 transplant recipients. Figure 3A shows that, when the graft was in dependent position, the volume of this lung was 30–50% smaller than that of the native lung (P < 0.001) and that both lungs showed a progressive decrease in volume on going from TLC to RV (P < 0.001). Although the change in volume between FRC + 1 liter and RV tended to be greater for the graft than for the native lung (0.89 ± 0.15 liter and 0.65 ± 0.25 liter, respectively), the difference did not reach statistical significance; the expiratory reserve volume was almost identical for the two lungs (0.22 ± 0.22 liter for the native lung and 0.24 ± 0.13 liter for the graft). As expected, changing the patient to the side with the graft in nondependent position (Fig. 3B) made invariably the volume of this lung larger and the volume of the native lung smaller (P < 0.001), except at RV where there was no difference in graft volume between the two postures. The difference in the volume of the two lungs was smaller with the graft in nondependent than in dependent position, but it was still statistically significant (P < 0.02 to 0.001). Figure 3B shows that, when the graft was in nondependent position, its volume decreased progressively when going from TLC to RV (P < 0.001). On the other hand, the volume of the native lung decreased between TLC and FRC (P < 0.001) but remained unchanged between FRC and RV; four patients showed a decrease in volume between FRC and RV (mean –0.13 liter), one patient showed no change, and five patients showed a paradoxical increase (mean 0.17 liter). As a result, the change in volume between FRC + 1 liter and RV was much greater for the graft (1.29 ± 0.16 liter) than for the native lung (0.38 ± 0.28 liter) (P < 0.001); similarly, the expiratory reserve volume averaged 0.75 ± 0.16 liter for the graft vs. –0.04 ± 0.16 liter for the native lung (P < 0.001) (Table 2).


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  		Table 2. Contributions of graft and native lung to expired volume

 

Figure 3
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  		Fig. 3. A: average values (±SE) for the volumes of the native lung and the graft (Tx) measured by computerized tomography in 10 single-lung transplant recipients for emphysema who were in lateral decubitus with the graft in dependent position. The 4 volumes measured correspond to total lung capacity, functional residual capacity (FRC) + 1 liter, FRC, and residual volume. For the sake of clarity, error bars are not shown (x-axis) when they are twice as great as those shown for individual lung volumes (y-axis). B: same as above, but data were obtained with the graft in nondependent position. One additional acquisition was made between FRC and residual volume.

 

   DISCUSSION
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
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Shortly after the introduction of lung transplantation in clinical practice in the early 1980s, it was recognized that pulmonary function is sensitive to complications affecting the allograft. Several studies reported that both acute infection and rejection can produce an obstructive ventilatory defect (12, 13, 19, 25, 26), and progressive airflow obstruction was identified as the functional hallmark of bronchiolitis obliterans, which is considered a manifestation of chronic allograft rejection (8, 9). Yet, the sensitivity and specificity of spirometry for the detection of allograft dysfunction are lower in patients with unilateral than bilateral grafts due to the confounding influence of the native lung (2, 16, 18).

Several imaging techniques have been proposed to overcome this problem and assess specifically the function of single grafts, including krypton-81m ventilation and/or technetium-99m perfusion scintigraphy (11, 20), single-photon-emission computerized tomography (4, 22, 23), thallium-201 scintigraphy (15), contrast-enhanced dynamic magnetic resonance imaging (3), and, more recently, helium-3 magnetic resonance imaging (10, 28). However, the complex and/or expensive nature of these techniques makes them ill-suited for wide clinical use.

Our group (7, 25, 26) and others (21) have previously demonstrated that the single-breath test, which is cheap, noninvasive, and easy to perform, may contribute to the detection of allograft dysfunction and in particular of BOS (8, 9) in recipients of heart-lung and bilateral lung transplantation. In the present study, we have expanded the use of this test to recipients of single-lung transplants for emphysema and have shown that the slope of the terminal portion of the alveolar plateau measured with the graft in nondependent position primarily reflects the distribution of ventilation in this lung.

Critique of methods.   A key issue in the interpretation of the present findings is whether the volume expired in the last part of the washout originated primarily, or even exclusively, from the graft. We attempted to address this question using CT studies, which showed that, when the graft was in nondependent position and the native lung was in dependent position, the former had a significant expiratory reserve volume, whereas the latter had either a very small expiratory reserve volume or even showed a paradoxical increase in volume on going from FRC to RV (attributable to a "pendelluft" phenomenon). In addition, we performed a complementary analysis in which we compared values of SN2 measured between 50 and 75% of the expired volume with those measured between 75 and 100% of the expired volume. When the graft was in dependent position, values measured over the two volume ranges were similar; however, when the graft was in nondependent position, values measured between 50 and 75% were significantly greater than those measured between 75 and 100% (P < 0.003). These findings are thus consistent with the CT data: SN2 values obtained with the graft in dependent position did not change over the last 50% of expiration because the two lungs contributed to the expired volume; in contrast, SN2 values obtained with the graft in nondependent position decreased in the last part of expiration due to the progressive reduction in the volume contributed by the native lung (Table 2, last row, and Fig. 3).

Because the current technology does not allow to measure dynamic changes in volume (5), the volumes of each lung were measured in static conditions at four or five different levels over the vital capacity range, rather than during a continuous expiration similar to the one used during the washout test. It should be stressed, however, that this expiration was performed at very low flow rates, which could be considered as approximating quasi-static conditions. In theory, the static conditions used for the CT acquisitions may increase the magnitude of the pendelluft phenomenon between the graft and the native lung. By decreasing the volume of the former and increasing the volume of the latter, this phenomenon could make the volumes of the two lungs (as assessed by CT) more different from those in dynamic conditions. This difference might translate into an overestimation of the vertical distance between the curves shown in Fig. 3, A and B, but it is not expected to change the slope of these curves, that is, the relative contribution of each lung to the expired volume (Table 2).

Present studies.   SN2 values measured between 75 and 100% of the expired volume in the transplant recipients with the graft in dependent position were greater than those found in the normal controls, indicating a more heterogeneous distribution of ventilation. In contrast, these values were similar to those found in the emphysema patients, which suggests that they reflected the very heterogeneous ventilation of the emphysematous native lung. This is supported by the CT studies, which showed that this lung contributed to the expiratory reserve volume when it was in nondependent position. A key observation of this study was that shifting the patient to the side with the graft in nondependent position significantly decreased SN2. This finding was observed in each patient, irrespective of the side of the transplant and of the time elapsed since surgery (which varied widely from 3.5 mo to more than 12 yr). We suggest that this effect of posture was related to the preferential emptying of the graft at low lung volumes when it was in nondependent position. The best explanation to account for both the normal SN2 values (Fig. 2) and the CT data (Fig. 3) obtained in this position is that the native lung contributed only a small fraction (if any) and that the graft contributed most (if not all) of the volume expired in the last 25% of the expired volume, which corresponded to the volume range where SN2 was measured. Therefore, when the graft was in nondependent position, SN2 measured between 75 and 100% of the expired volume likely reflected primarily the distribution of ventilation in this lung.

Values of SN2 in the three patients who were in BOS stage 1 were in the same range as those measured in the patients who were in BOS stage 0. It is possible that the slope of the alveolar plateau for helium, which is a better predictor of BOS than SN2 in patients with bilateral grafts (7), would have been increased in these three patients. Alternatively, the decline in lung function seen in these patients might be due to hyperinflation of the native lung (17) or to another cause unrelated to obliteration of the small airways (the diagnosis of bronchiolitis obliterans was not confirmed by histology); otherwise stated, the normal SN2 in the three patients might be explained by the fact that the decline in lung function was due to complications that did not make ventilation distribution more heterogeneous in the graft.

In conclusion, the present studies showed that, in patients with single-lung transplantation for emphysema, 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 nondependent position. Further studies are now required to 1) investigate whether this test can be applied to patients with native lung diseases other than emphysema and 2) assess the sensitivity and specificity of this test as a predictor of BOS.


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 ABSTRACT
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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).


   FOOTNOTES
 

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.


   REFERENCES
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