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(Chest. 2007;131:122-129.)
© 2007 American College of Chest Physicians

Lung Aeration During Sleep*

Jonas Appelberg, PhD; Tatjana Pavlenko, PhD; Henrik Bergman, MD; Hans Ulrich Rothen, MD, PhD and Göran Hedenstierna, MD, PhD

* From the Department of Clinical Physiology (Dr. Appelberg), Sundsvall Hospital, Sundsvall, Sweden; Department of Medical Sciences (Dr. Hedenstierna), Clinical Physiology, University Hospital, Uppsala, Sweden; Research and Development Centre (Dr. Pavlenko), Västernorrland County Council, Sundsvall, Sweden; Department of Radiology (Dr. Bergman), Sundsvall Hospital, Sundsvall, Sweden; and Department of Anaesthesia (Dr. Rothen), University Hospital, Bern, Switzerland.

Correspondence to: Göran Hedenstierna, MD, PhD, Department of Medical Sciences, Clinical Physiology, University Hospital, SE-751 85, Uppsala, Sweden; e-mail goran.hedenstierna{at}medsci.uu.se

Abstract

Background: During sleep, ventilation and functional residual capacity (FRC) decrease slightly. This study addresses regional lung aeration during wakefulness and sleep.

Methods: Ten healthy subjects underwent spirometry awake and with polysomnography, including pulse oximetry, and also CT when awake and during sleep. Lung aeration in different lung regions was analyzed. Another three subjects were studied awake to develop a protocol for dynamic CT scanning during breathing.

Results: Aeration in the dorsal, dependent lung region decreased from a mean of 1.14 ± 0.34 mL (± SD) of gas per gram of lung tissue during wakefulness to 1.04 ± 0.29 mL/g during non-rapid eye movement (NREM) sleep (– 9%) [p = 0.034]. In contrast, aeration increased in the most ventral, nondependent lung region, from 3.52 ± 0.77 to 3.73 ± 0.83 mL/g (+ 6%) [p = 0.007]. In one subject studied during rapid eye movement (REM) sleep, aeration decreased from 0.84 to 0.65 mL/g (– 23%). The fall in dorsal lung aeration during sleep correlated to awake FRC (R2 = 0.60; p = 0.008). Airway closure, measured awake, occurred near and sometimes above the FRC level. Ventilation tended to be larger in dependent, dorsal lung regions, both awake and during sleep (upper region vs lower region, 3.8% vs 4.9% awake, p = 0.16, and 4.5% vs 5.5% asleep, p = 0.09, respectively).

Conclusions: Aeration is reduced in dependent lung regions and increased in ventral regions during NREM and REM sleep. Ventilation was more uniformly distributed between upper and lower lung regions than has previously been reported in awake, upright subjects. Reduced respiratory muscle tone and airway closure are likely causative factors.

Key Words: airway closure • anesthesia • CT • lung aeration • lung volume • sleep • ventilation

Sleep is accompanied by a reduction in minute ventilation1 and in functional residual capacity (FRC).23 The reduction in FRC is approximately 7% during non-rapid eye movement (NREM) sleep and a little larger during rapid eye movement (REM) sleep.2

Several factors, such as central pooling of blood, a decrease in lung compliance, and a reduction of respiratory muscle tone, have been suggested as potential causes of the FRC reduction.234 The decrease in FRC could lead to closure of peripheral airways and impeded oxygenation of blood. A decrease in arterial oxygenation has been reported in healthy subjects during REM sleep,56 when muscle tone is most reduced. Previous studies23 on respiration during sleep, using different spirometric methods, have indicated that airway closure may occur in dependent lung regions during sleep, especially during REM sleep. However, the questions of whether aeration is impaired in dependent lung regions during sleep and whether the distribution of ventilation is altered have not been analyzed previously. The purpose of this study was to investigate the regional aeration of the lung during sleep in healthy subjects. To allow both regional analysis and measurements during the respiratory cycle, a technique based on spiral CT was developed.

Methods and Materials

Subjects
Ten healthy, nonsmoking subjects (7 men and 3 women; mean age, 34 ± 10 years [± SD]) were investigated awake and during sleep. Three additional men (mean age, 38 ± 16 years) were studied awake in order to develop the CT scan protocol. Informed consent was obtained from all subjects, and the regional ethics committee approved the study protocol in advance.

Spirometry and Airway Closure
Pulmonary function tests were performed in the afternoon with the subjects awake (Vmax 229; SensorMedics; Yorba Linda, CA). Spirometry was performed in the sitting position with measurements of vital capacity and FEV1. Values were calculated as percentage of predicted.7 Measurements of FRC, expiratory reserve volume (ERV), and airway closure, expressed as closing volume (CV), were performed with the subject lying on a bed in the supine position. FRC was determined by multiple-breath nitrogen washout, and airway closure by single-breath nitrogen washout.8

Sleep Recordings
For sleep recordings during the CT study, digital recording equipment (Galileo; Esaote Biomedica; Florence, Italy; and EMBLA; Flaga HF; Reykjavik, Iceland) was used. Two channels of EEG, electro-oculography, submental electromyography, and nasal and oral flow (three-port thermistor/nasal pressure sensor) were recorded. Arterial saturation was registered by using a finger pulse oximetry9 (EMBLA Oximeter, type M; Flaga HF; and 7100CO2SMO; Novametrix; Wallingford, CT). The digital processing of the signals causes approximately a 2- to 2.5-s delay on the computer screen. Therefore, a stretch-sensitive piezoelectric respiratory effort belt connected directly to an XY writer was also used to register respiratory movement simultaneously and to guide the CT scanning (see below). Sleep staging was performed according to standard criteria.10

CT in the Awake State and During Sleep
Aeration of the lungs was studied during the night by CT (Somatom Plus; Siemens; Erlangen, Germany; and LightSpeed Plus; GE Medical; Milwaukee, WI). All subjects were studied in the supine position. A minimum of 15 min of rest preceded the awake CT scans. In two subjects, awake CT scanning was performed after sleep.

Technical and Methodologic Aspects
At end-expiration, the position of the diaphragm was located from a frontal scout view covering the chest. A spiral scan (exposure time of 4 s) covering the basal 4 cm of the lung was then performed during normal breathing (Fig 1 , top, A). Slice thickness was 10 mm; table movement was 10 mm/s, and exposures were made at 165 mA and 120 kV. With a matrix of 512 x 512, the resulting picture element (pixel) measured approximately 0.6 x 0.6 mm. To validate the above technique, a spiral CT scan of the basal 4 cm of the lung was obtained during breath hold at FRC in six subjects, and both the lung tissue density and the gas/tissue ratio over the lung distance studied were analyzed.


Figure 1
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  		Figure 1. Top, A: Example of a CT recording during a breath. Exposure began at or close to end-expiration, as guided by the spirogram from the respiratory belt device. The recording (radiograph attenuation values against time) thus reflected the subject’s breathing and enabled detection of end-inspiratory and end-expiratory CT data. IMA = image. Bottom, B: Positioning of the four ROIs in the vertical direction. The ROIs were 2 cm in diameter and evenly distributed along the border of the lung, from the ventral (nondependent) to the dorsal (dependent) lung region.

 
Regional Aeration at FRC
Each spiral scan was reconstructed into 11 images, each 10-mm thick and with 3-mm increments. Regional aeration was then analyzed in each image by calculating the lung aeration (see below) in four circular regions of interest (ROIs)11 (Fig 1, bottom, B) and in a subsample (n = 5) also in one ROI located at the mid level of the lung near the mediastinum. The dynamic change in lung aeration over time, as assessed from the 11 reconstructed images at the four different ROIs, was related to respiration as recorded by the respiratory belt and by nasal and oral flow, allowing identification of expiratory and inspiratory phases (Fig 1, top, A). The lowest aeration value seen in the series of images (ie, at FRC) was identified, and lung aeration was compared between the awake state and sleep in each subject.

The density of each ROI was calculated from the radiograph attenuation, expressed in Hounsfield units (HU) between – 1,000 HU and – 100 HU. The HU scale spans from – 1,000 HU (air) to 0 HU (water) to + 1,000 HU or more (bone).12 The density of the lung in a particular pixel with an attenuation of x HU is as follows: lung density (grams per milliliter) = (x + 1,000)/1,000. Thus, if the attenuation in a pixel is – 800 HU, a common value in a well-aerated lung region, the density will be 0.2 g/mL. This value is the weighted mean of the lung tissue, blood, and gas in that particular pixel. The inverse of the lung density is the "specific lung volume" (1/lung density), equaling 5 mL/g in this example. The density of the lung tissue is usually taken as 1.065 g/mL, and its inverse value (0.939 mL/g) is the "specific lung tissue volume" (1/lung tissue density).1314 The aeration of the lung in each pixel per unit tissue can then be calculated as follows: volume of gas (milliliters)/weight of tissue (grams) = specific lung volume – specific lung tissue volume.

In the above example with a pixel of – 800 HU, the lung density is 0.2 g/mL and the specific lung volume is 5 mL/g. Correspondingly, the specific lung tissue volume is 0.939 mL/g. The pixel will thus contains 4.061 mL of gas per gram of lung tissue.

Regional Ventilation
In eight subjects, an analysis was also made of regional ventilation both in the awake state and during sleep. The aeration in a particular ROI (percentage of air) was calculated as follows: percentage of air: – x/10, where x is the mean HU of a particular ROI. This gives the percentage of air in an ROI.1213 The percentage of air at end-expiration (FRC) and at end-inspiration (FRC plus tidal volume) was calculated. By subtracting percentage of air at FRC plus tidal volume from that at FRC (change in percentage of air), a measure of regional ventilation was obtained.

Statistical Analysis
Data are presented as the mean ± SD unless otherwise indicated. Comparisons of lung aeration values between wakefulness and sleep were performed with the paired t test or the Wilcoxon signed-rank test when appropriate. The relationship between the difference in lung aeration at FRC between wakefulness and sleep, and FRC, expiratory reserve volume (ERV), CV, body mass index (BMI), age, sleep time, and time in CT was studied by correlation analysis (Pearson correlation coefficient) followed by regression analysis. The results were obtained using statistical software (SPSS, version 13.0; SPSS; Chicago, IL); p ≤ 0.05 was considered significant.

Results

Spirometry and Airway Closure
Characteristics of the subjects and spirometric data are given in Table 1 . The spirometric findings (vital capacity and FEV1) and CV (supine position) were normal. However, as expected the FRC and ERV measured in the supine position were lower than reference values acquired in the upright position. CV-ERV was close to zero, indicating airway closure near to, and in some subjects above, the FRC level.


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  		Table 1. Subject Characteristics and Awake Lung Function Data in the Awake State (n = 10)

 
Regional Aeration at FRC
Awake:
No significant change regarding gas/tissue ratio was seen in any of the four ROIs over the 4-cm horizontal (cranial/caudal) distance that was studied during end-expiratory hold. This is in line with previous reports of no substantial horizontal gradients either for lung density12 or for ventilation in the supine position.15 An increase in lung density from the ventral to the dorsal lung region was seen in the awake subject, in agreement with previous reports.1213

Sleep:
General information regarding CT scanning during sleep is given in Table 2 . The depth of sleep reached stages I-IV (NREM) and REM. A decrease in aeration was seen during sleep in the dorsal, most dependent lung region (ROI-4), from 1.14 ± 0.34 mL gas per gram of lung tissue during wakefulness to 1.04 ± 0.29 mL/g during NREM sleep (mean difference, 0.10 mL/g [9% change]; p = 0.034; Fig 2 ). In contrast, aeration increased from 3.52 ± 0.77 to 3.73 ± 0.83 mL/g (mean difference, 0.20 mL/g [6% change]; p = 0.007) in the most ventral, nondependent lung region (ROI-1) [Fig 2]. Near the mediastinum, lung aeration averaged 3.51 ± 0.65 mL/g during wakefulness and 3.41 ± 0.71 mL/g during NREM sleep (p = 0.465). In one subject, CT scanning was performed on two occasions during REM sleep. In this subject, a more marked fall in aeration (– 18% and – 23% for the two occasions) was noted during REM sleep (Fig 3 ).


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  		Table 2. Individual Sleep Data

 

Figure 2
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  		Figure 2. Left: Plot of lung aeration in the awake state and during NREM sleep at FRC. Bars represent the mean and SE (*p < 0.05, **p < 0.01). Right: Lung aeration at the levels of ROI-1 and ROI-4 in the awake state and during NREM sleep for each subject.

 

Figure 3
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  		Figure 3. CT scans from one subject in the awake state (top) and during NREM (center) and REM sleep (bottom). In this case, the aeration in the lowermost lung region (at the level of ROI-4) during wakefulness amounted to 0.84 mL/g, during NREM sleep (stage II) to 0.76 mL/g (– 10%), and during REM sleep to 0.65 mL/g (– 23%) [window, 400 HU; center, – 400 HU].

 
No significant correlation was found between the observed difference in lung aeration (between the wake state and sleep) and FRC, CV, ERV, BMI, age, sleep time, or time in CT. A negative correlation was found between awake FRC and decrease in dorsal lung aeration (ROI-4) during sleep (Fig 4 ). The lung aeration in the dependent lung region at different sleep stages is shown in Figure 5 . Owing to the limited number of observations, no statistical analyses to compare different sleep stages were performed but mean values indicate a larger decrease during slow wave sleep (stages III and IV) and REM sleep.


Figure 4
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  		Figure 4. Scatterplot and linear regression for the difference in lung aeration measured at FRC between wakefulness and sleep at ROI-4 (r = – 0.78; R2 = 0.60; p = 0.008). The value of R2 indicates that as much as 60% of the decrease in dorsal lung aeration was explained by the awake FRC. Thus, the lower the awake FRC, the larger was the decrease in dorsal lung aeration. No significant correlation was found between lung aeration and time in CT or sleep time. Pulse oximetry did not reveal any significant change in arterial oxygen saturation during sleep, precluding any correlation analysis with spirometry and CT scan data.

 

Figure 5
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  		Figure 5. Data plot showing the average change in lung aeration in the dependent lung region (ROI-4) from wakefulness to sleep at different sleep stages. The findings demonstrate a tendency toward a larger decrease in lung aeration from light to deep sleep and REM sleep. SWS = slow wave sleep (stages III and IV).

 
Regional Ventilation
Awake:
In the awake subject, regional ventilation was slightly but not significantly larger in the dependent than nondependent regions during a breath (mean of ROI 1,2: 3.8 ± 1.2{Delta}%; and of ROI 3,4: 4.9 ± 2.9{Delta}%; p = 0.16).

Asleep:
Ventilation was not significantly different from that in the awake state, with a fairly modest difference between the upper and lower regions (mean of ROI-1,2: 4.5 ± 1.4{Delta}%; and of ROI-3,4: 5.5 ± 2.6{Delta}%; p = 0.09).

Discussion

In the present study, using a novel approach of CT, new data have been obtained regarding aeration of the lung during sleep. The results indicate the occurrence of what has previously been anticipated but not shown, namely an increased lung density and loss of air in the dependent lung region during sleep.

FRC
Lung volume (FRC) decreases by approximately 7% during NREM sleep.236 The main finding in the current study is that lung aeration is reduced in the most dependent, dorsal region during NREM sleep (– 9%), while a slight increase in aeration occurs in the ventral lung region (+ 6%). The net result may thus be a fall in overall FRC during sleep. Aeration in the lung area close to the mediastinum showed no significant difference between the awake state and sleep. In one subject, a more marked decrease in lung aeration was noted during two periods of REM sleep (maximum, – 23%).

Several mechanisms, such as a decrease in respiratory muscle tone, alterations in respiratory timing, central pooling of blood, a decreased lung compliance, and a reduction in tonic inspiratory muscle activity, have been suggested as being potentially associated with the sleep-induced decrease in FRC.234 Our finding of loss of air in the dorsal region and increased aeration in the ventral part may be compatible with reduced muscle tone.16 The loss of tone allows the elastic forces of the lung tissue to pull in the rib cage and the diaphragm until the outward forces of the chest wall and the inward forces exerted by the lung have established a new balance. Loss of diaphragm tone facilitates the transmission of higher abdominal pressure into the thoracic cavity, giving rise to a larger difference in pleural pressure surrounding ventral and dorsal lung tissue.17 The effect of this will be increased expansion of ventral lung regions and decreased in dorsal lung regions.16 It is also known that respiratory muscle activity is reduced during NREM sleep18 and is even more reduced during REM sleep1920 and that sleep is accompanied by a decrease in transdiaphragmatic pressure and impairment of respiratory muscle efficiency.21

The lower the FRC in the awake state, the greater was the loss of air in the dorsal lung region during sleep. This finding suggests that conditions that cause a low FRC will have greater consequences for the aeration of the lung during sleep. Obese patients have reduced lung volumes, and the proportion of such patients is high among those who have obstructive sleep apnea.22 We have previously reported23 that the degree of reduction of ERV during the wake state is a predictor of the severity of apnea and the desaturation frequency during sleep.

Interestingly, there seem to be ventilatory similarities between sleep and anesthesia. Anesthesia is also accompanied by a fall in FRC, by 0.4 to 0.5 L,24 and oxygenation is impaired.25 Important causes of the decreased oxygenation are atelectasis in dorsal (dependent) lung regions, as can be observed by CT,26 and airway closure,27 although conflicting reports have also been presented.28 Atelectasis and airway closure are promoted by the fall in FRC and can explain almost 75% of the oxygenation impairment in the anesthetized subject.27 Thus, there is a fall in FRC during both sleep and anesthesia, although greater during anesthesia.24 Moreover, an increase in FRC in ventral areas during anesthesia has also been shown or anticipated.1729 An exception is anesthesia with ketamine, which preserves tone and does not lower FRC.30

Ventilation
A slightly larger variation in lung density (percentage change of air) was noted in the dorsal than in the ventral lung region during spontaneous breathing, both in the awake state and during sleep. This is in accordance with previous studies123132 that have shown preferential ventilation in lower lung regions. However, the vertical difference was not as marked as has been reported from many earlier studies. Differences in techniques (CT vs scintigraphy) may have contributed to this discrepancy. However, the supine position and restful conditions, both during awake state and sleep, lower the FRC but do not reduce the lung volume at which airway closure occurs.33 This promotes occurrence of airway closure near to FRC or within the breath, as seen in the present study during awake state. Airway closure was not measured during sleep but might be expected, if anything, to have occurred further above FRC. The fall in FRC may thus be a major determinant of regional aeration and ventilation. It has also been shown that ventilation is larger in ventral than in dorsal regions when the subject is breathing at low lung volumes.34

The present study does not fully characterize the effects of sleep on lung aeration. Since the sleep-awake circadian rhythm has a small but significant effect on pulmonary function,35 the CT study was performed during the night. After the CT scanning the subject often woke up and had difficulties in falling asleep again. As a result, in most of the subjects, lung aeration could be analyzed for one sleep stage only. Furthermore, the pattern of inspiration and expiration may be distorted during sleep, especially at sleep onset and during REM sleep when periodic breathing is common.36 Standardization of the procedure of CT scanning is therefore important. In most of the subjects, lung aeration was analyzed in sleep stages II, III, and IV, in which respiration is mostly regular in both amplitude and frequency.36 During sleep, it was obviously not possible to use spirometry, for example, to check at what lung volume the scans were performed or to ask the subjects to hold their breath at the FRC level, as has been done in other studies1237 on awake subjects. Instead, before performing a CT scan during sleep, the respiratory pattern was judged as regular and nondistorted from the oronasal flow recording.

The study design allowed us to perform a spiral scan over a 4-cm segment of the basal lung region during sleep, with the subject lying in the supine position. Thus, the apical lung region could not be analyzed regarding aeration. However, previous studies37 on this issue have not shown any significant differences in lung density between apical and basal lung areas during wakefulness. Owing to the effect of gravity, a ventrodorsal difference in density is to be expected. This difference will be caused by a vertical change in intrapleural pressure, increasing both ventilation and perfusion down the vertical axis.38

It might be argued that dependent lung regions will become denser over time when a subject is lying immobile on the CT table. However, the observed change in lung aeration during sleep seems to occur almost instantly, and we found no correlation between degree of such change and length of time in the supine position or sleep time. Moreover, the two subjects who were studied awake after a preceding period of sleep showed the same pattern of decrease in aeration during sleep as the subjects who had been studied awake first, before sleep. Healthy, awake subjects who were resting supine for more than an hour showed no decrease in aeration in dependent lung regions.26 These observations are also consistent with data reported by Ballard et al,3 who found no relation between study or sleep time and changes in FRC during sleep. They reported that the change in FRC occurred within 30 min of sleep and then remained relatively constant during NREM sleep, whereas a further decrease was seen during REM sleep. Moreover, during natural sleep under comfortable conditions, several changes in position occur during the night that could partly counteract or reduce possible effects of gravity on an increase in lung density during sleep.

In conclusion, reduced aeration of dependent lung regions and an increase in ventral regions were seen during NREM sleep in the supine position. A decrease in FRC and reduced respiratory muscle tone may contribute to the observed alterations in aeration and ventilation.

Acknowledgements

The authors are grateful for the assistance of Maj Olofsson and Lena Nilsson, radiograph technicians, Anders Persson, MD, PhD, and Pia Frånberg, physicist.

Footnotes

Abbreviations: BMI = body mass index; CV = closing volume; ERV = expiratory reserve volume; FRC = functional residual capacity; HU = Hounsfield unit; NREM = non-rapid eye movement; REM = rapid eye movement; ROI = region of interest

The authors have no conflicts of interest to disclose.

This study was supported by grants from the Swedish Medical Research Council (No. 5315), the Swedish Heart and Lung Foundation, the Uppsala County Association Against Heart and Lung Diseases, and the Mid Sweden’s Research and Development Centre.

Received for publication February 9, 2006. Accepted for publication September 8, 2006.

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