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(Chest. 2004;125:2083-2090.)
© 2004 American College of Chest Physicians

Lung Density Measurements in Spontaneous Pneumothorax Demonstrate Airtrapping*

Hans J. M. Smit, MD, PhD; Richard P. Golding, MD; Franz M. N. H. Schramel, MD, PhD, FCCP; Walter L. Devillé, MD; Radu A. Manoliu, MD, PhD and Pieter E. Postmus, MD, PhD, FCCP

* From the Department of Pulmonary Medicine (Dr. Smit), Rijnstate Hospital, Arnhem; and the Departments of Pulmonary Medicine (Drs. Schramel and Postmus), Radiology (Drs. Golding and Manoliu), and Epidemiology and Biostatistics (Dr. Devillé), Vrije Universiteit Medical Centre, Amsterdam, the Netherlands.

Correspondence to: Pieter E. Postmus, MD, PhD, FCCP, Department of Pulmonary Medicine, Vrije Universiteit Medical Centre, PO Box 7057, 1007 ME Amsterdam, the Netherlands; e-mail: long{at}vumc.nl


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Purpose: Idiopathic spontaneous pneumothorax (SP) is the result of leakage of air from the lung parenchyma through a ruptured visceral pleura into the pleural cavity. This rupture is thought to be caused by an increased pressure difference between parenchymal airspace and pleural cavity. We hypothesize that rather peripheral airway inflammation leads to obstruction with check valve phenomena and by that to airtrapping in the lung parenchyma, which precedes spontaneous pneumothorax.

Setting: University hospital.

Materials and methods: Forty-one matched healthy volunteers (21 smokers and 20 nonsmokers), and 41 patients with SP (21 patients with and 20 patients without bullae) underwent spirometrically controlled high-resolution CT density measurements with automatic contour tracing at 10% and at 90% of vital capacity.

Results: Patients with SP showed lower mean lung density (MLD) values and higher percentages of Hounsfield units (HU) below – 900 HU (pixel index [PI]) compared to the healthy volunteers on expiratory scans. This enhanced airtrapping phenomenon is seen in both the SP lung (MLD, p = 002; PI, p = 0.01) and the contralateral lung (MLD, p = 0.009; PI, p = 0.05) compared to the control subjects. The difference with control subjects is independent of smoking behavior and bullae.

Conclusions: Peripheral airway obstruction with airtrapping was found, and it is supposed to play an important role in the pathogenesis of spontaneous pneumothorax.

Key Words: emphysema • high-resolution CT • lung density • spontaneous pneumothorax • tomography


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
A quantitative assessment of density characteristics on lung parenchyma can be done by automatic computer calculations on high-resolution CT (HRCT) slices,12345 with automatic contour tracking to include only the lung parenchyma.6789 Lung attenuation parameters are related to grams per cubic centimeter and are dependent on lung tissue, the level of inflation, and perfusion.6710111213 Smoking induces destruction of alveolar tissue, resulting in enlarged airspaces. This will be found on inspiratory scans, and smoking also induces bronchiolar inflammation14 with obstruction due to check valve phenomena, especially resulting in airtrapping during expiration.23 The inspiratory/expiratory ratio can reveal additional information, because it includes the different lung functional characteristics within the individual, such as restriction and obstruction.

Primary or idiopathic spontaneous pneumothorax (SP) is a disease in which degeneration of pulmonary tissue is found. Schramel et al15 gave an overview of the pathogenetic hypothesis. Although it is a disease without any known origin or cause, and without any known underlying disease (in the current definition16), a causal relationship with smoking is likely, because 70 to 80% of the patients with SP smoke,1718 and smoking cessation reduces the chances of recurrence of SP.19

In a high percentage of patients, blebs and bullae (emphysema-like changes [ELCs]), are found in the pneumothorax lung.202122 It is assumed that this is the result of the bronchial obstruction with check valves, however, it is not very likely that ELCs cause the SP but are a cophenomenon.23 This means that there is theoretically no rationale for bullectomy as the appropriate therapy for SP. Since SP typically occurs in patients 20 to 40 years old,2425 more generalized emphysematous abnormalities will probably not be very pronounced, and therefore difficult to diagnose by standard lung function testing.24 In many patients with SP, one might expect to find smoking-related bronchiolitis with check valve phenomena and trapped air in the periphery of the lungs.314 In the pathogenesis of SP, it has been proposed that peripheral airway obstruction is probably more important than ELCs.15 Whether this bronchiolitis already results in airspace distention at an earlier stage than is visualized on HRCT scans or at thoracoscopy in patients with SP is unclear. The goal of the study was to compare lung density of patients with SP and normal, healthy, age-matched volunteers at a fixed level of inspiration in order to detect more generalized tissue destruction, as in patients with emphysema, and also at a fixed level of expiration to detect bronchiolitis-related airtrapping.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Subjects
Four groups of age-matched individuals participated in the study: 20 healthy volunteers, never-smokers, without any known pulmonary disease; 21 healthy smoking volunteers without any known pulmonary disease; 21 patients with SP without any pulmonary disease prior to the SP, who nonetheless had documented bullous abnormalities detected on previous CT scan or with video-assisted thoracoscopy (VAT); and 20 patients with SP without bullous abnormalities detected on previous CT scan or with VAT. Subject characteristics are shown in Table 1 . The lung function parameters of the patients with SP and healthy volunteers were all in the normal range, with or without smoking and with and without visible bullae (FEV1 percentage of predicted, FEV1/vital capacity [VC] percentage, mean expiratory flow at 50% predicted, total lung capacity percentage of predicted, residual volume percentage of predicted, carbon monoxide diffusion capacity corrected for alveolar volume [KCO] percentage of predicted.). Six patients had bilateral SP, and 13 patients had ipsilateral recurrent SP. Five control subjects had one ELC of < 2 cm on the HRCT scan. The 41 patient with SP all had normal {alpha}1-antitrypsin levels.


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  		Table 1.. Subject Characteristics*

 
The normal individuals were recruited by advertisement, the inclusion criteria being age matching with the SP group, and absence of any pulmonary disease. The patients with SP were consecutive patients treated in our hospital from January 1995 until June 1997. The medical ethical committee of the hospital approved of the study design. The lung function and CT scans were made at least 3 months after the SP. Thirty-one patients with SP were treated by powder talcage during VAT, 6 patients underwent bullectomy and pleurectomy, and 4 patients were treated conservatively with bed rest and/or chest tube drainage.

In all 82 individuals, information concerning smoking behavior, recurrent pneumothorax and treatment, and pulmonary complaints was obtained by questionnaire. Lung function tests2627 were performed within 2 weeks of the HRCT scans (Table 1).

Spirometrically Controlled HRCT
Slices were made at three fixed levels: the main carina, the upper level of the aortic arch, and halfway between the aortic arch and lung apex. Inspiratory and expiratory slices were made at all three levels. Daily calibration of the equipment was performed. The technique has been described by Kalender et al.28

The spirometric control was performed as follows: immediately before the scan with the patient in supine position, VC was determined twice using the electronic spirometer. When a > 200-mL difference was found between two consecutive VC measurements, another two measurements were made, and the mean value was used. The three inspiratory scans were made, automatically, at 90% of the VC (VC90%) by closure of a valve in the spirometer, which was connected to the CT scanner, at the time of scanning; and three expiratory scans were made in the same way at 10% of the VC (VC10%). The hand-held spirometer was placed cranially to the individual, without touching the spirometer itself, to prevent unwanted heating of the spirometer.

HRCT Technique and Evaluation
Scanning parameters were as follows: 140 kV, 146 mA, 1-mm collimation, and window settings of – 400 Hounsfield units (HU) to – 1,000 HU. Scans were performed at three levels at both VC10% and VC90%.5 No contrast medium was used. The CT scanner was a Somaton plus 4, equipped with Spiro and Pulmo software (Siemens; Erlangen, Germany).

Density measurements were performed with the Pulmo software as described by Kalender et al.28 The contours of the lungs, excluding the mediastinum, trachea, large bronchi, and large solitary bullae, were automatically determined. Left, right, and combined lungs were measured separately. Density values of the overall range (mean lung density [MLD], + 3,071 to – 1,024 HU), for the specific range between – 900 HU and – 1,000 HU, as well as the percentage of the area in the histogram with HU in this – 900 to – 1,000 HU range (pixel index [PI]) were available (Fig 1 ). Subtraction of the mean HU values of VC90% inspiratory scans from those of VC10% expiratory scans and the ratio between VC10% and VC90% HU values were also measured.213



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  		Figure 1.. Expiratory HRCT measurement of left, right, and both lungs combined using automatic contour detection and spirometric control.

 
Statistical Analysis
For categorical values, the {chi}2 test was used. The Student t test for independent groups was used to determine differences in continuous variables. Multiple regression analysis was performed to determine the relative effect of smoking behavior on the lung density parameters. Analysis of variance was used to study between groups differences, adjusted for smoking behavior. All statistical analyses were performed in SPSS 6.1 for Windows (SPSS; Chicago, IL). Differences were considered significant at p < 0.05. Multiple testing was corrected by Bonferroni correction.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Pneumothorax Side, Healthy Side, and Healthy Control Subjects
Table 2 shows densitometric differences between the mean of both lungs of the control subjects, and the pneumothorax side and contralateral side in patients with SP. The expiratory density differences are significant between lungs of healthy control subjects and the pneumothorax lung of patients with SP, but also between the lungs of healthy control subjects and the contralateral (healthy) side of the patients with SP. The differences between the pneumothorax side and the contralateral (healthy) side are not significant. The VC90% – VC10% and VC10%/VC90% ratio values confirm these differences. The differences are corrected for the smoking behavior of the subjects. After the Bonferroni correction, differences in MLD remain significant for VC10% between control subjects and the pneumothorax side of the patients with SP, and for VC90% – VC10% and VC10%/VC90% ratio between control subjects and the pneumothorax lung as well as the contralateral lung of the patients with SP.


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  		Table 2.. Densitometrical Differences for the Pneumothorax Lung, the Contralateral Lung, and the Healthy Control Subjects Corrected for Smoking Behavior*

 
The subgroup of nonsmokers shows that the contralateral lung sides of the nonsmoking patients with SP (n = 10) have significantly lower attenuation values in expiration than the control subjects (n = 20) [MLD at VC10%, p = 0.001; PI at VC10%, p = 0.07]. We failed to show statistical differences between smoking and nonsmoking control subjects and between smoking and nonsmoking patients with SP.

Bullous Abnormalities
Table 3 lists the different patient characteristics and density values of patients with previously detected bullae (on previous CT scans or at thoracoscopy). Although there are more smokers in the group with bullae, the percentage of recurrent SP or bilateral cases is even lower than in the group without bullae. No significant density differences are found between patients with SP with and without bullae after correction for the smoking behavior. After Bonferroni correction, the difference of the PI at VC10% remains significant between patients with SP without bullae and control subjects without bullae.


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  		Table 3.. Patients With SP: Relationships With Characteristics, Bullae, and Density*

 
No significant density differences are found between the bullectomy (n = 5) and nonbullectomy patients (n = 29), except for the PI at VC10% (p = 0.03). The patients with SP without bullae show significant lower MLD and higher PIs than the control subjects without bullae.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
With HRCT, a sensitive technique has become available by which it is possible to perform density calculations on the different structures of the lungs.2 In particular, the extent and severity of emphysema can now be determined in a quantitative and qualitative fashion.12345

Besides measuring the MLD of the overall HU range,6 it is also possible at specific subranges with more "sensitivity" for air (the "air" subrange < – 900 HU). The mean HU in this subrange between – 900 HU and – 1,000 HU may represent the severity of parenchymal abnormalities, but does not describe the quantity of the tissue involved. The PI is the percentage of the area under the curve (pixel histogram) of a specific subrange (– 900 to – 1,000 HU), and indicates the quantity of the involved tissue.61011 All these density parameters are related to grams per cubic centimeter, and are dependent on the level of inflation and perfusion, besides the tissue itself.

The cut-off level of the "emphysema range" of < – 900 HU is based on other studies.282930 Müller et al6 calculated the cut-off level slightly differently at – 910 HU, possibly because they used IV contrast medium.

We chose three slice levels, which refer to anatomic structures and are therefore reproducible and comparable in both the same and different subjects. The two slices obtained above the main carina level were specifically chosen because the ELCs in patients with SP are mostly located in the upper third or fourth of the thorax.202122 The main carina level was chosen to get a more general impression of the lung tissue.

To compare scans of different individuals, it is obligatory to make the scans at the same level of respiration, because the amount of air in the lungs is highly influenced by the respiratory status. Therefore, spirometrically controlled scanning was performed.2831 Reproducibility within 5% can be expected.32 We have chosen to make inspiratory scans automatically at 90% and expiratory scans at 10% of the supine-measured VC. This is a practical and reproducible method.230 Scans made at 100% and 0% of VC are not practical, due to fatigue or coughing, and are probably difficult to reproduce in patients. To include both the inspiratory and expiratory abnormalities found within one individual, we used the values resulting from the VC10%/VC90% ratio.

Since a contralateral SP frequently occurs in patients who once have had an SP, it is likely that the structural abnormalities are present in both lungs; therefore, density measurements should preferably be done in the non-SP lung to exclude the effects of treatment of the pneumothorax on the density and structure of the lung. Obviously, bilateral SP precludes this. Despite the fact that we demonstrated in an earlier study13 that there is a significant but small density difference between the left and right lung in healthy volunteers, we think these differences are irrelevant because the prevalence of pneumothorax is equal on both sides. In the current study, we found that both lungs of the patients were abnormal compared to the healthy volunteers although the pneumothorax side showed more pronounced density differences than the healthy side, suggesting that the abnormalities might be more pronounced on the pneumothorax side.

Sixty-seven to 89% of the patients with SP show ELCs during VAT or on CT scans,2122 suggesting a causal relationship between ELCs and SP, although this has never been proven. Whether the ELCs are comparable to generalized emphysema as can be found in patients with COPD should be determined by the measurements at inspiration. Patients with SP had higher mean densities on the inspiratory scans than control subjects, while lower values would be expected in the case of emphysema. Factors that might explain this finding are the chronic inflammation and the possibility of scar tissue. This has been described in patients with SP,22 and might be due to a recurrent process of rupturing and healing of parenchyma especially in the apex of the lung. Compliance measurements, however, do not show restrictive abnormalities.33 Schramel et al25 indicated that lung function parameters of patients with spontaneous pneumothorax are normal. We did perform static lung function and diffusion capacity. Only total lung capacity and KCO differences between patients with SP with and without ELCs could be found. Since this was the only consistent conclusion, we left these data out of the article. Even in patients treated with pleural talcage for SP, compliance measurements are within the normal range. Based on this, it is unlikely that the ELCs found in patients with SP are the results of the same destructive mechanism as is present in patients with COPD and emphysema. This is supported by the lack of signs of development of emphysema after > 22 years of follow-up in patients treated for SP.33 In SP, these seem to be preferably located subpleural; in COPD, a more panlobular distribution is to be expected.34

In scuba divers, a correlation between peripheral airway obstruction and the occurrence of pneumothorax has been reported, suggesting a possible causative role for airtrapping in SP.35 Patients with acute or chronic bronchitis do not appear to have many measurable inflammatory parameters such as elevated C-reactive protein or leukocytes. This bronchitis, including smokers’ bronchiolitis, is therefore difficult to measure other than in histologic specimen. Cottin et al14 described peripheral airway inflammation in operated patients with SP who were smokers. This supports the assumed relationship between SP, ELCs, and peripheral airway obstruction. Both ELCs and pneumothorax could result from pressure increases in trapped air behind an obstruction in small airways. The expiratory scans indicated the presence of trapped air in the patients with SP. This finding is comparable to the results reported by Lamers et al2 in patients with chronic bronchitis, and Newman et al36 in asthmatic patients. Both found signs of trapped air in these patients. Tanaka et al37 did not find differences in the amount of airtrapping between current smokers, ex-smokers, and nonsmokers; all subjects in this study were without symptoms and with normal lung function.

The attenuation parameters showed significant differences between patients with SP and control subjects. The PI and MLD values confirmed the finding that the patients with SP have significantly more "air" on the expiratory scans. This effect is independent of their smoking behavior, suggesting that the smoking patients with SP have more peripheral airway obstruction than the healthy smokers. There was no difference between control smokers and control nonsmokers, although a trend was measurable at some slice levels. The young age group and therefore still restricted amount of pack-years may contribute to this fact.

Table 3 reveals that the group of patients with SP and bullae contained more smokers than the group without bullae, as has been shown before,2438 but all of the other characteristics are comparable, including the recurrence rate. No differences in density were found between the group with one pneumothorax and the group with recurrent SP. This supports our assumption that the abnormalities described are present in a more-or-less uniform pattern.

A strong support for the independent factor of airtrapping is the significant difference between control subjects and patients with SP without ELCs on the expiratory scans, because this difference remains after correction for their smoking behavior. Again, no differences on the inspiratory scans were found, confirming the value of expiratory scans. Because bullae and smoking behavior are related, we compared the patients and control subjects without ELC. The density differences remained present when corrected for smoking behavior as well, suggesting a peripheral airway obstruction in patients with SP, which is not dependent on smoking or bullae. In comparing the patients with and without bullectomy, it seems that bullectomy did not influence the density measurements. It seems rather that the patients undergoing bullectomy have more severe airtrapping.

Many patients received treatment to prevent recurrence of the SP. This therapy may influence densitometric results. Talcage, however, would probably result in shrinking of subpleural blebs, and bullectomy reduces the number of air-filled bullae. This would, when present, actually reduce the inspiratory density differences compared to control patients. No trend toward such a mechanism was found in our data. In fact, the opposite was found, which supports our hypothesis of airtrapping. Scar tissue (> – 900 HU) as a result of therapeutic intervention may influence the MLD but cannot influence the PI, because this only includes < – 900 HU. The pneumothorax lung and contralateral lung showed no different density values, suggesting that indeed the scar tissue in the treated lung does not influence the results. To exclude this effect of talcage or bullectomy, however, we compared the contralateral lung of the patients with SP and the control subjects. The differences between patients with SP and healthy control subjects were confirmed by this approach.

This study proves that patients with SP have different lung densities than matched control subjects. These findings support the hypothesis that trapped air, possibly with peripheral check valve phenomena, is a much more important factor in contracting SP than preexisting bullae.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
Automatic spirometry-controlled HRCT densitometry is an applicable method to determine pulmonary differences between healthy subjects and patients with SP. Patients with SP have lower lung density values than control subjects on expiratory scans (but not on inspiratory scans), suggesting that airtrapping is a contributing factor in the pathogenesis of SP. This is also present in the nonpneumothorax lung of these patients. It is not dependent of smoking behavior or ELCs.


   Footnotes
 
Abbreviations: ELC = emphysema-like change; HRCT = high-resolution CT; HU = Hounsfield units; KCO = carbon monoxide diffusion capacity corrected for the alveolar volume; MLD = mean lung density; PI = pixel index; SP = idiopathic spontaneous pneumothorax; VAT = video-assisted thoracoscopy; VC = vital capacity; VC10% = 10% of vital capacity; VC90% = 90% of vital capacity

This study was supported by a grant from AstraZeneca.

Received for publication May 9, 2003. Accepted for publication January 13, 2004.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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