Wegener's granulomatosis

Objectives: To compare CT virtual bronchoscopy (VB) to CT alone and to conventional bronchoscopy for evaluation of central airway stenoses in patients with Wegener's granulomatosis.

Design: Prospective observer study, in which 18 thin-section helical CT scans of the trachea and bronchi of 11 patients with Wegener's granulomatosis were obtained. VB was performed using surface rendering and was evaluated by one bronchoscopist and one radiologist in a blinded fashion. Bronchoscopic correlation within an average of 1.8 days of CT was available.

Measurements and results: VB displayed 188 of 198 bronchi (95%). Thirty-two of 40 stenoses (80%) were detected by VB by at least one of two physicians (double reading), and 22 of 40 stenoses (55%) were detected by a third physician reading only the CT.

Conclusions: VB depicts bronchi to the segmental level and detects the majority of central airway stenoses in patients with Wegener's granulomatosis. A team approach is useful to attain optimal clinical benefit from VB for these patients. (CHEST 2002; 121:242-250)

Key words: bronchoscopy; CT; endobronchial stenosis; Wegener's granulomatosis

Abbreviations: AZ = area under the receiver operating characteristic curve; FOB = fiberoptic bronchoscopy; ROC = receiver operating characteristic; VB = virtual bronchoscopy

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Wegener's granulomatosis is a necrotizing vasculitis that affects the airways, sinuses, and kidneys. Airway and pulmonary complications of Wegener's granulomatosis include subglottic stenosis, tracheal and endobronchial inflammation and stenoses, granulomatous pulmonary nodules, and alveolar and cavitary infiltrates. (1-6) Symptoms can include cough, hemoptysis, chest pain, and dyspnea. (7)

Chest radiographs and CT play important roles in the detection of these pulmonary complications. (8-12) A new, three-dimensional image reconstruction and display technique called virtual bronchoscopy (VB) has been shown to be feasible for noninvasive airway evaluation. (13-16) VB consists of endoscope-like images of the airway and is produced from high-resolution helical CT scans of the thorax. The purpose of this report is to compare CT VB to CT alone and to fiberoptic bronchoscopy (FOB) for evaluation of central airway stenoses in patients with Wegener's granulomatosis.

MATERIALS AND METHODS

Patient Population

A prospective study of patients with known Wegener's granulomatosis was conducted. The patients included five women and six men with a mean ([+ or -] SD) age of 38 [+ or -] 13 years (range, 21 to 56 years) and mean disease duration of 12 [+ or -] 7 years (range, 6 to 28 years). For all but one subject, conventional bronchoscopy correlation was available. For one subject, tracheoscopy was available. The mean interval between endoscopy and CT was 1.8 [+ or -] 4.1 days (range, 0 to 17 days; within i day of CT for 14 of 18 studies). The study was performed with the approval of our Institutional Review Board, and written informed consent was obtained.

Bronchoscopy

Conventional bronchoscopy was performed by a board-certified pulmonologist. A bronchoscopist (J.H.S.) recorded findings on a diagram of the airways at the time of the bronchoscopy for all but four studies. For four studies, the bronchoscopy report in the patients' medical records was used. All sites of abnormal bronchial narrowing [greater than or equal to] 20% of the expected lumen diameter based on comparison to the diameter of a normal proximal lumen or to the diameter of other normal bronchi in the same study used as a reference were considered evidence of stenosis at bronchoscopy. Low-grade stenoses may be underreported in the four bronchoscopies extracted from the medical record. Bronchoscopy was used as the "gold standard" technique for detection of airway stenoses.

Twelve of 18 bronchoscopies were videotaped and reviewed by a second board-certified pulmonologist/bronchoscopist (M.J.C.) blinded to the clinical findings. This review was done to determine interobserver agreement for FOB.

CT Scanning

Axial helical CT scans of the thorax from the level of the proximal trachea in the lower neck through the lung bases were obtained at end-inspiration (HiSpeed Advantage; General Electric Medical Systems; Milwaukee, WI). In two scans, scanning included the subglottis as well. The acquisition technique used 3-mm collimation, 6-mm table feed (helical pitch, 2.0), 140 kilovolt peak, 160 milliampere-seconds, and 512 x 512 matrix. (15) During each 15- to 20-s breathhold, 9- to 12-cm contiguous sections were obtained.

The reconstruction parameters were for CT interpretation: a 3-mm table increment yielding 50 to 85 images and a high-frequency lung algorithm; and for VB, a 1-mm table increment, yielding 150 to 250 images and a high-frequency bone algorithm. A smaller table increment was used for VB to reduce stair-stepping artifact. We used a larger table increment for CT interpretation because of the impracticality of viewing several hundred images per patient.

The field of view was 20 to 30 cm (depending on patient size). This field of view was set to maximally magnify the central airways without clipping terminal airway branches. Much of the chest wall was usually clipped with these settings since the chest wall was not needed for airway analysis or VB reconstruction.

Image Processing

The stack of CT images was transferred from a picture archiving system to a graphics workstation (Onyx Infinite Reality 2; Silicon Graphics; Mountain View, CA) for viewing using our research endoscopy software package and previously described techniques. (15,17) This software uses interactive surface rendering to produce a realistic endoscopic display of the bronchial lumen. An exoscopic view of the bronchial anatomy (ie, a view taken from outside the airways showing the entire three-dimensional airway model) computed using surface rendering was used for anatomic localization. (15,17) The standardization of these visualization parameters greatly simplified user interaction.

VB was performed by one participant (R.M.S.) who interactively negotiated the airways of each patient on the computer screen by use of movements of the computer mouse. The flight path paradigm simulated movements of an actual endoscope by withdrawing the simulated endoscope to the nearest proximal bifurcation before inspecting each distal airway. This technique allowed the observers to maintain their sense of anatomic localization. The virtual bronchoscopy simulations were recorded on standard videotape to isolate any effects relating to the use of the computer workstation or software that could bias the results.

The standardized viewpoints on the tape were as follows: (1) exoscopic view, frontal, turn 180 [degrees], posterior, turn 180 [degrees]; (2) exoscopic view close-ups, anterior projection-pan down trachea, right bronchi, left bronchi, then posterior projection, right bronchi, left bronchi; (3) endoscopic view, begin at tracheal inlet, trachea, right lung bronchi, left lung bronchi; upper lobes, then middle lobe/lingula, then lower lobes. Pull back virtual endoscope to bifurcation before entering smaller branches.

Image Analysis Methods

The videotapes of the virtual bronchoscopies were interpreted by one bronchoscopist (physician 1, M.J.C.) and one radiologist (physician 2, B.J.W.), who were blinded to patient identity and clinical findings through the use of random code numbers. The axial CT scans were interpreted prospectively by one radiologist (physician 3, R.M.S.), who was blinded to the clinical findings. The axial CT images were recorded on hard-copy films at standard lung window settings (level, -550 Hounsfield units; width, 2,000 Hounsfield units). Interpretation consisted of analysis of the subglottic area, trachea, mainstem bronchi, and lobar bronchi.

Virtual endoscopies were evaluated using a flowsheet that listed all bronchi to the segmental level and included an anatomic diagram. The physicians were instructed to identify stenoses on the diagram. For each stenosis, the physicians recorded their estimate of degree of stenosis using numbers from 1 to 100%. Only central airways (trachea through lobar bronchi) were analyzed. The distal extent of visualized bronchi was marked on the anatomic diagram.

For each bronchus at virtual bronchoscopy, the observers rated their diagnostic confidence using a 5-point Likert scale. The confidence scale went from 0 (complete confidence that the bronchus was normal) to 4 (complete confidence the airway was stenotic). Intermediate values indicate increasing levels of confidence that a stenosis is present. A rating anywhere from 1 to 4 indicated that a stenosis was present, with at least some confidence. Confidence ratings were used for a receiver operating characteristic (ROC) analysis (see below).

The length of the stenosis (in millimeters) was determined retrospectively (by co-author N.R.A.) from the three-dimensional VB model. Stenotic length measurements were made by pointing and clicking on the left mouse button at one end of the stenosis, moving to the opposite end of the stenotic region, and once again clicking with the left mouse button. (17) Care was taken to remain in the same plane to ensure proper measurement.

Statistical Analysis

An ROC analysis of the confidence level data from VB was analyzed using the software program ROCFIT (Charles E. Metz, PhD; Kurt Rossmann Laboratories, Department of Radiology, University of Chicago; Chicago, IL). (18) This program determines the sensitivity of a test (in this case, stenosis detection using VB compared to FOB) at different thresholds of confidence, and then computes the area under the ROC curve (Az), which is a measure of the diagnostic utility of a test relative to a "gold standard." We used the BOC analysis to assess whether the physicians could detect stenoses compared to the "gold standard" of bronchoscopy. The degree of stenosis was not considered in the ROC analysis.

Sensitivity for stenosis was computed on a per-patient and per-bronchus basis. Any stenosis recorded by the physicians, regardless of confidence, was used in the computation (confidence levels 1 to 4). Fisher's Exact Test was used to compare sensitivities. This may overestimate statistical significance since some subjects underwent more than one VB and are not truly independent. Interobserver agreement between the bronchoscopists was assessed using Cohen's [kappa]. The analyses exclude 10 bronchi not visualized at FOB in one subject who underwent tracheoscopy only. Evaluation of the degree of stenosis excluded five subtotal stenoses for which "percent stenosis" was not recorded (three stenoses from bronchoscopies extracted from the medical record, two for which percent stenosis was not recorded and the videotape was unavailable).

RESULTS

The following images show the capability of VB to accurately depict the stenotic airways with reference to matching bronchoscopic images, starting with the subglottis and continuing anatomically from the main bronchi to the tertiary bronchi. Figure 1 is of a subglottic stenosis shown antegrade on FOB and retrograde on VB. One of the features of VB is the ability to maneuver the virtual camera to give airway images that give a better perspective on stenosis location.

[FIGURE 1 OMITTED]

Figure 2 shows the progression of a bronchus intermedius stenosis over the course of a year. Exoscopic VB views provide an accurate perspective as to the location and length of the lesion.

[FIGURE 2 OMITTED]

Figure 3 shows the main carina. Here, the exoscopic VB view gives the added knowledge that there are two stenotic regions present in the bronchus intermedius. Without the ability for the scope to pass through the proximal stenosis, this information would not be available on FOB.

[FIGURE 3 OMITTED]

Figures 4, 5 show stenoses of the right upper lobe and left upper lobe bronchi, respectively. Note how the orientation of the image in Figure 5, top left, A differs from that in top right, B due to the rotation and flexion of the bronchoscope.

[FIGURES 4-5 OMITTED]

Of the central airways, the trachea and mainstem bronchi were always seen on VB. The lingular and left-upper-division bronchi were seen with the lowest frequency (each at 79%; 13 of 18 bronchi). Overall, 188 of 198 bronchi (95%) were present and visible on VB.

Of 38 stenoses (excluding 2 in the subglottis) assessed by FOB, all but 5 stenoses were in the bronchus intermedius or lobar bronchi. The spatial distribution of stenosis was as follows: left mainstem bronchus (n = 5), right upper lobe bronchus (n = 5) bronchus intermedius (n = 12), right middle lobe (n = 6), left upper lobe (n = 9), and left lower lobe (n = 1) bronchi. There was moderate agreement between bronchoscopists' stenosis assessments by FOB ([kappa] = 0.65).

There were an average of 2.2 stenoses (40 stenoses in 18 patients) per patient-study. The mean stenosis narrowing was 67% (range, 9.0 to 100%). At VB, physician 1 found 58% (23 of 40) and physician 2 found 40% (16 of 40) of the stenoses reported at FOB. At CT, physician 3 found 55% (22 of 40) of the stenoses reported at FOB. Using VB, at least one physician was able to detect 80% (32 of 40) of the stenotic regions as detected by the FOB. This result was a statistically significant improvement compared to the CT readings by physician 3 (p = 0.01). For the stenoses correctly detected by each physician examining VB, there was no statistical difference in the percent stenosis noted on VB vs the percent stenosis noted on FOB: physician 1 (two-tailed paired t test, p = 0.89), mean difference (VB - FOB) [+ or -] SD, 0.6 [+ or -] 17.8, (95% confidence interval, -7.5 to 8.6); physician 2 (two-tailed paired t test, p = 0.52), mean difference, -3.9 [+ or -] 21.2 (95% confidence interval, -15.9 to 8.1).

The frequency that airways were visible distal to the stenosis at FOB was 50% (20 of 40) and at VB was 65% (25 of 40). Although FOB and VB both provide the capability to see some airways beyond stenoses, seven airways distal to the stenoses were visible at VB but not FOB. However, the presence or absence of abnormalities in these seven airways as depicted by VB cannot be confirmed since neither bronchoscopic nor pathologic correlation is available. The majority of stenoses where airways beyond were detected only on VB were located in the left upper lobe bronchus (57%; four of seven stenoses).

When airways were patent distal to the stenosis on VB, stenosis length was measured. The majority of stenoses measurable on VB were located in the bronchus intermedius (52%; 13 of 25 stenoses; one bronchus intermedius had 2 stenoses). The mean stenosis length was 0.74 [+ or -] 0.34 cm (range, 0.34 to 1.47 cm).

The subglottis was analyzed separately. FOB demonstrated two subglottic stenoses in patients for whom the subglottis was scanned using CT. Both subglottic stenoses were detected by VB but neither were detected using CT. At CT, the subglottic area was described as being thickened and/or irregular.

Sensitivity for stenosis detection, reported using the bronchus and the patient as units of measure, were as follows: VB per bronchus, physician 1 sensitivity = 58%, physician 2 sensitivity = 40%; VB per patient-study, physician 1 sensitivity = 75%, physician 2 sensitivity = 75%. In comparison, the CT sensitivity (physician 3) per bronchus was 55% and per patient-study was 93%. Specificity for stenosis detection was as follows: VB per bronchus, physician 1 specificity = 93%, physician 2 specificity = 93%; VB per patient-study, physician 1 specificity = 100%, physician 2 specificity = 50%. CT specificity per bronchus was 93% and per patient-study was 50%.

There were multiple instances where bronchi appeared abnormal but not stenotic at CT or FOB. The sensitivity and specificity results described above use strict criteria for stenosis presence, but if the criteria were broadened to include abnormal bronchi, the results are improved. For example, CT sensitivity and specificity per bronchus would be slightly higher (63% and 95%, respectively) if six abnormal bronchi at CT were considered true-positive results instead of false-negative findings (CT diagnoses, bronchial wall called irregular rather than stenotic [n = 3] or false-positive; FOB diagnoses, edematous or widened bronchus [n = 2] or granulation tissue present [n = 1]).

ROC analysis results were as follows: the AZ value for physician 1 was 0.93 [+ or -] 0.02, and the AZ value for physician 2 was 0.77 [+ or -] 0.14. These results indicate good-to-excellent diagnostic utility of VB for detection of stenosis.

DISCUSSION

We found that the VB technique is capable of visualizing the central airways and detecting stenoses in patients with Wegener's granulomatosis. Ninety-five percent of the central airways were visualized. Using consensus readings, VB sensitivity for stenosis detection was 80%. The fidelity of the VB images is striking when compared to the corresponding conventional bronchoscopic images. Added benefits of VB over FOB include visualizing airways beyond tight stenoses, visualizing an extra stenosis within a particular bronchus, and measuring stenosis length.

Based on these findings, potential uses of VB are as a prebronchoscopy test for identifying whether any airways are abnormal, to measure changes in stenoses over time or in response to treatment, or to use in children or adults too ill to tolerate conventional bronchoscopy. Unstable stenoses demonstrating evidence of progression over time could motivate referral for interventional bronchoscopy. A team approach appears to be important to extract the best possible clinical utility from VB.

There are several reasons why stenoses could have been missed. First, some of the missed lesions were misinterpreted as being at the limits of the VB model due to inadequate resolution to depict distal branches. Second, four of eight stenoses (50%) missed by both physicians viewing VB were located in the right middle lobe bronchus. We believe stenoses in the right middle lobe bronchus are commonly missed because of poor longitudinal resolution. This occurs because the right middle lobe bronchus is usually oriented horizontally within the axial scan plane and its walls are less well depicted than those bronchi that course perpendicular to the scanning plane (such as the bronchus intermedius). Third, only 2 of 8 missed stenoses were > 50% stenotic. It may be difficult to identify noncritical stenoses that may be incorrectly ascribed to normal variation rather than pathology. Fourth, the physicians may have been inadequately trained in VB interpretation, specifically in how to correctly evaluate the three-dimensional model. Fifth, FOB may have determined a stenosis was present when in fact the bronchus was normal. This may occur because interindividual variation of bronchial diameters may be misinterpreted as mild stenoses at FOB. In addition, FOB is not a perfect "gold standard" because of interobserver variability for stenosis assessment. We found only moderate agreement between observers for the subset of bronchoscopies reviewed by two bronchoscopists ([kappa] = 0.65). Although the ability of bronchoscopy to directly visualize airways is still a compelling argument that FOB is an appropriate "gold standard," CT has been shown to be highly accurate for assessing airway caliber. (19)

The reconstruction algorithm tends to produce tapered distal airways at the limits of segmentation that could be misinterpreted as a stenosis; the opposite also could occur: a tapering stenosis could be misinterpreted as the limit of segmentation. This proved to be detrimental especially when comparing the results of the left upper lobe. Physician 1 correctly identified all nine of the left upper lobe stenoses, whereas physician 2 did not identify any. Physician 2 indicated that the left upper lobe was not resolved in six of these cases, mistaking a stenosis for poor resolution. The way the three-dimensional model is generated presents another potential problem, in the sense that the airways beyond the stenosis are not always rendered. These problems may in part be resolved by improving the quality of the image segmentation either by developing better segmentation algorithms or acquiring higher-resolution CT data. Using VB in conjunction with the CT may reveal unsuspected nodules, atelectasis, or infiltrates that can guide the physician in locating stenotic regions; in clinical practice, this would be done routinely.

When a stenosis was located, VB, in comparison to FOB, reported a higher rate of airway detection distal to that stenosis. This proved to be the case for a significant number (7 of 40) of stenoses (18%). Therefore, in situations where patent airways were detected distal to the stenosis, VB provides information not attainable with bronchoscopy.

VB may provide some benefit in the subglottic region where CT examination did not reveal either of two stenoses and VB detected both. The airway normally tapers in that region, making differentiation between normal and abnormal tapering difficult. It is clear that more data in the subglottic region are needed, but initial data do suggest a potential benefit of VB over CT when examining the subglottic area, traditionally a very difficult area to evaluate with imaging.

VB of the upper airway, trachea, and central bronchi has been reported in a number of clinical settings. (13,20-26) Our work confirms previous reports that concluded VB techniques offer the advantage of visualizing airways beyond the stenosis in main bronchi. (24,26) We are also in agreement with Neumann et al, (25) who concluded that the performance of VB strongly depends on observers' experience with three-dimensional imaging techniques. Ferretti et al (22) concluded that with spiral CT data, simulations of > 90% of the patients' central airways were of good quality. This compares favorably with our results, which indicated a 95% bronchi inner-wall detection rate, all with good quality.

Reported sensitivities for stenosis detection with VB range from 94 to 100%. (22,27-29) Our lower sensitivity (80%) may be in part due to a different spatial distribution of lesions, including more peripheral lesions or to the absence of a mass. For example, in two of the four articles that specifically evaluate stenoses, (22,27) the stenosis was usually due to a carcinoma or other mass. In a third report, (28) all 21 stenoses were in the upper airway or trachea. In a fourth report, (29) 18 of 39 stenoses were in the trachea. In our study, there were only five stenoses in the trachea/mainstem bronchi region.

Ferretti et al (30) concluded that axial CT remains the technique of choice to detect and characterize benign airway abnormalities. In that study, the incremental benefit of VB was found to be small. They, however, looked at a wide range of pathology (not only stenoses) that were predominantly located proximally (in the trachea or mainstem bronchi in 90% of eases). In our study, sensitivity for stenosis detection at CT using single observers was comparable to that of VB despite the distal location of the stenoses and the larger 3-mm slice index used for interpretation of the axial CT images. When readings of VB by two observers were combined, VB had greater sensitivity than CT (p = 0.01).

One possible limitation of this study is that our patient population had a high incidence of airway disease. As a result, the observers may have been biased to detect abnormalities. However, this enabled us to more accurately measure the VB technique against the FOB technique since the stenoses were abundant. Another limitation is that results of four bronchoscopies were extracted from the medical record and therefore may have underestimated the number of stenoses in those subjects.

Anticipated improvements in CT resolution with the new multislice helical scanners should enhance the resolution of VB. (31) The longitudinal resolution of multislice helical CT can be three times greater than that of single-slice helical CT. This will enable depiction of more distal airways.

Overall, VB augments conventional CT due to enhanced detection in the subglottic region and improved stenosis measurement, and FOB due to improved airway detection distal to the stenosis without added discomfort to the patient. When used in a team approach in conjunction with FOB and conventional CT, VB may provide clinically useful information not otherwise available. With further advancement in CT imaging, VB will continue to improve as a useful tool in airway stenosis detection.

ACKNOWLEDGMENT: We thank the CT technologists in the Department of Diagnostic Radiology at the National Institutes of Health Clinical Center for patient scanning; Lynne Pusanik, BSME, MEng, for software engineering; and Andrew Dwyer, MD, for critical review of the article.

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* From the Diagnostic Radiology Department (Drs. Summers and Wood, and Mr. Aggarwal) and Division of Critical Care Medicine (Drs. Cowan and Shelhamer), Warren Grant Magnuson Clinical Center; and National Institute of Allergies and Infectious Diseases (Drs. Sneller and Langford), National Institutes of Health, Bethesda, MD.

This work was supported by the intramural research programs of the Diagnostic Radiology Department, Clinical Center.

Manuscript received January 8, 2001; revision accepted July 24, 2001.

Correspondence to: Ronald M. Summers, MD, PhD, Diagnostic Radiology Department, National Institutes of Health, Bldg. 10, Room 1C660, 10 Center Dr, MSC 1182, Bethesda, MD 20892-1182; e-mail: rms@nih.gov

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