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Ann Thorac Surg 2005;79:365-374
© 2005 The Society of Thoracic Surgeons

Review

Is Virtual Bronchoscopy an Efficient Diagnostic Tool for the Thoracic Surgeon?

Catherine M. Jones, MBBSa, Thanos Athanasiou, MD, PhDa,*

a The National Heart and Lung Institute Imperial College of Science, Technology and Medicine, Department of Cardiothoracic Surgery, St. Mary's Hospital, London, United Kingdom

* Address reprint requests to Dr Anthanasiou, Robotic and Minimally Invasive Cardiothoracic Surgery, 70 St Olaf's Rd, Fulham, London SW6 7DN, UK
tathan5253{at}aol.com


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Conclusion
 References
 
Virtual bronchoscopy has emerged over the past decade as a potentially complementary investigation to conventional bronchoscopy in the diagnosis, grading, and monitoring of pulmonary disease. A meta-analysis reporting on the use of virtual bronchoscopy has not yet been performed. The primary aim of this study is to evaluate its diagnostic accuracy compared to the gold standard investigation of conventional bronchoscopy (fiberoptic or rigid). Quantitative data synthesis included the calculation of independent sensitivity and specificity, construction of summary receiver operating characteristic curves, pooled analysis, and sensitivity analysis. Seventeen studies were identified comprising 459 patients. The calculated pooled sensitivity was 84% (95% CI, 78% to 89%), specificity 75% (95% CI, 62% to 85%) and area under the curve was 0.92, which shows good diagnostic performance. Meta-analysis confirms virtual bronchoscopy is very discriminating in the evaluation of patients with significant airway stenosis that is due to a wide spectrum of pathologic conditions. It can potentially have a beneficial role in selected thoracic patients (with bronchoesophageal fistulas, postlung transplantation, anastomoses, and suspected foreign body aspiration).


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Conclusion
 References
 
Virtual bronchoscopy has emerged over the past decade as a potentially complementary investigation to conventional bronchoscopy in the diagnosis, grading, and monitoring of pulmonary disease [1]. Virtual bronchoscopy (VB) is the conversion of anatomic images generated by helical computer tomography (CT) into three-dimensional images analogous to conventional bronchoscopy (CB) [2, 3]. Despite advances in virtual simulation, it has been regarded as an unproven investigation, to be used when CB is poorly tolerated.

A number of studies have evaluated the accuracy of VB in diagnosing suspected tracheobronchial pathologies [4, 5]. However, patient characteristics and imaging methods have varied. We believed there was a need to meta-analyze these studies with the following aims:

  1. To calculate an overall estimation of VB's diagnostic accuracy.
  2. To assess diagnostic accuracy dependence on study design, patient characteristics (underlying disease), anatomic characteristics (stenosis grading), and test limitations (technical limitations in image production).
To achieve these aims, we compared VB with the gold standard investigation of CB (fiberoptic [FOB] or rigid [RB] bronchoscopy.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Conclusion
 References
 
Literature Search
A literature search (MEDLINE) for studies reporting on VB, published between 1965 and 2003 (current at December 28, 2003), was performed. The following searching keywords were used: "virtual bronchoscopy," "bronchoscopy/*methods and comparative studies" and "three dimensional computer tomography and bronchi" limited to "human subjects." Articles were also identified using the function "related articles" in PubMed. No language restrictions were made.

Eligibility Criteria and Data Extraction
We considered all studies that reported a direct comparison of CB findings with VB or three-dimensional CT (3-DCT) findings. Studies that reported only on axial CT, or adjunctive VB with CB, were excluded. There was no limit on lesion type in the analysis of overall VB efficacy compared with CB. For summary receiver operating characteristic (SROC) analysis, both sensitivity and specificity are required. Thus, studies that compared only known positive CB results with VB or 3-DCT were included in the general analysis and discussion, but were excluded from SROC analysis.

We extracted the data independently and, in the case of discrepancy, a decision was made by consensus. Care was taken to avoid including studies that reported on the same patient populations. Extracted information included author, date, design, patient age, gender, airway visualization, technical limitations, study endpoints, diagnostic confirmation (biopsy, surgery, no confirmation), and verification bias. This refers to nonconfirmation of negative test results with the reference standard, which occurs when the reference standard is invasive or otherwise undesirable [6]. In this analysis, this constituted failure to compare VB findings with CB, or to confirm histologically diagnoses of malignancy.

Where possible, two-by-two contingency tables were created for the endpoint of correct patient diagnosis. True-positive findings (TPF) were defined as the same abnormal diagnosis on both CB and VB. True-negative findings (TNF) were defined as a normal result on both CB and VB. False-positive findings (FPF) were defined as examinations with abnormal results on VB but normal with CB. False-negative findings (FNF) were an abnormal CB diagnosis but a noncorresponding VB diagnosis.

Endpoints and Definitions
The primary endpoint in our analysis was "correct patient diagnosis" on VB compared with CB. As secondary endpoints we considered lesion pathology (malignant vs benign) and degree of stenosis. The definition of airway stenosis varied between studies, thus multiple thresholds were compared. Data were analyzed by using a stenosis definition as luminal narrowing of at least 25%, and for 50% lumen diameter narrowing.

The effect of collimation interval and study design on the accuracy of VB was examined. Small collimation is known to reduce image artifact. Studies using at most 3-mm collimation were analyzed for better accuracy. Prospective trials were also analyzed separately to examine the effect of study design.

Statistical Analysis
For all study subgroups that had control and trial groups, the number of TPF, TNF, FPF, and FNF were calculated. Overall pooled sensitivity and specificity, with 95% confidence intervals (CI), were estimated. In addition, SROC analysis was performed to examine the interaction between sensitivity and specificity, and to quantify test performance using area under the curve (AUC), diagnostic odds ratio (DOR) and Q value [7–10].

Analysis was conducted using SPSS Version 11.0 for Windows (SPSS Inc, Chicago, IL) and Meta-Test Software, Version 0.9 (developed by Joseph Lau).

This study was undertaken in accordance with previously reported guidelines for meta-analyses that evaluate diagnostic tests [6, 11].


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Conclusion
 References
 
Eligible Studies
We identified 345 articles by using search keywords ("virtual bronchoscopy," 105 articles; "bronchoscopy/*methods and comparative studies," 192 articles; and "three dimensional computer tomography and bronchi," 48 articles). An examination of "related articles" in MEDLINE added five more studies to the abstract list, resulting in the full-text retrieval of 29 studies [2, 4, 5, 12–37]. Two studies were conducted by the same team [2, 4]; the second report [2] was included in the meta-analysis as this was more recent and encompassing, with more patients included. In one case, it was not possible to determine whether two series by the same authors [12, 13] overlapped, so only the most recent paper was used [12]. This left 27 studies in which VB and CB findings were analyzed (Table 1). Two studies by the same institution investigated different patient groups and thus both were included [23, 24].


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  		Table 1. Study Characteristics

 
Description of Gold Standard for Comparison
Twenty studies used FOB as the gold standard, two used RB, and five studies did not specify between the two methods. We included FOB as a variable in subgroup analysis. Eleven studies reported adequate data [2, 16, 19, 21, 22, 27, 29, 33–36] and underwent SROC analysis. No study compared VB to RB with video assistance.

Verification Bias
Every patient underwent both the test (VB) and the reference standard (CB); thus, the primary endpoint verification bias is zero. All seven studies that examined only malignant lesions verified diagnosis by biopsy [23, 24, 27], surgery [22] or either one [2, 16, 33]. Thus the verification bias for this subgroup, which relies upon histology as well as the reference standard, is also zero.

Technical Characteristics
Throughout the analysis, 3-D technical methods vary. This affects image artifact, quality, and accuracy. The advances in 3-D simulation since the first of the studies was published [19] means that artifact has been reduced. Tube current, voltage, pitch, and collimation were extracted and are presented in Table 2.


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  		Table 2. Technical Parameters Used in the Individual Studies

 
Statistical Data Synthesis and SROC Results
Sensitivity analysis of pooled sensitivity and specificity, diagnostic odds ratio (DOR), Q value (a measure of data heterogeneity), and AUC are presented in Table 3. Slope and intercept values represent the logarithm curve that was used to calculate SROC.


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  		Table 3. Sensitivity Analysis

 
Individual study results for the primary endpoint are presented in Table 4. From the 17 studies [2, 12, 15–17, 19–24, 27, 29, 33–35] that calculated sensitivity and specificity for this endpoint, pooled sensitivity of 84% (95% CI, 78% to 89%) and specificity of 75% (95% CI, 62% to 85%) were obtained. Heterogeneity of sensitivity and specificity results prevailed across the studies (Fig 1), which enabled SROC analysis. Calculated DOR was 26.84 and AUC was 0.92 (Fig 2A and 2B) which show good diagnostic performance.


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  		Table 4. Individual Study Results for Primary Endpoint of Patient Diagnosis Comparing VB to CB (Gold Standard)

 


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  		Fig 1. Heterogeneity of sensitivity (left) and specificity (right) results across the studies (overall dataset).

 


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  		Fig 2. Summary receiver operating characteristic analysis for the overall dataset. Crosses refer to pooled sensitivity and specificity values, shaded areas refer to 95% confidence intervals for these pooled values. Numerals on the graph were allocated by the software to represent the studies used for the analysis. (A) Calculated diagnostic odds ratio was 26.84. (B) Area under the curve was 0.92, which shows good overall diagnostic performance of virtual bronchoscopy. (FPR = false positive ratio; TPR = true positive rate.)

 
There were 250 patients in 8 studies of malignancy [2, 12, 16, 22–24, 33, 34]. SROC analysis showed pooled sensitivity of 86%, specificity of 77%, and AUC of 0.93 (Fig 3).



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  		Fig 3. Summary receiver operating characteristic analysis for patients with malignancy. The analysis showed pooled sensitivity of 86%, specificity of 77% and area under the curve of 0.93. Numerals across the figure were allocated by the software to represent studies used during the analysis. The crosses refer to the pooled sensitivity (top) and specificity (bottom), with the shaded areas representing the 95% confidence intervals of these pooled values.

 
Specificity was homogeneous for the malignancy, fiberoptic, and stenosis greater than 50% subgroups, leading to the production of a partial AUC. These were extrapolated by Meta-Test to calculate the equivalent AUC over the entire specificity range (0–1). Each resulting AUC value is close to 1 (Table 3). SROC analysis was not possible for the stenosis threshold of 25%, as all specificity values in the studies were 100%.

Pooled analysis for subgroups of prospective trials (AUC, 0.91), stenosis of at least 50% (AUC, 0.99) and FOB (AUC, 0.92) are also summarized in Table 3.

False-Positive Findings (FPF)
Overall, the studies reported 51 FPF. Mucous secretions caused 9 (18%), and artifact caused at least 5 (10%). Lee [20] reported 20 FPF in 30 patients with tuberculosis and bronchogenic carcinoma; however, these include FPF on axial CT. Finkelstein and colleagues [2] noted no FPF within the view of CB. Of note, 11 additional lesions found during VB were beyond the scope of CB; 6 were surgically assessed and were found to be true lesions. Salvolini and colleagues [34] also noted a case of an additional lesion that was later confirmed by surgery. Thus, VB had advantages in these cases, which were true positives not revealed by CB. Overall, there did not appear to be a particular patient characteristic which increased the risk of FPF.

False-Negative Findings (FNF)
The 27 studies reported 62 FNF. These included 5 mucosal lesions [2], and 14 (23%) mild stenoses, 2 moderate stenoses, and 6 peripheral stenoses. VB missed 17 (28%) cases [27, 29] of dynamic airway lesions. Lee [20] reported 22 cases of missed stenosis; however, stenosis definition was undefined. In summary, dynamic and mild peripheral stenotic lesions are the most likely lesions to be missed, regardless of other patient characteristics.

Lesion Severity Analysis
Eleven studies [2, 5, 12, 14, 16–18, 22, 23, 27, 35] reported diagnostic accuracy based on severity. Most studies define severe stenoses as 50% luminal narrowing. Of the 153 mild-to-moderate stenotic lesions on FOB, 138 were diagnosed by VB (90.1%), and all 119 severe stenoses on FOB were seen on VB (100%). Three studies [16, 24, 27] reported 6 cases of severity overestimation, and 11 of underestimation. All severe stenoses were correctly located and graded. This suggests that diagnosis of severe lesions is highly sensitive, irrespective of patient characteristics.

Airway Visualization
Eight studies evaluated bronchial visualization [2, 13, 16, 17, 23, 25, 28, 34]. Of 28 subsegmental bronchi evaluated, none are visualized on VB, compared with 14 (50%) on CB [28]. Although subsegmental bronchi are seen in other studies [5, 12, 23], quality is unmentioned. VB visualized 71% (314/ 442) of segmental bronchi [28, 34] compared with CB (86%) [28]. Across the eight studies, 79% (1072/1358) of the airways are seen on VB. VB visualization was superior to CB only in poststenotic airways when the bronchoscope was unable to pass occlusions.

Pathologies Investigated
The pathologies investigated by VB are presented in Table 5. VB was employed for a wide range of pathologic conditions, most notably malignancy (63%). Of interest are patients with bronchoesophageal fistulas, postlung transplantation, and foreign body aspiration.


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  		Table 5. Patient Pathology

 
Seventeen patients had bronchoesophageal fistula [17, 18, 20, 30, 34, 36]. All cases were correctly diagnosed by VB, sometimes using retrospective views [20]. One case was diagnosed by VB and later surgically confirmed, despite a normal CB [34].

There were 27 patients postlung transplantation [14, 19, 21, 29, 35, 37] who were evaluated for anastomotic abnormalities. VB accurately showed 2 cases of anastomotic infection and 2 cases of dehiscence, but overdiagnosed mucosal abnormalities in normal anastomotic sites [19, 21] and failed to diagnose 2 cases of stenosis [14, 35]. VB performs well in evaluating anastomotic sites, but cannot match CB accuracy.

Haliloglu [15] examines VB accuracy in pediatric foreign body aspiration. Twenty-three children with suspected foreign body aspiration underwent VB before RB, with 100% sensitivity and specificity.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Conclusion
 References
 
Over the last decade, many single-center studies have compared VB to CB by using different diagnostic thresholds and technological limitations. Meta-analysis of these studies is the next logical step in order to calculate the accuracy of VB in evaluating suspected airway disease secondary to respiratory pathologies. Each study included in this meta-analysis showed good sensitivity for VB, suggesting that this new diagnostic tool has a significant role in the diagnosis of several types of respiratory pathology.

The results of our analysis on the primary endpoint of "correct patient diagnosis" when comparing VB with CB are encouraging. They show a pooled sensitivity of 84%, with a specificity of 75% and an AUC of 0.92, suggesting an acceptable diagnostic accuracy. The results of this meta-analysis confirm VB as a valid diagnostic tool, suggesting that it can be used as a complementary investigation in the diagnosis and management of tracheobronchial airway disease.

VB has a similar diagnostic performance in both malignant and benign disease. It has a limited role as a screening tool for bronchogenic cancer because it is not able to visualize premalignant mucosal conditions (erythema, color, irregularity, friability). Further refinements are required in acquisition capability and image display techniques for it to be able to evaluate mucosal surface changes [4]. VB does, however, have the potential to aid transbronchial biopsy by localizing extrabronchial masses [38, 39]. Cross-referencing with axial CT or multiplanar reconstructions offers extraluminal information, showing a virtual "bronchus sign." Although VB cannot replace CB in biopsy, there is some evidence that preliminary VB may be useful in transbronchial biopsy [38]. At present, evidence in the literature is not sufficient to define the role of VB as a staging tool in lung cancer.

Our meta-analysis shows the very good discriminatory ability of VB in localizing and grading stenotic lesions, the clinical significance of which varies with severity. A low diagnostic threshold (25% of lumen diameter) identifies many lesions of subclinical importance, which is useful in the monitoring and staging of disease. Stenoses causing 50% luminal narrowing are more likely to warrant intervention; therefore, the performance of VB in these situations is also of interest. In patients with dynamic airway disease (tracheomalacia, impaired true vocal cord mobility, and innominate artery compression), its performance is less impressive, with less than 50% sensitivity [27, 29, 37]. This result in not surprising, as VB uses static imaging.

Study design can affect diagnostic accuracy of a test [40], with prospective studies less likely to be biased from previous examination findings, and the patients not having a confirmed diagnosis. Our sensitivity analysis suggests that the prospective studies included in this paper showed no significant differences in the calculated diagnostic accuracy of VB. An AUC of 0.91 is a significant result, which suggests that VB performs well when prospectively evaluated.

From the technical aspect, collimation of 3 mm or less has become routine. There is no calculated improvement using this standard compared with an overall standard of collimation, but also no drop in performance. This suggests that the artifact incurred from high collimation is unlikely to affect overall diagnostic performance of VB. Specific artifacts have been previously reported; however, few incidences have occurred where this has resulted in the images being rendered unusable. It is important to note that little difference exists in the current, voltage, or pitch used in the studies.

CB is the gold standard in endobronchial evaluation of the tracheobronchial tree. The main types are FOB and RB. Both pass an endoscope into the tracheobronchial system and directly visualize the mucosa. CB uses direct mucosal vision to diagnose and monitor airway disease and to take histologic samples. Its drawbacks are patient sedation, invasiveness, operator-dependence, poor postocclusion visualization, and variable visualization of small airways with different sized endoscopes. RB requires general anesthesia, but can traverse strictures and manage secretions and bleeding. This gives RB an advantage over FOB and VB in the presence of thick secretions or massive hemoptysis. Aspects of CB that could be improved are visualization, invasiveness, and reproducibility.

We would like to emphasize that evaluation of strictures can be done with axial CT, which is clinically valuable and less costly than VB. In a previous study that evaluated bronchial anastomoses in lung transplant recipient patients, it was demonstrated that although VB was more accurate than axial CT with regards to presence, severity, and length of stenosis, no statistically significant difference was achieved [21]. Further research is required to compare the two modalities in different types of pathology.

VB has both advantages and disadvantages. It is operator-independent, noninvasive, reproducible, and able to retrogradely visualize poststenotic airways. Real-time image evaluation allows a viewer-format analogous to CB. Although the overall visualization of the airways is good, subsegmental bronchus visualization is inferior to CB [2, 16, 17, 23, 25, 28]. VB is susceptible to motion artifact, requires breath holding, gives unreliable mucosal and dynamic disease diagnosis, necessitates radiation, and cannot provide samples for histology. The value of VB for is reduced for dynamic, mucosal, and peripheral airways lesions compared to fixed central stenotic lesions, where accuracy is high. The balance of these advantages and disadvantages has not been fully addressed.

In posttransplantation anastomoses and bronchoesophageal fistula, results are encouraging but numbers are small [14, 17, 18–21, 29, 35–37]. The few incidences of incorrect diagnosis show that VB cannot replace CB for these groups. One of the dangers of invasive bronchoscopy in these patients is the risk of worsening tracheal defects and directly harming the patient. VB eliminates this risk at the expense of diagnostic accuracy. In our opinion, VB cannot replace CB in this subgroup and further research is required.

The study by Haliloglu and colleagues [15] suggests that rigid bronchoscopy is not always necessary for the diagnosis of foreign body aspiration in young children. It is however, the only study to date on the subject, suggesting the need for further research. Another pediatric study by Lam and colleagues [36] showed that VB accurately locates tracheoesophageal fistulas and directs treatment based on the gap between upper and lower esophageal pouches. VB can also diagnose congenital bronchial origin abnormalities. Pediatric VB studies [15, 27, 29, 36, 37] are occasionally compromised by the inability of infants to suspend respiration and by their smaller airways.

Patients with suspected airway disease routinely undergo bronchoscopy and axial CT. Replacing CB with VB would reduce the number of investigations with minimal added radiation exposure. The cost-effectiveness of implementing routine VB has not yet been investigated.

VB can be a training tool for anesthetists, physicians, and thoracic surgeons; with simulated training, the skills and knowledge of trainees can be objectively assessed and improved [41–44]. There is a case report on the role of VB in the diagnosis of tracheal rupture [45], which is otherwise unreported in the literature.

Target patients for VB include those with unexplained hemoptysis, suspected endobronchial lesions, and confirmed stenosis for planning treatment and follow-up, especially when stenting, brachytherapy, or laser therapy is indicated. VB can also detect congenital airway abnormalities, postinfectious or postoperative airway fistula and dehiscence, and assess bronchiectasis and small airway disease. VB indications for the thoracic surgeon include measuring airway lumen before stenting, segmentectomy, or sleeve resections, and in infiltrative esophageal carcinoma [24].

Limitations of Our Study
A problem with CB, which incorporates FOB and RB, as a gold standard is that it cannot visualize postoccluded airways, which are visualized on VB. Any additional information on VB is thus unable to be corroborated. Video-assisted RB has not been compared with VB in the literature.

Extrapolation of partial AUC by the Meta-Test software loses accuracy in very homogeneous data. Analysis was performed on high specificity values, which suggests that good specificity is associated with good sensitivity. It does not, however, evaluate the sensitivity of VB when specificity is low. Small patient numbers mean that a different result could alter the sensitivity or specificity of a study, and produce a different AUC. This problem can be overcome by performing larger multi-center, randomized controlled trials on VB.

Meta-analyses gather available literature and summarize the results. Publication bias means that positive results may be more likely to be published. Meta-analysis therefore may be biased towards a positive result because of the tendency for positive results to be published. There may also be possible error in pooling methods, comparison of different histology methods, or patient classifications.


   Conclusion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Conclusion
References
 
This meta-analysis confirms good accuracy of virtual bronchoscopy in the overall diagnosis in patients with suspected airways lesions. It shows excellent accuracy in the diagnosis of severe stenotic lesions, and high accuracy in lower grade stenoses. The accuracy of VB in the diagnosis of obstructive lesions or endoluminal disease in the face of malignancy is excellent. However, VB is not reliable in diagnosis of dynamic airway or mucosal lesions. A small collimation interval does not appear to markedly improve the accuracy of VB, despite increased image artifact with large collimation. Small-group data show promising results in patients with posttransplantation anastomoses, foreign body aspiration, and fistulas. VB is technically reliable and consistently shows adequate airways visualization and clinically insignificant image artifact. It is noninvasive, operator-independent, fast, reproducible, and can be drawn from CT images, which are often clinically indicated. It cannot facilitate therapeutic maneuvers, provides no direct mucosal view, and cannot evaluate dynamic airways disease. The clinical use of VB is expanding with more and more centers moving from experimental to clinical applications. In conclusion, further research is therefore required to delineate the uses of VB as an adjunct to conventional bronchoscopy in the setting of suspected airways disease.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Conclusion
 References
 

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