Overview of airway involvement in tuberculosis

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bs_bs_banner Journal of Medical Imaging and Radiation Oncology 57 (2013) 576 581 RADIOLOGY PICTORIAL ESSAY Overview of airway involvement in tuberculosis Arundeep Arora, Ashu Seith Bhalla, Manisha Jana and Raju Sharma Department of Radiodiagnosis, All India Institute of Medical Sciences, New Delhi, India A Arora MD; AS Bhalla MD; M Jana MD, FRCR; R Sharma MD. Correspondence Dr Ashu Seith Bhalla, Department of Radiodiagnosis, All India Institute of Medical Sciences, Room No. 69, New Delhi 29, India. Email: ashubhalla1@yahoo.com Conflict of interest: The authors have nothing to disclose. Summary Pulmonary tuberculosis is a ubiquitous infection and a re-emerging medical and socioeconomic problem resulting in increasing mortality and morbidity, especially in Asian countries. We aim to review the spectrum of imaging findings in airway involvement in tuberculosis through characteristic radiological images and to assess the role of computed tomography and imageguided interventions in the diagnosis and management of pulmonary tuberculosis. Key words: airway; bronchial stricture; tuberculosis. Submitted 9 July 2012; accepted 14 September 2012. doi:10.1111/1754-9485.12017 Introduction Tuberculosis (TB) is second only to human immunodeficiency virus (HIV)/acquired immunodeficiency as the greatest killer worldwide due to a single infectious agent. In 2010, 8.8 million people fell ill with TB and 1.4 million died from TB. Over 95% of TB deaths occur in low- and middle-income countries. TB is a leading killer of people living with HIV, causing one-quarter of all deaths. 1 With timely detection and adequate treatment, people with the disease quickly become non-infectious and eventually cured. The treatment challenges are compounded by the emergence of multi-drug-resistant and extensively drug-resistant TB and HIV-associated TB. TB is an airborne infectious disease caused by Mycobacterium tuberculosis with respiratory system being the most commonly involved. 2 The involvement of airways is much less common than the lung parenchyma. The various forms of airway involvement in acute and chronic diseases have been summarised in Table 1. Radiological findings in acute airway involvement Tracheobronchitis The common CT findings of airway TB in the acute stage are smooth or irregular wall thickening (Fig. 1) causing luminal narrowing, with long segmental involvement of the bronchi. 3,4 Other findings may include endotracheal ulcerated polypoid mass due to granulomatous inflammation or bronchial narrowing with peribronchial cuff of soft tissue. 5 There is a distinct propensity to involve the distal trachea, with associated involvement of the main bronchi and the presence of parenchymal TB in most patients, suggesting that the pathological mechanism is implantation of acid-fast bacilli and lymphatic submucosal spread of the infection in the trachea and main bronchi from parenchymal lesions. 4 Extrinsic compression by lymph node Lymph node involvement is mostly unilateral, with the hilar and paratracheal regions being most commonly involved, followed by the subcarinal nodes. 6 Collapse is generally visible on the chest radiograph (Fig. 2a) if external compression of the lumen is complete or if lymph nodes have herniated into the airway (Fig. 3). Segmental or lobar collapse (Fig. 2b) with obstructive pneumonia, hyperinflation, cavities or mucoid impaction distal to the obstructed bronchus may also be seen on CT scans. 5 The bronchus intermedius is commonly affected with complete airway obstruction, resulting in collapse of the right middle and right lower lobes. 7 Ball-valve effect results in unilateral hyperinflation because of the fact that air is trapped by the check valve effect of an incompletely obstructed airway. The involved lung or lobe is enlarged, has attenuated vascular markings and can herniate across the midline if severe air trapping is present. 8 576 Journal of Medical Imaging and Radiation Oncology 2013 The Royal Australian and New Zealand College of Radiologists

Airway involvement in tuberculosis Table 1. Spectrum of airway involvement in acute and chronic form of tuberculosis Fig. 1. Acute on chronic involvement of right lower lobe bronchus. Lung window of CT thorax reveals irregular walls of right lower lobe bronchus (black arrow, a and b) and multiple tree-in-bud acinar nodules (white arrow, a) secondary to endobronchial spread of infection. Acute Tracheal involvement tracheitis tracheal compression by lymph nodes Bronchial involvement bronchitis compression by lymph nodes node-bronchial fistula Small airway involvement bronchiolitis Chronic/sequelae Tracheal stenosis Bronchial involvement bronchiectasis bronchostenosis broncholithiasis secondary amyloidosis Bronchiolitis Bronchogenic dissemination is the most common means of spread in the progressive primary form of TB. In the series by Im et al., 9 centrilobular nodules or branching linear structure 2 4 mm in diameter on CT scans was the earliest CT findings of bronchogenic dissemination. Centrilobular lesions consisted of solid caseation material within or around the terminal or respiratory bronchioles. Multiple branching linear structures of similar calibre that originate from a single stalk, the tree-in-bud appearance (Fig. 1a), are commonly seen in patients with extensive bronchogenic spread, the stalk thought to represent a lesion that affects the last-order bronchus within the secondary pulmonary lobule and the bud thought to represent Fig. 2. Extrinsic compression by tubercular lymph node. Chest radiograph (a) and chest CT (b) showing right lower lobe collapse with mediastinal window (c) showing partly calcified lymph node compressing the right lower lobe bronchus. Fig. 3. Lymph node eroding into main bronchus. Radiograph (a) showing right lower lobe consolidation. Computed tomography section showing erosion of peribronchial lymph node into the lumen (arrow, b). Lung window showing distal patchy consolidation (arrows, c). Fig. 4. Bronchostenosis. Computed tomography thorax reveals diffuse narrowing of the lingular lobe bronchus (white arrow, a) and segmental collapse in distal lung parenchyma (white arrow, b). Coronal minip projection showing multiple areas of bronchostenosis (white arrows, c) involving left upper lobe and lingular lobe. Journal of Medical Imaging and Radiation Oncology 2013 The Royal Australian and New Zealand College of Radiologists 577

A Arora et al. Fig. 5. Bronchiectasis. Chest radiograph (a) with bronchiectasis in bilateral lung fields. Computed tomography image (b) showing cystic bronchiectasis in both lungs. lesions in the bronchioles and alveolar ducts. These branching opacities are considered a sure marker of the activity of the disease. Radiological findings in chronic airway involvement Tracheal stenosis Endotracheal TB is a relatively uncommon (about 4%), localised form of endobronchial TB, which may cause acute respiratory distress. 10 Only 150 cases have been reported worldwide. 11 The clinical manifestations of endobronchial TB are varied, which include chronic and productive cough, barking cough, chest pain, haemoptysis, generalised weakness, dyspnoea and fever, and hence, the diagnosis needs a high index of suspicion. Chest radiographs may be normal, and multiplanar CT and/or bronchoscopy are needed for the diagnostic confirmation. Surgical resection and bronchoplastic reconstruction have long been regarded the standard treatment. 12 Bronchostenosis Smooth narrowing of airways resistant to medical treatment with minimal wall thickening has been observed in patients with fibrotic disease. The left main bronchus is more frequently involved in fibrotic disease, whereas active disease involves equally both bronchi. 3,4 Bronchial stenosis may cause diffuse or segmental narrowing of main or segmental bronchi (Fig. 4). Multiplanar and Fig. 6. Broncholith. Computed tomography thorax with calcified density in right main bronchus (arrow, a) with bronchial wall thickening causing complete occlusion of bronchial lumen with central consolidation (arrow, b). Note that the gas density posterior to the broncholith is the oesophagus. three-dimensional (3D) images provide a valuable insight into global understanding of tracheobronchial disease, particularly for evaluating focal stenosis of the airways. Especially useful in evaluating the longitudinal extent of bronchial lesions, multiplanar and 3D images are indispensable to serve as a virtual road map for bronchoscopy, for surgical planning and for follow-up evaluation of treatment response. Compared with axial images only, 3D reformatted images allow us to predict if a given lesion is endobronchial, submucosal or peribronchial, which has important therapeutic implications. 13 Once endobronchial TB has progressed to the advanced stage, defined as causing more than 25% obstruction of the bronchial lumen as demonstrated by CT or bronchoscopy, local steroid application for treating the stenosis is not effective. Conversely, local treatment is useful for mild or superficial mucosal inflammatory lesions, causing less than 25% obstruction, which is better demonstrated with bronchoscopy than CT. 14 Bronchiectasis Bronchiectasis as a sequel of reactivation TB is commonly found in the apical or posterior segments of the upper lobes. Bronchiectasis most often consists of a combination of traction bronchiectasis and fibrosis. The mechanism for its causation includes destruction and fibrosis of the lung parenchyma, resulting in retraction and irreversible bronchial dilatation. In addition, proximal bronchial stenosis and/or broncholithiasis 5 may secondarily result in distal obstructive pneumonitis and bronchiectasis (Fig. 5). An additional mechanism may be due to the endobronchial spread of infection and Fig. 7. Localised bronchodilation due to broncholith in right middle lobe. Computed tomography thorax reveals dilation of the right middle lobe distal bronchus (arrows, a and c) and broncholithiasis (arrow, b). 578 Journal of Medical Imaging and Radiation Oncology 2013 The Royal Australian and New Zealand College of Radiologists

Airway involvement in tuberculosis Fig. 8. Bronchocoele. Computed tomography thorax shows multiple lymph nodes with central necrosis (arrows, a). Low density filling in and occluding the left lower bronchus (arrows, b). subsequent damage to bronchial walls as bronchiectasis is often seen in areas without surrounding fibrosis or proximal stenosis. Broncholithiasis Broncholithiasis is characterised by calcified peribronchial lymph nodes that either erode into or cause major distortion of an adjacent bronchus, with a right-sided predominance 15 (Fig. 6). Findings of calcium near an area of pulmonary collapse (Fig. 7) should arouse suspicion of a broncholithiasis. 15 Segmental collapse, which overinflation with air trapping well demonstrated on expiratory slices, bronchiectasis or obstructive bronchocoele (Fig. 8), may also be seen. 5,16 Clinical signs of haemoptysis or pneumonitis may be the presenting symptom. Fig. 9. Amyloidosis of tracheobronchial wall. Axial CT image showing smooth wall thickening of the trachea in a patient with previously treated tuberculosis. Biopsy showed amyloidosis. Secondary amyloidosis Amyloidosis is characterised by the deposition of abnormal proteinaceous material in extracellular tissue. It may be idiopathic or seen as sequelae to chronic inflammatory, hereditary or neoplastic pathogeneses. It can occur in three forms: diffuse interstitial deposits, single or multiple pulmonary nodules and, most commonly, submucosal tracheobronchial deposits. 17 The classic radiographic appearance of tracheobronchial disease is Fig. 10. Fluoroscopic balloon dilation of bronchus intermedius stricture. Fluoroscopic spot images reveal measurement of the stricture segment (arrow, a), CT minip image demonstrating the stricture better (arrow, b), passage of balloon over metallic guide wire (arrow, c) and dilation of stricture (arrow, d). Fig. 11. Computed tomography in bronchial stricture for pre-procedure planning. Coronal minip (a), coronal multiplanar reformat (b) and virtual bronchoscopy (c) showing severe luminal narrowing of left main bronchus (arrows). Journal of Medical Imaging and Radiation Oncology 2013 The Royal Australian and New Zealand College of Radiologists 579

A Arora et al. Fig. 12. Fluoroscopic balloon dilation of left main bronchus tight fibrous stricture, same patient as in Fig. 10. Fluoroscopic spot images reveal passage of balloon over metallic guide wire (arrow, a) and dilation of stricture (arrow, b). Post-dilation minip images reveal partial dilation of the stricture (arrow, c and d). The patient improved significantly after three dilatation sessions. nodular and irregular mural thickening (Fig. 9) with narrowing of the tracheal lumen. 18 Lobar or segmental collapse may be seen with endobronchial obstruction due to amyloid deposition. Less often, a raised, tumour-like mass of amyloid material (amyloidoma) can be seen and may be mistaken for a neoplasm. 19 Although bronchoscopic biopsy is the mainstay of diagnosis, caution is advised as there is increased risk of bleeding because the amyloid deposits within the vascular wall may inhibit hemostasis. 20 Endobronchial balloon dilatation High-pressure balloon dilatation has now become a wellaccepted treatment for non-neoplastic tracheobronchial strictures. Advantages of endobronchial treatment include avoidance of thoracotomy, short hospital stay and better recovery. Moreover, repeat procedures may be performed in case of treatment failure. Pre-procedure evaluation includes CT with multiplanar reformations (Figs 10,11) for proper estimation of stricture length and fibre optic bronchoscopy to differentiate retained secretion from stenosis. However, such strictures can be fibrotic and tight (Fig. 12), which have resulted in reports of low primary and secondary patency rates (24% and 20%, respectively) after high-pressure balloon dilatation. 21 Although temporary stent placement is safe and effective in selected patients, stent placement in benign tracheobronchial strictures may have associated problems, such as tissue hyperplasia and stent migration, and can make surgery impossible. 22 Conclusion TB still poses a major challenge among infectious diseases and causes significant morbidity in its acute form and through sequelae. Airway involvement, though uncommon, when present can worsen the severity of the symptoms as well as long-term outcome of the patient. Computed tomography, with its 3D imaging capabilities, is a very effective diagnostic modality for illustrating the nature and extent of airway involvement. Balloon dilation or stenting provide an effective therapeutic option and may obviate the need for surgery for airway strictures. References 1. World Health Organization. Fact sheet no. 104. Tuberculosis. 2012. [Cited 31 Aug 2012.] Available from URL: http://www.who.int/mediacentre/ factsheets/fs104. WHO Website. 2. Jeong YJ, Lee KS. Pulmonary tuberculosis: up-todate imaging and management. AJR 2008; 191: 834 44. 3. Moon WK, Im JG, Yeon KM, Han MC. Tuberculosis of the central airways: CT findings of active and fibrotic disease. AJR 1997; 169: 649 53. 4. Kim Y, Lee KS, Yoon JH et al. Tuberculosis of the trachea and main bronchi: CT findings in 17 patients. AJR 1997; 168: 1051 6. 5. Beigelman C, Sellami D, Brauner M. CT of parenchymal and bronchial tuberculosis. Eur Radiol 2000; 10: 699 709. 6. Andreu J, Cáceres J, Pallisa E, Martinez-Rodriguez M. Radiological manifestations of pulmonary tuberculosis. Eur J Radiol 2004; 51: 139 49. 7. Goussard P, Gie R. Airway involvement in pulmonary tuberculosis. Paediatr Respir Rev 2007; 8: 118 23. 8. Goussard P, Gie R. Airway involvement in pulmonary tuberculosis. S Afr Med J 2007; 97: 986 8. 9. Im J-G, Itoh H, Shim Y-S et al. Pulmonary tuberculosis: CT findings, early active disease and sequential change with anti-tuberculous therapy. Radiology 1993; 186: 653 60. 10. Morrone N, Abe N. Bronchoscopic findings in patients with pulmonary tuberculosis. J Bronchol 2007; 14: 15 8. 11. Belhassen S, Boudaya MS, Ayadi A et al. Tuberculosis of the trachea. Thorac Surg 2006; 82: 1900 1. 12. Hsu H-S, Hsu W-H, Huang B-S, Huang M-H. Surgical treatment of endobronchial tuberculosis. Scand Cardiovasc J 1997; 31: 79 82. 13. Lee KS, Yoon JH, Kim TK, Kim JS, Chung MP, Kwon OJ. Evaluation of tracheobronchial disease with helical CT with multiplanar and three-dimensional reconstruction: correlation with bronchoscopy. Radiographics 1997; 17: 555 67. 14. Tetikkurt C, Tetikkurt S, Bayar N, Ozdemir I. Endobronchial involvement in miliary tuberculosis. Pneumon 2010; 23: 135 40. 15. Conces DJ, Tarver RD, Vix VA. Broncholithiasis: CT features in 15 patients. AJR 1991; 157: 249 53. 580 Journal of Medical Imaging and Radiation Oncology 2013 The Royal Australian and New Zealand College of Radiologists

Airway involvement in tuberculosis 16. Leung AN. Pulmonary tuberculosis: the essentials. Radiology 1999; 210: 307 22. 17. Rubinow A, Celli BR, Cohen AS, Rigden BG, Brody JS. Localized amyloidosis of the lower respiratory tract. Am Rev Respir Dis 1978; 118: 603 11. 18. Kwong JS, Mueller NL, Miller RR. Diseases of the trachea and main-stem bronchi: correlation of CT with pathologic findings. Radiographics 1992; 12: 645 57. 19. Utz JP, Swenswn SJ, Gertz MA. Pulmonary amyloidosis: the Mayo clinic experience from 1980 to 1993. Ann Intern Med 1996; 124: 407 13. 20. Prince JS, Duhamel DR, Levin DL, Harrell JH, Friedman PJ. Nonneoplastic lesions of the tracheobronchial wall: radiologic findings with bronchoscopic correlation. Radiographics 2002; 22: S215 30. 21. Lee KH, Ko GY, Song HY, Shim TS, Kim WS. Benign tracheobronchial stenoses: long-term clinical experience with balloon dilation. J Vasc Interv Radiol 2002; 13: 909 14. 22. Kim JH, Shin JH, Song HY, Shim TS, Yoon CJ, Ko GY. Benign tracheobronchial strictures: long term results and factors affecting airway patency after temporary stent placement. AJR 2007; 188: 1033 8. Journal of Medical Imaging and Radiation Oncology 2013 The Royal Australian and New Zealand College of Radiologists 581