REVIEW ARTICLE

Endobronchial Tuberculosis
Surender Kashyap, Prasanta Raghab Mohapatra and Varinder Saini1
Department of Pulmonary Medicine, Indira Gandhi Medical College, Shimla, Himachal Pradesh and Department of Chest Diseases and Tuberculosis, Government Medical College1, Chandigarh, India

ABSTRACT
Endobronchial tuberculosis (EBTB) is defined as tuberculous infection of the tracheobronchial tree with microbial and histopathological evidence. It is seen in 10-40% of patients with active pulmonary tuberculosis. More than 90% of the patients with EBTB have some degree of bronchial stenosis. Ten to 20 percent have normal chest radiograph. Therefore, a clear chest radiograph does not exclude the diagnosis of EBTB. Bronchoscopic sampling has been the key to the diagnosis producing more than 90% yield on smear as well as on culture. Bronchoscopy and computed tomography are the methods of choice for accurate diagnosis of bronchial involvement and assessment for the surgical interventions. Characteristic HRCT findings of EBTB are patchy asymmetric centrilobular nodules and branching lines (tree-in-bud appearance). Early supervised antituberculosis therapy results in minimal structural and functional residua. Corticosteroid therapy may not influence the outcome of endobronchial tuberculosis. Early diagnosis and prompt treatment, before the development of fibrosis is important to prevent complications of endobronchial tuberculosis, such as bronchostenosis. Key words : Tuberculosis, Endobronchial tuberculosis (EBTB).

[Indian J Chest Dis Allied Sci 2003; 45 : 247-256]

INTRODUCTION
All that wheezes is not asthma (Mc Conkey) 1 . A patient with constitutional symptoms of tuberculosis but also complaining of wheeze and with a normal chest radiograph and sputum smear positive for Mycobacterium tuberculosis is most likely to be a case of endobronchial tuberculosis (EBTB). Tuberculosis remains a rampant infectious disease of global importance. Despite extensive global control efforts on the part of the World Health Organization and local health agencies, the tuberculosis epidemic continues to ravage the

developing world. Endobronchial tuberculosis is defined as tuberculous infection of the tracheobronchial tree with microbial and histopathological evidence2. EBTB is a highly infectious disease that remains a diagnostic challenge. EBTB is present in 10-40% of patients with active pulmonary tuberculosis, and more than 90% of the patients with EBTB have some degree of bronchial stenosis3. It may present as a troublesome therapeutic problem due to its sequel of cicatricial stenosis. Morten4 was the first to describe endobronchial tuberculosis in 1698. The

[Received : January 6, 2003; accepted after revision : June 17, 2003] Correspondence and reprints request : Dr Surender Kashyap, Professor and Head, Department of Pulmonary Medicine, Indira Gandhi Medical College, Shimla-171 001, Himachal Pradesh, India; Tele. : 91-0177-2883422, 2805502; Telefax : 91-0177-2658339; E-mail : <surenderkashyap@hotmail.com>.

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occurrence of EBTB has decreased with the advent of effective chemotherapy. Laryngeal tuberculosis is the most infectious form of disease that results from either pooling of infected secretions in the posterior larynx or hematogenous dissemination to the anterior larynx. Most patients with laryngeal disease also have active pulmonary disease, which can be mild and may go unrecognized5 . EBTB is generally found in the younger age group with more than half of the cases being seen at less than 35 years of age6.

PATHOGENESIS
Five potential mechanisms have been suggested for the development of endobronchial infection due to M. tuberculosis7 : (1) direct extension from adjacent parenchymal focus; (2) implantation of organisms from the infected sputum; (3) hematogenous dissemination; (4) lymph node erosion into the bronchus; and (5) through lymphatic drainage from parenchyma to the peribronchial region. Myerson 8 has suggested alternative mechanism of retrograde passage of tubercle bacilli through lymphatics from bronchioles and subsegmental bronchi. Perforation of a tuberculous lympnode into the bronchi has been considered in some adults9. Initially, the mass protrudes into the bronchial wall and may obstruct the lumen; the node may be seen as a greyishyellow mucosa, and the lumen wall as hemorrhagic and granulating. A fistula may develop from which caseous material extrudes, forming caseous lumps in the sputum. Computed tomographic (CT) scan, plain tomogram, or bronchograms may demonstrate excavation of the node radiographically. Gradually, the opening closes and there is subsequent induration of the node. Finally, fibrosis develops with scarring of the bronchial wall. In some cases, bronchostenosis with distortion of bronchial anatomy follows.

complication of primary TB and is caused by encroachment of enlarged nodes on the bronchi. The nodes become fixed to the bronchial walls due to inflammatory changes and the infection progresses through the walls of the bronchi to the mucosal lining, ultimately leading to ulceration or granulation tissue. In early stages the mass protrudes into bronchial wall and may obstruct the bronchial lumen. A node may erode through the bronchial wall with extrusion of the caseous material 10,11. EBTB usually starts as a submucosal tubercle that progresses to ulcer formation. Granulation tissue that is generally formed looks like polypoid mass. These ulcers heal by fibrosis. The degree of fibrostenosis depends on the depth of the ulcer. Once ulceration occurs, there is some degree of residual fibrosis even with treatment. Healing of EBTB occurs along with resolution of the parenchymal lesions12. In upto 90% cases, there is radiographic evidence of obstruction with segmental atelectasis, occurring most frequently in the right middle lobe and anterior segment of the right upper lobe10,11. In patients with EBTB, bronchial stenosis may develop within 3 to 6 months.

CLINICAL FEATURES
EBTB may have insidious onset, simulating bronchogenic carcinoma, or may be acute, mimicking asthma, foreign body aspiration and pneumonia. Symptoms of EBTB may develop even after completion of therapy. EBTB is more common in young adults with a female predominance 6,13. Fifteen percent of geriatric patients may also have EBTB 14. The barking cough that is not responsive to an antitussive medication, but responds to steroids along with anti-tuberculosis treatment may be a feature of EBTB 9. Bronchorrhea can occur in active endobronchial tuberculosis15 . Sputum production is variable. Hemoptysis may occur but is seldom massive. Lymph node rupture may cause chest pain that may be sharp or dull in sternal or parasternal region. Dyspnea is often associated with atelectasis of the lung. Physical examination may reveal diminished

NATURAL HISTORY
The natural history of EBTB is well understood. EBTB in children is usually a

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breath sounds and localized low-pitched wheeze or rhonchi. Upto 25 to 35% of EBTB may have features of collapse. Classical monophonic wheeze may be heard in about 15% of the patients 13. Endobronchial tuberculosis with expectoration of tracheal cartilage has been reported16. Dull and sharp chest pain can occur anteriorly due to enlargement and rupture of the lymph nodes. Constitutional symptoms including fever, weight loss, anorexia and night sweat are not usually prominent in EBTB. Serious sequelae especially with tracheal involvement such as respiratory failure, collapse of dependent portion of lungs, failure of endobronchial intubation for general anaesthesia, the need of tracheostomy, or death by suffocation have been reported17,18.

Sputum Examination All suspected patients of EBTB should be subjected to sputum smear and culture examination for M. tuberculosis. Yield of sputum smear for AFB is not as high as in parenchymal involvement even in an optimal laboratory setup with meticulous sputum examination. In recent studies, sputum positivity in EBTB has been demonstrated from 16 to 53.3 percent21-23. However, EBTB with ulceration and mucosal involvement has higher sputum positivity and yield is even greater with sputum culture when compared to smear (73.6 vs 53.3%)13, 23. Chest Radiograph Ten to 20 percent paients with EBTB may have a normal chest radiograph13. Thus, a clear chest radiograph does not exclude the diagnosis of endobronchial TB. Bronchial stenosis occurs in 10-40 percent of patients with active pulmonary tuberculosis24. Radiologic manifestations of tuberculous bronchostenosis include persistent segmental or lobar collapse, lobar hyperinflation, obstructive pneumonia and mucoid impaction24 (Figure 1). Volume loss on chest radiography may indicate development of bronchial stenosis, and fibreoptic bronchoscopy should be considered in such cases2. Erosion of calcified hilar nodes into adjacent bronchi, known as broncholithiasis, may also result in

DIAGNOSIS
Although sputum examination is the essential and first step towards the diagnosis of EBTB, bronchoscopy and computed tomography are the methods of choice for accurate diagnosis of bronchial involvement and assessment for surgical intervention. Fibreoptic bronchoscopy is indicated in patients in whom chest radiographs, physical signs or symptoms suggest the possibility of endobronchial tuberculosis. Due to the potential utility of early antituberculosis treatment and use of corticosteroids in reducing the lymph node size and mucosal swelling, the above procedures should be carried out at the earliest. Typical bronchoscopic finding is the presence of white gelatinous granulation tissue. The mucosa is nodular, red, vascular and some times ulcerated. It may simulate a bronchogenic carcinoma13,19. Nucleic acid amplification tests, such as PCR and other methods for amplifying DNA and RNA, may facilitate rapid detection of M. tuberculosis in respiratory tract specimens. Recommendations for interpretation and use of nucleic acid amplification have been recently updated by the Centers for Disease Control and Prevention20.

Figure 1. Chest radiograph showing nonhomogeneous opacity in left upper- and mid-zones.

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segmental collapse or over inflation 25 . Bronchiectasis is another a complication of EBTB, usually involving upper lobes. Computed Tomography (CT) Scan Volumetric computed tomography has the advantage of acquiring both multiplanar and three-dimensional (3D) images, thus enabling precise diagnosis and evaluation of the extent of disease involving the airways. Multiplanar and 3-D images appear to be useful for global understanding of the status of the tracheobronchial tree, particularly for evaluation of focal stenosis of the airways26. Characteristic HRCT findings of EBTB are patchy asymmetric centrilobular nodules and branching lines (Figure 2) that may have unilateral or bilateral distribution 27, 28 . Multiple branching linear structures of similar caliber originate from a single stalk (the tree-in-bud appearance). The stalk is thought to represent a lesion that affects the last order bronchus within the secondary pulmonary lobule and the bud is thought to represent a lesion that is in the bronchioles and alveolar ducts28. In CT scan, there are foci of illdefined nodular densities which are peribronchiolar in location and markedly variable in size, including the lesions as small as 2-3 mm. These nodular densities may become confluent 29. Tuberculous mediastinal lymp

nodes are usually of low density (necrotic) on chest CT. CT is also a useful adjunct to direct endoscopic visualization, CT accurately depicts the bronchial abnormality in 93% to 100% cases. CT findings include isolated (41% to 43%) lung segmental bronchial narrowing with concentric wall thickening (Figure 3), complete endobronchial obstruction (32%) and extrinsic obstruction by adjacent adenopathy (23% to 50%)30.

Figure 3. CT scan of thorax showing bronchial involvement with bronchial wall thickening in the left lung.

Usually, tuberculosis heals following therapy resulting scar formation in the parenchyma. Such scars cause distortion of bronchovascular bundles, irregular fibrotic bands and small irregular nodular densities with surrounding pericicatricial emphysema. These changes attributable to healed lesions have been noted in the areas remote from the endobronchial lesion. Fibreoptic Bronchoscopy Bronchoscopic sampling has been the key to the diagnosis of EBTB, producing more than 90 percent yield on smear as well as on culture6-13. In diagnosing EBTB, the experience of the bronchoscopist is also of great importance for eliciting the bronchoscopic findings that contribute to the diagnosis. Even if biopsy fails to supply tangible results, the bronchoscopic changes, supported by clinical and radiological findings, may be sufficient to establish the diagnosis of EBTB. A bronchoscopic biopsy is the most reliable

Figure 2. CT scan of thorax showing tree-in-bud appearance in the left lung.

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method for diagnosing EBTB31, because a needle aspiration can provide only a cytological diagnosis. However, needle aspiration can be used for obtaining materials from segments of a lobe where the forceps cannot reach. Different bronchoscopic specimens including biopsy, brushing and washings should be obtained as practicable. These specimens provide variable yield. Bronchial biopsy may be positive in 30.35% to 84% patients21,31. Bronchial brushing has provided a high yield of 84.88% in a study from China 21. Similarly, bronchial washings have also yielded variable results ranging from 10% to 37.5 percent22,31. A widely accepted classification defining EBTB by FOB has the following seven subtypes: (i) actively caseating, (ii) edematous-hyperemic, (iii) fibrostenotic, (iv) tumorous, (v) granular, (vi) ulcerative, and (vii) nonspecific bronchitis23. The prominent lymph nodes are seen as greyishyellow masses through the bronchial mucosa. Hemorrhage and granulation tissue may also be seen. Fistula formation and caseous material draining into bronchus may also be observed. Early bronchoscopic findings consist of erythema, mucosal granularity including discrete submucosal tubercles, and shallow mucosal ulcers (Figures 4 and 5). Findings indicative of more advanced disease are deep
Figure 5. Bronchoscopic view of left lower lobe in a 17-year-old girl showing nodularity in addition to mucosal hyperemia. Bronchial biopsy of the same patient revealed caseating granuloma.

ulcers, hyperplastic inflammatory polyps, tumour like collections of granulation tissue and bronchial stenosis 32,33. The exudative lesion consists of mucosal erythema, swelling and white caseous exudates with or without granulation tissue. The lesions are described as ulcerative when bronchial mucosa shows predominantly ulcerations. The cicatricial lesions have hypertrophic mucosa and distorted lumen with or without polypoid lesions. The bronchoglandular lesions are manifested as one or more eccentric round indentations into bronchial lumen on bronchoscopic examination. Such lesions have involvement of peribronchial or paratracheal lymph node(s) on CT23. Diffuse mucosal congestion with edema (suggestive of inflammation) and mass lesion were most common bronchoscopic findings in three different studies2,31,34.

COMPLICATIONS
Bronchial stenosis and strictures are irreversible, relatively common and delayed complications of EBTB, occurring in spite of adequate anti-tuberculosis treatment. Bronchostenosis may develop in 60 to 95% cases and may even involve the main stem bronchi. Worst outcome can be the development of airway obstruction due to involvement of the

Figure 4. Endobronchial mucosa showing diffuse hyperemia with mucosal edema and exudates on bronchoscopy. Bronchial washing and brushing specimens revealed Mycobacterium tuberculosis.

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trachea. Bronchiectasis is also a common complication of EBTB and most commonly develops as paracicatricial process, secondary to pulmonary destruction and fibrosis (traction bronchiectasis). It also may result from central bronchostenosis and distal bronchial dilatation. Bronchiectasis is typically asymptomatic and usually occurs in the upper lobes 22. When bronchiectasis is symptomatic, hemoptysis is the most common symptom.

laser, curettage, resection and anastomasis 13,19,40,43,44. Balloon dilatation and selfexpanding stent insertion is an effective treatment for bronchial stenosis 44 . Use of endobronchial stent should only be considered in lesions of proximal location when other dilatational methods have failed2. The role of steroid therapy in reversing or preventing bronchostenosis is not clear. Although, EBTB frequently leads to bronchial stenosis, there are no specific therapies to prevent this sequel. The use of corticosteroids remains controversial and there have been no prospective studies about the effectiveness of corticosteroids. These drugs, however been used, sometimes with encouraging results. Potential benefits may be because of two reasons. First, it reduces the bronchial narrowing to promote drainage and reduce the extent of post-stenotic lung damage, and secondly, it may help to reduce the long-term evolution of high-grade bronchial stenosis45. Use of oral steroid in EBTB, in addition to standard chemotherapy seems to prevent the complication of EBTB such as bronchostenosis to some extent41,46. Verhaeghe et al47 have demonstrated rapid healing and complete resolution of endobronchial tuberculosis by local endoscopic injection of corticosteroids in different sittings. Recent studies have demonstrated that aerosolized streptomycin and corticosteriods in addition to conventional chemotherapy may lead to faster healing of ulcerative lesions in EBTB and also help to prevent bronchial stenosis38,39,48. Stenotic lesions may require repeated dilatations14. However, INH inhalation in the doses of 200 mg/day in addition to standard chemotherapy has also been used to prevent bronchostenosis in patients with EBTB 49, 50. Bronchostenosis caused by EBTB may present with severe respiratory symptoms, atelectasis and secondary pneumonitis. Surgical treatment such as bronchoplasty may be contemplated for EBTB particularly when the response to antituberculosis chemotherapy is poor. In addition to checking progression of the disease, bronchoplasty helps

DIFFERENTIAL DIAGNOSIS
Lung cancer is most important differential diagnosis. However, other differential diagnoses are simple inflammation, sarcoidosis, bronchial asthma, atelectasis, foreign body aspiration, pneumonia and endobronchial actinomycosis35. Sarcoidosis also involves the endobronchi and may manifest with endobronchial inflammation closely resembling EBTB. Bronchostenosis due to sarcoidosis that may develop in certain cases needs to be differentiated from EBTB carefully36. There is a need to have a high index of suspicion to exclude atelectasis due to EBTB in children with either acute or chronic respiratory tract symptomatology. However, in patients with acquired immune deficiency syndrome (AIDS), endobronchial Kaposi's sarcoma (EKS) should be considered37.

TREATMENT
Early diagnosis and treatment may alter the natural course of EBTB. Bronchoscopy is essential for diagnosis and treatment planning. Early introduction of conventional chemotherapy containing INH, rifampicin, pyrazinamide and ethambutol should control the progression. Duration and regimens are the same as for standard short course chemotherapy and most of the studies have advocated six to nine months duration for chemotherapy2,23,28,32,38-42. Role of DOT (Directly Observed Treatment) in EBTB is not extensively studied, although one recent study has shown favourable results 28. Other modalities include corticosteriods, balloon dilatation, self expanding metallic stent,

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to preserve lung function. Appropriate chemotherapy should be given for 9-12 months perioperatively to prevent a recurrence of disease and re-stenosis51. Bronchoplastic surgery is the best treatment for bronchial stricture involving both the main bronchi 52 . Bronchoscopic curettage with forceps of the pseudomembranes coupled with systemic steroid therapy has been reported to enhance the drainage among selective patients13. Laser bronchoscopy is a newly established procedure employed in interventional bronchoscopy. A small series by Tscheikuna has demonstrated the benefit of laser bronchoscopy is patients with high-risk endobronchial obstructive lesions43. In another Russian study, endobronchial laser therapy along with alfa tocoferol and endobronchial instillation of sodium thiosulphate in nine patients of post tuberculous fibrous stenosis of large bronchi provided a steady state dilatation of the airway lumen53.

PROGNOSIS
The prognosis of actively caseating type and edematous-hyperemic type EBTB is grave, resulting in fibrostenosis in two thirds of patients. The prognosis is good for granular and non-specific bronchitic type EBTB. However, the prognosis of tumorous type is poor, frequently resulting in bronchial stenosis despite adequate treatment. Antituberculous chemotherapy is effective in controlling the infection, but does not prevent residual bronchostenosis. Early treatment with steroid therapy may be effective in certain groups of EBTB.

response and may encroach upon the regional bronchus. Partial obstruction caused by external compression by the enlarged lymph node leads to hyperinflation of the distal lung segment. Occasionally, these lymph nodes lead to complete obstruction of the bronchus resulting in atelectasis of the segment54. More often the inflamed caseous nodes attached to the bronchial wall erode through it, leading to EBTB or a fistulous tract55. Consequent upon these changes EBTB in children often presents with localized wheezing and sublobar atelectasis and consolidation attributable to the erosion of the inflamed lymph nodes into the bronchial lumen. The extrusion of infected material into the bronchus can spread infection to the lung parenchyma. At times EBTB manifests clinically as foreign body aspiration in children 56,57. Because of the short- and long-term sequelae of EBTB, including bronchial stenosis and postobstructive bronchiectasis, therapy is indicated to relieve peribronchial obstruction. In a small series of 29 pediatric cases with primary tuberculosis and bronchial obstruction, randomization to prednisolone was associated with a favourable outcome by both radiographic and bronchoscopic appearances58. Endobronchial Tuberculosis in Geriatric Age Approximately 90% of cases of tuberculosis involving elderly persons are caused by reactivation of primary infection 59 . Endobronchial tuberculosis occurs in adults mostly by superficial ulceration in the bronchus caused by secretions containing high numbers of live TB bacilli from cavitary lesions. EBTB is observed in about 15% of elderly patients with pulmonary TB and bronchial stenosis may occur in about 60% of cases 14. As malignancy and pneumonia are common among the elderly, EBTB is perhaps underestimated. Cough usually is the main symptom. Chest pain, wheeze, hemoptysis may be seen in addition to constitutional symptoms of tuberculosis. Constitutional symptoms of tuberculosis such as weakness, anorexia and fatigue are marked with no difference in the bronchoscopic findings when compared to other age groups.

ENDOBRONCHIAL TUBERCULOSIS IN SPECIAL SITUATIONS

Endobronchial Tuberculosis in Children Most cases of primary infection with tuberculosis remain asymptomatic. However, with the progression of the disease the lymph nodes located in hilar and paratracheal regions become enlarged due to host inflammatory

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Endobronchial Tuberculosis in HIV Patients HIV leads to marked depression of cellular immunity with progressive destruction of CD4+ lymphocytes. The absence or incomplete formation of granulomata and dissemination of mycobacteria in HIV infected patients appears to be directly proportional to the circulating CD4+ lymphocytes. There is no firm conclusion from the available literature that EBTB is more common in subjects with HIV infection. However, it is expected that EBTB should be more frequent in association with HIV infection because, it is a frequent manifestation of primary tuberculosis due to depressed cell mediated immunity and also, the usual mechanism for development of EBTB is a direct airway infiltration from adjacent tuberculous mediastinal lymph nodes that are commonly noticed in patients with HIV infection. On the other hand, a possible explanation for underestimation of EBTB in HIV infected patients may be the infrequent use of fibreoptic bronchoscopy in patients with positive acid-fast bacilli on sputum smear examination; and therefore, endobronchial pathology may go undetected37,60. Certain specific diseases may present with endobronchial abnormalities, including EBTB. It is important to know the bronchoscopic appearances of the lesions such as Kaposi's sarcoma, aspergillosis, lymphoma and lung cancer because some of these lesions may require biopsy and special stains. In the setting of HIV, it is also important to consider the risks and benefits of the biopsy of endobronchial lesions58.

sufficient treatment.

CONCLUSION
EBTB is relatively uncommon manifestation of a common disease. Diagnosis of EBTB is frequently delayed until the onset of serious bronchial stenosis with resultant atelectasis and bronchiectasis. Symptoms and signs are due mainly to the co-existant pulmonary tuberculosis. Inflamed mucosa is the most common bronchoscopic finding. The exact pathogenesis of EBTB is not yet completely understood and the course of EBTB differs according to the type. Despite adequate treatment, development of bronchial stenosis may occur. Future studies should focus on the pathogenesis of bronchial inflammatory reaction, resulting fibrosis and prevention of bronchial stenosis at an early stage.

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