Bronchiectatic Air Bronchograms in Pulmonary Tuberculosis: A Case Report and Literature Review

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1 MILITARY MEDICINE, 175, 5:370, 2010 Bronchiectatic Air Bronchograms in Pulmonary Tuberculosis: A Case Report and Literature Review Lt Col Robert A. Jesinger, USAF MC * ; Capt Elizabeth A. Ballard, USAF MC * ; Maj David R. Allton, USAF MC ; Maj Jason W. Lane, USAF MC ; Col Les Folio, USAF MC (Ret.) ABSTRACT We report a case of a 61-year-old Filipino-American male who developed pulmonary tuberculosis after travel to the Philippines. His history, presentation, imaging findings, and clinical course are presented as well as a discussion of the interesting imaging features in his case. Our case highlights the importance of having a high index of suspicion for tuberculosis in the setting of bronchiectatic air bronchograms as well as the value of computed tomography (CT) imaging in pulmonary tuberculosis. INTRODUCTION Pulmonary tuberculosis (TB) (caused by Mycobacterium tuberculosis ) remains an important public health problem, especially in countries where military personnel may be deployed. Timely diagnosis can be difficult since the clinical and radiologic features of TB may mimic those of other diseases. The following case report discusses an interesting imaging finding of bronchiectatic-like airway changes within (and as a result of ) pulmonary consolidation and airway infection in the setting M. tuberculosis. The computed tomography (CT) findings made active pulmonary TB a primary concern that was later confirmed with microbiology and surgical pathology. CASE REPORT A 61-year-old HIV-negative Filipino-American man with a past medical history of seasonal allergic rhinitis was admitted for worsening dyspnea, dry cough, and fatigue. The patient was working as a contractor for the United States military and reported a recent 6-month-long trip to the Philippines. During his trip, he felt in good health while he traveled into villages and worked among the local population. He also visited several family members in the Philippines during his trip. He underwent a screening chest radiograph ( Fig. 1 ) before his trip, which revealed no abnormalities. After his return to the United States, he began to experience a dry cough. Over the next 3 months, he developed mild shortness of breath and fatigue. He saw a primary care provider for a chief complaint of wheezing, but he was found to be afebrile with normal vital signs (pulse oximetry of 99% on Departments of *Radiology and Infectious Disease, David Grant USAF Medical Center, 101 Bodin Circle, Travis AFB, CA Department of Radiology and Radiological Sciences, Uniformed Services University of the Health Sciences, 4301 Jones Bridge Road, Bethesda, MD The views expressed in this article are those of the authors and do not reflect the official policy or position of the U.S. government, the Department of Defense, or the Department of the Air Force. room air) and had no significant physical exam findings. His symptoms were attributed to seasonal allergies, and he was prescribed loratadine and benzonatate capsules for his cough. He continued to complain of subjective wheezing several times per day and a new fullness in his chest, so he returned to his primary care clinic for reassessment. While he remained afebrile with stable vital signs, a new faint endexpiratory wheeze was noted in the bilateral lung apices, which resolved after deep breaths. His physical exam was otherwise unremarkable. A chest radiograph was obtained ( Fig. 2 ), which demonstrated new peripheral nodular opacities in the right upper lobe. He had a reported history of Bacillus Calmette-Guerin (BCG) immunization as a child and a distant history of exposure to a relative in the Philippines infected with TB. He was treated for community-acquired pneumonia as an outpatient with azithromycin with initial improvement in his wheezing. A repeat chest radiograph was obtained in follow-up ( Fig. 3 ), which demonstrated developing consolidation in the right upper lobe with new peripheral nodular opacities in the right lower lobe and left upper lobe. As a result, an infectious disease specialist was consulted, and the patient was admitted to the hospital. Admission vital signs included a temperature of 99 F and pulse oximetry of 95% on room air, respiratory rate of 16, heart rate of 96, and blood pressure of 129/96. He stated that his wheezing was improved but that his dry cough, mild shortness of breath, and fatigue had not changed. He was placed in respiratory isolation as the imaging findings were concerning for pulmonary TB. Ceftriaxone and azithromycin were begun for coverage of community-acquired pneumonia. At no time in the recent past did he receive a fluoroquinolone. Three consecutive daily-induced sputum samples were obtained; AFB smears prepared from concentrated specimens were all negative. As the suspicion for TB was high, two additional daily sputum samples were negative. Routine sputum and serum bacterial cultures, urinary Legionella antigen, and urinary Histoplasma antigen returned negative. Serum Coccidioidomycosis IgG and IgM performed by immunodiffusion (Armstrong Labs, Brooks City Base, Texas) both 370 MILITARY MEDICINE, Vol. 175, May 2010

2 FIGURE 1. Normal posterior anterior (PA) chest radiograph in a 61-yearold male before overseas travel to the Philippines. FIGURE 3. Posterior anterior (PA) chest radiographs in a 61-year-old male 6 months after return from his trip (obtained at the time of hospital admission), demonstrating developing consolidation in the right upper lobe (curved black arrow) with new hazy peripheral nodular opacities (black arrowheads) in the right lower lobe and left upper lobe. FIGURE 4. Unenhanced axial computed tomography (CT) images of the chest, demonstrating bronchiectatic airways (black arrowheads) in the right upper lobe with surrounding consolidation. Peripheral centrilobar nodules ( tree-in-bud appearance) are noted scattered throughout the lungs (white arrowheads). FIGURE 2. Posterior anterior (PA) chest radiographs in a 61-year-old male 3 months after return from his trip, demonstrating hazy peripheral nodular opacities (black arrowheads) in the right upper lobe. returned negative. Despite antibiotic therapy for communityacquired pneumonia, his symptoms continued to worsen. A noncontrast chest computed tomography (CT) examination was performed ( Figs. 4 and 5 ), which demonstrated noncavitating multilobar consolidations with associated right upper lobe bronchiectasis. No pleural effusions were noted. The chest radiograph findings of peripheral nodular opacities were seen as peripheral hazy centrilobular nodules ( tree-in-bud pattern) in the left upper lobe and right lower lobe. While the developing unilateral upper lobe bronchiectatic changes are suspicious for a chronic infection, the additional findings of worsening consolidation with a tree-in-bud pattern was typical for active pulmonary TB. Additionally, a calcified nodule was noted in the right upper lobe in association with calcified lymph nodes in the right hilum, likely related to an old granulomatous infection, possibly TB ( Fig. 6 ). A repeat chest CT with intravenous radiographic contrast (100 ml of Omnipaque 300) also demonstrated nonspecific mediastinal adenopathy (Fig. 7 ). MILITARY MEDICINE, Vol. 175, May

3 FIGURE 5. Unenhanced axial 3-mm-thick maximum-intensity projection (MIP) computed tomography (CT) image of the chest, demonstrating bronchiectatic airways (black arrowheads) in the right upper lobe with surrounding consolidation. Peripheral centrilobar nodules ( tree-in-bud appearance) are noted in the left upper lobe (white arrowhead). FIGURE 7. Contrast-enhanced axial computed tomography (CT) images of the chest, demonstrating multiple, small (less than 1 cm in size) lymph nodes in the pretracheal and right hilar regions (black arrows). The increased number of visualized lymph nodes along with their morphologic fullness was interpreted as pathologic. Note the calcifications in the right hilum associated with the right upper lobe calcified nodule (white arrows). FIGURE 6. Unenhanced axial computed tomography (CT) image of the chest, demonstrating a calcified nodule in the right upper lobe in association with a calcified right hilar lymph node (white arrows), consistent with a Ghon complex. In the context of the patient s history, the clinical and imaging findings were concerning for active pulmonary tuberculosis. Bronchoscopy and bronchoalveolar lavage (BAL) were performed. An AFB smear prepared from a concentrated BAL sample was negative, and a cytopathology sample prepared from the BAL displayed no fungal elements or AFB. Due to laboratory financial constraints, nucleic acid amplification testing was not performed on any of the samples. The patient s clinical course continued to worsen over the next week, and follow-up portable chest radiographs (not shown) demonstrated progression of the consolidations. The evolving imaging findings continued to strongly point toward a diagnosis of pulmonary TB. Given the initially unrevealing microbiologic evaluation for an infectious organism, and worsening patient symptoms despite broadening IV antibiotics, a video-assisted thoracoscopy (VATS) and right upper lobe wedge biopsy was performed to obtain a tissue diagnosis. Initial frozen section demonstrated noncaseating granulomas ( Fig. 8 ), and special stains for acid-fast bacilli and fungus were initially read as negative. However, on postoperative day one, an AFB culture from the BAL obtained 2 weeks before revealed AFB growth in the liquid culture medium. AFB staining was performed and serpiginous structures consistent with cording typically seen in TB were visualized. RIPE (rifampin, isoniazid, pyrazinamide, ethambutol) therapy for pulmonary tuberculosis was initiated. Over the next few days, the patient reported a significant improvement in symptoms. Final speciation confirmed M. tuberculosis (by high-performance liquid chromatography [HPLC] at the Napa-Solano County health department). On the basis of this culture result, lengthy repeat examination of the original pathology slides demonstrated the presence of few acid fast bacilli ( Fig. 9 ). The patient s sputum smears for AFB remained negative, and he 372 MILITARY MEDICINE, Vol. 175, May 2010

4 FIGURE 8. Microscopic pathology image (hematoxylin-eosin stain, low power 100 ), demonstrating noncaseating granulomas with giant cells (*). FIGURE 10. Posterior anterior (PA) chest radiograph in our patient obtained 3 months after initiating therapy for pulmonary tuberculosis. Note the progressive clearing of pulmonary consolidations when compared with Figure 3. FIGURE 9. Microscopic pathology image (Kinyoun acid-fast stain, high power 600 ), demonstrating scattered mycobacteria (arrowheads). was discharged home on hospital day 27 to continue RIPE by directly observed treatment. He completed a 6-month course of RIPE and his clinical symptoms completely resolved. A repeat chest radiograph ( Fig. 10 ) 3 months after initiating treatment noted partial clearing of the pulmonary consolidations. DISCUSSION Pulmonary tuberculosis cases and annual TB rates in the United States recently reached all-time lows, with only 12,898 incident cases reported in Although this news is initially encouraging, more than half (7,541) of these cases were in immigrants, with the majority of these cases involving four countries of origin: Mexico (1,742 cases), the Philippines (855), India (598), and Vietnam (580). 1 In addition, the highest prevalence of total cases was among individuals from countries in Asia. Given the current spectrum of United States military operations, considerable risk of acquiring TB exists for deployed U.S. military personnel. A key factor in diagnosis of pulmonary tuberculosis is simply awareness that the disease still lurks. Timely diagnosis can be difficult since the clinical and radiologic features may mimic those of other diseases. Clinical history, exposure history, sputum cultures, and chest radiography are important tools in diagnosing pulmonary TB. Pulmonary tuberculosis has historically been classified as primary (initial infection usually seen in children) or postprimary (reactivation disease usually seen in adults). 2 Imaging findings in primary and postprimary pulmonary TB often overlap, and the division between primary and reactivation tuberculosis is by no means clear cut. Primary pulmonary TB typically appears as air-space consolidation in the lower lobes, and mediastinal adenopathy is a key feature.3 Host immune response often controls primary TB, usually resulting in pulmonary granuloma formation as well as calcified fibrotic hilar/mediastinal lymph nodes (Ghon s complex). In contrast, reactivation pulmonary TB typically appears as nodular and linear areas of interstitial pulmonary opacification, predominantly in the upper lobes, with cavitation being a key feature, as opposed to adenopathy. 4,5 Our case demonstrates features of both primary and reactivation TB, making exact classification difficult. In either form of active pulmonary TB, bronchiectatic-like changes can be seen in up to 20% of patients as a result of airway infection. These changes are usually not well seen on chest radiographs but are often more apparent on chest CT. Active airway infection usually results from local spread of TB via lymphatic channels into the submucosa of the airway, and imaging may reveal irregular airways with wall thickening, stenoses, and mural enhancement, all of which can resolve with medical treatment. 6,7 Irreversible bronchiectasis is more commonly seen in inactive disease as a result of destruction MILITARY MEDICINE, Vol. 175, May

5 and fibrosis of the lung parenchyma with secondary bronchial dilatation (traction bronchiectasis). 6 9 Chronic airway and pulmonary parenchymal infections from many causes may result in organization and fibrosis, resulting in bronchiectaticlike airway changes; however, observing ongoing bronchiectatic airway changes in the setting of worsening consolidation makes active pulmonary infection a major clinical concern. As this case report demonstrates, diagnosis of pulmonary TB can be difficult, and CT imaging can play a key role in the diagnosis. In addition to findings of consolidation, cavitation, and mediastinal adenopathy, bronchiectatic-like airway changes in the setting of airway infection and consolidation (bronchiectatic air bronchograms) are a visually striking finding in pulmonary TB. With the availability of CT imaging on deployment and in overseas military bases, this finding may be more commonly encountered. To date, case reports of bronchiectatic air bronchograms have been reported in a child with cystic fibrosis 10 and in a patient with postobstructive bronchiectasis due to peanut impaction. 11 We have not encountered this descriptive term applied to pulmonary TB. Our case demonstrates that M. tuberculosis may be a more important cause of bronchiectatic air bronchograms in the current military environment. Awareness of these imaging findings may be of interest to military medical professionals given the prevelance of tuberculosis in overseas locations and the potential utilization of chest CT in its assessment, both postdeployment and in the deployed environment. ACKNOWLEDGMENTS The authors express their appreciation to Dr. Steve DeMartini for preparing the pathology images in this case and to Dr. Bang Huynh and Dr. David Bigelow for reviewing the initial versions of this article. REFERENCES 1. Pratt R, Robison V, Navin T, Bloss E : Trends in tuberculosis United States. MMWR Morb Mortal Wkly Rep 2008 March 20, 2009 ; 58 (10) : McAdams HP, Erasmus J, Winter JA : Radiologic manifestations of pulmonary tuberculosis. Radiol Clin North Am 1995 ; 33 (4) : Leung AN, Muller N, Pineda PR, et al : Primary tuberculosis in children: radiographic manifestations. Radiology 1992 ; 182: Burrill J, Williams CJ, Bain G, Conder G, Hine AL, Misra RR : Tuberculosis: a radiologic review. Radiographics 2007 ; 27: Kim HY, Song KS, Goo JM, Lee JS, Lee KS, Lim TH : Thoracic sequelae and complications of tuberculosis. Radiographics 2001 ; 21: Curvo-Semedo L, Teixeira L, Caseiro-Alves F : Tuberculosis of the chest. Eur J Radiol 2005 ; 55: Moon WK, Im JG, Yeon KM, Han MC : Tuberculosis of the central airways: CT findings of active and fibrotic disease. AJR Am J Roentgenol 1997 ; 169: Cartier Y, Kavanagh PV, Johkoh T, Mason AC, Muller NL : Bronchiectasis: accuracy of high-resolution CT in the differentiation of specific diseases. AJR Am J Roentgenol 1999 ; 173: Shin MS, Ho K : Computed tomography of bronchiectasis in association with tuberculosis. Clin Imaging 1989 ; 13 (1) : Huisman C, de Graff CS, Boersma WG : Unilateral air bronchogram in a patient with cystic fibrosis. Chest 2002 ; 121 (4) : Torres de Amorim e Silva CJ, Fink AM : Case 137: pneumonia and bronchiectasis secondary to unrecognized peanut impaction. Radiology 2008 ; 248: MILITARY MEDICINE, Vol. 175, May 2010

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