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'f; Capt Elizabeth A. Ballard, USAF MC*; Maj David R. Aliton, USAF MCp, Maj Jason W. Lane, USAF MCt; Col Les Foiio, USAF MC (Ret.)f

ABSTRACT We report a case of a 61-year-old Filipino-Ametican 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 "bronchiectatie air bronchograms" as well as the value of computed tomography (CT) imaging in pulmonary tuberculosis.

INTRODUCTION Pulmonary tuberculosis (TB) (caused by Mycohacterium tuberculosis) remains an important public healtb problem, especially in countries wbere military personnel may be deployed. Timely diagnosis can be difficult since tbe clinical and radiologie features of TB may mimic tbose of other diseases. Tbe following case report discusses an interesting imaging finding of bronchiectatic-likc airway changes witbin (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 witb microbiology and surgical patbology. 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. Tbe patient was working as a contractor for tbe United States military and reported a recent 6-montb-iong trip to tbe Pbilippines. During bis trip, be felt in good bealth while he traveled into villages and worked among tbe local population. He also visited several family members in tbe Philippines during his trip. He underwent a screening cbest radiograph (Fig. 1) before his trip, which revealed no abnormalities. After bis return to tbe United States, he began to experience a dry cough. Over the next 3 montbs, be developed mild shortness of breath and fatigue. He saw a primary care provider for a chief complaint of "wheezing." but be was found to be afebrile witb normal vital signs (pulse oximetry of 99% on

room air) and bad 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 bis chest, so he returned to bis primary care clinic for reassessment. Wbile be remained afebrile with stable vital signs, a new faint endexpiratory wheeze was noted in tbe bilateral lung apices., which resolved after deep breaths. His physical exam was otherwise unremarkable, A chest radiograph was obtained (Fig. 2), wbicb 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 tbe Pbilippines infected with TB. He was treated for community-acquired pneumonia as an outpatient with azitbromycin with initial improvement in his wbeezing. 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 tbe patient was admitted to the hospital. Admission vital signs included a temperature of 99F and pulse oximetry of 95% on room air. respiratory rate of 16, heart rate of 96. and blood pressure of 129/96. He stated tbat bis wbeezing was improved but tbat bis dry cougb, mild sbortness of breatb. and fatigue bad not cbanged. He was placed in respiratory isolation as the imaging Undings 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 Huoroquinolone. Three consecutive daily-induced sputum samples were obtained: AFB smears prepared from concentrated specimens were all negative. As tbe suspicion for TB was high, two additional daily sputum samples were negative. Routine sputum and serum bacterial cultures, urinary Lef^ionella antigen. and urinary Histoplasma antigen returned negative. Serum Coccidioidomycosis IgG and IgM performed by immunodiffusion (Armstrong Labs, Brooks City Base, Texas) botb

Departments of *Radiology and $Infecliou Disease. David Grant USAF Medical Ceiiier. 101 Bodin Circle, Travis AFB. CA 94335. tDepartment of Radiology and Radiological Scietices. Uniformed Services University of the Heahh Sciences. 4301 Jone.s Bridge Road. Bethesda, MD 20814-4712. The views expressed in this article are those of the authors and do not reect the ofhcial policy or position of the U.S. government, the Department of Defense, or the Department of the Air Force.

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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 ihe lime of hospital admission), demonstrating developing consolidation in the righl upper lobe (curved black arrow) with new hazy peripheral nodular opacities (black arrowheads) in the right lower lobe and left upper lobe.

FIGURE 4. Uncnhanced axial computed tomography (CT) images of the ches!, demonstrating bronchiectalic airways (black arrowheads) in ihe right upper lobe with surrounding consolidation. Peripheral centriiobar nodules ("iree-in-bud" appearance) are noted scattered throughout the lungs (white arrowheads).

FIGURE 2. Posterior-anterior (PA) chest radiographs in a 61-year-old male ^ months after return from his trip, demonstrating hazy peripheral nodular opacities (black anowheads) in the right upjwr 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 noduUir 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 radiographie contrast (100 mL of Omnipaque 3(X)) also demonstrated nonspecific mediastinal adenopathy (Fig. 7).

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FIGURE 5. Unenhanced axial 3-mm-thick mas i mum-intensity projection (MIPl compuled tomography (CT) image of the chesl. demonsirating bmnchieciatic airway,s (black arrowheads) in ihe right upper Inbe wiih suiTounding consolidation. Peripheral centrilobar nodules C'tree-in-biid" appearance) are noted in the lel'i upper lobe (while arrowhead).

FIGURE 7. Conirast-enliaiiced axial computed totiiography (t'T) images nt Ihe chest, demonstrating mullipie, smali (less than I cm in si/c) lymph riinjes in the pretracheal and right hilar regions (black arrows). The increased number of visualized lymph nodes along with their morphologic Fullness was interpreied as pathologic. Note the calcifications in the right hilum associated with the right upper lobe calcified nodule (white arrows).

FIGURE 6. UneiilianuciJ asial computed Uiinography (CT) image of the chesl. demonslraling a calciiied nodule in ihe right upper lobe in association with a calcined right hilar lymph node (white arrows), consistent with a Ghon complex.

in the context ofthe patient's history, the clinical and imaging fmdings 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 ofthe 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

microbiologie 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. tubercukms {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

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F I G U R E 8.

M K I S L U I ' K |j;iiliulii^_\ iiiKi^L' ilifMiiiii\_\lLii-eosin s t a i n , l o w

puwtT l(H)x), demimslrating tinncasealing granuliHTias with giant cells (*).

FIGURE 10. Poslerior-atiterior (PA) chesi radiograph in otir paiieni ohtaincd 3 nuinihs ;itter initi;tlinj: therapy for pulmonary lu here ulosis. Note the progressive clearing of pulmonary consolidations when compared wiih Figure 3.

FIGURE 9. Microscopic pathology innige iKinyuun acid-fasi stain, high power 6il(Jx), 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 hi.s clinical symptom.s completely resolved. A repeat chest radiograph (Fig. 10) 3 months after initiating treatment noted partial clearing of the pulmonary consolidations.
I

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 radiologie 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).- Imaging tindings 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.' Host immune response often controls primary TB, usually resulting in pulmonai-y granuloma formation as well as calcified fibrotic hilar/mediastinal lymph nodes (Ghon's complex). In contrast, reactivation pulmonary TB lypically 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.^ ^ 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.'''^ Irreversible bronchiectasis is more commonly seen in inactive disease as a result of destruction

DISCUSSION Pulnu)niiry tuberculosis cases and annual TB rates in the United States recently reached all-time lows, with only 12,898 incident cases reported in 2008.' 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).' In addition, the highest prevalence of total cases was among individuals from countries in Asia. Given the current spectrum of United States

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and fibrosis ofthe lung parenchyma with secondary bronchial dilatation (traction bronchiectasis).^"* 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'" and in a patient with postobstructive bronchiectasis due to peanut impaction." 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 tbe deployed environment.

ACKNOWLEDGMENTS
The authors express their appreciation to Dr, Steve DeMartJni tor preparing the pathology images in (his case and to Dr. Bang Huynh and Dr. David Bigelow for reviewing ihe initial versions ofihis article.

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