International Journal of Infectious Diseases 32 (2015) 87–93

Review

Imaging in tuberculosis

Evangelia Skoura a, Alimuddin Zumla b, Jamshed Bomanji a,*a Institute of Nuclear Medicine, University College Hospitals NHS Trust, London NW1 2BU, UKb Division of Infection and Immunity, Centre for Clinical Microbiology, University College London, and NIHR Biomedical Research Centre,

University College London Hospitals, London, UK

A R T I C L E I N F O

Article history:

Received 14 November 2014

Received in revised form 28 November 2014

Accepted 1 December 2014

Corresponding Editor: Eskild Petersen,Aarhus, Denmark

Keywords:

Pulmonary tuberculosis

Extrapulmonary tuberculosis

Computed tomography

Positron emission tomography

Fluorodeoxyglucose

Magnetic resonance imaging

S U M M A R Y

Early diagnosis of tuberculosis (TB) is necessary for effective treatment. In primary pulmonary TB, chest

radiography remains the mainstay for the diagnosis of parenchymal disease, while computed

tomography (CT) is more sensitive in detecting lymphadenopathy. In post-primary pulmonary TB, CT

is the method of choice to reveal early bronchogenic spread. Concerning characterization of the infection

as active or not, CT is more sensitive than radiography, and 18F-fluorodeoxyglucose positron emission

tomography/CT (18F-FDG PET/CT) has yielded promising results that need further confirmation. The

diagnosis of extrapulmonary TB sometimes remains difficult. Magnetic resonance imaging (MRI) is the

preferred modality in the diagnosis and assessment of tuberculous spondylitis, while 18F-FDG PET shows

superior image resolution compared with single-photon-emitting tracers. MRI is considered superior to

CT for the detection and assessment of central nervous system TB. Concerning abdominal TB, lymph

nodes are best evaluated on CT, and there is no evidence that MRI offers added advantages in diagnosing

hepatobiliary disease. As metabolic changes precede morphological ones, the application of 18F-FDG PET/

CT will likely play a major role in the assessment of the response to anti-TB treatment.

� 2015 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-

nc-nd/4.0/).

Contents lists available at ScienceDirect

International Journal of Infectious Diseases

jou r nal h o mep ag e: w ww .e lsev ier . co m / loc ate / i j id

1. Introduction

Tuberculosis (TB) remains a global emergency despite substan-tial investment in health services over the past two decades.Patients with sputum-negative pulmonary TB (PTB) and extra-pulmonary TB (EPTB) are difficult to diagnose and may be missedat all points of care. Diagnostic imaging is challenging becausesigns of TB may mimic those of other diseases such as neoplasms orsarcoidosis. Clinical signs and symptoms in affected adults can benon-specific and a high level of pre-test clinical suspicion based onhistory is fundamental in the diagnostic work-up. The globalimpact of TB is extremely important, considering that an estimated9.0 million people developed TB in 2013 and 1.5 million died fromthe disease, according to the recent World Health Organization(WHO) global tuberculosis report 2014.

Early diagnosis promotes effective treatment and leads to areduced onward transmission of TB. This article gives a review ofimaging patterns of chest TB as may be detected on conventionalradiography and computed tomography (CT). The main aim is to

* Corresponding author.

E-mail address: jamshed.bomanji@uclh.nhs.uk (J. Bomanji).

http://dx.doi.org/10.1016/j.ijid.2014.12.007

1201-9712/� 2015 The Authors. Published by Elsevier Ltd on behalf of International Solicense (http://creativecommons.org/licenses/by-nc-nd/4.0/).

improve the radiologist’s familiarity with the spectrum of imagingfeatures of this disease in order to facilitate timely diagnosis.Furthermore, we consider the emerging role of alternativemethods of imaging, such as magnetic resonance imaging (MRI),which can be helpful and highly accurate for a better definition ofsome of the signs of TB.

Although new imaging methods are now being used, conven-tional radiography remains the initial modality for suspected PTB andfor mass screening purposes.1 CT and MRI are the modalities of choicefor the evaluation of specific body parts.1 Positron emissiontomography/computed tomography with the use of 18F-fluorodeox-yglucose (18F-FDG PET/CT) is a non-invasive imaging method thathas been used widely for the differentiation of malignant frombenign lesions. However, 18F-FDG also accumulates in inflammatorycells such as neutrophils, activated macrophages, and lymphocytes atthe site of inflammation or infection.2 Consequently, 18F-FDG uptakeis observed in PTB, in tuberculoma, and in other TB-related lesions.3,4

Using PET/CT, pulmonary and extrapulmonary TB involvement isassessed simultaneously, with time- and cost-saving implications.

Although any organ of the body can be involved, the lungremains the most commonly involved organ in TB. The imagingappearances of TB are described below for both pulmonary andextrapulmonary involvement.

ciety for Infectious Diseases. This is an open access article under the CC BY-NC-ND

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E. Skoura et al. / International Journal of Infectious Diseases 32 (2015) 87–9388

2. Pulmonary tuberculosis

Classically, PTB can be divided into a primary and a post-primary pattern, each presenting with characteristic radiologicalfeatures. In practice, however, it is very difficult to draw distinctlines between these radiographic patterns, and there is consider-able overlap in the radiological manifestations.5

2.1. Primary tuberculosis

Primary TB is due to first-time exposure to Mycobacteriumtuberculosis. At radiology, primary PTB manifests as four mainentities – parenchymal disease, lymphadenopathy, pleural effu-sion, and miliary disease – or any combination thereof.1

Chest radiography continues to be the mainstay of diagnosis.Typically, parenchymal disease manifests as consolidation in anylobe, with predominance in the lower and middle lobes.6 In thesecases, the bacterial infections are much more likely to be the causeof such radiological features and hence the findings are non-specific, although primary infection should be suspected inindividuals at risk of exposure to TB. Multilobar consolidationcan be seen in almost 25% of cases.1 In approximately two-thirds ofcases, the parenchymal lesion resolves without sequelae onconventional radiography.6 In the remainder, a radiological scarpersists that can be calcified in up to 15%, while persistent mass-like opacities called tuberculomas are seen in approximately 9% ofcases.6 Frequently, the only radiological evidence suggestive ofprevious TB is the so-called Ranke complex: the combination of aparenchymal scar, calcified or not (Ghon lesion), and calcified hilarand/or paratracheal lymph nodes.5 Destruction and fibrosis of thelung parenchyma result in the formation of traction bronchiectasiswithin the fibrotic region.5

The most common abnormality in children is lymph nodeenlargement, which is seen in 90–95% of cases; by comparison, inadults the percentage reaches up to 43%.7 Right paratracheal andhilar lymph nodes are the most common sites of nodal involve-ment, although involvement is bilateral in about a third of cases. CTis more sensitive than plain radiography in detecting tuberculouslymphadenopathy. It reveals nodes often measuring more than2 cm, with a very characteristic, but not pathognomonic, ‘rim sign’that consists of a low-density centre, representing caseousnecrosis, surrounded by a peripheral enhancing rim due togranulomatous inflammatory tissue.8,9

In contrast to lymphadenopathy, the prevalence of radiographi-cally detectable parenchymal involvement is significantly lower inchildren up to 3 years old (51%) than in older children, among whomthe prevalence is similar to the reported percentage in adults(80%).7,8 Also, evolution to cavitary disease is rare in children.5

Figure 1. Arrows indicate a mildly 18F-FDG avid right lower lobe nodule measuring 1.5tuberculosis.

Concerning the role of 18F-FDG PET/CT, two distinct patterns ofPTB have been described: (1) the lung pattern, related to arestricted and slight hypermetabolic infection, with 18F-FDGuptake in areas of lung consolidation � cavitation surrounded bymicronodules and mild uptake within lymph nodes, and (2) thelymphatic pattern, related to a systemic and intense infection, withmore enlarged and 18F-FDG-avid hilar and mediastinal lymphnodes.10

A limitation to the use of 18F-FDG PET/CT for the assessment of asingle pulmonary nodule, especially in endemic areas, is theinability to distinguish tubercular from malignant lesions(Figure 1).11 Studies investigating the diagnostic value of dualtime-point 18F-FDG PET/CT imaging have shown limited promise,but further investigations in larger series of patients arewarranted.12,13

2.2. Post-primary tuberculosis

Post-primary PTB is one of the many terms (includingreactivation, secondary, or adulthood) applied to the form of TBthat develops and progresses under the influence of acquiredimmunity.5 The most common radiographic manifestation of post-primary PTB is focal or patchy heterogeneous, poorly definedconsolidation involving the apical and posterior segments of theupper lobes and the superior segments of the lower lobes(Figure 2).14,15 In the majority of cases, more than one pulmonarysegment is involved.6 Cavitation, the radiological hallmark of PTB,is radiographically evident in 20–45% of patients (Figure 3), whileair-fluid levels in the cavity occur in 10% of cases.14,15 Cavitationmay progress to endobronchial spread and results in a typical ‘tree-in-bud’ distribution of nodules in addition to cavitation; this isconsidered a reliable marker of active TB.16 High-resolution CT isthe method of choice to reveal early bronchogenic spread, with 2-to 4-mm centrilobular nodules and sharply marginated linearbranching opacities around terminal and respiratory bronchioles(tree-in-bud sign).16 The tree-in-bud sign is the constellation ofsmall centrilobular nodules and concomitant branching opacities,which mimics the branching pattern of a budding tree.17 Thecentrilobular nodules are peripheral, spare the subpleural lung,and denote the inflammatory lesions in the bronchioles andperibronchial alveoli.16,17 Hilar or mediastinal lymphadenopathyis uncommon in post-primary PTB, seen in only 5–10% of patients(Figure 4).18,19

Although pulmonary tuberculomas are most often the result ofhealed primary PTB, a pulmonary tuberculoma is the main or onlyabnormality on chest radiographs in approximately 5% of patientswith reactivation.20 The CT scan shows a round or oval granuloma,measuring from 0.4 to 5 cm in diameter, with a wall lined by

cm (SUVmax 2). The differential diagnosis for this nodule would include cancer or

Figure 2. Trans-axial CT section showing a patchy, heterogeneous, poorly defined consolidation with cavitating lesion in the upper lobe of the right lung.

E. Skoura et al. / International Journal of Infectious Diseases 32 (2015) 87–93 89

inflammatory granulomatous tissue or encapsulated by connectivetissue.21 Tuberculomas can cavitate, while calcification is found in20–30% of them.21 In 80% of cases, satellite lesions are observed inthe immediate vicinity of the main lesion.5 Because of increasedglucose metabolism caused by active granulomatous inflammation,tuberculomas may accumulate 18F-FDG.22 Maximum standardizeduptake values (SUVmax) tend not to be significantly different fortuberculous and malignant lesions.23,24 One study has suggestedthat unlike 18F-FDG PET, the 11C-choline PET scan can help todifferentiate between lung cancer and tuberculoma, becausetuberculoma shows low tracer uptake on 11C-choline PET scan.25

2.3. Radiological patterns in primary and/or post-primary PTB

Miliary pulmonary disease affects between 1% and 7% ofpatients with all forms of TB.6 It is usually seen in the elderly,infants, and immunocompromised persons.6 Initially, standardradiographs are normal in 25–40% of cases.26 CT can demonstratemiliary disease before it becomes radiographically apparent, andits characteristic findings consist of innumerable 1- to 3-mm-diameter nodules randomly distributed throughout both lungs,often associated with intra- and interlobular septal thickening.14,27

The nodules usually resolve within 2–6 months with treatment,without scarring or calcification; however, they may coalesce toform focal or diffuse consolidation.6

A pleural effusion is seen in approximately one-fourth ofpatients with primary PTB and in 18% of post-primary PTB.26

Although, usually observed in association with parenchymal

Figure 3. Left panel: CT image showing a 1.6 � 1.2-cm cavitating lesion (arrow) in the upPET scan (small arrow) (SUVmax 2.2). Bottom left panel: Fused

18F-FDG PET/CT image s

and/or nodal disease, pleural effusion has been reported to be theonly radiographic finding indicative of primary PTB in approxi-mately 5% of adult cases.26 Pleural effusion is usually unilateral andon the same side as the primary focus of PTB, while complicationssuch as effusion, empyema, and bronchopleural fistula are rare.6 TheCT scan of patients with post-primary pleural effusion typicallyshows smooth thickening of visceral and parietal pleura.28

Ultrasonography often demonstrates a complex septated effusion.6

Fibrothorax with diffuse pleural thickening, but without pleuraleffusion on CT, suggests inactivity.29 The 18F-FDG PET/CT scan maydemonstrate diffusely intense 18F-FDG uptake in thickened pleurathat can be confused with pleural mesothelioma.30

2.4. Differentiation between active and inactive TB

TB makes its presence felt on imaging long after the resolutionof disease. Sometimes a question that needs to be answered iswhether the infection is active or not. Active disease is in generalcharacterized by the presence of centrilobular nodules, tree-in-budpattern, thick-walled cavities, consolidation, miliary nodules,pleural effusions, or necrotic lymphadenopathy.1 Resolution tothin-walled smooth cavities, fibrosis, and parenchymal, nodal, orpleural calcifications often denotes inactive disease.1

Chest radiographs may be normal or show only mild or non-specific findings in patients with active disease.26 The diagnosis ofPTB with radiography is initially correct in only 49% of all cases:34% for primary and 59% for post-primary PTB.26 On the otherhand, CT can correctly diagnose 91% of cases of PTB and correctly

per lobe of the right lung. Right panel: this lesion shows mild 18F-FDG uptake on the

howing the same cavitating avid lesion (arrow).

Figure 4. Left panel: Multiple intensity projection image showing 18F-FDG uptake in the mediastinal and bilateral hilar lymph nodes (arrows). Right panel: Multiple fusedtrans-axial section 18F-FDG PET/CT images showing hilar and mediastinal lymph nodes (arrows).

E. Skoura et al. / International Journal of Infectious Diseases 32 (2015) 87–9390

characterize 80% of patients with active disease and 89% withinactive disease.31

CT is more sensitive than radiography in the detection andcharacterization of both parenchymal disease and mediastinallymphadenopathy.9,32 In a study that compared the two methods,high-resolution CT showed cavities in 58% of patients with activePTB, whereas chest radiographs in only 22%.32 The diagnosis of activePTB was based on positive acid-fast bacilli in sputum and changes onserial radiographs obtained during treatment.32 CT may also showpleural disease that is not evident on chest radiography and behelpful in the evaluation of pleural complications.33

CT features predictive of highly infectious/active PTB includethe following:34 (1) consolidation involving the apex or theposterior segment of the right upper lobe or the apico-posteriorsegment of the left upper lobe, (2) consolidation involving thesuperior segment of the right or left lower lobe, (3) a cavity lesion,(4) clusters of nodules, and (5) absence of centrilobular nodules.High-resolution CT is better than chest radiography in predictingactive PTB, with a sensitivity of 96% versus 48%.35

It has been reported that 18F-FDG PET is able to differentiateactive PTB from old or inactive disease, as active tuberculoma hassignificantly higher SUVmax values compared with inactivetuberculoma.3 When a SUVmax of 1.05 (at 60 min) was used asthe cut-off, the sensitivity and specificity were 100% and 100%,respectively.3 A recent study concluded that 18F-FDG PET/CT hasthe potential to become a tool for monitoring the treatmentresponse in selected cases of EPTB or multidrug resistance.36 Aninteresting study of patients with radiographic lesions suggestiveof old healed TB aimed to gather information on the metabolicstatus of TB lesions using 18F-FDG PET/CT imaging.37 The authorsshowed that patients with old healed TB lesions with a higherSUVmax may be at higher risk of active TB.

37 Further investigation isneeded to confirm these results.

3. Extrapulmonary tuberculosis

Despite recent advances in imaging, the diagnosis of extra-pulmonary involvement sometimes remains difficult.38 The

imaging of some frequent extrapulmonary sites of TB is reviewedbelow.

3.1. Musculoskeletal tuberculosis

Approximately 50% of cases of skeletal TB involve the spine.6

Spondylodiscitis, also known as Pott’s disease, is the mostcommon form.39 The infection begins in subchondral bone andspreads slowly to the intervertebral disk space and the adjacentvertebral bodies, commonly in the lower dorsal and upper lumbarspine.40 Failure to identify and treat these areas of involvement atan early stage may lead to serious complications such as vertebralcollapse, spinal compression, and spinal deformity.38 Plainradiography is normal early in the disease.1 The first sign maybe demineralization of the endplates with resorption and loss ofdense margins. As the disease progresses, radiography will showprogressive vertebral collapse with anterior wedging and gibbusformation.1 MRI is the preferred imaging modality in thediagnosis and assessment of tuberculous spondylitis.41,42 Be-cause of the often multifocal nature of spinal TB, the MRI imagingof the entire spinal column could be more effective in the earlydiagnosis of the disease.43 In cases of spinal TB, the spinal cord issusceptible to myelopathy secondary to compression from anepidural abscess.6 The collapsed vertebra along with theepidural collection/abscess is also best evaluated on MRI.6 Afterantibiotic administration is initiated, repeat imaging is advised atapproximately 4-week intervals or at any time if neurologicaldeterioration occurs.44

As tubercular lesions demonstrate high 18F-FDG uptake, 18F-FDG PET/CT is a promising technique for the diagnosis of spinalinfection (Figures 5 and 6).45–48 An interesting finding was that63.6% of patients with spinal TB had clinically occult non-contiguous multifocal skeletal involvement at the time ofwhole-body 18F-FDG PET/CT scan.49

Besides the spine, any part of the musculoskeletal system canbecome involved, but the large joints of the lower limbs are mostcommonly affected. Imaging findings in musculoskeletal TB areoften non-specific. MRI is the most sensitive modality for earlydiagnosis and complete delineation of the disease.1

Figure 5. CT (left panel) and 18F-FDG PET/CT fused images (right panel): trans-axial and sagittal sections. Moderate to intense 18F-FDG uptake is seen in a paravertebral softtissue mass lesion extending from the level of T7–T10 vertebrae with associated lytic sclerotic changes in T7–T9 vertebrae and collapse of the T8 vertebra (arrows). The lesion

infiltrates into the spinal canal at the level of the T8 vertebra and involves the spinal cord (small arrow). The lesion is seen to extend along the left costal margin, with faint 18F-

FDG uptake and foci of calcification, likely representing a cold abscess (courtesy of Prof. B.R. Mittal).

E. Skoura et al. / International Journal of Infectious Diseases 32 (2015) 87–93 91

3.2. Central nervous system (CNS) tuberculosis

TB of the CNS is a highly devastating form of the disease. Variousforms of involvement of the CNS are observed: parenchymal,meningeal, calvarial, spinal, or any combination thereof.1 MRI isgenerally considered superior to CT in detecting and assessing CNSTB.50 Parenchymal involvement is most frequently seen in the form ofa tuberculoma, which may be single or multiple. In the paediatric agegroup it is seen more frequently in the cerebellum, whereas in adultsit has a predilection for the cerebral hemispheres and basal ganglion.The appearance of a tuberculoma varies on MRI depending on itsstage of maturation.50,51 A non-caseating granuloma is hyperintenseon T2 and hypointense on T1 and shows solid enhancement, while asolid caseating granuloma is usually hypointense on both T1 and T2images. On CT, tuberculomas appear as round or lobulated soft tissuemasses with varying attenuation and homogeneous or ringenhancement.1 Miliary TB is often associated with TB meningitisand presents as small (

Figure 6. Multiple intensity projection image (left panel) and fused trans-axial section 18F-FDG PET/CT images (right panel) showing 18F-FDG uptake in multiple lymph nodes(SUVmax 6.8) (porta hepatis, portacaval, para-aortic, retroperitoneal, bilateral internal iliac, left external iliac, and left inguinal (arrows)) and heterogeneous

18F-FDG uptake in

the grossly enlarged spleen (SUVmax 10.2) (arrow) and in bones (T8 vertebra coupled with paravertebral soft tissue uptake (SUVmax 17.6), L3 vertebral body anteriorly (SUVmax11.6), and the right sacral alae (SUVmax 6.7) (arrows)) (courtesy of Dr A. Alshammari).

E. Skoura et al. / International Journal of Infectious Diseases 32 (2015) 87–9392

Few reports are available on 18F-FDG PET/CT imaging inabdominal TB, showing that the appearance of abdominal TB isnon-specific and varied (Figure 6).56–58

4. Assessment of treatment response

This is potentially the most important clinical application of 18F-FDG PET/CT in TB. During anti-TB treatment, some bacillus-negativetuberculomas do not decrease in size and may even increase, makingit difficult for the physician to decide whether or not to modifytreatment. In these cases, 18F-FDG PET/CT imaging may help, as thechanges in glycolytic activity within the inflammatory lesion,measured by 18F-FDG uptake, correlate well with the clinicalmarkers of response.49 Several studies have confirmed the value of18F-FDG PET/CT in the follow-up and evaluation of the treatmentresponse, especially in patients with extrapulmonary involvementand when drug resistance is prevalent.57,59–63 In pulmonary andextrapulmonary TB, a decrease of approximately one-third inSUVmax has been reported after 1 month of anti-TB treatment whenthere is a good response.60 Initial data has shown that SUVmax (bothearly and delayed) of involved lymph nodes and the number ofinvolved lymph node basins are significantly higher in non-responders than in responders.64 These findings warrant furtherconfirmation in larger cohorts of patients.

After 4 months of anti-TB treatment 18F-FDG PET/CT can alsoevaluate the treatment response in patients with high sensitivity andspecificity, using the value of 4.5 as the SUVmax cut-off.

62

Other authors have aimed to monitor the metabolic changes inspinal TB during the course of therapy.49 The mean changes inSUVmax at various time points – from baseline to 6, 12, and18 months, from 6 to 12 months, from 6 to 18 months, and from 12 to18 months – were calculated and found to be highly significant (p-value

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Imaging in tuberculosis1 Introduction2 Pulmonary tuberculosis2.1 Primary tuberculosis2.2 Post-primary tuberculosis2.3 Radiological patterns in primary and/or post-primary PTB2.4 Differentiation between active and inactive TB

3 Extrapulmonary tuberculosis3.1 Musculoskeletal tuberculosis3.2 Central nervous system (CNS) tuberculosis3.3 Abdominal tuberculosis

4 Assessment of treatment response5 Tuberculosis in HIV patientsReferences