Pediatr Radiol (2004) 34: 861875 DOI 10.

1007/s00247-004-1236-2

MINISYMPOSIUM

Savvas Andronikou Nicky Wieselthaler

Modern imaging of tuberculosis in children: thoracic, central nervous system and abdominal tuberculosis

Received: 2 March 2004 Accepted: 17 April 2004 Published online: 15 September 2004 Springer-Verlag 2004

S. Andronikou (&) N. Wieselthaler Radiology Department, Red Cross Childrens Hospital, Klipfontein Rd, Rondebosch, 7700 Cape Town, South Africa E-mail: docsav@mweb.co.za Tel.: +27-21-6585422 Fax: +27-21-6585101 S. Andronikou (&) N. Wieselthaler School of Child and Adolescent Health, University of Cape Town, Cape Town, South Africa

Abstract Tuberculosis (TB) can affect any organ in the body. Children are a high-risk group for contracting the disease and pose a constant challenge to clinicians with regard to making a denitive diagnosis. Radiologists are playing a more active role in diagnosing TB, and armed with more accurate diagnostic investigations such as CT and MRI, they must face the cost implications as well as technical limitations. This review aims to guide the reader through the modern imaging techniques useful for diagnosing TB of the thorax, central nervous system and abdomen in children. The more specic features of each modality in the particular anatomical regions are highlighted.

Keywords Tuberculosis Lung Brain Meninges Abdomen MRI CT Ultrasound Radiography Children

Introduction
The incidence of tuberculosis (TB) is increasing in both the developing and the developed worlds [1] and children in particular represent a high-risk group for acquiring the disease [2]. Infection is usually acquired via the lungs, making pulmonary TB the commonest form of tuberculous infection [3, 4]. The organism gains access to the blood stream via the lymphohaematogenous route and may then aect any organ [3, 5]. The incidence of extrapulmonary TB is increasing, especially because of HIV [3, 5]. Diagnosis of TB, however, is often dicult and imprecise [3, 4, 6, 7] and

is conrmed in less than 40% of cases. This is because of non-specic symptoms [1, 8], non-productive cough for sputum collection [4, 6], the low yield of gastric aspirates (3060%) [2, 6, 9, 10] and the unreliability of Mantoux testing in young children [3, 6, 11]. Growth of the organism for denitive diagnosis, especially from CSF for tuberculous meningitis (TBM), takes from 2 to 6 weeks and the diagnostic yield is low [2]. The result is that diagnosis often relies on imaging [6, 7]. This review will guide the reader through the variety of images that represent TB in children and will highlight the cross-sectional features of TB that may improve diagnostic accuracy.

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Thoracic TBpulmonary, mediastinal, pleural and pericardial

Plain radiographs Plain radiographs are eective in demonstrating airspace disease (one-quarter of patients; Fig. 1), the parenchymal nodule that represents the Ghon focus (Fig. 1), diuse interstitial disease (one-third of patients; Fig. 1) and eusions (uncommon; Fig. 1) [4, 6]. It is the presence of lymphadenopathy that is of diagnostic importance, however [7]. Plain radiographs have been shown to be insensitive for the detection of lymphadenopathy [11, 12] and there are signicant inter- and intra-observer dierences in the detection of lymphadenopathy by lm readers [13]. On plain radiographs, lymphadenopathy is seen on the AP radiograph as a lobulated density occupying the hilum and obliterating the hilar point [14]. The hilum assumes an outwardly convex appearance (Fig. 2). Because of the presence of a thymus and other normal structures making up the mediastinum and hilum on the AP lm, lymphadenopathy may be masked [14]. The position, contour and calibre of the trachea are useful for determining the presence of mediastinal lymphadenopathy on the AP lm (Fig. 2). On frontal radiographs, lymphFig. 1 Plain radiographic features of pulmonary TB in children. a There is bilateral parenchymal air-space disease (worse on the right). The right main bronchus and bronchus intermedius show reduced calibre and the carina is splayed, suggesting the presence of lymphadenopathy. b This radiograph clearly demonstrates the Ghon complex, because both the parenchymal granuloma in the left upper lobe and the left mediastinal node are calcied. Calcication in childhood pulmonary TB is unusual. c Miliary TB is represented on plain radiographs by multiple bilateral diusely distributed small nodules. d Tuberculous pleural eusion is rare in childhood. In this patient the eusion outlines the major ssure. No overt hilar or mediastinal lymphadenopathy is identied

adenopathy may be sharply dened and lobulated, or can be ill-dened with vague borders [15]. Lateral lms are still in use in South Africa because they are believed to assist in determining the presence of hilar lymphadenopathy [4, 13, 15]. Lateral radiographs demonstrate lymphadenopathy as lobulated densities seen posterior to the bronchus intermedius [14]. The lymphadenopathy completes the inferior portion of a doughnut-shaped density; the upper half is seen in normal individuals as an up-side-down horse-shoe made up of the right and left main pulmonary arteries and the aortic arch (Fig. 3) [14]. Displacement of and impression on the tracheobronchial tree as well as splaying of the carina can be shown with high-kilovolt ltered radiographs [15] (Fig. 4). The routine use of high-kilovolt radiographs has been shown to be unwarranted [16]. CT scanning CT scanning is considered the modality of choice for lymph node detection in the chest [14, 17, 18]. The disadvantages, however, include limited availability, high radiation dose, the need for IV contrast medium and the necessity in certain cases for sedation. CT has shown

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Fig. 2 Tuberculous lymphadenopathy on plain frontal radiographs. a This radiograph demonstrates increased density, lobulation and enlargement of the right hilum with lling of the hilar point. These features represent lymphadenopathy and there is accompanying left lower lobe air-space disease/collapse. b This radiograph also demonstrates enlargement of the right hilum and lling of the hilar point which assumes a convex lobulated lateral margin. There is an associated small eusion in the minor ssure. c On this radiograph, the trachea is displaced to the left and it is bowed with a concave right margin, in keeping with right paratracheal lymphadenopathy. There is accompanying air-space disease in the right lower lobe as well as rounded air-space disease in the right upper lobe projecting separately from the mediastinum

lymphadenopathy in up to 60% of TB cases with normal chest radiographs [12]. Using CT scanning we have shown at our institution a high incidence of thoracic
Fig. 3 Lateral radiographic demonstration of tuberculous lymphadenopathy. a Lymphadenopathy is visualized as a high-density lobulated mass occupying the position posterior to the bronchus intermedius and the position below the bifurcation of the trachea. Enlarged nodes in these locations result in the formation of a doughnut shape at the hilum, by completing the lower half of the inverted horseshoe formed by the normal main pulmonary artery (anteriorly), the left main pulmonary artery (superiorly) and the aortic arch (posteriorly). b In this patient, the bronchus intermedius is not visible but there is a rounded hilar mass, rather than an inverted horseshoe, indicating lymphadenopathy

Fig. 4 High-kilovolt radiograph demonstrating lymphadenopathy. High-kilovolt lm demonstrates left main bronchus attenuation by presumed lymphadenopathy which was not evident on the conventional radiograph

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Fig. 5 CT scan appearances of tuberculous lymphadenopathy. a Anterior mediastinal and right paratracheal lymphadenopathy is demonstrated on this contrast-enhanced CT scan of the chest. The anterior mediastinal nodes can be distinguished from thymus by the curvilinear enhancement referred to as being ghost-like. This is a more common pattern of enhancement than the widely reported low-density rim-enhancing lymphadenopathy ascribed to tuberculous disease. When the right paratracheal lymphadenopathy is nonenhancing and must be dierentiated from normal thymus, it is useful to look at other distant sites such as the subcarinal region for associated lymphadenopathy because TB lymphadenopathy is most often multifocal. b On this contrasted CT scan the more typical pattern of low-density rim-enhancing lymphadenopathy is seen in the subcarinal and right hilar positions. The right-sided parenchymal air-space disease and eusion support the diagnosis

lymph nodes in children with suspected TB, but less than 50% of these had nodes greater than 1 cm [17]. This raises the issue of what size of thoracic lymph node should be considered pathological on CT in children [17,

18]. We have found the subcarinal node group to be the commonest site for lymphadenopathy, but that multiple sites are usually aected [17]. Intravenous contrast medium should always be used to distinguish lymph nodes from normal vessels, but even with the use of contrast medium we have diculty distinguishing right paratracheal and anterior mediastinal nodes from the thymus. Ghost-like enhancement (Fig. 5) is more common than the characteristic low-density ringenhancing lymphadenopathy described by other authors [14, 15, 17, 19] (Fig. 5). We found calcication to be an uncommon feature of tuberculous lymphadenopathy in children [4, 17]. CT is also useful for demonstrating pleural and pericardial disease (Fig. 6) including pleural thickening, enhancement, uid collections and calcied brothorax (Fig. 6) [19]. Axillary lymphadenopathy is demonstrated regu-

Fig. 6 CT scan features of pleural and pericardial tuberculous disease. a There is a large right pleural eusion. A loculated eusion is also present on the left anteriorly. Focal pleural thickening is present on the right adjacent to the heart and on the left at the mid thoracic level. b The right focal pericardial abscess is well demonstrated with CT. c There is severe widespread tuberculous pleural thickening on the left with calcication and loculated areas of pleural uid. The lung is small and consolidated. On the right there are at least two areas of focal pleural thickening. d A patient with pulmonary TB shows anterior mediastinal and paratracheal lymphadenopathy, and demonstrates bilateral axillary lymphadenopathy

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larly on CT in patients with suspected pulmonary TB, but is only moderately sensitive and poorly specic for the presence of intrathoracic lymphadenopathy (personal observation; Fig. 6). High-resolution CT of the chest is ideal for demonstrating acute blood-borne disseminated disease in the lung; the phenomenon known as miliary TB (Fig. 7). We have not identied criteria to distinguish the nodular pattern from that of HIVassociated lymphoid interstitial pneumonitis. Plain radiographs demonstrate miliary TB relatively well (Fig. 7) and the indication for high-resolution CT (HRCT) may be limited.

Magnetic resonance imaging The use of MRI for demonstrating intrathoracic lymphadenopathy is limited because of the sedation/ anaesthetic and respiratory gating requirements, as well as the limited availability in countries where TB is endemic. Necessity for sedation and anaesthesia are not warranted at present. Lymphadenopathy is well demonstrated on STIR imaging as high-signal masses in recognized regions. Incidental identication of lymphadenopathy occurs during imaging of TB spondylitis, which sometimes also reveals miliary disease (Fig. 7), and these features must be recognized as supportive evidence for the diagnosis.

Central nervous system tuberculosis

Tuberculosis usually accesses the intracranial compartment via the blood stream, but may also result from direct spread of calvarial (Fig. 8) or middle ear infection. Central nervous system (CNS) TB may be focal, in the form of a tuberculoma or a tuberculous abscess, or may be more widespread, in the form of meningitis and arachnoiditis. Focal lesions Computed tomography Tuberculomas form 99% of all focal TB lesions and usually occur without tuberculous meningitis (TBM). On CT these lesions are iso- or hyperdense to cortex before administration of IV contrast medium. This feature dierentiates these lesions from abscesses, which are of low density and are usually larger than 2 cm [2022]. Tuberculomas may be ring enhancing or nodular/discoid enhancing, and show surrounding oedema. They are usually single, smaller than 2 cm in size and they rarely calcify [2022]. TB abscesses, which are larger and also rim-enhance, are of low density cen-

Fig. 7 Modern and conventional imaging of miliary TB. a Highresolution CT scanning (HRCT) demonstrates bilateral symmetrical interstitial nodules, typical of miliary TB. b The conventional radiograph demonstrates the nodular pattern of miliary TB very well and the necessity for HRCT is questionable. c Incidental demonstration of miliary TB in the lungs in a patient during spinal imaging for tuberculous arachnoiditis

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Fig. 8 Calvarial tuberculous osteitis with meningeal involvement. a Coronal CT scan on bone windowing demonstrates bone destruction of the right squamous temporal bone and sphenoid wing with soft-tissue swelling in keeping with but not diagnostic of tuberculous osteitis. b Contrast-enhanced axial images in the same patient demonstrate meningeal involvement which has occurred via the calvarial portal of entry

trally. They are therefore indistinguishable from pyogenic abscesses and can also be confused with neoplasms. (Fig. 9). Magnetic resonance imaging Tuberculomas have a characteristic low signal on T2weighted images and on T1-weighted images the signal is isointense to that of cortex [2325]. There is accompanying surrounding oedema and rim enhancement occurs after IV gadolinium administration (Fig. 10). Sometimes the centre of a tuberculoma may show some hyperintensity as the gummatous necrosis gives way to caseous necrosis [23, 24]. TB abscesses, however, have features inseparable from pyogenic abscesses (Fig. 11), with T2 hyperintensity and T1 hypointensity, surrounding oedema and rim enhancement [25, 26]. TB meningitis Computed tomography This is the most severe and life-threatening form of TB in children [23, 2729]. Even though the CNS is involved in a more diuse manner, TBM may be asymmetrical, unilateral and even focal. CT scanning has become essential for rapid diagnosis and detection of the complications of TBM. Diagnosis should be based on identifying basal enhancement as this is (in our experience) the most sensitive nding, and it is characteristic of TBM. Basal enhancement may be subtle on CT scanning and has variable appearances. These are demonstrated in Fig. 12. Basal enhancement has ill-dened edges

compared with normal vessel enhancement and usually aects the suprasellar, middle cerebral artery and sylvian cisterns [29]. The double-line sign represents meningeal enhancement of two adjacent lobes and visualization of the vessel between these results in a triple-line sign. In about 50% of patients the meningeal exudates/granulation tissue produced can be identied on non-contrast scans as hyperdensity in the basal cisterns [30] (Fig. 13). This is the most specic sign of TBM and similar appearances are only found in patients who have subarachnoid haemorrhage or intrathecal contrast medium. Infarcts, due to the vasculitis which complicates TBM, are determinants of prognosis, with bilateral basal ganglia infarcts having a very poor prognosis [4, 31] (Fig. 14). Infarcts also occur adjacent to areas of severe meningeal and cisternal inammation due to direct extension of disease into the parenchyma, and are known as border-zone infarction. Hydrocephalus is the other major complication of TBM and is usually of the communicating type, which does not often require shunting. The appearances may be confused with cerebral atrophy, a common accompanying feature in malnourished ill children. True non-communicating hydrocephalus may result in markedly enlarged ventricles, periventricular lucency and features of raised intracranial pressure. This improves dramatically after shunting procedures [3134] (Fig. 15). The triad of basal enhancement, hydrocephalus and infarct has the same specicity as cisternal hyperdensity prior to contrast medium administration. In countries with nancial constraints, a diagnosis on non-contrast scanning may be essential for preserving resources.

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Fig. 9 CT features of cerebral tuberculoma and tuberculous abscess. a The right frontal tuberculoma typically shows an isodense centre to cortex, rim enhancement and surrounding oedema. This is the most common appearance of focal tuberculous lesions of the brain. b A variable pattern of enhancement of tuberculoma may be the result of dierent amounts of central necrosis. This patient who presumably has very little necrosis in the centre of a tuberculoma shows discoid or nodular enhancement with surrounding oedema. c The tuberculous abscess, which represents less than 5% of all focal cerebral tuberculous lesions, characteristically demonstrates a low-density centre with rim enhancement and surrounding oedema. d A TB abscess in this patient should be distinguished from a tuberculoma because it is larger than 2 cm in size and has a lowdensity centre. It is indistinguishable from a pyogenic abscess. Lack of a soft-tissue nodule/component dierentiates this from most neoplasms

Magnetic resonance imaging MRI is an excellent tool for detecting basal enhancement, which stands out against the ow voids in the vessels of the circle of Willis, and for the detection of infarction (Fig. 16). It is, however, unlikely to make an impact on the diagnosis of TBM worldwide, because of the limited availability in areas where it is needed most and also because of the technical considerations of lifesupport equipment and requirement for anaesthesia/ sedation in younger children [24, 35]. Spinal arachnoiditis is thought to be uncommon, but the MRI features may be identied in more cases of TBM if the cord were to be imaged more often. MRI with IV gadolinium is the modality of choice for making the diagnosis and this demonstrates enhancement of the dura-arachnoid complex around the cord, enhancing nodules and even

segmental signal abnormality and enhancement of the cord itself (Fig. 17) [36].

Abdominal TB
Abdominal TB is less common in children than in adults [3], but the incidence is rising due to the HIV epidemic. Both US and CT play a role in the diagnostic imaging of abdominal TB. Ultrasound US is better than CT for detecting ascites and can also demonstrate organ lesions, lymph nodes and masses (Fig. 18).

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Fig. 10 MRI features of tuberculoma. a An uncharacteristically large tuberculoma in the left cerebellar hemisphere demonstrates the typical MRI signal of a tuberculoma on T2weighted images. The gummatous necrosis which predominates during this stage is seen as a hypointensity, while early caseating necrosis is seen as a small high-signal area in the very centre of the lesion. There is signicant surrounding oedema. b T1-weighted gadoliniumenhanced imaging of the same lesion shows that the lesion is predominantly isointense to cortex and shows rim enhancement

Computed tomography CT demonstrates lymphadenopathy, organ lesions, conglomerate masses and omental cakes to the best advantage. Typical lymphadenopathy is in the porta hepatis and in the para-aortic region, but can also

involve the mesenteric nodes with typical fanning out of the vessels and marginalization of the bowel loops. Lymph nodes may be calcied or show calcication over time, but the most characteristic appearance is that of ring-enhancing nodes with low-density centres. Organ lesions are seen as low-density multifocal areas,

Fig. 11 T2-weighted MRI of a TB abscess shows that, unlike a tuberculoma, it has a high-signal centre and surrounding oedema, which is indistinguishable from a pyogenic abscess

Fig. 12 Patterns of basal enhancement on CT in patients with TBM. a Enhancement of the basal meninges may be a subtle CT feature. Identication of double lines of enhancement adjacent to each other as seen at the central right middle cerebral artery cistern is abnormal. This represents abnormal meningeal enhancement lining abutting frontal and temporal lobes (refer to MRI conrmation Fig. 16). Another positive feature of abnormal meningeal enhancement in this patient is circumferential enhancement of the infundibular recess of the third ventricle, which cannot be confused with vessels of the circle of Willis. b In more advanced disease the contents of the suprasellar cistern may enhance. This may be due to enhancement of vascularized granulation tissue or extravascular leak of contrast material. In this patient the enhancement is thick and nodular which suggests the presence of meningeal-based granulomas. Border zone and basal ganglia infarction is also present on the right. c Basal enhancement may be asymmetrical and focal. In addition to the left middle cerebral artery cistern enhancement and border zone infarction, there is sylvian cistern enhancement. When compared with the normal right sylvian cistern where the sylvian vessels are seen in cross section as separate dots, the features on the right are likened to the dots being joined (join the dots sign). d The Y on its side sign can also help to distinguish subtle enhancement from normal circle of Willis vessels. In this patient it is easy to compare the markedly abnormal right side where the enhancement around the medial temporal lobe contributes the second arm of the Y on its side. On the normal left side there is no vessel large enough to contribute this component of the Y

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most commonly in the liver and spleen, and rarely in the pancreas. Over time these lesions may show calcication. Inammatory masses composed of bowel loops with adherent omentum and lymphadenopathy are best demonstrated on CT, as are omental cakes, seen immediately deep to the abdominal wall. A combination of the above CT features, especially when lymphadenopathy is rim enhancing or calcied, is highly suggestive of the disease. Bowel contrast studies are not usually performed in children (Fig. 19) [4, 15].

Urogenital TB
Urogenital TB is rare, but renal disease with papillary destruction and cavitation is well described. The imaging modalities should include US and IV urography if better calyceal visualization is desired. Common US ndings include echogenic calyces and mixed or echo-free areas in the position of the pyramids indicating cavitation (Fig. 20) [15, 37].The ovaries can be involved in TB as can any other organ in the body

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Fig. 13 Hyperdensity in the basal cisterns on unenhanced CT scanning. a The hyperdensity in the suprasellar and middle cerebral artery cisterns seen on these non-contrasted CT images of a child with TBM corresponds with the area of basal enhancement after contrast medium administration and is highly specic for the diagnosis of TBM. b Hyperdensity is also noted in the ambient and sylvian cisterns, and either represents exudate or granulation tissue in the cisterns in patients with TBM

and may result in diagnostic confusion with diseases such as lymphoma and leukaemia (Fig. 21) [15].

Conclusions
Tuberculosis can aect any organ in the body. The lung is the commonest site of infection as it is the portal of entry. Imaging should be directed at not only making the diagnosis, but also at detecting the complications of TB. New modalities such as CT for pulmonary TB and MRI for TBM should undergo constant revision for improved detection and new signs. Pitfalls of improved imaging should also be noted such as detection of normal-sized lymph nodes on CT and increased radiation dose. Imaging should be as basic as possible at rst, including the continued use of chest radiographs. Equivocal results should prompt further imaging. Denitive ndings should end the imaging series unless other complications are sought. When results are negative, do not discount TB, but rely on clinical suspicion to guide further imaging. For pulmonary TB, begin with a chest radiograph; for intracranial TB, begin with a CT and for abdominal CT begin with US. Until clinical and laboratory testing improves in sensitivity, specicity and speed of diagnosis, radiologists will be called to make the diagnosis as fast and as accurately as possible. Radiologists must use the opportunity oered by the failure of other tests to apply multiple and especially new imaging techniques as a diagnostic solution for TB in children.

Fig. 14 Infarction. Infarcts most commonly involve the basal ganglia and internal capsules as a result of vasculitis involving the perforating branches of the middle cerebral arteries passing through the inammatory exudate. Bilateral basal ganglia infarctions, as in this patient, carry a high mortality. In this patient there are also extensive infarcts in the cerebellar hemispheres

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Fig. 15 Hydrocephalus. a, b When hydrocephalus is non-communicating (as in this patient), transependymal uid shift may occur, resulting in a periventricular hypodensity. This type of hydrocephalus can be conrmed with air encephalography and requires ventricular drainage. Communicating hydrocephalus occurs more Fig. 16 MRI features of TBM. a MRI demonstrates enhancement of the suprasellar and middle cerebral artery cisterns more eectively than does CT. b Another example of basal enhancement demonstrating the ow-void within the vessels of the circle of Willis, standing out against the prominent basal enhancement in the suprasellar cistern. c Coronal gadoliniumenhanced MRI conrms the double-line sign described for CT. The meningeal enhancement is lining abutting lobes. The enhancing lines are not confused with normal vessels which demonstrate ow void. d Gadolinium-enhanced MRI in this patient with TBM demonstrates nodular meningeal enhancement which is the result of meningeal-based granulomas

frequently and may be indistinguishable in its CT appearance. c Ventricular drainage is only necessary in a few patients with noncommunicating hydrocephalus, but results in eective decompression of the ventricular system and resolution of the periventricular hypodensity

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Fig. 18 US imaging of abdominal TB. a US is an eective way of demonstrating the ascites associated with TB of the abdomen. In this patient there are septations and strands evident within the ascites. b When there is no bowel gas obscuring visualization, US can demonstrate tuberculous lymphadenopathy at the porta hepatis and para-aortic regions eectively. c Lymphadenopathy may be accompanied by multiple organ lesions. In this patient there are low echogenicity lesions in the liver. d Hepatic parenchymal granulomas may calcify and then appear echogenic casting acoustic shadows. e Multiple small TB granulomas or abscesses within the spleen, may only be visible with the use of a linear high-resolution probe. f Conglomerate masses composed of matted lymph nodes, bowel and omentum may be identied on US

Fig. 17 Tuberculous arachnoiditis. Sagittal gadolinium-enhanced MRI of the spinal cord demonstrates enhancement around the conus medullaris and lower thoracic cord including abscess formation compressing the cord anteriorly and posteriorly

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b Fig. 19 a Axial contrast-enhanced CT of the abdomen demonstrates TB lesions in the liver and spleen, which are hypodense relative to the parenchyma. Calcied lymphadenopathy is typically present in the para-aortic region. b CT scan demonstrates lymphadenopathy better than US. In this patient the mesenteric adenopathy is displacing the bowel loops to the periphery of the abdomen and is fanning out the mesenteric vessels. Omental caking is a rare CT presentation but is well demonstrated in this patient immediately deep to the abdominal wall on the right. c CT is an ideal way of demonstrating abdominal masses typically in the right iliac fossa, composed of lymph nodes, bowel and omentum

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Fig. 20 US in renal TB. a The US appearance of renal TB may mimic hydronephrosis when there is papillary necrosis. b Cavitation at the medullary pyramids is more obvious when it projects beyond the calyx and is larger than the major calyx

Fig. 21 Ovarian TB. Massive enlargement of the ovaries on a transverse and b longitudinal imaging as a result of tuberculous involvement

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