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Review Article

Acta Radiologica
2015, Vol. 56(5) 557–564
! The Foundation Acta Radiologica
The imaging spectrum of pulmonary 2014
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DOI: 10.1177/0284185114533247
acr.sagepub.com

Luciano Cardinale, Daniela Parlatano, Francesco Boccuzzi,


Maurizio Onoscuri, Giovanni Volpicelli and Andrea Veltri

Abstract
Tuberculosis has still an important impact on public health because it is an important cause of death, particularly in
developing countries.
On the other hand recent studies have shown that tuberculosis is again becoming concentrated in big cities of Western
Europe, especially among immigrants, drug addicts, poor people, and the homeless, despite progress in reducing national
rates of the disease.
Diagnostic imaging is challenging for radiologists because signs of tuberculosis may easily mimic other diseases such as
neoplasms or sarcoidosis. Clinical signs and symptoms in affected adults can be non-specific and a high level of pre-test
clinical suspicion based on history is fundamental in the diagnostic work-up. Impact of tuberculosis in the world is
extremely important considering the high incidence estimated during 2011 that was 8.7 million cases. This article gives a
review of imaging patterns of chest tuberculosis as may be detected on conventional radiography and computerized
tomography (CT). The main aim is to improve radiologist’s familiarity with the spectrum of imaging features of this
disease and facilitate timely diagnosis. Furthermore, we consider the emerging role of alternative methods of imaging,
such as magnetic resonance imaging (MRI), that can be helpful and highly accurate for a better definition of some signs of
tuberculosis.

Keywords
Thorax, CT, conventional radiography, lung, tuberculosis, adults and pediatrics
Date received: 25 January 2014; accepted: 6 April 2014

cases of tuberculosis in 2011 in the world; among these,


Introduction about 15% were human immunodeficiency virus
Tuberculosis is an infectious disease caused by (HIV)-positive. There were estimated 170 per 100,000
Mycobacterium tuberculosis, a rod-shaped, non- population rates prevalent cases of tuberculosis in 2011.
spore-forming, aerobic bacterium, often neutral to However, because of insufficient case detection and
Gram’s staining. Pulmonary tuberculosis has been clas- incomplete notification, reported cases represent only
sified into primary and post-primary tuberculosis. 60% of the total number of new cases. About 60% of
Primary tuberculosis occurs in patients not previously cases are in the South-East Asia and Western Pacific
exposed to Mycobacterium tuberculosis. Within 2 years regions. The African region has 24% of the world cases,
after the infection, primary tuberculosis usually results and the highest rates of cases and deaths per capita (3).
in active disease (1). Post-primary or reactivated tuber- In the past, primary tuberculosis was considered a
culosis occurs in patients who have been previously
infected and have developed a certain degree of
acquired immunity. Reactivated tuberculosis may San Luigi Hospital, University of Turin, Orbassano, Italy
result from both endogenous reactivation (more
Corresponding author:
often) and exogenous re-infection (super-infection) Daniela Parlatano, San Luigi Hospital, University of Turin, Regione
(2). The burden of disability and death due to tubercu- Gonzole 10, Orbassano, Torino 10043, Italy.
losis is immense, with an estimated 8.7 million incident Email: daniela.parlatano@gmail.com
558 Acta Radiologica 56(5)

childhood disease while post-primary tuberculosis was


known as a typical form of adulthood infection.
However, despite progress in reducing national rates
of the disease in most of the developed countries, it
still affects high-risk urban groups such as people who
originate from high tuberculosis burden areas of Asia
and Africa, homeless people, and people abusing drugs
or alcohol. It is therefore important to immediately
identify the disease to treat correctly infected patients
and prevent it spreading. This is not always an easy
task because symptoms of presentation may be subtle
and non-specific. Moreover, the radiologic signs of the
disease are often misleading. Indeed, tuberculosis may
be diagnosed in about 25% of cases initially misinter-
Fig. 1. Primary tuberculosis in a small child. Antero-posterior
preted as lung cancer (4).
chest X-ray demonstrates homogeneous consolidation with air
bronchogram in the right middle lung zone.
Clinical manifestations Source: Courtesy of C Defilippi, Pediatric Hospital Regina
Margherita, Turin.
The key in diagnosing tuberculosis is a high index of
suspicion. Clinical signs and symptoms of pulmonary usually unilateral and evidenced through radiographs
tuberculosis in adults are often nonspecific, whereas approximately in 70% of children with primary tuber-
complete absence of symptoms occurs in approximately culosis (Fig. 1) (2). At CT studies, the appearance of the
5% of adult cases (5). The most frequent respiratory parenchymal consolidations in primary tuberculosis is
symptom is cough for more than 2 weeks, but also most commonly dense and homogeneous but may also
hemoptysis and pleuritic chest pain may be considered be linear, patchy, nodular, or mass-like (2). In nearly
classic complaints, while dyspnea may be present in two-thirds of cases, the parenchymal focus resolves
case of extensive lung involvement. Systemic manifest- without sequelae at conventional radiography; in the
ations include low-grade fever, anorexia, fatigue, night remaining cases, the parenchymal focus can calcify,
sweats, and weight loss that may persist for weeks to thus initiating the Ghon focus (1). Satellite calcified
months (6). The most common hematologic associated foci and persistent mass-like opacities, called
manifestations are high white blood cells count and Tuberculomas, can be found in approximately 9% of
anemia, both occurring in 10% of patients (7), and patients. Lymph node enlargement is the hallmark of
raised inflammation indexes. Clinical manifestations primary tuberculosis in childhood. This condition is
of tuberculosis are highly influenced by age and encountered in about 95% of children affected by
immune status of the infected patient. Diagnosis of tuberculosis; on the other hand, radiographic evidence
tuberculosis in elderly is frequently delayed because of lymph nodes enlargement is far less common in
classic symptoms rarely occur or may be confused by adults (43% of cases) (10,11). Lymphadenopathies are
other chronic diseases. A cryptic presentation with usually unilateral and located in the hilum or para-tra-
fever of unknown origin, often accompanied by pan- cheal regions (Fig. 2a). On computed tomography
cytopenia or leukemic reaction, is particularly common (CT), which is more sensitive than chest radiography
(8). The clinical manifestations of tuberculosis in for assessing lymphadenopathy, enlarged nodes typic-
HIV-infected people depend on the severity of their ally show central low attenuation, representing caseous
immunosuppression. In people with advanced disease, necrosis, whereas peripheral rim enhancement repre-
pulmonary tuberculosis is often accompanied by extra- sents the vascular rim of the granulomatous inflamma-
pulmonary involvement (9). tory tissue (12) (Fig. 2b and c). The combination of a
Ghon focus and a calcified hilar node is called Ranke
Complex and is suggestive of previous tuberculosis
Imaging findings in primary tuberculosis infection. Pleural tuberculosis is considered a complica-
Primary tuberculosis manifests with three main entities: tion of primary tuberculosis, although in up to 19% of
parenchymal disease, lymphadenopathy, and pleural detected cases may occur in association with post-pri-
effusion. On chest film, parenchymal disease typically mary disease (13). It is usually unilateral, on the same
manifests as dense, homogeneous parenchymal consoli- side as the primary focus, but can also occur in patients
dation, predominantly located in the middle and lower without any evidence of parenchymal disease. A
lobes, especially in adults. Airspace consolidation, bronchopleural fistula must be ruled-out in the diagno-
related to bronchiolo-alveolar caseous exudate, is sis when an air-fluid level is identified (14). Tuberculous
Cardinale et al. 559

Fig. 2. (a) Posteroanterior chest X-ray shows tuberculosis manifesting primarily as lymphadenopathies with right hilar and sub-carinal
masses (white arrows). Same patient as in Fig. 1. Contrast-enhanced axial (b) and coronal (c) CT scan obtained with mediastinal
window setting (same patient as Fig. 1) show enlarged confluent right hilar and subcarinal lymph nodes with peripheral rim
enhancement and central low attenuation due to caseous necrosis.
Source: Courtesy of C Defilippi, Pediatric Hospital Regina Margherita, Turin.

effusions contain high quantity of proteins and often encountered in one-third to two-thirds of patients
show fibrin strands and septa on thoracic ultrasound (18). Cavitation, which is the hallmark of this form of
imaging (15). Very often septa that have been imaged pulmonary tuberculosis, may be evident in half of the
by ultrasound are not detected by CT. In these cases patients. The cavitation process may be single or mul-
CT usually shows homogeneous fluid in the pleural tiple and usually creates a lesion surrounded by thick
cavity, but is more panoramic and therefore more sen- walls with irregular margins, which may be significantly
sitive than plain chest radiography and lung ultrasound reduced after treatment (Fig. 3a). In a minority of
in diagnosing associated parenchymal diseases. After cases, the cavity may contain a small quantity of
contrast administration, pleural layers enhance and fluid, usually visualized as an air-fluid level (19).
are revealed as a smooth thickening of the visceral When the amount of fluid content is significantly
and parietal pleural surfaces separated by a variable high, superinfection by other bacteria should be sus-
amount of fluid (split pleura sign) (13). pected (20). Bronchogenic spreading of the disease
occurs when an area of caseous necrosis liquefies and
Imaging findings in reactivation communicates with the bronchial tree. It is identified
radiographically in 20% of post-primary tuberculosis
tuberculosis
cases as multiple, ill-defined 5–10-mm nodules. These
Reactivation tuberculosis tends to involve predomin- nodules are in a segmental or lobar distribution invol-
antly the apical and posterior segments of the upper ving the dependent lung zone, distant from the cavita-
lobes and the superior segments of the lower lobes. tion process (21). On CT scans, bronchogenic spread
These specific locations are explained by relative can be identified in 95% of patients with post-primary
higher oxygen tension and impaired lymphatic drainage tuberculosis (22). A significant finding on thin-section
(16). An atypical distribution of the disease involving in CT is the ‘‘tree-in-bud’’ pattern, consisting of 2–4-
the anterior segment of the upper lobes or the lower mm centrilobular nodules and sharply marginated
segment of the basal lobes has been reported in linear branching opacities (23). Tree-in-bud opacities
approximately 5% of cases of post-primary tubercu- may also be detected in other infections, even if the
losis (17). In most cases, more than one pulmonary pattern characterized by a combination of multiple
segment may be involved, while bilateral disease is cavitations or nodular opacities in suggestive clinical
560 Acta Radiologica 56(5)

Fig. 3. Postprimary pattern of tuberculosis in a 55-year-old woman. (a) Axial CT scan of the upper lobes shows an area of cavitation
in the right lung, surrounded by thick walls with irregular margins. (b) Axial CT scan at levels of main bronchi shows centrilobular
nodules and mucoid impaction of contiguous branching bronchioles producing a tree-in-bud appearance, which reflects the presence
of endobronchial spread.

Fig. 4. Miliary tuberculosis in a young adult. (a) Detail (apex of the right lung) of postero-anterior chest radiograph shows multiple
small nodular areas of increased opacity. (b) High-resolution CT scan with lung windowing at the level of carena demonstrates
numerous fine, bilateral, unifom-sized, discrete nodules in a random distribution with associated thickening of interlobular septa and
fine intralobular networks.

settings, allows the diagnosis of pulmonary tuberculosis Other signs easily detected by high resolution CT
(24) (Fig. 3b). Tuberculoma, defined as a sharply mar- (HRCT) are thickening of interlobular septa and fine
ginated rounded or oval lesion usually measuring in the intralobular networks (27). This latter pattern can be
range of 0.5–4 cm in diameter, is the predominant par- differentiated from the tree-in-bud because the margins
enchymal lesion in 3–6% of cases. Tuberculomas are of the nodules are well defined and the distribution is
typically solitary lesions, but may be multiple and sur- uniform, on the contrary the tree-in-bud nodules are
rounded by small ‘‘satellite’’ nodules with regular or poorly defined and have a patchy distribution. The
irregular margins, often containing calcifications (25). nodules usually resolve within 2–6 months of specific
Miliary tuberculosis refers to the hematogenous dis- treatment, in most cases without scarring or any calci-
semination of tuberculosis. It can occur in both primary fication (28).
and post-primary disease, being somewhat more fre-
quent in reactivation tuberculosis (26). Chest radiog-
raphy is usually normal at the onset of symptoms,
Late complications
while the typical radiographic findings characterized Bronchiectasis and residual cavities are sequelae of pul-
by diffuse small nodules are seen in 85% of cases monary tuberculosis, detected at thin-section CT scans,
during more advanced clinical phases of the disease respectively, in 71–86% and 12–22% of patients with
(Fig. 4a). CT allows accurate early diagnosis when resolved disease. These lesions typically involve the
small nodules, typically 1–3 mm in size (Fig. 4b) or apical or posterior segments of the upper lobes (2). A
macronodules, resulting from fusion of several granu- bronchial dilatation or, more commonly, a residual
lomas, are detected even in asymptomatic patients. tuberculous cavity may be colonized by Aspergillus
Cardinale et al. 561

Fig. 6. Pleural and chest wall tuberculosis (empyema necessita-


Fig. 5. Cavitary tuberculosis associated with aspergilloma in an
tis) in a 73-year-old woman. Contrast-enhanced axial CT scan at
83-year-old man. Coronal CT scan shows volume loss of the
level of left pulmonary artery using mediastinal window setting
right upper lobe with dependent soft-tissue aspergilloma within
shows pleural fluid collection and visceral pleural calcification in
the cavity. Note the air crescent sign (the nodule is separated by
right hemithorax, suggesting chronic tuberculous empyema.
a crescent-shaped lucency from the adjacent cavity wall).
Lentiform chest wall lesion showing central low attenuation,
consistent with focal tuberculous chest wall abscess, is also seen.
with development of a mycetoma. The typical CT sign
consists of an intracavitary mass, usually surrounded The radiographic manifestations of HIV-associated to
by air (the ‘‘air crescent sign’’) (29) (Fig. 5). pulmonary tuberculosis depend on the degree of
Involvement of the tracheobronchial tree is common immunosuppression (33). HIV patients with almost
in the postprimary form and, if not recognized and preserved cellular immune function show radiographic
properly treated, bronchial scar stenosis is a frequent findings similar to those of non HIV-infected individ-
complication that may even lead to obstructive atelec- uals. Patients with a CD4 T-lymphocyte count <200/
tasis, pneumonia and bronchiectasis. mm3 have a higher prevalence of mediastinal or hilar
Empyema necessitatis is an uncommon complication lymphadenopathy, frequent nodular or multinodular
of a tuberculous empyema in which the inflammatory image pattern with a lower prevalence of cavitations,
mass spontaneously bores into the soft tissues of the and often extra-pulmonary involvement as compared
thoracic wall, forming a subcutaneous abscess that with HIV-seropositive patients with a CD4 T-lympho-
sometimes opens to the skin (30). The plain chest film cyte 200 mm3 (32).
shows signs of chronic pleural disease with pleural
thickening that may show calcification. CT shows a Emerging role of magnetic resonance
pleural collection associated with an abscess located
at the chest wall level (Fig. 6).
imaging (MRI)
Using MRI in the diagnostic management of patients
Tuberculosis in immunocompromised affected by lung tuberculosis is a challenge that may
have some advantages but also some disadvantages.
hosts
Absence of ionizing radiation is obviously a great
Impairement of the host immunity is a well-known pre- advantage. However, the small number of signal gen-
disposing factor in tuberculosis. Unusual or atypical erating protons, susceptibility artifacts related to the
manifestations are common in immuncompromised multiple air-tissue interfaces and motion artifacts that
patients. For example, diabetic and other immunocom- require fast imaging or triggering and gating techniques
promised patients have a higher prevalence of multiple are disadvantages that should always be considered
cavities and frequent non-segmental distribution of the (34). MRI has shown an excellent contrast resolution
lesions (31). Miliary forms and disseminated disease are and appears to be more accurate than non-contrast-
also associated with severe immunosuppression (32). enhanced CT in revealing lymph node involvement,
Tuberculosis is the first cause of death from oppor- pleural abnormalities, and parenchymal caseation
tunistic infections among HIV-infected patients. (35). Furthermore, signal intensity of lymph nodes
562 Acta Radiologica 56(5)

may differ depending on the degree of evolution: on T2- the differential diagnosis. While in the past primary
weighted fast recovery fast spin-echo (FR FSE T2) tuberculosis was mainly a pediatric disease, nowadays
FAT SAT sequence slight hyperintensity may indicate it is more common in young adults (age 18–25 years).
flogistic lymphoid hyperplasia, high hyperintensity is The differential diagnosis with systemic diseases such as
suggestive of liquefactive necrosis and central isointen- sarcoidosis, Hodgkin’s lymphoma (HL), and some
sity associated to peripheral hyper-intensity may indi- respiratory viral conditions, on occasion may represent
cate caseosis (36). Excellent contrast resolution makes a real challenge for the radiologist and the clinician.
MRI superior to CT in assessing pleural involvement in Indeed morphologic findings of these diseases are
case of subtle or loculated effusions, not seen on CT characterized by the presence of pathological hilar and
(37). MRI can therefore be considered as an interesting mediastinal homogeneous enhancing lymph nodes that
alternative to CT in subgroups of patients such as chil- can be hardly differentiated from tuberculosis manifest-
dren or pregnant women. ations. On the other hand, lymphadenopathies in tuber-
culosis show a heterogeneous enhancement with
rim-enhancing and central low attenuation that may
Radiological differential diagnosis be considered highly specific (38). However, these find-
The differential diagnosis between tuberculosis and ings are not fully pathognomonic and, especially in cases
some associated pathologic conditions is an emerging of tuberculosis without parenchymal lesions, lymphono-
problem, as pulmonary tuberculosis may easily reveal dal biopsy is the only way to reach a reliable diagnosis. If
aspects that can create diagnostic doubts in the radio- primary tuberculosis is more common among young
logic imaging studies. Differential diagnosis can be par- adults, post-primary tuberculosis is more common
ticularly challenging when tuberculosis mimicks among adults. Post-primary tuberculosis findings often
sarcoidosis, lymphoma, and pulmonary neoplasms determine a further differential diagnostic problem with
(Fig. 7). Changes in epidemiology characteristics of solid neoplasms, giving isolated opacities on chest radi-
the disease can be one of the causes of difficulties in ography or CT scan accompanied by negative sputum.

Fig. 7. (a) Coronal CT scan of a central mass with surrounding locoregional lymph nodes suspected to be a pulmonary neoplasm but
which was established to be tuberculosis. (b) Axial CT scan showing narrowed apical bronchus and surrounding mediastinal lymph
nodes. (c) Axial CT scan showing a pulmonary peripheral tubercular lesion characterized by spiculated margins, in differential diagnosis
with peripheral adenocarcinoma.
Cardinale et al. 563

Indeed, the presence of acid fast bacilli in sputum or


Conclusions
a positive skin test do not rule out the co-existence of Although a slow reduction in the incidence of tubercu-
tuberculosis and cancer. CT imaging is helpful for the losis has been reported in developed countries, tuber-
accurate evaluation of the morphologic and densito- culosis is still a major challenge on the list of the most
metric aspects of the lesion, detection of lymph nodes serious infectious diseases in the world, even in the 21st
enlargement, and the possible presence of metastases. century. Chest radiography is the mainstay in the radio-
Diffuse, central, or lamellar calcifications may be clues logical evaluation of suspected or proven pulmonary
to the imaging diagnosis of tuberculosis over malig- tuberculosis. CT is useful in the clarification of certain
nancy. Positron emission tomography CT (PET-CT) misleading findings and may also be helpful in the
could be another useful tool in case of a challenging determination of disease activity. Nowadays, the radio-
differential diagnosis, however, tuberculosis still logical presentation of tuberculosis is changing, with
remains a frequent cause of false-positive diagnoses fading of the classical distinction between primary
on PET-CT because tuberculomas may even show and post-primary disease. The traditional imaging con-
hypermetabolic pattern on F18-FDG-PET raising cept of primary and reactivation tuberculosis has
problems of overlapping findings with tumor masses. recently been challenged on the basis of DNA finger-
Surgery or biopsy may occasionally be the only solu- prints, and radiologic features depend on the level of
tion to obtain a correct diagnosis (39). host immunity rather than the elapsed time after the
infection. Radiologists must be aware also that new
Response to treatment and ‘‘imaging forms of the diseases may present and should be pre-
pared for their prompt recognition, thus helping to
healing’’ concept
avoid a delayed treatment, which is associated with
Complete recovery of parenchymal abnormalities high rates of mortality.
usually require from 6 months to 2 years on radio-
graphs and up to 15 months on CT scans (28). Funding
Lymphadenopathies may persist for several years This research received no specific grant from any funding
after treatment. However, absence of improvement of agency in the public, commercial, or not-for-profit sectors.
radiological findings after 3 months of chemotherapy in
adults, suggest infection by drug-resistant organisms or References
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