AJR 2005; 184:757-764
© American Roentgen Ray Society
Pulmonary Disease in Patients with AIDS: High-Resolution CT and Pathologic Findings
Edson Marchiori1,
Nestor L. Müller2,
Arthur Soares Souza, Jr.3,
Dante Luiz Escuissato4,
Emerson Leandro Gasparetto4 and
Tomás Franquet5
1 Department of Radiology, Hospital Clementino Fraga, Universidade Federal
Fluminense e Universidade Federal do Rio de Janeiro, Rio de Janeiro,
Brazil.
2 Department of Radiology, Vancouver General Hospital, University of British
Columbia, 899 W 12th Ave., Vancouver, BC V5Z 1M9, Canada.
3 Department of Radiology, Hospital de Base da Faculdade de Medicina (FAMERP) e
Instituto de Radiodiagnóstico Rio Preto, São José do Rio
Preto, São Paulo, Brazil.
4 Department of Diagnostic Radiology, University of Paraná, Curitiba,
Brazil.
5 Departmento de Radiologia, Hospital de Sant Pau, Avda San Antonio M. Claret
167, Barcelona 08025, Spain.
Received May 4, 2004;
accepted after revision July 23, 2004.
Address correspondence to N. L. Müller
(nmuller{at}vanhosp.bc.ca).
Introduction
The advent of new prophylactic and treatment options has resulted in a
considerable increase in the length of survival of HIV-infected patients.
However, pulmonary parenchymal complications remain the main cause of
morbidity and mortality in these patients
[1]. Early diagnosis and
treatment of these complications are important to improve survival.
The risk of developing specific pulmonary complications is influenced by
the degree of immunosuppression
[2]. Patients with fewer than
500 CD4 cells/mm3 are at increased risk for developing bacterial
pneumonia, pulmonary tuberculosis, and lymphoproliferative disorders. The risk
for these complications increases further as the patients become more
immunocompromised. When the CD4 cell count falls below 200
cells/mm3, the patients are also at increased risk for developing
Pneumocystis carinii pneumonia and disseminated tuberculosis. Fungal
infections, Cytomegalovirus pneumonia, AIDS-related lymphoma, and Kaposi's
sarcoma usually occur in severely immunocompromised patients (< 100 CD4
cells/mm3) [2].
In most patients with AIDS, a confident diagnosis of the pulmonary
complications can be made by a combination of clinical, radiographic, and
laboratory findings. However, 5–10% of patients with AIDS and pulmonary
disease have normal or nonspecific radiographic findings
[3]. High-resolution CT is more
sensitive than radiography for revealing parenchymal abnormalities in patients
with AIDS and is superior to radiography in the differential diagnosis of the
pulmonary complications seen in these patients
[3].
Several studies have shown that the highresolution CT findings of pulmonary
disease seen in patients who do not have AIDS reflect the macroscopic
pathologic findings. However, limited information is available about the
correlation of the high-resolution CT and pathologic findings in patients with
AIDS. The aim of this pictorial essay is to illustrate the high-resolution CT
and pathologic findings of the most common pulmonary complications in patients
with AIDS.
P. Carinii Pneumonia
The most common high-resolution CT manifestation of P. carinii
pneumonia consists of patchy or confluent, symmetric, bilateral ground-glass
opacities. Less common manifestations include bilateral areas of
consolidation, interlobular septal thickening, intralobular linear opacities,
cystic lesions, and nodules [1,
3]. The combination of
ground-glass opacities and superimposed intralobular linear opacities results
in a pattern commonly referred to as crazy paving
(Fig. 1A).
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Fig. 1A. —32-year-old man with AIDS and Pneumocystis carinii
pneumonia. High-resolution CT scan shows bilateral areas of ground-glass
attenuation. Note sharp demarcation between abnormal and normal parenchyma and
mild smooth thickening of some of interlobular septa.
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The ground-glass opacities and areas of consolidation reflect the presence
of alveolar filling by a foamy exudate, constituted mainly of surfactant,
fibrin, and cellular debris [1]
(Fig. 1B). The organisms are
typically seen within this foamy exudate as small bubbles
[4]. Interlobular septal
thickening and intralobular linear opacities can result from interstitial
edema or cellular infiltration. The nodules reflect the presence of
granulomatous inflammation consisting of clusters of epithelioid histiocytes
and multinucleated giant cells
[4]. Rarely, granulomas
secondary to P. carinii pneumonia may undergo necrosis and
cavitate.
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Fig. 1B. —32-year-old man with AIDS and Pneumocystis carinii
pneumonia. Photomicrograph of histologic specimen shows septal thickening
(straight arrows) secondary to edema and cellular inflammatory
infiltrates separating two secondary lobules. Note partial filling of air
spaces by inflammatory infiltrate (curved arrows), which accounts for
ground-glass opacities seen on CT scan (A). (H and E, x40)
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Cystic lesions are seen on high-resolution CT in 10–30% of AIDS
patients with P. carinii pneumonia. They can reflect the presence of
bullae, intraparenchymal cysts, or, occasionally, necrotizing granulomas. Some
of the cysts have been shown to be secondary to tissue invasion by P.
carinii followed by necrosis. The cysts are usually bilateral and involve
mainly the upper lobes. Patients with cysts have an increased propensity to
develop pneumothorax [4].
Occasionally, P. carinii pneumonia may result in interstitial
fibrosis that can be mild or severe. The fibrosis is manifested on CT by the
presence of irregular linear opacities, traction bronchiectasis, and
architectural distortion [1,
4].
Tuberculosis
Patients with AIDS are at increased risk of developing tuberculosis. The
manifestations of tuberculosis in HIV-positive patients are influenced by the
degree of cellular immune compromise
[5]. In patients who have CD4
cell counts greater than 200 cells/mm3, the findings tend to be
similar to those seen in reactivation tuberculosis in the normal host. In
these patients, the most common high-resolution CT manifestations consist of a
single or, less commonly, multiple 1- to 3-cm-diameter nodules; consolidation;
cavitation involving mainly the upper lobes; and centrilobular nodular and
branching linear opacities resulting in a tree-in-bud pattern. The
characteristic histologic lesion of tuberculosis is a necrotizing granuloma
that can expand, resulting in consolidation and typically cavitation.
Endobronchial spread to the bronchioles results in centrilobular nodular
opacities and a tree-in-bud pattern.
In more severely immunocompromised patients, the radiologic manifestations
tend to resemble those of primary disease and consist predominantly of areas
of consolidation, miliary disease (Figs.
2A and
2B), pleural effusion, and
lymph node enlargement [4,
5]. Lymph node enlargement
results from inflammation of the lymphatic vessels within the nodes and of the
nodes themselves. The enlarged nodes typically contain necrotizing granulomas.
Up to 20% of severely immunocompromised AIDS patients with pulmonary
tuberculosis have radiographs that show normal findings
[2]. High-resolution CT in
these patients usually shows small nodules and lymph node enlargement
[2].
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Fig. 2B. — 42-year-old woman with AIDS and miliary tuberculosis.
Photomicrograph of whole-mount, low-power histologic section reveals multiple
granulomas (arrows) with necrotic centers. (H and E, x40)
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Bacterial Pneumonia
The imaging findings of bacterial pneumonia in patients with AIDS are
similar to those observed in immunocompetent patients and consist
predominantly of single or multifocal areas of consolidation
[2]. Lobar pneumonia is
characterized by the spread of bacteria and inflammatory exudates between the
alveolar air spaces, a pattern seen most commonly in Streptococcus
pneumoniae pneumonia. A lobular distribution is characterized by
centrilobular inflammation that is concentrated around respiratory bronchioles
(Figs. 3A and
3B), with spread to the
surrounding alveolar ducts and alveolar spaces. Bronchopneumonia can result
from a variety of grampositive and gram-negative bacteria, most commonly those
in the Staphylococcus, Streptococcus, Pseudomonas, Klebsiella,
Enterobacter, and Haemophilus genera.
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Fig. 3A. —44-year-old woman with AIDS and bacterial pneumonia. High-resolution
CT scan shows foci of air-space consolidation with adjacent ground-glass
attenuation in dorsal lung regions. Also note branching linear and nodular
opacities resulting in tree-in-bud pattern (arrows).
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Fig. 3B. —44-year-old woman with AIDS and bacterial pneumonia. Photomicrograph
of histologic specimen shows bronchiolar bifurcation with inflammatory
infiltrate in lumen (straight arrow) and in peribronchiolar region
(curved arrows), corresponding to tree-in-bud pattern shown on
high-resolution CT. (H and E, x40)
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Histoplasmosis and Coccidioidomycosis
Patients with AIDS who are exposed to histoplasmosis and coccidioidomycosis
are at increased risk of developing disseminated disease. The high-resolution
CT findings consist of a miliary pattern
(Fig.
4A
), or, less
commonly, diffuse air-space consolidation
[4]. The miliary lesions result
from hematogenous dissemination and consist of small foci of acute
inflammation with neutrophils, macrophages, and granulomas. Diffuse air-space
consolidation is typically associated with large numbers of organisms in the
alveoli and an inflammatory response consisting of neutrophils with a mixture
of fibrin, RBCs, and macrophages.
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Fig. 4B. —19-year-old man with AIDS and miliary histoplasmosis.
Photomicrograph of histologic section reveals granulomas, some of which are
confluent in parenchymal interstitium. (H and E, x40)
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Invasive Pulmonary Aspergillosis
The most common high-resolution CT finding of invasive pulmonary
aspergillosis in patients with AIDS is the presence of thick-walled cavitary
lesions. The predominant histologic abnormalities consist of tissue invasion,
abscess formation, and angioinvasion with or without infarction. The cavitary
lesions reflect the presence of pulmonary infarction and abscess formation
[6]. Less common CT findings
include single or multiple nodules, patchy areas of consolidation, and pleural
effusions [6]. The nodules may
have a surrounding halo of ground-glass attenuation. The nodules reflect the
presence of infarction and histologically display coagulating necrosis and
fungus hyphae; the halo is due to surrounding hemorrhage (Figs.
5A,
5B,
5C, and
5D).
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Fig. 5A. —62-year-old man with AIDS and invasive pulmonary aspergillosis.
High-resolution CT scan obtained at level of upper lobes shows nodule with
surrounding halo of ground-glass attenuation (arrows) in right upper
lobe.
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Fig. 5B. —62-year-old man with AIDS and invasive pulmonary aspergillosis.
High-resolution CT scan obtained at level of middle and lower lobes shows
small nodules in lingula and left lower lobe (arrows) and localized
scarring in right lower lobe.
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Fig. 5C. —62-year-old man with AIDS and invasive pulmonary aspergillosis.
Photomicrograph of histologic specimen of one of small nodules shows necrotic
center (straight arrows) surrounded by leukocytic infiltrate
(curved arrows) and more peripherally by alveolar hemorrhage
(arrowheads). (H and E, x40)
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Fig. 5D. —62-year-old man with AIDS and invasive pulmonary aspergillosis. On
photomicrograph of histologic specimen, black of Grocott-Gomori
methenamine–silver nitrate stain reveals hyphae of Aspergillus
organisms with radial distribution inside nodule from center to periphery.
(x40)
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Cryptococcosis
Cryptococcosis in patients with AIDS usually manifests as disseminated
disease, the main clinical manifestation being meningitis. The pulmonary
manifestations are variable and include bilateral nodular or reticular
opacities, bilateral consolidation, or miliary nodules
[1]
(Fig. 6A). The histologic
response to cryptococcal infection depends on the immune status of the
patient. In patients with normal or nearly normal immune response, the
organisms result in nodular granulomas similar to those seen in other fungal
pulmonary infections [4]
(Fig. 6B). In severely
immunosuppressed patients, there may be extensive tissue infiltration by
organisms in a pneumonic fashion, with little tissue response.
Cytomegalovirus Pneumonia
Cytomegalovirus is commonly detected on bronchoalveolar lavage fluid in
AIDS patients. In most cases, it is an incidental finding, there being no
associated pulmonary complication. In a small number of patients, however,
Cytomegalovirus organisms can result in disseminated infection and pneumonia.
The high-resolution CT findings are heterogeneous and include bilateral
ground-glass opacities, patchy bilateral consolidation, and multiple nodules
or masslike areas of consolidation
[1]
(Fig. 7).
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Fig. 7. —38-year-old man with AIDS and Cytomegalovirus pneumonia.
High-resolution CT scan shows bilateral nodules (straight arrows),
focal ground-glass opacities (curved arrows), and consolidation
(arrowhead).
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Kaposi's Sarcoma
The characteristic high-resolution CT manifestations of Kaposi's sarcoma
consist of peribronchovascular interstitial thickening and irregular or
ill-defined nodules in a predominantly peribronchovascular distribution (Figs.
8A,
8B,
8C, and
8D). These findings reflect
the propensity of Kaposi's sarcoma cells to infiltrate predominately the
perihilar peribronchovascular interstitium
[7] (Figs.
8A,
8B,
8C, and
8D). Other common findings
include thickening of the interlobular septa, lymphadenopathy, and pleural
effusion. The interlobular septal thickening can result from infiltration by
tumor cells or edema (Figs.
8A,
8B,
8C, and
8D).
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Fig. 8A. —34-year-old man with AIDS and Kaposi's sarcoma. High-resolution CT
scan shows marked peribronchial thickening, perivascular nodularity
(straight arrows), nodules along interlobar fissures (curved
arrows), and thickening of interlobular septa.
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Fig. 8B. —34-year-old man with AIDS and Kaposi's sarcoma. High-resolution CT
scan obtained at more caudal level than A shows extensive interlobular
septal thickening and centrilobular nodules (arrows).
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Fig. 8C. —34-year-old man with AIDS and Kaposi's sarcoma. Photomicrograph of
histologic specimen shows edema and tumor cells, which produce thickening of
interlobular septa (arrows). (H and E, x40)
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Fig. 8D. —34-year-old man with AIDS and Kaposi's sarcoma. Photomicrograph of
histologic specimen shows tumor cells infiltrating peribronchiolar connective
tissue, which results in centrilobular nodules seen on high-resolution CT. (H
and E, x40)
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Lymphoma
AIDS-related lymphoma is typically a high-grade B-cell non-Hodgkin's
lymphoma. It most commonly originates in extranodal locations in the lungs,
bone marrow, central nervous system, and bowel.
The most common pulmonary manifestation consists of multiple nodules or
masses measuring 1–5 cm in diameter. The nodules reflect the presence of
a dense focal monomorphic cellular infiltrate. Less common findings include
localized or multiple areas of consolidation, interlobular septal thickening,
centrilobular nodules, and, occasionally, reticular infiltrates that may have
a peribronchovascular distribution (Fig.
9A). The air-space consolidation results from the filling of the
alveoli by tumor cells. The peribronchovascular thickening is secondary to the
infiltration of the peribronchovascular bundles by neoplastic cells. Extension
to the interstitium along the bronchioles results in centrilobular nodules
(Fig. 9B). The thickening of
the interlobular septa and the pleural surface reflects the presence of
infiltration of these regions by tumor cells
[8].
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Fig. 9A. —52-year-old man with AIDS and non-Hodgkin's lymphoma.
High-resolution CT scan shows bilateral consolidation in predominantly
peribronchial distribution, nodule in lingula (straight arrow), and
few centrilobular nodules (curved arrows).
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Fig. 9B. —52-year-old man with AIDS and non-Hodgkin's lymphoma.
Photomicrograph of histologic section shows infiltration around bronchiole and
arteriole by tumor cells. Such infiltration results in centrilobular nodular
opacities seen on high-resolution CT. (H and E, x40)
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Lymphocytic Interstitial Pneumonia
Lymphocytic interstitial pneumonia is a lymphoproliferative disorder seen
with increased frequency in patients with AIDS, particularly children. In most
of these patients, the disorder is benign and regresses spontaneously or with
treatment. Rarely, it evolves into lymphoma
[4]. The most common
high-resolution CT manifestations consist of poorly defined bilateral
centrilobular nodules, smooth or nodular thickening of the bronchovascular
bundles, and ground-glass opacities
[2]
(Fig. 10A). Histologically,
lymphocytic interstitial pneumonia is characterized by an interstitial
infiltrate of lymphocytes and plasma cells that involves the perilymphatic
interstitium along the bronchovascular bundles, resulting in bronchial wall
thickening and centrilobular nodules (Fig.
10B). Interlobular septal thickening and small subpleural nodules
are also commonly present. The cellular infiltrate typically extends diffusely
along the alveolar septa, resulting in ground-glass opacities visible on
high-resolution CT [4,
8].
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Fig. 10A. —24-year-old woman with AIDS and lymphocytic interstitial pneumonia.
High-resolution CT scan shows patchy bilateral ground-glass opacities, small
foci of consolidation, mild septal thickening (straight arrows), and
few small nodules (curved arrows).
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Fig. 10B. —24-year-old woman with AIDS and lymphocytic interstitial pneumonia.
Photomicrograph of histologic specimen shows lymphocyte aggregates resulting
in nodular appearance (straight arrows). In some areas, lesions are
abundant (curved arrows) and result in collapse of alveolar spaces,
which results in ground-glass opacities and air-space consolidation seen on
high-resolution CT. (H and E, x40)
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Nonspecific Interstitial Pneumonia
Nonspecific interstitial pneumonia is a relatively common abnormality in
patients with AIDS characterized histologically by mild to moderate
lymphocytic and plasma cell infiltration of the peribronchiolar, perivascular,
and interlobular septal interstitial tissue
[2]. It is distinguished from
lymphocytic interstitial pneumonia by the lack of involvement of the alveolar
interstitium [2,
4]. The clinical and radiologic
findings mimic those of P. carinii pneumonia
(Fig. 11). However,
nonspecific interstitial pneumonia typically is seen early in AIDS patients
with normal CD4 cell counts, whereas P. carinii pneumonia occurs
mainly in patients with CD4 cell counts of less than 200 cells/mm3
[2]. Nonspecific interstitial
pneumonia has a good prognosis, typically stabilizing or resolving
spontaneously or with treatment.
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Fig. 11. —7-year-old boy with AIDS and nonspecific interstitial pneumonia.
High-resolution CT scan shows patchy bilateral ground-glass opacities, small
foci of consolidation, and poorly defined centrilobular nodular opacities
(arrows).
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Introduction
P. Carinii Pneumonia
