AJR 2003; 180:1203-1209
© American Roentgen Ray Society
CT and Radiography of Bacterial Respiratory Infections in AIDS Patients
Chad W. Brecher1,
Galit Aviram2 and
Phillip M. Boiselle1
1 Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical
School, 330 Brookline Ave., Boston, MA 02215.
2 Department of Radiology, Tel-Aviv Sourasky Medical Center, Tel-Aviv,
Israel.
Received July 15, 2002;
accepted after revision September 20, 2002.
Presented at the annual meeting of the American Roentgen Ray Society,
Atlanta, April-May 2002.
Address correspondence to P. M. Boiselle.
Introduction
Recent changes in the demographics of HIV infection, along with advances in
therapy and prophylaxis, have influenced the relative frequency and patterns
of pulmonary infections associated with AIDS
[1,
2,
3]. Bacterial respiratory
infections, including infectious airways disease and pneumonia, currently
account for most pulmonary infections diagnosed in HIV-infected individuals in
the United States [4,
5].
The significance of bacterial pneumonia in HIV infection is underscored by
the inclusion of two or more episodes of bacterial pneumonia within a 1-year
period as an AIDS-defining illness for an HIV-infected patient, regardless of
the CD4 cell count [6].
Considering the frequency and significance of bacterial respiratory infections
in HIV-infected patients, radiologists should be familiar with radiologic
manifestations of these infections. For example, HIV-infected patients with
bacterial pneumonia most commonly present with chest radiographic findings of
focal consolidation and clinical symptoms of productive cough and fever of
less than 1 week's duration
[3]. We review the spectrum of
nontuberculous bacterial respiratory infections that occur in HIV-infected
individuals, with a special emphasis on imaging features.
Bacterial Pneumonia
HIV Infection and Risk of Bacterial Pneumonia
Although HIV infection is most closely associated with altered
cell-mediated immunity (which is manifested by a decrease in CD4 count), a
number of additional immune deficits may occur in association with HIV
infection [7,
8,
9], including a poor antibody
response due to B cell dysfunction and defects in chemotaxis, phagocytosis,
and intracellular killing by monocytes, macrophages, and neutrophils
[8,
9]. In addition, HIV-infected
individuals may experience impairment of local defenses, manifested by a
depression of specific IgA at the mucosal surfaces
[7,
9]. These immune abnormalities
all contribute to an increased risk of bacterial infection among HIV-infected
persons, particularly by encapsulated bacteria, such as Streptococcus
pneumoniae and Haemophilus influenzae.
The overall rate of bacterial pneumonia in HIV-infected persons is
approximately six times greater than that in the general population
[4]. The incidence of
pneumococcal pneumonia is five to 18 times greater than that in the general
population, and the development of pneumococcal septicemia is 100 times
greater [10]. It has been
estimated that greater than one third of all persons with AIDS will develop at
least one episode of severe bacterial pneumonia over the course of their HIV
infection [8]. Considering
these data, Afessa et al. [11]
found bacterial pneumonia to be the most frequent pulmonary complication (42%)
in a recent autopsy series of 233 HIV-infected individuals.
IV drug abusers constitute the HIV risk factor group with the highest
prevalence of bacterial infection. In this population, bacterial pneumonia
rates are more than double those of other HIV risk factor groups, regardless
of the CD4 lymphocyte count
[4]. A notable demographic
trend of HIV infection in the United States in the past decade has been an
increased frequency of HIV infection among IV drug abusers and a decreased
prevalence of infection among male homosexuals
[1]. This demographic trend has
contributed to the increased prevalence of bacterial respiratory infections in
AIDS patients.
Although bacterial pneumonia often occurs in the early stages of HIV
infection, the risk of bacterial infection increases steadily with declining
CD4 lymphocyte counts [4]. For
example, HIV-infected individuals with CD4 counts of less than 200
cells/mm3 have a fivefold increased prevalence of bacterial
pneumonia compared with infected persons with CD4 counts greater than 500
cells/mm3. Cigarette smoking has also been associated with an
increased risk of bacterial pneumonia among HIV-infected patients with CD4
lymphocyte counts of less than 200 cells/mm3
[4]. Smoking cessation has thus
been recommended as a means of decreasing the rate of bacterial respiratory
infections in this subgroup
[4].
Recent trends in the prophylaxis and treatment of HIV-infected individuals
have influenced the relative frequency of various pulmonary infections. For
example, the widespread use of prophylaxis for Pneumocystis carinii pneumonia
has dramatically decreased the incidence of this infection
[3]. The use of
trimethoprim-sulfamethoxazole as a P. carinii pneumonia prophylactic agent
also provides a lesser degree of protection from bacterial infection
[4].
The introduction of highly active antiretroviral therapy, a combination
therapy comprising a three-drug regimen of HIV protease inhibitors and
nucleoside analog reverse transcriptionase inhibitors, has also resulted in a
profound decrease in the rate of opportunistic infections in HIV-infected
individuals [12,
13]. Because the rate of
bacterial pneumonia increases with declining immune status in HIV infection,
one would expect that the overall rate of bacterial pneumonia would decline
with enhanced immune function associated with highly active antiretroviral
therapy [12]. Sullivan et al.
[12] studied the rate of
pulmonary infections in 1898 HIV-infected patients and found a significant
overall decline in bacterial pneumonia associated with the use of highly
active antiretroviral therapy. Another study by Wolff and O'Donnell
[13] found that bacterial
pneumonia was relatively more common in the era after the introduction of
highly active antiretroviral therapy compared with the era before this
introduction. However, Wolff and O'Donnell emphasized that their findings
reflected a relative increase in bacterial pneumonia compared with
opportunistic infections rather than a true increased risk for bacterial
pneumonia. In other words, highly active antiretroviral therapy is associated
with a greater decreased risk for opportunistic infections rather than for
bacterial pneumonia, thus resulting in an increase in the relative proportion
of pulmonary infections that are bacterial in origin.
Spectrum of Organisms
Similar to that in the general population, bacterial pneumonia in
HIV-infected individuals is usually community-acquired. S. pneumoniae
is the most common infecting organism
[4,
14]. H. influenzae,
Staphylococcus aureus, Escherichia coli, and Pseudomonas
aeruginosa account for most of the remainder of cases
[14,
15,
16]. P. aeruginosa
has been increasingly recognized as an important source of bacterial pneumonia
in HIV-infected individuals, particularly in those with neutropenia, steroid
use, multiple antibiotic therapy, myelosuppressive therapy, and indwelling
catheters [16,
17,
18]. Atypical agents such as
Legionella pneumophila and Mycoplasma pneumoniae are rarely
diagnosed in HIV-infected patients with community-acquired pneumonia
[19].
AIDS patients with advanced immune suppression are also vulnerable to a
host of unusual infectious agents, including Nocardia asteroides,
Rhodococcus equi, and Bartonella henselae and quintana. N.
asteroides is a soilborne aerobic actinomycete, acquired by inhalation.
It usually occurs in southern and rural regions of the United States and,
compared with urban areas, possibly reflects differential exposure of the
populations in these areas to soil-borne pathogens
[15]. The zoonosis R.
equi causes pneumonia in horses and other farm animals. Human infection
occurs exclusively in immunocompromised hosts, including AIDS patients with
CD4 cell counts of less than 200 cells/mm3
[20]. B. henselae and
B. quintana are additional unusual bacteria that are responsible for
the clinical syndromes of bacillary angiomatosis and peliosis in HIV-infected
patients. Exposure to cats and cat fleas is the main risk for infection with
B. henselae, which causes cat-scratch fever. Exposure to lice is the
main risk for infection with B. quintana, which causes trench fever
[15,
21].
Clinical and Radiographic Features of Common Bacterial Pathogens
HIV-infected patients with bacterial pneumonia usually have the same signs
and symptoms as those in the general population. Typically, they present with
a relatively rapid onset of clinical symptoms such as productive cough, fever,
shaking chills, pleuritic chest pain, and dyspnea. Symptoms are usually
present for less than 1 week before the patient seeks medical attention
[14,
22,
23,
24,
25,
26].
Recently, Gold et al. [27]
studied HIV patients with abnormal chest radiographic findings and a lack of
respiratory symptoms. None of the patients in this series had bacterial
pneumonia as a cause of the radiographic findings; in contrast, mycobacterial
infection was a common cause of infection. Thus, bacterial pneumonia is rarely
the cause of radiographic findings in the absence of symptoms.
Despite atypical manifestations and overlapping features among many
pulmonary complications of HIV infection, the chest radiograph is reasonably
accurate in depicting common complications such as bacterial pneumonia,
particularly when radiographic findings are correlated with clinical and
laboratory data [3]. The most
common radiographic pattern in bacterial pneumonia is focal consolidation
(Figs. 1A,
1B), which typically presents
in either a segmental or lobar distribution
[22,
23,
24,
27,
28,
29,
30,
31]. In two studies of
HIV-infected individuals with bacterial pneumonia by Boiselle et al.
[29] and Magnenat et al.
[22], focal consolidation was
observed in approximately 45-60% of patients. Similarly, a CT study by Sider
et al. [30] found that focal
segmental alveolar consolidation was usually associated with bacterial
pneumonia.

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Fig. 1B. Round pneumonia in 33-year-old HIV-positive woman. (Reprinted
with permission from [29])
Lateral chest radiograph localizes consolidation to right middle lobe.
Bacterial pneumonia may occasionally display round appearance. In such cases,
follow-up radiographs are important to document resolution and to exclude
neoplastic mass.
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The combination of focal consolidation seen on chest radiography and
clinical symptoms of less than 7 days' duration has a high specificity for the
diagnosis of bacterial pneumonia
[24]. In a study that assessed
the clinical, laboratory, and radiographic predictors of various respiratory
infections in HIV-infected hospitalized patients, Selwyn et al.
[24] found that the
combination of focal consolidation on chest radiography and a history of fever
for fewer than 7 days was associated with a sensitivity of 48% and a
specificity of 94% for the diagnosis of bacterial pneumonia.
In almost half of the cases of bacterial pneumonia, a radiographic pattern
other than focal consolidation is observed
[22,
29]. Thus, bacterial pneumonia
has been found to be more difficult to diagnose radiographically than either
P. carinii or pulmonary tuberculosis
[29]. Similarly, bacterial
pneumonia has been shown to frequently mimic other infections radiographically
[29]. For example, a bilateral
pattern of alveolar or interstitial opacities may be observed in bacterial
pneumonia, which can mimic P. carinii
[22,
29].
Bacterial infections may also present as solitary or multiple lung nodules
[29,
32,
33,
34,
35]. For example, in a recent
study regarding the cause of pulmonary nodules in HIV-infected patients,
bacterial pneumonia was the most common cause, followed by tuberculosis
[35]. Cavitary pulmonary
lesions (Fig. 2) are another
recognized radiologic finding often associated with bacterial pneumonia in
HIV-infected patients. In a study that investigated the cause of cavitary lung
disease on chest CT scans of HIV-infected patients, Aviram et al.
[36] found a bacterial cause
in 85% of cases. More than one pathogen was identified in most patients in
this series. The most frequently identified pathogens were P.
aeruginosa (Fig. 2) and
S. aureus (Fig. 3).
S. aureus is frequently associated with septic emboli among IV drug
abusers and typically presents radiographically as multiple cavitary nodules
(Fig. 3). This subset of
patients is also prone to develop empyemas
[37]. Less common bacterial
causes of cavitary nodules or cavitary consolidation include N.
asteriodes and R. equi infections. Mycobacterial and fungal
infections are important differential diagnostic considerations for these
findings.

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Fig. 2. Cavitary Pseudomonas aeruginosa in
47-year-old HIV-positive man with advanced immune suppression. CT scan (lung
window setting) at level of right upper lobe bronchus shows cavitary pneumonia
in right upper lobe. Note diffuse bilateral ground-glass opacities and
loculated pleural fluid collection lateral to area of cavitation.
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Fig. 3. Cavitary nodules due to septic emboli in 32-year-old woman
with risk factor of IV drug abuse. CT scan (lung window setting) at level of
superior segment bronchi shows multiple peripheral lung nodules, some of which
show cavitation. Note bilateral pleural effusions.
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Although conventional radiographs are the mainstay of imaging of bacterial
respiratory infections in HIV-infected persons, CT may be useful in selected
cases. For example, nodules, cavities, and pleural fluid collections (Figs.
4A,
4B and
4C) are often better delineated
on CT than on conventional radiographs. CT may thus be useful for further
characterizing atypical radiographic findings, for diagnosing complications of
infection such as abscess or empyema, and for guiding biopsy or drainage
procedures in selected cases.

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Fig. 4A. Pneumococcal pneumonia complicated by empyema in 33-year-old
HIV-positive man. Scout frontal image of chest from CT scan shows increased
opacity in left retrocardiac region with few air bronchograms.
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Fig. 4B. Pneumococcal pneumonia complicated by empyema in 33-year-old
HIV-positive man. Coned-down CT scan (soft-tissue window setting) of left
lower lobe shows necrotizing pneumonia and adjacent loculated pleural effusion
(E), which are due to empyema.
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Fig. 4C. Pneumococcal pneumonia complicated by empyema in 33-year-old
HIV-positive man. Coned-down CT scan (soft-tissue window setting) of left
upper lobe reveals additional loculated pleural fluid collection (E) in major
fissure.
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Parapneumonic pleural effusions are seen in a significant minority of cases
of bacterial pneumonia and are usually small
[29]. Thoracic empyema is more
common in IV drug abusers but has an overall low prevalence
[38]. Borge et al.
[38] postulated that the
impact of HIV on the cellular immune system may impair the development of
empyema.
Although intrathoracic lymph node enlargement is not usually evident on
chest radiographs, mildly enlarged nodes are frequently seen on CT scans of
patients with bacterial pneumonia
[29,
39]. However, mediastinal and
hilar lymphadenopathy are more frequently associated with mycobacterial
infection [30,
36,
39].
HIV-infected individuals with uncomplicated bacterial pneumonia due to
typical pathogens usually show a clinical and radiographic response to
antibiotic therapy, with a time course similar to that of normal hosts
undergoing treatment for community-acquired pneumonia
[14]. In contrast to that of
normal hosts, however, bacterial pneumonia in AIDS patients tends to progress
more rapidly (Figs. 5A,
5B and
5C) and is more often
complicated by cavitation and abscess formation
[37]. In general, resolution
of radiographic abnormalities from treated bacterial pneumonia tends to be
more rapid when compared with that in other lung diseases associated with HIV
infection [14].

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Fig. 5A. Rapidly progressive pneumococcal pneumonia in 50-year-old
HIV-positive man. (Reprinted with permission from
[3]) Portable frontal chest
radiograph reveals focal areas of consolidation in lingula and left lower
lobe.
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Fig. 5B. Rapidly progressive pneumococcal pneumonia in 50-year-old
HIV-positive man. (Reprinted with permission from
[3]) CT scan (lung window
settings) of lower chest obtained as part of abdominal CT scan 1 day after
A shows progressive consolidation in lingula and left lower lobe.
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Fig. 5C. Rapidly progressive pneumococcal pneumonia in 50-year-old
HIV-positive man. (Reprinted with permission from
[3]) Portable frontal chest
radiograph obtained 1 day after B shows rapid progression of pneumonia,
which now involves left lung diffusely. Patient was treated with intubation
for respiratory failure but responded to appropriate antibiotic therapy and
fully recovered.
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Bacteremia is more common in patients with HIV infection than in the
general population [10,
14]. Shah et al.
[40] reported that the
presence of bacteremia does not influence the radiographic pattern of
pneumococcal pneumonia in HIV-infected patients. HIV-infected patients with
bacteremia have a mortality rate similar to patients with seronegative
bacteremia [41].
Clinical and Radiographic Features Associated with Unusual Bacterial
Pathogens
HIV-infected individuals with advanced immune suppression are also at risk
for a variety of unusual organisms, including R. equi, N. asteriodes,
and B. henselae and B. quintana. Patients with R.
equi infection usually present with an indolent course of cough, fever,
and dyspnea. Radiographically, R. equi pneumonia usually presents
with one or more focal areas of consolidation, predominantly in the upper
lobes, with frequent cavitation
[42]
(Fig. 6). Additional features
may include empyema and lymphadenopathy
[31]. The clinical
presentation of N. asteriodes infection is similar to that of R.
equi [7]. The most common
radiographic presentation is a lobar or multilobar distribution of alveolar
consolidation, with an upper lobe predominance and frequent cavitation
[7].

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Fig. 6. Cavitary pneumonia due to Rhodococcus equi infection
in 34-year-old HIV-positive man. CT scan (lung window setting) obtained at
level of carina shows peripheral focus of cavitary consolidation in left upper
lobe. Note subtle foci of ground-glass attenuation in adjacent lung
parenchyma. (Courtesy of Costello P, Boston, MA)
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Bacillary angiomatosis, an infection caused by B. henselae and
B. quintana, is characterized by a neovascular proliferation
involving multiple sites in the body including the skin, liver, spleen, lymph
nodes, and lungs [43,
44]. Exposure to cats, cat
fleas, and lice are the main risk factors for this infection. Affected
patients typically present with angiomatous skin lesions that mimic Kaposi's
sarcoma. Clinical symptoms include fever, night sweats, cough, and occasional
hemoptysis. Bacillary angiomatosis has several radiographic manifestations in
the chest, including endobronchial lesions, parenchymal nodules
(Fig. 7), pleural effusions,
and chest wall masses [43,
44]. Mediastinal
lymphadenopathy is common and is characterized by intense enhancement after
administration of IV contrast material. One should strongly consider this
treatable infection in patients with suspected Kaposi's sarcoma who lack the
typical risk factor (homosexual contact) for this neoplasm
[15,
43,
44].

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Fig. 7. Lung nodules due to bacillary angiomatosis in 38-year-old
HIV-positive man who presented with skin lesions and had HIV risk factor of IV
drug abuse. CT scan (lung window setting) obtained at level of mainstem
bronchi shows numerous scattered lung nodules (arrows), which are
randomly distributed. Several nodules abut pleural surfaces (contrast
appearance with centrilobular nodules in
Figure 8 that spare pleural
surfaces). Random distribution of nodules can be seen in hematogenous spread
of infection or neoplasm. Note bilateral pleural effusions. (Courtesy of White
C, Baltimore, MD)
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Fig. 8. Pyogenic airways disease in 39-year-old HIV-positive man with
recurrent respiratory infections. High-resolution CT scan of lung bases shows
multilobar bronchial dilation, bronchial wall thickening, and bronchiolitis
(arrow). Note clustering of small nodular and branching opacities
that spare pleural surfaces. Such centrilobular distribution is highly
suggestive of infectious cause. Note minimal foci of peripheral consolidation
in right middle lobe and lingula. (Reprinted with permission from
[3])
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Pyogenic Airways Disease
HIV-infected patients are also at increased risk for developing infectious
airways disease such as bacterial tracheobronchitis and bronchiolitis
[45,
46,
47,
48]. Acute bacterial
bronchitis was the predominant lower respiratory infection in cohort members
of the Pulmonary Complications of HIV Infection Study Group
[45] who entered the study
with CD4 levels above 200 cells/mm3. The most common bacterial
organisms responsible for infectious airways disease include H.
influenzae, P. aeruginosa, Streptococcus viridans, and S.
pneumoniae [5,
46,
47].
Pyogenic airways infections lead to inflammatory changes to the walls of
the bronchi and bronchioles, resulting in airway wall thickening and dilation
[46]
(Fig. 8). These changes may be
irreversible if not treated early with antimicrobial agents
[46]. Bronchiectasis has been
noted to develop in a relatively short time after an episode of pulmonary
pyogenic infection in HIV-infected patients
[48]. This shortened time
frame suggests that AIDS patients may experience an accelerated form of
bronchiectasis. In a few HIV-infected individuals, bronchiectasis may occur in
the absence of a history of prior infections and may subsequently predispose
affected patients to future recurrent infections
[49]. HIV-infected patients
with pyogenic bronchitis or bronchiolitis typically present with dyspnea,
fever, and productive cough
[26]. Early in the course of
bacterial infectious airways disease, conventional chest radiographs may fail
to show any obvious abnormality
[46]. In some cases of
infectious bronchitis, bronchial wall thickening (tram tracks) may be observed
radiographically [46].
Extensive bronchiolitis may create an apparent interstitial pattern of
reticulonodular opacities that represents impacted bronchioles
[2]. This pattern is typically
symmetrically distributed, with lower lobe predominance. Such findings may
mimic P. carinii [2].
Chest CT, particularly high-resolution CT, is more sensitive and specific
than radiography for detecting inflammatory changes of the bronchi and
bronchioles [46]. Thus, in a
symptomatic patient with dyspnea, fever, and a productive cough, a
high-resolution CT scan may show findings of small airways disease despite the
absence of radiographic findings
[2].
The characteristic findings of infectious bronchiolitis on high-resolution
CT consist of centrilobular opacities arranged in a tree-in-bud pattern,
manifested by small, Y- and V-shaped opacities in the lung periphery
[2,
3]
(Fig. 8), which represent
bronchioles that are impacted with inflammatory secretions. Focal regions of
air trapping may also be evident on expiratory CT scans
[50]. Although bacteria are
the most common cause of small airways disease in AIDS patients, the
differential diagnosis for this pattern includes mycobacterial, viral, and
fungal infections.
In summary, bacterial respiratory infections, including bacterial airways
disease and pneumonia, account for most pulmonary infections in HIV-infected
patients. The most common radiographic pattern of bacterial pneumonia is the
presence of one or more areas of focal consolidation in a segmental or lobar
distribution. Bacterial pneumonia is also a common cause of lung nodules and
cavities. Pyogenic infectious airways diseases is challenging to diagnose
using conventional radiographs. In contrast, CT features are characteristic
and include bronchial dilation, wall thickening, and nodular and branching
centrilobular opacities.
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