Diagnostic and Interventional Imaging (2012) 93, 425—430

CONTINUING EDUCATION PROGRAM: FOCUS. . .

Benefit of CT scanning for assessing pulmonary

disease in the immunodepressed patient
C. Godet ∗, A. Elsendoorn , F. Roblot

Service de maladies infectieuses et médecine interne, CHU de Poitiers, 2, rue de la Milétrie,

86021 Poitiers cedex, France

KEYWORDS Abstract
Radiology; Introduction: Management of pulmonary disease in immunodepressed patients requires a clear
CT scan; diagnostic and therapeutic strategy and multidisciplinary cooperation.
Chest; Discussion: The diagnostic approach should take into account the type of immunodepression,
Opportunistic the clinical picture, the radiological signs and symptoms, and the microbiological, cytological
infection and even histological examination of the pulmonary or extrapulmonary specimens. The high-
resolution CT scan plays a central role and makes it possible to prioritize the diagnostic
possibilities.
Conclusion: The analysis of the literature shows three important points: the chest X-ray has
low diagnostic value; the CT scan of the chest can reveal lesions that cannot be detected on
a standard chest X-ray; the CT scan is helpful for early detection and monitoring of invasive
pulmonary aspergillosis.
© 2012 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.

The pulmonary diseases that occur in immunodepressed patients are common and serious.
Their etiologies are numerous and may be infectious or noninfectious. Their management
requires standardized pulmonary and immunohematological testing in order to suggest an
appropriate choice of diagnostic tests and treatments. Multidisciplinary cooperation among
pulmonologists, infectious disease specialists, oncologists, hematologists, radiologists,
microbiologists, and intensivists is preferable. Such an organization is essential, since
any diagnostic delay worsens the prognosis, which is dependent on the severity of the
pulmonary disease itself, but also on the immunodepression and underlying comorbidities.

∗ Corresponding author.
E-mail address: c.godet@chu-poitiers.fr (C. Godet).

2211-5684/$ — see front matter © 2012 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.diii.2012.04.001
426
The diagnostic process involves several factors:
• the type, duration, and degree of underlying immunode-
pression, which determines the microbiological possibili-
ties to consider;
• the interview and clinical examination (nonspecific);
• the analysis of signs and symptoms on the standard chest
X-ray (CXR) and especially the high-resolution CT scan
(HR-CT), which makes it possible to determine the eti-
ological possibilities;
• the results of microbiological or histological examina-
tions, which sometimes make it possible to confirm the
diagnosis.
Different types of immunodepression and
principal etiologies of pulmonary
conditions
Immunodepression is the result of a medical condition or
treatment that impairs the body’s defense mechanisms
for fighting infections. We can schematically define three
major types of immunodepression: neutropenic patients,
HIV-infected patients, and other types of immunodepressed
patients.
Neutropenic patients
Neutropenia is an immune deficiency essentially
involving phagocytosis. Profound neutropenia is defined
as a decrease in the neutrophil count to less than
500/mm3 .
During the initial phase of neutropenia, the causal
pathogens are mainly bacteria of the Gram-positive cocci
type, particularly Staphylococcus aureus, or Gram-negative
bacteria such as Pseudomonas aeruginosa. When neutrope-
nia lasts more than 5—7 days, fungal infections may occur
(aspergillosis, candidiasis, mucormycosis). If there is a his-
tory of aspergillosis, it may occur earlier. From a radiological
perspective, these patients have a particular presenta-
tion, since there may be an actual bacterial infection
with no parenchymal opacity, which may not manifest until
the neutropenia is corrected. Conversely, fungal infections
manifest radiologically, since contrary to bacterial infec-
tions, the radiological image does not correspond to an
inflammatory reaction associated with the infection, but
to invasion of the pulmonary parenchyma by aspergillar
hyphae (for example) and areas of infarction due to pul-
monary vascular invasion. This pathogenesis explains the
nodular or triangular (focal) nature of the opacity or radi-
ological image at this stage, said image being most often
surrounded by a halo of ground glass attenuation on the
CT scan, indicating the hemorrhagic nature of the nodule.
Furthermore, it is important to know that, while infectious
pulmonary complications predominate during the aplas-
tic phase, pulmonary opacities should also suggest other
problems such as intraalveolar hemorrhages, hydrostatic
or lesional pulmonary edema, and causes related to drug
toxicity.
This is a major diagnostic challenge, since prognosis
directly correlates with how quickly the underlying pul-
monary condition is treated.
C. Godet et al.
HIV-infected patients
Here, the immune deficiency is essentially linked to a
quantitative and functional CD4 T-cell deficiency. Even
though triple antiretroviral therapy has decreased the num-
ber of opportunistic infections that define onset of the
AIDS stage, such complications are still common in undiag-
nosed patients and those in therapeutic failure. Infectious
and noninfectious pulmonary complications in HIV patients
correlate with CD4 T-cell levels. Pneumocystosis is the
most common infectious complication in patients with
generally fewer than 200 CD4 T-cells/mm3 . Tuberculosis
occurs earlier in the course of HIV infection in patients
with a higher CD4 T-cell level. Some emergent noninfec-
tious pulmonary diseases have become important to know
since the introduction of antiretroviral therapies: immune
restoration syndrome, tumor conditions (Kaposi’s sarcoma,
aggressive lymphoid proliferation, lung cancer, etc.), dif-
fuse infiltrative disease (lymphoid interstitial pneumonia,
organizing pneumonia, smoking-related diffuse infiltrative
pneumonia, pulmonary drug toxicity, etc.) or even cardio-
vascular complications. The HR-CT appears to be a beneficial
tool for the differential diagnosis of these pulmonary
complications, since the analysis of signs and symptoms
considerably reduces the number of diagnostic possibilities,
guides the choice of endoscopic and biopsy specimens to
take, and makes it possible to subsequently assess treatment
response.
Bone marrow graft patients
Some patients who have undergone total body radia-
tion resemble asplenic patients and are very vulnerable
to pneumococcal infections. During conditioning, we find
that the risks related to chemo-induced neutropenia
are often prolonged; in particular, the risk of inva-
sive pulmonary aspergillosis is especially high. Then,
during bone marrow aplasia, these patients are particu-
larly susceptible to cytomegalovirus (CMV) infections and
mycoses such as pneumocystosis. Later, in cases of graft-
versus-host (GVH) disease, noninfectious diseases such as
bronchiolitis obliterans, organizing pneumonia, interstitial
lung disease, or pulmonary cytolytic thrombi should be
considered.
Organ transplant patients
These patients have complications associated with cellular
immune deficiency induced by immunosuppressant therapy.
They are particularly susceptible to intracellular pathogens
such as Legionella pneumophila, Mycobacterium tubercu-
losis and Nocardia asteroides. Aspergillus and Nocardia
infections represent two-thirds of the causes of infection
in heart transplant patients. Of note is the high risk of
CMV infection in lung transplant patients and of toxoplas-
mosis in heart transplant patients, particularly in patients
with no primary infection when the donor is seroposi-
tive. Furthermore, as in bone marrow graft patients and
GVH, noninfectious entities such as bronchiolitis obliterans,
organizing pneumonia, and interstitial lung disease may
manifest.
Benefit of CT scanning for assessing pulmonary disease in the immunodepressed patient
Patients receiving high doses of
corticosteroids
They have a granulocyte function deficiency essentially due
to chemotaxis, but also a decrease in cytokine produc-
tion and inhibition of T-cell activation. These patients are
particularly susceptible to the risk of pneumocystosis, and
frequent differential diagnosis problems versus a specific
underlying condition in the context of collagen disease, lym-
phoproliferative syndromes, and solid tumors treated with
chemotherapy. We compare them with patients treated with
other immunosuppressants.
Diagnostic approach
The diagnostic approach should take several factors into
account:
• the diathesis and underlying immunodepression, since the
possibilities are different depending on type and duration;
• the clinical workup, which is necessary but nonspecific,
and must determine the onset circumstances and nature
of the respiratory symptoms as well as the associated
signs;
• the radiologic signs and symptoms, where the HRCT scan
plays a central role and makes it possible to prioritize the
diagnostic possibilities based on the pattern or predomi-
nant semiotic component;
• the microbiological, cytological, or even histological
examinations of pulmonary or extrapulmonary specimens,
which sometimes make it possible to confirm the diagno-
sis.
Anamnesis
The nature of the underlying disease, the immunosuppres-
sants taken, and the foreseeable duration and profoundness
of the neutropenia are all fundamental elements in the
infectious risk assessment. One of the objectives is to draw
up the patient’s immunosuppression profile in order to assess
the pulmonary infection risks. Furthermore, it is important
to thoroughly evaluate the chronology of the events, i.e.,
duration of the immunodepression and other potentially
toxic therapies received (chemotherapy, radiation therapy,
immunotherapy, immunosuppressant therapies, etc.). The
stage of the underlying disease must be known, along with
its complications, in order to prioritize the differential diag-
noses. Examining the patient’s lifestyle (trips abroad, work
and recreational activities, etc.) makes it possible to detect
exposure to certain particular risks. Lastly, the nature and
effect of anti-infective treatments received at the time of
diagnosis of pneumonia, whether empirical, preemptive,
or prophylactic, must be known, because they help guide
the diagnostic approach and limit the number of possibili-
ties.
Clinical presentation
The clinical examination is essential but nonspecific. Apart
from fever, respiratory signs most often have little value in
determining a cause of infection. The existence of extratho-
racic signs can have great diagnostic value (pulmonary and
427
brain involvement in a seropositive patient could suggest
toxoplasmosis or cryptococcosis, for example). In addition,
such extrathoracic locations may make it possible to take
less invasive diagnostic specimens.
Microbiological diagnostic tests
Whether or not they are invasive, the benefit of a diagnostic
tool should be assessed on a case-by-case basis: expected
benefit versus benefit; impact of expected results on the
patient’s prognosis and choice of therapy. A sputum test is
useful for detecting bacteria, mycobacteria, and fungi. The
induced sputum test is important for diagnosing pneumo-
cystosis in patients who are seropositive for HIV. However,
in some cases (mycobacteria or mold), it is difficult to
distinguish between simple colonization and an actual infec-
tion.
The nasopharyngeal aspiration is cost-effective for
diagnosing respiratory viral infections (molecular tech-
niques) [1]. Detection of galactomannan in the serum or
bronchoalveolar lavage (BAL) is very useful in diagnos-
ing invasive pulmonary aspergillosis (IPA). However, the
results reported by Weisser in 107 patients with IPA show
that a CT scan provides an even earlier diagnosis [2].
Serological tests are also more likely to be positive in angio-
invasive forms (80%) than in broncho-invasive forms (60%)
[3].
Bronchoscopy, which is contraindicated in patients in
acute respiratory failure, remains the gold standard for
exploring pulmonary disease in immunodepressed patients
[4]. That test makes it possible to perform guided BAL, but
also bronchial and transbronchial biopsies, which improve
its diagnostic performance [5]. Pulmonary biopsies can
also be performed by transthoracically, guided by CT
scan, and surgically (video-assisted or open chest surgery).
Here too, the use of these diagnostic techniques in such
immunodepressed and sometimes severely thrombopenic or
neutropenic patients requires an assessment of the expected
risk/benefit ratio [6].
Role of imaging
Standard chest X-ray
This is the first test required for immunodepressed patients
suspected of having lung disease. It is helpful for detecting
intrathoracic abnormalities, but it is difficult to interpret
and its sensitivity is limited, as is its ability to determine an
etiology. In a series of autopsies in 45 leukemia patients with
lung involvement, CXR seemed helpful for diagnosing pul-
monary abnormalities but very inadequate for establishing
an etiological diagnosis, except in cases of acute respiratory
distress syndrome and pulmonary hemorrhage [7]. In another
series of immunodepressed patients not infected with HIV,
a correct diagnosis was made based on an analysis of the
CXR alone in 34% of cases [8]. The CXR was reported to be
normal in 6% of HIV-infected patients with an infection such
as pneumocystosis [9].
The CT scan of the chest
It can play an important role in the management of
persistent fever in immunodepressed patients. The two
428
populations in which the differential diagnostic aid provided
by a CT scan has been studied the most are HIV-infected
and neutropenic patients. In HIV-infected patients, the
HRCT is often essential for confirming or ruling out a
pulmonary condition and sometimes provides etiological
guidance [10—16].
In patients with febrile neutropenia, the HRCT is help-
ful for assessing a lung condition when the CXR is normal
or subnormal. In that case, it helps determine the eti-
ology and guide the collection of specimens such as BAL
[17,18]. A study of 87 neutropenic patients with fever last-
ing more than 2 days while on broad-spectrum antibiotic
therapy showed that more than half of the patients with
a normal CXR had abnormalities suggestive of pneumo-
nia on the HRCT [19]. Another series of 112 neutropenic
patients with a persistent fever and normal CXR reported
that the CT scan detected pneumonia in 60% of them [20].
In these two studies, the CT signs suggestive of pneumo-
nia preceded CXR abnormalities by an average of 5 days.
The authors concluded that any neutropenic patient with a
resistant fever after 48—72 hours of broad-spectrum antibi-
otic therapy and a normal CXR should have a CT scan of the
chest. In another study of 33 patients with febrile neutrope-
nia in whom the CXR was interpreted as normal or subnormal
in one-third and two-thirds of the cases, respectively, the
CT scan resulted in a treatment change in one-third of the
patients [21].
In neutropenic patients with IPA, even a repeated CXR
has low sensitivity and low specificity. When the CT scan
shows nodular opacities (and especially if those nodules
are surrounded by a halo of ground glass attenuation or
‘‘halo sign’’), an infection of fungal etiology (most often
aspergillar) should be suspected [22]. During the correction
of neutropenia phase, alveolar condensation with central
hypodense area or presence of a nodule with an ‘‘air cres-
cent’’ appearance are suggestive of IPA. If the CT scan is
normal, an extrapulmonary etiology of the fever must be
sought [22]. The high incidence of IPA and high morbidity and
mortality from this disease in febrile neutropenia patients
have led to numerous studies on the role of the CT scan in
the early diagnosis of IPA [23—25].
Several studies suggest that early routine use of the
CT scan in neutropenic patients provides a much earlier
diagnosis of aspergillar infection [26,27]. In one of those
studies, the time to diagnosis was reduced to 2—7 days
[27]. Early diagnosis and aggressive management greatly
determine the prognosis in these patients [23—28]. The
approach combining early CT scan and detection of circu-
lating galactomannan is probably the most successful [29].
Furthermore, contrast injection makes it possible to clarify
the relationships between lesions and vascular structures
(assessment of risk of hemoptysis), guide any diagnostic
transparietal puncture biopsy, monitor changes in images
during specific treatment, and take an inventory of resid-
ual lesions for purposes of potential ‘‘cleanup surgery’’.
The HRCT also benefits other immunodepressed patients.
Gulati assessed the diagnostic contribution of the HRCT in
21 kidney transplant patients suspected of having pulmonary
infections; compared with a CXR, the CT scan rectified the
etiological diagnosis in 11 patients (50%) [30].
The HRCT also clarified the etiology of pulmonary
complications in febrile patients who received a
C. Godet et al.
hematopoietic stem cell transplant (HSCT). One team
showed the CT scans were abnormal at least one week
ahead of positive serological tests in these patients [31].
The possibility of noninfectious pulmonary complications
should be borne in mind. These include specific conditions
related to the underlying disease, drug- or radiation-induced
toxicity, intraalveolar hemorrhaging, and hydrostatic pul-
monary edema. The CT scan also makes it possible to suggest
such complications when there is a nonspecific clinical pre-
sentation. Similarly, the HRCT is of major benefit for early
diagnosis of the late noninfectious pulmonary complications
that often mark the follow-up of HSCT patients and are
often related to GVH disease. Recently, the HRCT proved
its benefit for early screening of bronchiolar involvement
in various diseases such as bronchiolitis obliterans after
lung transplantation, before the onset of clinical or func-
tional respiratory effects [32—36]. In fact, the CXR is most
often initially normal and may remain so during the pro-
gression of bronchiolitis obliterans. The CT scan makes
it possible to do a morphological analysis of the bronchi
and bronchioli (dilatation, parietal thickness, etc.) and
to screen for incipient bronchiolar involvement by show-
ing air trapping during forced exhalation [34—40]. But
air trapping during exhalation may also be due to other
conditions, given the difficult medical history of HSCT
patients (radiation therapy, chemotherapy, infection, etc.)
[41,42].
Conclusion
Management of pulmonary disease in immunodepressed
patients requires a formal analysis to establish the best
diagnostic and therapeutic strategy and requires multidisci-
plinary cooperation. The initial diagnostic approach should
take into account the diathesis and underlying immunode-
pression, the clinical examination, and the radiological signs
and symptoms. Imaging, and especially the HRCT, plays a
central management role, making it possible to prioritize the
diagnostic possibilities based on the predominant pattern.
Microbiological, cytological, and histological examinations
of pulmonary or extrapulmonary specimens then sometimes
make it possible to confirm the diagnosis.
TAKE-HOME MESSAGES
• Management of pulmonary disease in immuno-
depressed patients requires a clear diagnostic
and therapeutic strategy and multidisciplinary
cooperation.
• The diagnostic approach should take into account
the type of immunodepression, the clinical picture,
the radiological signs and symptoms, and the
examination of the pulmonary or extrapulmonary
specimens.
• The high-resolution CT scan makes it possible to
prioritize the diagnostic possibilities and allows
early detection of conditions that are not visible
on the chest X-ray, such as invasive pulmonary
aspergillosis.
Benefit of CT scanning for assessing pulmonary disease in the immunodepressed patient
• Any neutropenic patient with a resistant fever after
48—72 hours of broad-spectrum antibiotic therapy
and a normal chest X-ray should have a CT scan of
the chest.
• The injection of contrast clarifies the relationships
between lesions and vascular structures (assessment
of risk of hemoptysis).
• Pulmonary opacities in immunodepressed patients
should suggest noninfectious diseases such as
intraalveolar hemorrhages, hydrostatic or lesional
pulmonary edema, and causes related to drug
toxicity or conditions related to the underlying
disease (tumors, systemic diseases, etc.).
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