DOI:10.2214/AJR.04.1592
AJR 2006; 187:W636-W643
© American Roentgen Ray Society
Cytomegalovirus Pneumonia After Stem Cell Transplantation: Correlation of CT Findings with Clinical Outcome in 30 Patients
Marius S. Horger1,
Christina Pfannenberg1,
Hermann Einsele2,
Robert Beck3,
Holger Hebart2,
Claudia Lengerke2,
Reinhard Vonthein4,
Manfred Wehrmann5,
Christoph Faul2 and
Claus Claussen1
1 Department of Diagnostic Radiology, Eberhard-Karls-University,
Hoppe-Seyler-Strasse 3, Tuebingen 72076, Germany.
2 Department of Hematology-Oncology, Eberhard-Karls-University, Tuebingen,
Germany.
3 Institute of Medical Virology, Eberhard-Karls-University, Tuebingen,
Germany.
4 Department of Medical Biometry, Eberhard-Karls-University, Tuebingen,
Germany.
5 Department of Pathology, Eberhard-Karls-University, Tuebingen, Germany.
Received December 19, 2004;
accepted after revision July 12, 2005.
Address correspondence to M. S. Horger
(mshorger{at}med.uni-tuebingen.de).
WEB
This is a Web exclusive article.
Abstract
OBJECTIVE. The purpose of our study was to assess the correlation
between early high-resolution CT findings of cytomegalovirus (CMV) pneumonia
in patients with blood disorders and their clinical outcomes.
CONCLUSION. The initial high-resolution CT findings in
immunocompromised patients with CMV pneumonia seem to predict the patient's
outcome being unfavorable in those forms of disease beginning mostly
bilaterally as diffuse or patchy ground-glass opacity followed by progressive
air-space consolidation. Also, a change in the CT morphology of pulmonary
lesions toward diffuse ground-glass opacity seems to correlate with an
unfavorable disease course.
Keywords: chest • cytomegalovirus pneumonia • diffuse alveolar damage • high-resolution CT • infectious diseases • transplantation
Introduction
Cytomegalovirus (CMV) pneumonia is still an important cause of morbidity
and mortality in immunocompromised patients, especially in recipients of
allogeneic hematopoietic stem cell transplants. Interstitial pneumonia has an
incidence in this latter group of 15% and is associated with a mortality rate
of 85% if left untreated [1].
Patients with nonhematologic disorders who are receiving long-term steroid
therapy are also prone to this infectious complication, as well as patients
with AIDS. The high-resolution CT manifestations of CMV pneumonia are known to
be polymorphous and to consist mainly of ground-glass opacities, air-space
consolidations, and a nodular or reticulonodular pattern that might be
suggestive of this diagnosis in an adequate clinical setting, but not
specific. The patient's outcome in this high-risk group is known to depend on
many risk factors such as the underlying disease, CMV seropositivity of the
host and donor, degree of immunosuppression, and early onset of antiviral
therapy, as well as on the severity of graft-versus-host disease after
hematopoietic stem cell transplantation.
The aim of this study was to evaluate the frequency of different initial
high-resolution CT findings in patients with CMV pneumonia and to correlate
those findings with the patients' outcomes, also taking into consideration the
influence of associated well-known risk factors for CMV infection. To our
knowledge, ours is the first report regarding prediction of the course of CMV
pneumonia using a particular CT pattern that occurs early in the course of the
disease.
Materials and Methods
Patients
We retrospectively reviewed serial high-resolution CT scans obtained in 30
consecutive patients from a total of 39 patients with CMV pneumonia after
hematopoietic stem cell transplantation. All cases were identified by a
prospective analysis of immunocompromised patients who developed clinical and
radiologic signs of pulmonary infection between January 1998 and May 2004, and
were then retrospectively evaluated with respect to the frequency of
high-resolution CT patterns of infection and their influence on the patient's
outcome.
Pulmonary CMV infection was diagnosed in all patients by isolating CMV in
cell cultures from bronchoalveolar lavage and also, in six patients, by
biopsy. In seven patients, bronchoalveolar lavage samples were also positive
for other pathogens, resulting in the exclusion of those patients from the
final evaluation. Two additional patients with positive CMV cultures from the
bronchoalveolar lavage had no CT signs of pulmonary infection and therefore
also were excluded from the study because the samples were considered to
probably be a result of oropharyngeal contamination without CMV pneumonia. For
isolation of CMV by cell culture, monolayers of human foreskin fibroblasts
were inoculated with 0.2 mL of bronchoalveolar lavage and maintained in
culture for up to 3 weeks. CMV was identified by its characteristic cytopathic
effect.
The mean time between the CT examination and the confirmation of pulmonary
CMV infection by virologic examination was 1.6 days (range, 0-6 days). In two
patients in whom the interval between CT and virologic diagnosis was longer
than 48 hours, the absence of significant interval change in the pattern of
parenchymal changes between the dates of CT and microbiologic diagnosis was
ensured with sequential chest radiographs. The median time between the
clinical onset of CMV pneumonia and the first CT investigation was 0.6 days
(range, 0-4 days). The median time between the first CT scan and the onset of
antiviral therapy was -1.7 days (range, -24 to 7 days); these figures also
include patients undergoing antiviral drug prophylaxis
(Table 1).
All patients were immunocompromised as a result of hematologic diseases as
follows: 11 patients had acute myelogenous leukemia, five patients had chronic
myelogenous leukemia, four patients had acute lymphoblastic leukemia, three
patients had non-Hodgkin's lymphoma, four patients had multiple myeloma, two
patients had severe aplastic anemia, and one patient had chronic lymphatic
leukemia (Table 2). The
patients were 19 men and 11 women who ranged in age from 26 to 60 years (mean
age, 42 years).
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TABLE 2: Initial CT Findings in Patients with Cytomegalovirus (CMV) Pneumonia:
Distribution and Association with Known Risk Factors
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CT was performed with either a single-detector CT scanner (Somatom Plus 4,
Siemens Medical Solutions) or an MDCT scanner (Volume Zoom, Siemens Medical
Solutions). All patients underwent between two and eight unenhanced CT
examinations (mean, 3.3 examinations) of the thorax. Scanning parameters for
helical CT of the chest with a single-detector CT scanner were 120 kVp, 120
mAs, 5-mm collimation, and a pitch of 1.5. Axial scans through the thorax were
obtained during full inspiration. Additional thin-section CT scans were
obtained with 1.0-mm collimation and at 10-mm slice intervals. On the Volume
Zoom scanner, a collimation of 4 x 1.0 mm and a slice width of 1.25 mm
were chosen. The table speed rotation was 6 mm, and the rotation time was 0.75
seconds with a pitch of 1.5. We used an increment of 1.2 mm. The tube voltage
was 120 kV and the tube current-time product was 100 mAs. Images were
reconstructed with a high-spatial-frequency algorithm (high-resolution CT)
B70s kernel. All scans were viewed at standard mediastinal windows (level, 35
H; width, 450 H) and lung windows (level, -700 H; width, 1,500 H).
The CT scans were reviewed separately by two experienced chest
radiologists, and conclusions were reached by consensus. Both reviewers of the
CT scans were aware of the results of the virologic examinations. The pattern,
distribution, and extent of pulmonary abnormalities were analyzed. The
infiltrates were classified as air-space consolidation, ground-glass opacity,
centrilobular ill-defined opacities, and reticulation.
Air-space consolidation was defined as an area having a dense increase in
attenuation and obscuration of the underlying vessels, showing different
morphology in the form of segmental, subsegmental, or patchy infiltrates.
Ground-glass opacity was defined as a hazy increase in lung attenuation
without obscuration of the underlying pulmonary vasculature and distributed in
either a diffuse or a patchy manner. Centrilobular abnormalities relating to
structures such as bronchioles or small arteries and consisting of ill-defined
nodules or ground-glass opacity were called centrilobular opacities. A
reticular pattern was defined as an interlacing line shadow suggesting a mesh
or net, and its presence was analyzed with regard to association with
ground-glass opacity or centrilobular abnormalities.
Ground-glass opacity or air-space consolidation distributed diffusely
throughout the parenchyma, without zonal predominance, was called diffuse; and
parenchymal infiltrates with lobular, segmental, or lobar distribution
involving one or both lungs were called focal.
Analysis of initial CT examinations was focused on the presence of one or a
combination of these CT signs. Finally, the predictive value of the CT
morphology of pulmonary infiltrates on outcome was also assessed, taking into
consideration the influence of other risk factors, including CMV
seropositivity, underlying disease, and the presence of graft-versus-host
disease. Twenty-eight of 30 allograft recipients showed seropositivity for CMV
before transplantation. Two patients were seronegative for CMV.
Graft-versus-host disease, which is known to be a risk factor in patients
after allogeneic stem cell transplantation because of sustained
immunosuppressive therapy, occurred in 16 patients. For statistical purposes,
we classified all patients as either graft-versus-host disease-positive or
graft-versus-host disease-negative, irrespective of the degree of
posttransplantation complications. This information is available in
Table 2.
We also differentiated early versus late initiation of therapy with respect
to therapy onset (initiated > 72 hours or < 72 hours before respiratory
failure requiring mechanical ventilation). Three of 12 of the deceased
patients had received early antiviral treatment, whereas in nine patients
antiviral therapy was started late in the course of disease, either the same
day the CMV pneumonia became clinically manifest (n = 8) or the day
before (n = 1). The duration of therapy in the group of deceased
patients ranged from 1 to 24 days (mean, 5 days).
Twelve patients (40%) of 30 in our cohort died during the acute episode of
CMV pneumonia.
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Fig. 1 —44-year-old man with chronic myeloid leukemia after
allogeneic transplantation. Thin-section high-resolution CT scan shows diffuse
bilateral ground-glass opacity (arrow) sparing some lung segments.
This CT finding was initial manifestation of pulmonary infection in this
patient, progressing at follow-up to ground-glass opacity and air-space
consolidation (not shown). Patient died 3 days after follow-up despite
intensive antiviral therapy.
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Fig. 2 —42-year-old man with acute myeloid leukemia after allogeneic
bone marrow transplantation. Thin-section high-resolution CT scan reveals
scattered parenchymal small, mostly ill-defined centrilobular opacities.
Lesions resolved at follow-up after antiviral therapy.
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Fig. 3 —Thin-section high-resolution CT scan in 56-year-old woman
with acute myeloid leukemia shows small confluencing centrilobular nodule-like
opacities (arrow) accompanied by fine reticulation. At follow-up, no
progress of cytomegalovirus pneumonia was noted, but patient died later due to
fulminant angioinvasive aspergillosis. Diagnosis was confirmed by autopsy.
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Fig. 4 —High-resolution CT scan in 45-year-old man with multiple
myeloma after allogeneic transplantation initially shows patchy infiltrates
consisting of ground-glass opacity and consolidation due to pulmonary
cytomegalovirus infection. Patient died 14 days after imaging despite
intensive antiviral therapy.
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Statistics
For all mentioned clues of outcome, odds ratios were estimated one by one
into 95% CIs. The confidence level was not adjusted for multiplicity because
the analysis was meant to rank risks only and to give hints for power
calculations of follow-up studies. In a logistic regression analysis
(estimated using the software JMP IN, version 5.1, SAS Institute, 2003) from
outcome on transplantation-related factors (graft-versus-host disease, host
CMV seropositivity, donor CMV seropositivity) and treatment-related factors
(therapy onset), the CT signs were screened for their diagnostic value one by
one.
Results
The most common high-resolution CT findings are listed in
Table 2. Fifteen patients
showed focal pulmonary abnormalities and 15 patients presented with bilateral
diffuse pulmonary infiltrates. Focal infiltrates were multiple in 13 patients
and solitary in two patients. Seventeen patients (57%) showed larger areas of
ground-glass opacity, some of them (n = 13) progressing at follow-up
to diffuse air-space consolidations; six patients (20%) initially showed
air-space consolidations, and seven patients (23%) presented with small
ill-defined centrilobular opacities. Eighteen of the 30 patients with CMV
pneumonia presented one pattern of pulmonary infection only, whereas 12
patients showed a mixed pattern consisting of two or more of the previously
mentioned high-resolution CT findings.
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Fig. 6 —57-year-old man with acute myelogenous leukemia after
allogeneic peripheral blood stem cell transplantation. High-resolution CT scan
shows lobular ground-glass opacities and delineation of secondary lung lobules
due to lymphedema (arrow). At follow-up (not shown), diffuse opacity
of both lungs was seen, suggesting diffuse alveolar damage. Patient died 4
weeks after follow-up despite sustained antiviral therapy.
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Fig. 7 —34-year-old woman with acute lymphoblastic leukemia after
allogeneic bone marrow transplantation. High-resolution CT scan reveals
coexisting focal bilateral zones of ground-glass opacity (white
arrow) or consolidation (black arrow).
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For statistical purposes, we classified pulmonary infiltrates in patients
with mixed forms according to the predominant pattern of infection (see
Table 1). Thus, 11 patients
showed areas of ground-glass opacification
(Fig. 1) only. Ground-glass
opacity was associated with a second pattern of infection in seven patients:
air-space consolidation (n = 5) and centrilobular opacities
(n = 2). An association of ground-glass opacity with two other CT
patterns of infection was not found in any patient, but a combination of all
four previously mentioned CT findings was observed in only one patient.
Four patients presented exclusively with ill-defined nodule-like
centrilobular opacifications (Fig.
2). An association of the centrilobular opacification pattern of
CMV infection with a second CT feature was found in six patients: air-space
consolidation (n = 2), ground-glass opacity (n = 3), and
reticulation (n = 1). In Figure
3, a mixed reticular and centrilobular ground-glass opacity
pattern of CMV pneumonia is shown. In cases in which the dominant pattern of
infection consisted of centrilobular opacity, there was no association with
more than one other CT finding of infection. Air-space consolidation was the
sole CT manifestation of infection in three patients. An association with a
second CT pattern was found in six patients, five of whom had accompanying
ground-glass opacity, and in one patient air-space consolidation and
centrilobular opacities were encountered together. Ground-glass opacity or
large lung parenchymal air-space consolidations were found in eight patients
in a patchy, bilateral distribution (Fig.
4). In 12 patients, air-space consolidation or large ground-glass
opacity involved only focal lung parenchymal zones
(Fig. 5). No preferential
location was seen among the lung upper, middle, or lower zones. The
centrilobular opacities measured less than 1 cm in all 12 patients. In two
patients, centrilobular opacities were associated with small air-space
consolidations in a patchy distribution.
Twelve patients (40%) of 30 in our cohort died during an acute episode of
CMV pneumonia. All of these 12 patients belonged either to the group showing
large diffuse ground-glass opacity or to the group showing focal ground-glass
opacity (Figs. 6 and
7). All these cases progressed
at follow-up to diffuse bilateral opacifications accompanied by a mesh of
largely interlobular lines. One patient in this group showed primarily small
centrilobular opacities on CT. CMV reactivation was documented at the same
time. and antiviral therapy was promptly administered. At CT follow-up 2 weeks
later, the ill-defined centrilobular opacities showed almost complete
resolution. However, shortly thereafter the patient presented again with
clinical symptoms of infection despite ongoing antiviral therapy. Follow-up CT
showed CMV infiltrates morphologically different from those initially reported
but rather corresponding to the CT manifestations of the 12 patients who died
from CMV pneumonia (Figs. 8A,
8B, and
8C).
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Fig. 8A —60-year-old man with acute myelogenous leukemia after
induction therapy. During bone marrow regeneration, small ill-defined
centrilobular opacities (arrow) were seen in both lungs on CT. At
that time, cytomegalovirus pneumonia (CMV) reactivation was documented. After
antiviral therapy, centrilobular opacities resolved almost completely.
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Fig. 8B —60-year-old man with acute myelogenous leukemia after
induction therapy. Two weeks after A, despite sustained antiviral
therapy, patient again developed symptoms of pulmonary infection. At that
time, new CT pattern of pulmonary infection consisting of patchy ground-glass
opacity and septal edema was seen.
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Fig. 8C —60-year-old man with acute myelogenous leukemia after
induction therapy. Three days after B, CT scan shows ground-glass
opacity and air-space consolidation, suggesting diffuse alveolar damage.
Patient died of CMV pneumonia a few days later despite intensive antiviral
therapy.
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Statistically, a large area of ground-glass opacity was the only factor for
which the CI for the odds ratios did not span the value 1
(Table 3). After adjustment for
treatment factors, ground-glass opacity was an even stronger predictor of a
lethal outcome, whereas air-space consolidation seemed to indicate a favorable
outcome, as did focal lesions and especially small centrilobular opacities.
Late-onset therapy was the worst risk factor. A diffuse pattern of parenchymal
infiltrates was found more often in patients who died of the infection. CMV
seropositivity seemed to be of minor importance in this study because most of
the transplant recipients proved to be already seropositive.
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TABLE 3: Odds Ratios (OR) and 95% CIs of Outcome for Treatment Factors and CT
Signs, with the Latter Adjusted by the Former
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Histologic data from two deceased patients were available and correlated
with the findings on thin-section CT. Interstitial fibroblastic proliferation
and lymphocytic infiltration associated with type II pneumocyte (i.e.,
alveolar cell) hyperplasia, intraalveolar exudates, and hyaline membrane
formation were found in both patients, presenting at high-resolution CT in a
pattern of diffuse ground-glass opacity and air-space consolidation. Both
patients presented at follow-up with clinical signs of adult respiratory
distress syndrome. Immunohistochemical analysis showed abundant CMV-positive
giant cells.
Discussion
CMV pneumonia is a frequent life-threatening infectious complication in
severely immunocompromised patients. Particularly, in patients recovering from
bone marrow or peripheral blood stem cell transplantation, CMV is a major
cause of morbidity and mortality. The incidence of CMV pneumonia is considered
to be about 20%, with a mortality rate of approximately 80% over a 10-year
period [2]. CMV pneumonia is
usually diagnosed on the basis of clinical symptoms such as fever, dyspnea,
hypoxemia, and lung parenchymal infiltrates on chest radiography or CT, in
combination with the isolation of CMV from bronchoalveolar lavage by cell
culture. In addition, CMV pneumonia can be diagnosed histologically by showing
CMV cells associated with inflammatory reaction and tissue destruction.
Because of its superiority over radiographic diagnosis in characterizing
atypical pneumonia, CT should be performed early in the course of the disease
to assess the pattern of pulmonary infiltration and its extent in an effort to
correctly classify the pulmonary infection. For this purpose, experience in
this diagnostic field is mandatory and consists mainly of awareness and
mastering the major radiologic signs of CMV pneumonia, especially on CT.
Thin-section CT findings of CMV pneumonia are known from previous publications
and consist of a mix of patterns, most commonly ground-glass opacity,
air-space consolidation, and nodular opacities
[3,
4].
Our results are concordant with those describing the frequency of specific
CT findings in patients with CMV pneumonia. Thus, ground-glass opacity was the
most common high-resolution CT finding in our study, observed in 56% of the
investigated patients, which is similar to that reported by other authors
[5,
6]. Patients with large areas
of ground-glass opacity on high-resolution CT were all prospectively
classified correctly as suspicious for CMV pneumonia. However, small
centrilobular (nodule-like) opacities and reticular opacities, which are also
common CT findings, proved difficult to differentiate from other viral
pneumonias, or Pneumocystis carinii pneumonia, especially the latter
in AIDS patients, although the association of these two pathogens is known to
be high [7]. Large nodular
opacities and focal parenchymal consolidations are also nonspecific findings
that often create difficulties in the diagnosis, particularly in the
differentiation from pulmonary mycosis, but they were fortunately not very
often found and were not accompanied by a typical halo in any patient.
However, the main purpose of this study was to determine if any correlation
existed between CT patterns of CMV pneumonia and the patient's outcome. To
establish the eventual predictive value of a certain CT pattern of pulmonary
infection on the outcome, we had to first analyze the influence of other
accompanying known risk factors for CMV infection on the course of this
disease. The most common risk factors for CMV infection consisted of acute and
chronic graft-versus-host disease, positive serology for CMV of recipient or
donor before transplantation, and typical transplantation-related problems,
such as a higher risk for unrelated or mismatched transplants and delayed
recovery of the CMV-specific cytotoxic T-cell response. The onset of antiviral
therapy—that is, the CMV prophylaxis—in each individual patient
also plays a decisive role in disease management. Our results show a
recognizable influence on the outcome by some of these risk factors. The late
onset of antiviral therapy had relevant negative influence on the disease
course, as anticipated [8].
CMV seropositivity, however, was so widespread in our series that it was
diagnostically useless. Other published data dealing with the frequency of CMV
pneumonia in larger series of hematopoietic stem cell transplant recipients
and other immunosuppressed patients have shown a higher risk of infection in
sero-positive patients than in those who were sero-negative (3.3% vs 0%) and
also a higher frequency of hematologic malignancies than in patients with
solid tumors (5.0% vs 1%)
[9].
Irrespective of the impact of these risk factors, including CMV
seropositivity and graft-versus-host disease, on the course of the disease,
all deceased patients with CMV pneumonia in our study had similar CT
morphology of their pulmonary infiltrates, initially and at follow-up. Most
(91%) presented early in the diagnosis either a diffuse or a patchy pattern of
pulmonary ground-glass opacity that developed at follow-up to progressive
interlobular septal thickening and air-space consolidation. Only one patient
showed initially a different CT manifestation of pulmonary infection,
represented by small ill-defined centrilobular opacities that turned, after
temporarily regression, into the typical CT pattern of CMV pneumonia
encountered in all other deceased patients. Thus, the uniformity of initial CT
findings in patients whose respiratory function had deteriorated at follow-up,
suggests the possibility of predicting an unfavorable course of the disease
using this particular CT pattern of infection.
The transformation of the nodular pattern into a patchy or diffuse
interstitial pattern of infiltration during sustained antiviral therapy might
suggest viral cytotoxicity or the presence of additional immune mechanisms.
Cytomegalovirus is known to cause direct tissue damage, but the pathogenesis
of CMV-induced pulmonary disease is complex, and contradictory hypothesis have
been presented
[10-14].
Pathologists usually differentiate two patterns of CMV pneumonia, one
consisting of small, mostly well-defined hemorrhagic nodules scattered
throughout the lung parenchyma, and the second a diffuse type affecting most
of the parenchyma and showing histologic features of diffuse alveolar damage
or interstitial pneumonia
[15-17].
Some have also speculated that the diffuse ground-glass opacity pattern
might represent endogenous pulmonary infection or extension of the nodular
form to involve most of the lung
[18,
19] and that this diffuse form
of pulmonary manifestation could represent an early manifestation of diffuse
alveolar damage [20]. The CT
pattern of pulmonary infection observed in all of our deceased patients could
have been the expression of early diffuse alveolar damage, which is also
sustained by the histologic features, obtained at follow-up, in two patients
in this group. That some patients belonging to the group with an unfavorable
CT pattern of infection survived CMV pneumonia might reflect the influence of
the other risk factors, especially of the degree of immunosuppression.
In conclusion, the only common radiologic feature in all patients with a
fatal outcome of CMV pneumonia was the uniform initial CT pattern of pulmonary
infection presenting as bilateral, diffuse, or patchy ground-glass opacities
followed by progressive consolidation. Therefore, we believe that these CT
findings, and a sudden change of CT pattern of CMV infection at follow-up to
the diffuse, bilateral ground-glass opacity pattern, resembling diffuse
alveolar damage, should be regarded as a sign that accurately predicts an
unfavorable course of the disease.
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Abstract
Introduction
