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DOI:10.2214/AJR.04.1592
AJR 2006; 187:W636-W643
© American Roentgen Ray Society

Clinical Observations

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).

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Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
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
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
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
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
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).


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  		TABLE 1: Time Between First Symptoms of Cytomegalovirus Pneumonia, First CT Examination, and Therapy Onset

 

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

 

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.


Figure 1
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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.

 


Figure 2
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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.

 


Figure 3
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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.

 


Figure 4
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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.

 
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
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Discussion
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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.


Figure 5
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  		Fig. 5 —55-year-old man with acute myelogenous leukemia. High-resolution CT scan shows focal consolidation in peribronchial distribution (arrow). Patient recovered after antiviral therapy.

 


Figure 6
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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.

 


Figure 7
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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).

 
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).


Figure 8
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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.

 

Figure 9
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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.

 

Figure 10
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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.

 

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

 

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
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 Introduction
 Materials and Methods
 Results
 Discussion
References
 
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.


References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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