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1
Department of Radiology, University of Wisconsin Hospital and Clinics, E3/311
Clinical Science Center, 600 Highland Ave., Madison, WI 53792-3252.
2
Department of Radiology, University of British Columbia Hospital and Health
Sciences Centre, Vancouver Hospital and Health Sciences Centre, Heather
Pavilion, 855 W. 12th Ave., Vancouver, B.C., Canada V5Z1M9.
3
Department of Radiology, University of Michigan Medical Center, 1500 E.
Medical Center Dr., Ann Arbor, MI 48109-0326.
Received January 11, 2000;
accepted after revision February 16, 2000.
Presented at the annual meeting of the American Roentgen Ray Society,
Washington, DC, May 2000.
Abstract
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MATERIALS AND METHODS. The authors retrospectively reviewed the medical records of 262 patients with transplanted lungs at two lung transplantation centers. Patients with a documented pneumonia and correlating abnormal findings on CT (39 patients with 45 pneumonias) were included in the study.
RESULTS. Of 45 pneumonias, Cytomegalovirus (n = 15), Pseudomonas (n = 7), and Aspergillus (n = 8) organisms were the most common single responsible infectious agents. The most common CT findings of pneumonia consisted of consolidation (n = 37; 82%), ground-glass opacification (n = 34; 76%), septal thickening (n = 33; 73%), pleural effusion (n = 33; 73%), and multiple (n = 25; 56%) or single (n = 2; 4%) nodules. No significant difference in the prevalence of findings was revealed among bacterial, viral, and fungal pneumonias (p >.05, chisquare test). Of 25 pneumonias in patients with a single transplanted lung, parenchymal abnormalities involved both lungs in 12 (48%), only the transplanted lung in 11 (44%), and only the native lung in two (8%).
CONCLUSION. The manifestations revealed on CT of bacterial, viral, and fungal pneumonia after lung transplantation are similar, consisting of a combination of consolidation, ground-glass opacification, septal thickening, pleural effusion, or multiple nodules. Therefore, these findings cannot be used to suggest the infectious organisms in this patient population.
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Patients ranged in age from 18 to 67 years (mean age, 45 years) at time of CT scanning. Twenty-three patients (51%) were women and 19 patients (49%) were men. Underlying pulmonary diseases leading to transplantation included emphysema (n = 22, including eight with alpha1-antitrypsin deficiency), cystic fibrosis (n = 7), pulmonary fibrosis (n = 5), Eisenmenger's syndrome (n = 3), primary pulmonary hypertension (n = 1), and sarcoidosis (n = 1). All infectious episodes were documented by one or more of the following methods: bronchoalveolar lavage (n = 16), bronchoscopic biopsy (n = 14), sputum culture (n = 6), autopsy (n = 1), bronchoalveolar lavage and biopsy (n = 5), bronchoalveolar lavage and sputum culture (n = 2) and bronchoalveolar lavage, biopsy and sputum culture (n = 1). Cytomegalovirus (CMV) pneumonia was diagnosed by laboratory findings of characteristic inclusion bodies in material obtained at bronchoscopy or autopsy or by a positive respiratory culture and histopathologic evidence of interstitial pneumonia. Diagnosis of bacterial infection was based on a positive culture of sputum or bronchoscopic aspirate, often combined with a positive blood, lung tissue, or pleural fluid culture. Fungal infection was diagnosed from culture and histologic evidence of tissue invasion.
CT was performed with a variety of protocols, including high-resolution CT (1-mm collimation at 10-mm intervals) combined with helical scanning (5-mm collimation at 10-mm intervals) through the bronchial anastomoses without IV contrast material (n = 25), helical CT (10-mm collimation at 10-mm intervals) with IV contrast material (n = 3), high-resolution CT (1.5-mm collimation at 10-mm intervals) without IV contrast material (n = 9), high-resolution CT (1-mm collimation at 10-mm intervals) without IV contrast material (n = 1), helical CT (10-mm collimation at 10-mm intervals) without IV contrast material (n = 5), helical CT (5-mm collimation at 10-mm intervals) without IV contrast material (n = 1), and helical CT (5-mm collimation at 10-mm intervals) with IV contrast material (n = 1). All CT was performed between 0 and 7 days of documentation of the infectious episode (mean time, 5 days). No patient underwent antimicrobial therapy more than 5 days before CT.
CT findings were reviewed for the presence of nodules (single or multiple, size, margins, zonal distribution, halo sign of a surrounding area of ground-glass attenuation, cavitation), areas of consolidation (lobar distribution, cavitation), ground-glass opacification (lobar distribution), septal thickening, pleural effusion, thickening or enhancement of the pleura, enlarged hilar or mediastinal lymph nodes (<1 cm in short-axis dimension), and bronchial anastomotic complication (stricture, dehiscence, endoluminal debris).
CT findings were initially interpreted by the collaborating chest radiologist (who had access to the patient history) at the home institution and subsequently by one other chest radiologist. In the few instances of interobserver disagreement, a consensus was reached. Frequency of CT findings for bacterial, viral, and fungal pneumonias was evaluated with a chi-square test.
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Bacterial Pneumonia
Of 16 bacterial pneumonias (Table
2), infectious organisms included Pseudomonas (n
= 7), Staphylococcus (n = 3), and one each of
Streptococcus, hemophilus, gram-positive cocci not otherwise
specified, gram-negative cocci not otherwise specified, Legionella,
and combined Pseudomonas and Staphylococcus.
Seven (44%) of 16 pneumonias had multiple nodules with diameters of 1-3 mm (n = 4), 4-10 mm (n = 2), or 1-3 cm (n = 4) on CT. One mass (>3 cm) was revealed. Three pneumonias had a combination of differently sized nodules. Nodule margins were irregular (n = 6) or both smooth and irregular (n = 1). Three pneumonias had branching nodular and linear opacities ("tree-in-bud" pattern) (Figs. 1 and 2), three had a halo of ground-glass opacification surrounding the nodules, and one had nodule cavitation. Fairly equal upper lung zone (apex to carina), middle lung zone (carina to inferior pulmonary veins), and lower lung zone (below inferior pulmonary veins) distribution was shown.
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Consolidation was present in 15 (94%) of 16 pneumonias predominantly in the right middle lobe (n = 7), right lower lobe (n = 12), and left lower lobe (n = 9). Only two cases involved the right upper lobe and three, the left upper lobe. Nine pneumonias had consolidation involving more than one lobe (Fig. 3). The consolidation was unilateral in eight pneumonias, bilateral in seven, and when bilateral, usually asymmetric (n = 4).
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Ground-glass opacification was seen in 13 (81%) of 16 pneumonias and involved all lobes fairly equally (12 right upper lobe, 11 right middle lobe, 13 right lower lobe, seven left upper lobe, and 10 left lower lobe), with 12 pneumonias having more than one lobe involved (Fig. 4). Ground-glass opacification was unilateral (n = 5) or bilateral (n = 9), with bilateral involvement asymmetric (n = 5) or symmetric (n = 4).
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Thirteen (81%) of 16 pneumonias had septal thickening, subjectively graded as mild (n = 6) or extensive (n = 7) (Fig. 5A,5B). Twelve (75%) of 16 pneumonias had pleural effusions (11 right, 11 left, and 10 bilateral), one had thick or enhancing pleura, and two had enlarged hilar (n = 1) or mediastinal (n = 1) lymph nodes.
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Eight (50%) of 16 pneumonias had consolidation and ground-glass opacification; four (25%) had nodules, consolidation, and ground-glass opacification; two (13%) had nodules and ground-glass opacification; one (6%) had nodules and consolidation; and one (6%) had consolidation alone. Of the seven cases of bacterial pneumonia involving a single transplanted lung, four (57%) involved the transplanted lung only, three (43%) involved both lungs, and none involved only the native lung (Table 3).
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Viral Pneumonia
All 15 cases of viral pneumonia (Table
2) were caused by CMV. Nine pneumonias (60%) were associated with
nodules on CT that were multiple in eight and single in one. Nodule size was
1-3 mm (n = 7), 4-10 mm (n = 3), and 1-3 cm (n =
2). Two pneumonias had nodules of more than one size
(Fig. 6), and one had nodules
associated with branching linear opacities (tree-in-bud appearance). Fairly
equal zonal distribution of nodules was noted.
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Ten (67%) of 15 pneumonias had consolidation involving the right upper lobe (n = 5), right middle lobe (n = 4), right lower lobe (n = 5), left upper lobe (n = 3), left lower lobe (n = 5), or more than one lobe (n = 6). The consolidation was unilateral in seven and bilateral in three. When bilateral, consolidation was always asymmetric.
Ten (67%) of 15 pneumonias had areas of ground-glass opacification involving the right upper lobe (n = 7), right middle lobe (n = 8), right lower lobe (n = 7), left upper lobe (n = 4), left lower lobe (n = 6), or more than one lobe (n = 8). Unilateral involvement was seen in five, and bilateral involvement in five, of which four were asymmetric and one symmetric.
Eleven (73%) of 15 pneumonias had septal thickening that was mild in seven and extensive in four (Fig. 7). Ten (67%) of 15 pneumonias had pleural effusions (eight right, five left, and three bilateral). Thick or enhancing pleura was seen in three and right bronchial anastomotic stenosis was seen in one.
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Four (27%) of 15 pneumonias had nodules and ground-glass opacification; three (20%) had both consolidation and ground-glass opacification; three (20%) had nodules, consolidation, and ground glass opacification; three (20%) had consolidation only; one (7%) had nodules and consolidation; and one (7%) had nodules only. Of 11 cases involving a single transplanted lung, only the transplanted lung was involved in six (55%), both lungs in four (36%), and only the native lung in one (9%) (Table 3).
Fungal Pneumonia
All eight cases of fungal pneumonia
(Table 2) were caused by
Aspergillus organisms. Seven (88%) of eight pneumonias had nodules
that were multiple (n = 6) or single (n = 1)
(Fig. 8). The nodules varied in
size from 1-3 mm (n = 4), 4-10 mm (n = 3), and 1-3 cm
(n = 3); and one patient had a mass (>3 cm). Three patients had
nodules of more than one size. The nodules had irregular (n = 6),
smooth (n = 1), or both smooth and irregular (n = 1)
margins. The tree-in-bud pattern was seen in one case of pneumonia. Two cases
had nodules with cavitation (Fig.
9). A fairly equal distribution of upper, middle, and lower lung
zone involvement was seen with all three zones involved in five of the eight
cases.
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Six (75%) of eight pneumonias had consolidation that involved predominantly the lower lobes (six right lower lobe, three left lower lobe, and one each of right upper, right middle, and left upper lobes). Three pneumonias had consolidation involving more than one lobe. Consolidation was unilateral in three and bilateral in three. Bilateral involvement was always asymmetric.
Seven (88%) of eight pneumonias had ground-glass opacification that involved all lobes fairly equally (four right upper lobe, three right middle lobe, six right lower lobe, four left upper lobe, and four left lower lobe) (Fig. 10). Ground-glass opacification was unilateral (n = 2) or bilateral (n = 5), and when bilateral was symmetric (n = 2) or asymmetric (n = 3).
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Five (63%) of eight pneumonias had septal thickening that was mild in four and extensive in one. Five pneumonias had pleural effusions (three right, four left, and two bilateral), and one had right bronchial anastomotic stenosis.
Five (63%) of eight pneumonias had a combination of nodules, consolidation, and ground-glass opacification; one (13%) had nodules and ground-glass opacification; one (13%) had nodules only; and one (13%) had consolidation and ground-glass opacification. Of three cases involving a single transplanted lung, only the native lung was involved in one (33%), and both lungs in two (67%) (Table 3).
Mycobacterial Pneumonia
One patient with bilateral transplanted lungs had mycobacterial disease
caused by Mycobacterium tuberculosis
(Table 2). CT findings showed
multiple 1- to 3-mm nodules with smooth margins in a subpleural distribution
in the right upper, middle, and lower lung zones; focal consolidation in the
right lower lobe (Fig. 11); mild septal thickening; small right pleural effusion; and right hilar and
mediastinal lymph node enlargement.
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Pneumonia of Mixed Cause
Five cases of mixed pneumonia (Table
2) included fungal and bacterial (n = 3), bacterial and
viral (n = 1), and fungal and viral (n = 1). Three (60%) of
five pneumonias had nodules, five (100%) had consolidation, and four (80%) had
ground-glass opacification. CT findings showed septal thickening in three
(60%, two mild, one extensive), pleural effusions in five (100%, five right,
five left, and four bilateral), left bronchial anastomotic stenosis in one,
and debris or exudate in subsegmental bronchi in one (Fig.
12A,12B).
Of four cases involving a single transplanted lung, only the transplanted lung
was involved in one (25%), and both lungs in three (75%)
(Table 3).
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The widespread institution of antibiotic prophylaxis and careful manipulation of immuno-suppressive drugs have greatly decreased perioperative infection-related morbidity. Antibacterial, antiviral, antipneumocystis, and more recently, antifungal prophylaxis are all used [16]. The universal use of trimethoprim-sulphamethoxazole has virtually eliminated infection caused by Pneumocystis and probably a number of other infections (e.g., Nocardia organisms) [16].
Bacterial Pneumonia
Bacteria are the most common cause of infection in patients having
undergone lung transplantation
[15]. In our study, bacteria
alone accounted for 16 (36%) of 45 pneumonias. Although the incidence of
bacterial pneumonia is highest in the first month after transplantation,
bacterial pneumonia continues to be a major infectious complication throughout
the transplant recipient's life
[3]. Bacterial pneumonia is
usually caused by Staphylococcus aureus, Enterobacteriaceae,
Pseudomonas aeruginosa, or other gram-negative organisms
[11,
17,18,19].
In our series, Pseudomonas organisms alone accounted for seven (35%)
of 20 bacterial pneumonias. Pneumonia caused by a single bacterial species is
most common, but mixed organism and anaerobic infections may occur
[20]. Fifteen (94%) of the 16
bacterial pneumonias in our series were caused by a single bacterial
organism.
Isolation of Pseudomonas organisms from the lung allograft occurs more frequently and earlier after transplantation in recipients with cystic fibrosis [21]. Although infections related to Pseudomonas organisms also occur more frequently in recipients with cystic fibrosis, no increase in mortality was seen. In fact, most major transplantation centers show no difference in survival rates for lung transplant recipients with cystic fibrosis and all other lung transplant recipients [1]. Of our nine cases of pseudomonas pneumonia, (including one case of combined pseudomonas and staphylococcal pneumonia and one case of combined pseudomonas and aspergillus pneumonia), the underlying disease before transplantation was cystic fibrosis in three cases (33%).
The most common CT pattern in patients with bacterial pneumonia was consolidation and ground-glass opacification seen in eight (50%) of 16 patients. However, nodules, consolidation, and ground-glass opacification were all common manifestations of bacterial pneumonia, occurring in 44%, 94%, and 81% of cases, respectively. Nodules were various sizes, multiple, irregular, and involved all lung zones. A tree-in-bud pattern was seen in three (19%) of 16 bacterial pneumonias. Consolidation tended to occur in the right middle and both lower lobes. Ground-glass opacification tended to involve all lobes. Septal thickening and pleural effusions were common and seen in 81% and 75% of bacterial pneumonias, respectively.
Viral Pneumonia
CMV is the most significant viral infection and the most common
opportunistic infection occurring after lung transplantation
[22]. CMV infection most
commonly develops between 1 and 4 months after transplantation and varies from
asymptomatic infection to fulminant pneumonia
[23]. CMV pneumonitis develops
in approximately one third of heart-lung transplant recipients
[24,
25]. Acute and chronic
allograft rejection is treated by increasing the dose of immunosuppressive
drugs, which further increases susceptibility to CMV infection. The viral
infection creates a state of immune activation, increasing the risk of
rejection. This cycle generates significant diagnostic and treatment dilemmas
[26]. Ganciclovir prophylaxis
reduces both the incidence of CMV pneumonitis and the severity of infection,
while delaying the onset of chronic rejection
[26,
27].
CMV infection can take one of three forms. Primary infection, the most serious, occurs in seronegative recipients who receive a graft from a seropositive donor. Seropositive recipients may develop reinfection if the donor had been infected by a different CMV strain, or they may reactivate their disease after immunosuppression. Other less common atypical viral pathogens include herpes simplex (less common now that acyclovir prophylaxis is routine), varicella zoster (most common manifestation is mucocutaneous involvement), and Epstein-Barr virus (having an important role in the development of lymphoproliferative disorders) [28].
Nodular opacities with coalescence are a typical radiographic manifestation of CMV infection [29]. CT findings include ground-glass opacification, air-space consolidation, airway dilatation, bronchial wall thickening, and small pleural effusions [4, 30,31,32]. It has been reported that in single-lung transplant recipients, CMV pneumonitis often affects only the transplanted lung [4]. In this series, CMV infections occurred in 11 patients with a single transplanted lung. The transplanted lung alone was involved in six (55%) of 11, both lungs in four (36%), and the native lung only in one (9%).
No common CT pattern was found among our patients with CMV pneumonia. Nodules, consolidation, and ground-glass opacification were all common CT findings, occurring in 60%, 67%, and 67% of pneumonias, respectively. Nodules tended to be multiple and various in size and to involve all lung zones. A tree-in-bud pattern was seen in one (7%) of 15 cases of CMV pneumonia. Consolidation and ground-glass opacification involved all lobes equally. Septal thickening and pleural effusions were common, occurring in 73% and 67% of cases, respectively.
Fungal Pneumonia
Fungal pneumonias are less common than CMV pneumonia after transplantation
but are associated with a higher mortality
[3,
33,
34]. Fungal pneumonias usually
occur between 10 and 60 days after transplantation
[3,
35]. In the case of
single-lung transplantation, fungal pneumonia can involve the native lung;
however, this situation is rare, with the transplanted lung more commonly
involved [33,
36]. However, in our series of
three patients with a single transplanted lung and fungal pneumonia, the
native lung was solely involved in one patient (33%), and both lungs were
involved in the other two patients (67%).
Lung transplant recipients have a much higher incidence of aspergillosis compared with other immunocompromised patients [37]. Infection with Aspergillus organisms occurs most commonly 2-6 months after transplantation [38]. Locally invasive or disseminated aspergillus infection accounts for 2-33% of post-lung transplantation infections and 4-7% of all lung transplantation deaths [6, 8, 37, 39,40,41]. In our series, Aspergillus organisms were the sole infectious agent in eight (18%) of 45 pneumonias.
The lung is the presumed portal of entry for fungal spores, and direct invasion of the lung or airway is present in most transplant recipients dying of invasive aspergillosis. This lung involvement was confirmed in one study in which invasive disease had a 100% mortality rate, and 80% of the patients with invasive disease had fungal invasion of the transplanted lung [42]. Although half of patients have Aspergillus airways colonization at some point after transplantation, invasive aspergillus disease is found in only 3% of patients [42]. Patients with Aspergillus fumigatus airways colonization in the first 6 months after transplantation are 11 times more likely to develop invasive disease than those not colonized with A. fumigatus during this period [42]. The total number of Aspergillus organisms infections does not differ between patients with and without cystic fibrosis, and the isolation of Aspergillus organisms from the respiratory tract occurs in 30-50% of patients in both groups [43]. In our eight cases of aspergillus pneumonia, three patients (38%) had cystic fibrosis.
The most common CT pattern among our patients with fungal pneumonia was a combination of nodules, consolidation, and ground-glass opacification, occurring in five (63%) of eight patients. Nodules tended to be multiple and various in size, have irregular margins, and involve all lung zones fairly equally. The tree-in-bud pattern was seen in one patient (13%) with fungal pneumonia. Although nodules were more frequently seen in fungal compared with other types of pneumonia, this pattern was not statistically significant. Consolidation tended to involve the lower lobes and to be multifocal. Ground-glass opacification tended to involve all lobes fairly equally. Septal thickening and pleural effusions were common, each occurring in 63% of patients with fungal pneumonia.
Mycobacterial Pneumonia
The incidence of pulmonary tuberculosis after lung transplantation is
estimated to be between 2% and 3.8%
[44,
45]. The exact incidence is
unknown but presumably is low, with only 12 instances of M.
tuberculosis infection after lung transplantation reported in the medical
literature
[45,46,47,48,49,50].
In our series of 45 pneumonias, we had only one case of tuberculosis.
Pulmonary tuberculosis after lung transplantation is probably transmitted via
the donor allograft [44]. The
infection typically occurs 1.5-9 months after surgery (median time, 3.5
months) [44]. Our case
occurred 4 months after surgery. Tuberculosis in the transplanted lungs has no
characteristic radiographic pattern
[46,47,48].
The findings include subtle bronchial narrowing, pleural effusions, multiple
bilateral small nodules, multiple bilateral upper and lower lobe cavitary
lesions, pulmonary consolidation, mediastinal lymph node enlargement, and a
solitary pulmonary nodule, similar to the CT findings of multiple nodules,
consolidation, septal thickening, pleural effusion and lymph node enlargement
that were seen in our patient.
Because this study was retrospective, differences were seen in CT protocols from the two contributing medical centers. If some patients were not scanned with high-resolution protocol, underestimation of the incidence of ground-glass opacification could have resulted. The frequency of lymph node enlargement could have been underestimated on CT performed without IV contrast material or with high-resolution CT. The frequencies of different infectious organisms that we report cannot be assumed to be an accurate reflection of the true overall frequency because only cases with abnormal findings on CT and clear documentation of pneumonia were included in the study. As with chest radiography, it may be that patients can have pneumonia and normal findings on CT. Although we were careful to exclude any cases of pneumonia with the possibility that the patient had coexistent disease in the lungs, coexisting conditions such as bronchiolitis obliterans, which are patchy in distribution, can be difficult to diagnose even with openlung biopsy. Some patients were treated presumptively for pneumonia but did not have documentation of an infectious organism and were excluded from the study. In some cases of documented pneumonia, the patient did not have CT within 7 days of diagnosis, and these patients were also excluded.
In summary, the most common abnormal pattern with bacterial pneumonia seen on CT was consolidation and ground-glass opacification; and with fungal pneumonia, the abnormal pattern was a combination of nodules, consolidation, and ground-glass opacification. No predominant pattern was seen with viral pneumonia, although nodules, consolidation, and ground-glass opacification were common findings. When nodules, consolidation, ground-glass opacification, septal thickening, or pleural effusion is seen on CT in a patient with a transplanted lung, they are not helpful in making a specific infectious diagnosis. Lymph node enlargement is uncommonly seen with all types of pneumonia. Pneumonia in patients with a single transplanted lung tended to involve only the transplanted lung, except fungal pneumonia, which involved either the native or both lungs.
CT is useful in the lung transplant population when chest radiographs show nonspecific abnormal findings or when the radiographic findings are normal with the patient showing clinical findings of pulmonary disease. Our study showed that CT does not distinguish between viral, bacterial, and fungal pneumonias. However, it does show areas of lung that can be targeted with bronchoscopic biopsy.
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