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Respiratory Viral Infections in Lung Transplant Recipients: Radiologic Findings with Clinical Correlation¹

¹ From the Departments of Radiology (L.D.M., H.P.M.); Medicine, Division of Pulmonary and Critical Care Medicine (S.M.P., V.F.T.); Pathology (D.N.H., N.G.H.); and Surgery, Division of Cardiothoracic Surgery (R.D.D.); Duke University Medical Center, Box 3808, Erwin Rd, Durham, NC 27710, and the Durham Veterans Administration Hospital, NC (D.N.H., N.G.H.). Received November 27, 1998; revision requested December 29; final revision received March 17, 1999; accepted July 1. Address reprint requests to H.P.M. (e-mail: mcada003@mc.duke.edu).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To evaluate radiologic findings of respiratory viral infection in lung transplant recipients with clinical correlation.

MATERIALS AND METHODS: Over 5 years, 21 episodes of respiratory viral infection (parainfluenza [n = 9], respiratory syncytial virus [n = 8], adenovirus [n = 5], influenza [n = 2]) were diagnosed 6–727 days (mean, 270 days) after lung transplantation in 20 recipients. Chest radiographs, computed tomographic (CT) images, and clinical records were reviewed.

RESULTS: Sixteen episodes of respiratory viral infection were diagnosed in patients with symptoms of lower respiratory tract infection or acute allograft dysfunction; five were diagnosed in asymptomatic patients. Chest radiographs were abnormal in 11 (52%) episodes; findings included heterogeneous or homogeneous opacities and masslike consolidation. All patients with radiographic abnormalities were symptomatic. Chest radiographs were unchanged from baseline in 10 (48%) episodes; in one, CT revealed findings not depicted at radiography. Adenoviral infection (n = 5) was typically symptomatic, was associated with new radiographic abnormalities, and was rapidly lethal (n = 4). Infection with parainfluenza and/or respiratory syncytial virus was commonly asymptomatic and was not associated with radiographic abnormalities; affected patients had good outcomes.

CONCLUSION: Respiratory viral infections are important causes of morbidity and mortality in lung transplant recipients. Radiographic abnormalities in patients with respiratory viral infections were usually accompanied by symptoms of lower respiratory tract infection. Adenoviral infection was frequently accompanied by progressive pulmonary opacity and fatal outcome.

Index terms: Bronchoscopy • Lung, CT, 60.1211 • Lung, infection, 60.206, 60.2062, 60.2066, 60.2069, 60.458 • Lung, transplantation, 60.458

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
The first clinically successful lung transplantation was performed in 1983 (1). Since then, improvements in donor management, lung preservation, surgical techniques, infection prophylaxis, immunosuppression, and rejection management have resulted in improved survival and decreased morbidity. Lung transplantation is now considered an acceptable therapy for the treatment of many endstage lung diseases, including emphysema, pulmonary fibrosis, and cystic fibrosis.

Infection remains a major cause of morbidity and mortality in lung transplant recipients. Bacterial pneumonia and opportunistic infection with organisms such as cytomegaloviruses and Aspergillus organisms account for most serious infections after transplantation (2–5). However, community-acquired respiratory viral infections, such as those caused by respiratory syncytial virus, influenza, parainfluenza, or adenovirus, are increasingly recognized as causes of serious pneumonia in lung transplant recipients (6–11). While the radiologic features of bacterial, fungal, or cytomegaloviral pneumonia are well known (3), the findings of respiratory viral infection in lung transplant recipients are poorly documented.

The purpose of this study was to review the radiologic findings for respiratory viral infection in our lung transplant population and to correlate these findings with clinical features and outcomes.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Between November 1992 and May 1998, 182 lung transplantations were performed at Duke University Medical Center, Durham, NC, in 176 patients who were at least 18 years of age. Twenty-one episodes of respiratory viral infection were identified in 20 patients who had undergone unilateral (n = 15) or bilateral (n = 5) lung transplantation. The clinical features in the first 10 episodes were previously reported (6). Infection was diagnosed in seven men and 13 women, who ranged in age from 21 to 65 years (mean age, 48 years). Indications for transplantation were pulmonary emphysema (n = 13), cystic fibrosis (n = 5), or idiopathic pulmonary fibrosis (n = 2).

Diagnosis of respiratory viral infection was made in 19 episodes on the basis of positive findings from direct fluorescence antibody testing (n = 7), viral culture (n = 11), or both (n = 1) in specimens obtained at bronchoalveolar lavage. Diagnosis of respiratory viral infection was made in two episodes by means of immunoperoxidase staining for adenovirus in specimens obtained at open lung biopsy (n = 1) or at autopsy (n = 1).

Over the study period, all transplant recipients received prophylactic treatment for infection with Pneumocystis carinii, yearly influenza vaccinations, prophylactic treatment for infection with cytomegalovirus (in selected cases), and standard immunosuppressive treatment (6). Routine surveillance fiberoptic bronchoscopy was performed at 1, 3, 6, and 12 months after transplantation. In addition, fiberoptic bronchoscopy with bronchoalveolar lavage or transbronchial biopsy was performed if patients had clinical or radiologic abnormalities at any time after transplantation. All specimens were routinely sent to the laboratory for viral culture. Virus-specific direct fluorescence antibody assays were routinely performed on specimens obtained at bronchoalveolar lavage after January 1995.

Clinical records were available for all patients and were reviewed by one author (S.M.P.) for signs and symptoms at the time of diagnosis, results of pertinent diagnostic tests, response to therapy, and outcome. Clinical symptoms were categorized as those due to lower respiratory tract infection, upper respiratory tract infection, or neither.

Chest radiographs (erect posteroanterior and left lateral [n = 15], supine anteroposterior [n = 3], or erect anteroposterior [n = 3]) were obtained in all patients on the day of diagnostic fiberoptic bronchoscopy. The radiographs were jointly reviewed by two thoracic radiologists (L.D.M., H.P.M.) who were aware that all patients had proved respiratory viral infection but who were unaware of the patient's clinical status at the time the radiograph was obtained; agreement was reached by consensus. The chest radiographs were compared with baseline radiographs and were classified according to pattern (unchanged from baseline, heterogeneous opacities, homogeneous opacities) and distribution of abnormalities. The presence or absence of associated findings, such as pleural effusion or adenopathy, and findings on follow-up chest radiographs were also recorded.

Chest computed tomographic (CT) images that were obtained within 1 week of the documented infection were available for three patients and were also jointly reviewed by the two thoracic radiologists who were aware that all patients had proved respiratory viral infection but who were unaware of the patient's clinical status at the time CT was performed; agreement was reached by consensus. CT findings of ground-glass opacity, consolidation, bronchial wall thickening, and bronchial dilatation and distribution of abnormalities were recorded.

Means were calculated by using Excel, version 5.0 (Microsoft, Redmond, Wash). The Fisher exact test for group comparisons was performed by using SAS, version 6.12 (SAS Institute, Cary, NC).

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Twenty patients had 21 episodes of documented respiratory viral infection that were diagnosed between 6 and 727 days (mean, 270 days) after transplantation. Thus, 20 (11%) of 176 adult lung transplant recipients at our institution had at least one episode of respiratory viral infection over 5 years. All infections caused by respiratory syncytial virus or influenza occurred in winter or early spring. Infections with parainfluenza or adenovirus were distributed throughout the year. Clinical data and radiologic findings are summarized in Tables 1 and 2, respectively.

View larger version (156K): [in this window] [in a new window]   Figure 1. Infection with respiratory syncytial virus in a 56-year-old man (patient 8) who presented with cough and fever 4 months after undergoing left lung transplantation for emphysema. Posteroanterior chest radiograph shows heterogeneous perihilar opacities (arrows) in the left lung, which was a new finding when compared with prior radiographs.

View larger version (125K): [in this window] [in a new window]   Figure 2a. Infection with respiratory syncytial virus in a 50-year-old woman (patient 9) who presented with cough and fever 7 months after undergoing right lung transplantation for an -1-antiprotease deficiency. (a) Initial anteroposterior chest radiograph shows diffuse heterogeneous opacity in the right middle and lower lobes and a small ipsilateral loculated pleural effusion (arrow) in the minor fissure. (b) Anteroposterior chest radiograph obtained after 1 week of therapy with ribavirin shows the pulmonary opacities and effusion have resolved.

View larger version (129K): [in this window] [in a new window]   Figure 2b. Infection with respiratory syncytial virus in a 50-year-old woman (patient 9) who presented with cough and fever 7 months after undergoing right lung transplantation for an -1-antiprotease deficiency. (a) Initial anteroposterior chest radiograph shows diffuse heterogeneous opacity in the right middle and lower lobes and a small ipsilateral loculated pleural effusion (arrow) in the minor fissure. (b) Anteroposterior chest radiograph obtained after 1 week of therapy with ribavirin shows the pulmonary opacities and effusion have resolved.

View larger version (97K): [in this window] [in a new window]   Figure 3a. Infection with adenovirus in a 53-year-old man (patient 16) who presented with cough and fever 9 months after undergoing right lung transplantation for an -1-antiprotease deficiency. (a) Anteroposterior chest radiograph shows a nearly completely opaque right hemithorax and a hyperinflated native left lung. (b) Anteroposterior chest radiograph obtained 5 days later, after drainage of pleural fluid, shows homogeneous opacity (arrows) in the middle and lower lobes. The patient died of adenoviral sepsis 3 days later. (c) Immunoperoxidase staining for adenovirus in a specimen obtained at autopsy shows multiple cells with dark-staining nuclei (arrows) that line the bronchial walls; this is diagnostic for adenoviral infection. (Original magnification, x250.)

View larger version (100K): [in this window] [in a new window]   Figure 3b. Infection with adenovirus in a 53-year-old man (patient 16) who presented with cough and fever 9 months after undergoing right lung transplantation for an -1-antiprotease deficiency. (a) Anteroposterior chest radiograph shows a nearly completely opaque right hemithorax and a hyperinflated native left lung. (b) Anteroposterior chest radiograph obtained 5 days later, after drainage of pleural fluid, shows homogeneous opacity (arrows) in the middle and lower lobes. The patient died of adenoviral sepsis 3 days later. (c) Immunoperoxidase staining for adenovirus in a specimen obtained at autopsy shows multiple cells with dark-staining nuclei (arrows) that line the bronchial walls; this is diagnostic for adenoviral infection. (Original magnification, x250.)

View larger version (101K): [in this window] [in a new window]   Figure 3c. Infection with adenovirus in a 53-year-old man (patient 16) who presented with cough and fever 9 months after undergoing right lung transplantation for an -1-antiprotease deficiency. (a) Anteroposterior chest radiograph shows a nearly completely opaque right hemithorax and a hyperinflated native left lung. (b) Anteroposterior chest radiograph obtained 5 days later, after drainage of pleural fluid, shows homogeneous opacity (arrows) in the middle and lower lobes. The patient died of adenoviral sepsis 3 days later. (c) Immunoperoxidase staining for adenovirus in a specimen obtained at autopsy shows multiple cells with dark-staining nuclei (arrows) that line the bronchial walls; this is diagnostic for adenoviral infection. (Original magnification, x250.)

View larger version (97K): [in this window] [in a new window]   Figure 4a. Infection with adenovirus in a 52-year-old woman (patient 17) who presented with cough and fever 1 year after undergoing right lung transplantation for emphysema. (a) Initial posteroanterior chest radiograph (collimated to the right lung) shows a poorly marginated masslike opacity (arrow) in the lower lobe. Note the postsurgical pleural thickening (arrowheads) in the upper right hemithorax. (b) Posteroanterior chest radiograph obtained 3 days later shows homogeneous opacification in the right lung. The patient died of adenoviral sepsis 6 days later.

View larger version (104K): [in this window] [in a new window]   Figure 4b. Infection with adenovirus in a 52-year-old woman (patient 17) who presented with cough and fever 1 year after undergoing right lung transplantation for emphysema. (a) Initial posteroanterior chest radiograph (collimated to the right lung) shows a poorly marginated masslike opacity (arrow) in the lower lobe. Note the postsurgical pleural thickening (arrowheads) in the upper right hemithorax. (b) Posteroanterior chest radiograph obtained 3 days later shows homogeneous opacification in the right lung. The patient died of adenoviral sepsis 6 days later.

View larger version (108K): [in this window] [in a new window]   Figure 5a. Infection with adenovirus in a 21-year-old man (patient 15) who presented with cough and fever 21 months after undergoing bilateral lung transplantation for cystic fibrosis. (a) Initial posteroanterior chest radiograph (close-up of the right lung) shows heterogeneous and peribronchial opacities (arrows) in the lower lobe. (b) Chest CT image (lung window settings, 10-mm collimation) shows poorly defined centrilobular opacities in the right lower lobe (arrows). (c) Posteroanterior chest radiograph obtained 1 month after the image in a confirms the complete resolution of previous findings.

View larger version (96K): [in this window] [in a new window]   Figure 5b. Infection with adenovirus in a 21-year-old man (patient 15) who presented with cough and fever 21 months after undergoing bilateral lung transplantation for cystic fibrosis. (a) Initial posteroanterior chest radiograph (close-up of the right lung) shows heterogeneous and peribronchial opacities (arrows) in the lower lobe. (b) Chest CT image (lung window settings, 10-mm collimation) shows poorly defined centrilobular opacities in the right lower lobe (arrows). (c) Posteroanterior chest radiograph obtained 1 month after the image in a confirms the complete resolution of previous findings.

View larger version (99K): [in this window] [in a new window]   Figure 5c. Infection with adenovirus in a 21-year-old man (patient 15) who presented with cough and fever 21 months after undergoing bilateral lung transplantation for cystic fibrosis. (a) Initial posteroanterior chest radiograph (close-up of the right lung) shows heterogeneous and peribronchial opacities (arrows) in the lower lobe. (b) Chest CT image (lung window settings, 10-mm collimation) shows poorly defined centrilobular opacities in the right lower lobe (arrows). (c) Posteroanterior chest radiograph obtained 1 month after the image in a confirms the complete resolution of previous findings.

View larger version (141K): [in this window] [in a new window]   Figure 6a. Infection with influenza and parainfluenza viruses in a 27-year-old woman (patient 20) who developed symptoms of pneumonia 6 days after undergoing bilateral lung transplantation for cystic fibrosis. (a) Initial anteroposterior chest radiograph shows bilateral homogeneous opacities. (b) Anteroposterior chest radiograph obtained 19 days later shows progressive pulmonary consolidation that is consistent with diffuse lung injury. The patient died 1 week later.

View larger version (147K): [in this window] [in a new window]   Figure 6b. Infection with influenza and parainfluenza viruses in a 27-year-old woman (patient 20) who developed symptoms of pneumonia 6 days after undergoing bilateral lung transplantation for cystic fibrosis. (a) Initial anteroposterior chest radiograph shows bilateral homogeneous opacities. (b) Anteroposterior chest radiograph obtained 19 days later shows progressive pulmonary consolidation that is consistent with diffuse lung injury. The patient died 1 week later.

Infection with parainfluenza and/or respiratory syncytial virus was accompanied by concomitant infection with other pathogens in 43% (six of 14) of the episodes. One patient with an isolated infection caused by parainfluenza had new findings on chest radiographs. Isolated infection with respiratory syncytial virus was not associated with new radiographic findings in any affected patient. Heterogeneous perihilar opacities were noted in one patient with concomitant infections caused by respiratory syncytial virus and cytomegalovirus (Fig 1) and in another patient with concomitant infections caused by respiratory syncytial virus and P boydii (Fig 2).

Adenovirus occurred as the sole pathogen in four (80%) of five affected patients, three of whom had a fulminant, rapidly fatal course. Initial chest radiographs in these three patients showed new abnormalities, which included heterogeneous opacities, focal masslike consolidation, homogeneous opacity, and pleural effusion (Figs 3, 4). Subsequent radiographs in these three patients showed rapid progression to diffuse homogeneous parenchymal opacification. The fourth patient in whom adenovirus was the sole pathogen had a milder clinical course and recovered fully. Initial chest radiographs showed peribronchial opacities (Fig 5) that had resolved on subsequent radiographs. One patient was asymptomatic when infection with adenovirus was diagnosed, and initial radiographs in this patient were unchanged from baseline. However, P aeruginosa was cultured from the bronchoalveolar lavage fluid in this patient, who subsequently died of pseudomonal sepsis.

Influenza virus was isolated from the bronchoalveolar lavage fluid from two patients; parainfluenza virus was cultured from both, and cytomegalovirus was cultured from one. One affected patient developed symptoms of pneumonia 6 days after transplantation and had a rapidly progressive, fatal course (Fig 6).

Eight (40%) of the 20 patients died during the study period. In four patients, death was directly attributed to respiratory viral infection (with adenovirus [n = 3] or parainfluenza and influenza combined [n = 1]). The other deaths were attributed to lymphoproliferative disorder after transplantation (n = 1) or to other infections (n = 3).

Respiratory viruses were the only pathogens isolated in 13 (62%) of the 21 episodes of infection. In these 13 episodes, chest radiographs were unchanged from baseline in seven and were abnormal in six. Of the seven patients with unchanged chest radiographs, one was asymptomatic, three had symptoms of lower respiratory tract infection, and three had symptoms of upper respiratory tract infection; all seven survived. Of the six patients with abnormal chest radiographs, all patients had symptoms of lower respiratory tract infection; four died. This difference in survival was statistically significant (P = .02), as determined by using the Fisher exact test.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Like all patients who undergo transplantation, lung transplant recipients are at risk for serious opportunistic infection because of long-term immunosuppression. They are also particularly susceptible to infection because the allograft is exposed to the environment and because ciliary clearance is impaired, lymphatic drainage is interrupted, and the cough reflex is typically absent in the graft (2). For these reasons, infection is more common in the graft than in the native lung in recipients of single-lung transplants (4,12). In our series, radiographic findings of respiratory viral infection were always confined to the graft, at least initially.

Respiratory viruses, such as adenovirus, respiratory syncytial virus, parainfluenza virus, and influenza virus, uncommonly cause serious infections in the lower respiratory tract in healthy adults. However, in immunocompromised patients, infection occurs with high rates of morbidity and mortality (13–15). The role of these agents in causing infection in lung transplant recipients has been appreciated only recently (6–10).

Twenty (11%) of 176 lung transplant recipients in our series had documented respiratory viral infection during the study period, and four (20%) of these patients died of respiratory viral infection. It is likely that the true incidence of respiratory viral infection in our population was higher than 11% because routine direct fluorescence antibody testing of specimens obtained at bronchoalveolar lavage was not implemented until 1995, which was approximately one-third into the duration of the study. Previously, identification of a virus required culturing, which was slow and difficult. All of our cases were diagnosed after direct fluorescence antibody testing of the bronchoalveolar lavage fluid became routine, and one-third of the cases were diagnosed with findings from direct fluorescence antibody testing alone.

While infection with cytomegalovirus typically occurs in the first few months after transplantation (3,4,11), respiratory viral infection occurred, on average, 9 months after surgery. These data suggest that most respiratory viral infections in lung transplant recipients are community-acquired. However, infection was diagnosed in five patients during their hospitalization for transplantation, which suggests that nosocomial transmission of viruses from infected family members, visitors, or hospital staff also occurs. Because these organisms are thought not to exist as latent infectious agents or as colonizers (with the possible exception of adenovirus), donor-to-recipient transmission is unlikely unless the donor is acutely infected (15).

Parainfluenza and respiratory syncytial viruses were the most common isolates in our study. Affected patients were usually asymptomatic or had very mild clinical symptoms. This experience is in contrast to that of Wendt et al (7) and Holt et al (8), who reported no cases of infection with parainfluenza in asymptomatic lung transplant recipients. The reason for this discrepancy is uncertain but may be due to the increased sensitivity of direct fluorescence antibody testing in the diagnosis of respiratory viral infection compared with that of viral culture alone. Chest radiographs in these patients usually showed either minimal or no new abnormalities. We found that a comparison with baseline radiographs was helpful in the detection of subtle findings such as heterogeneous perihilar opacities or bronchial wall thickening in these patients. More extensive radiographic abnormalities, including diffuse homogeneous consolidation, have been described in immunocompromised patients with respiratory syncytial viral or parainfluenza pneumonia (13,15,16), but these were not seen in our population.

In our series, patients with infections caused by adenovirus were usually acutely ill with symptoms of lower respiratory tract infection. Of the viral pathogens we studied, adenovirus was associated with the highest rate of mortality; three of five affected patients died of adenoviral pneumonia and sepsis. This experience is similar to that of other immunocompromised patients with adenoviral pneumonia (9–11,13,17). We found the initial radiographic findings in these patients to be variable, but they typically were more extensive than those seen in patients with infections caused by respiratory syncytial virus or parainfluenza. Most affected patients developed progressive, homogeneous consolidation in the allograft over days to weeks. Pleural effusion was an uncommon manifestation and was seen in one (20%) of five affected patients.

Influenza was an uncommon pathogen in our series and was never a sole isolate. The clinical and radiographic manifestations of infection caused by influenza were variable. One patient developed severe pneumonia, which progressed to adult respiratory distress syndrome, and died. The second patient presented with only minimal symptoms, had few radiologic abnormalities, and recovered. This spectrum of findings is similar to that described in the general population (16).

Several patients in our series presented with lower respiratory tract symptoms, had respiratory viral infections that were diagnosed at bronchoscopy, and had chest radiographs that were unchanged from baseline radiographs. Only one of these patients underwent CT, which revealed bronchial wall thickening and ground-glass opacities. It has been suggested that thin-section CT can be useful in immunocompromised patients with normal chest radiographs and suspected infections (18). Had CT been performed in our symptomatic patients who had negative radiographs, it is possible that subtle abnormalities could have been detected. However, it is unlikely that such findings would have substantially altered clinical management. This contention is supported by the fact that all patients, symptomatic or not, with radiographs that were unchanged from those at baseline, did well and did not have clinical deterioration, whereas patients with radiographic abnormalities tended to have a more serious clinical course, and some died.

In summary, our experience emphasizes the importance of diagnosing respiratory viral infection in lung transplant recipients. Respiratory viral infection occurs over a wide time span after transplantation and is manifested in a broad spectrum of clinical and radiologic findings. New radiographic abnormalities in patients with isolated respiratory viral infections appear to be a marker for more severe infection and are associated with unfavorable clinical outcomes. Unfortunately, the radiographic findings for respiratory viral infection are nonspecific, and other causes of clinical deterioration—such as edema, adult respiratory distress syndrome, rejection, or infection with bacterial, fungal, or other viral pathogens—must be excluded in these patients.

	Footnotes

 
Author contributions: Guarantors of integrity of entire study, L.D.M., H.P.M., S.M.P.; study concepts and design, H.P.M., S.M.P.; definition of intellectual content, H.P.M., S.M.P.; literature research, S.M.P., L.D.M.; clinical studies, D.N.H., N.G.H., L.D.M., H.P.M.; data acquisition, L.D.M., H.P.M., S.M.P.; data analysis, L.D.M., S.M.P.; statistical analysis, S.M.P.; manuscript preparation, L.D.M., H.P.M., S.M.P.; manuscript editing, D.N.H., H.P.M., S.M.P.; manuscript review, R.D.D., V.F.T.

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