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(Chest. 2001;119:169-175.)
© 2001 American College of Chest Physicians

Spectrum of Aspergillus Infection in Lung Transplant Recipients*

Case Series and Review of the Literature

Borna Mehrad, MD; Giuseppe Paciocco, MD; Fernando J. Martinez, MD, FCCP; Tammy Clark Ojo, MD; Mark D. Iannettoni, MD and Joseph P. Lynch, III, MD, FCCP

* From the Department of Medicine (Drs. Mehrad, Paciocco, Martinez, Clark Ojo, and Lynch), Division of Pulmonary and Critical Care Medicine, and Department of Surgery (Dr. Iannettoni), Section of Thoracic Surgery, University of Michigan Medical School, Ann Arbor, MI.

Correspondence to: Joseph P. Lynch III, MD, FCCP, Medical Director, Lung Transplantation Program, University of Michigan Medical Center, 3916 Taubman Center, Box 0360, Ann Arbor, MI 48109-0360


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: (1) To define the incidence and natural history of Aspergillus colonization and infection in lung transplant recipients, and (2) to assess the impact of prophylaxis, surveillance, and therapy on the incidence and outcome of the disease.

Design: Retrospective review of 133 consecutive single or bilateral lung transplantations performed at a single institution, and review of the published literature.

Results: Airway colonization, isolated tracheobronchitis, and invasive pneumonia due to Aspergillus species occurred in 29%, 5%, and 8% of our series, and in 26%, 4%, and 5% of the pooled published data (all series, including ours), respectively. Greater than 50% of all diagnoses were made in the first 6 months after transplantation in both our series and the published literature. Incidence of progression from airway colonization to invasive disease was 1 in 38 in our series and 3 of 97 (3%) in the pooled published data. In patients with isolated tracheobronchitis, all 6 patients in our series and 41 of 50 patients (82%) in all published series, including ours, responded to antifungal therapy and/or surgical debridement. Among patients with invasive pneumonia or disseminated disease, however, 5 of 10 patients in our series and 26 of 64 patients (41%) in the pooled series survived their infection.

Conclusions: The role of antifungal therapy in Aspergillus airway colonization in lung transplant recipients is unclear. Data support a strategy of scheduled screening bronchoscopy followed by aggressive treatment for isolated Aspergillus tracheobronchitis in lung transplant recipients.

Key Words: Aspergillosis • fungal • immunocompromised host • lung diseases • lung transplantation


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The incidence of invasive aspergillosis has increased dramatically over the past 2 decades, in tandem with the increasing number of immunocompromised patients, including organ transplant recipients.1 2 The organism is ubiquitous in the environment and difficult to avoid,3 4 5 the diagnosis is elusive and often delayed,6 7 and the prognosis, even with the best available therapy, is poor.8 Lung transplant recipients are a unique subset of patients susceptible to invasive aspergillosis, in which the transplanted organ is continuously exposed to the environment and its potential pathogens. Aspergillus airway colonization and isolated tracheobronchial infection (without parenchymal disease) are entities distinct from invasive Aspergillus pneumonia, which occur disproportionately in lung transplant recipients and may represent earlier stages of infection. Lung transplantation centers have employed a number of strategies, including prophylaxis, mycologic surveillance, and early empiric treatment, to reduce the incidence and mortality of invasive aspergillosis in lung transplant recipients, but the data supporting these strategies are limited to uncontrolled case series and expert opinions.9

The aim of this article is to describe our experience and summarize the available literature regarding (1) the incidence and natural history of Aspergillus colonization and infection in lung transplant recipients, and (2) the impact of therapy on tracheobronchitis and invasive infection.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
We reviewed the medical records of all patients who underwent lung transplantation at our institution between November 1990 and August 1998, and collected evidence of Aspergillus infections. All patients received an immunosuppressive regimen consisting of corticosteroids (methylprednisolone, 200 mg/d postoperatively, switched to oral prednisone, 0.5 mg/kg/d, tapered to 0.1 mg/kg/d over 6 months); azathioprine, 2 mg/kg/d; and cyclosporine A; as well as prophylactic ganciclovir (in patients receiving organs from cytomegalovirus [CMV]-seropositive donors) and trimethoprim-sulfamethoxazole. Episodes of acute rejection were treated with IV methylprednisolone, 1g/d for 3 days, followed by oral prednisone, 20 mg/d for 1 week, then tapered to prerejection maintenance dose. All patients underwent surveillance bronchoscopy at 3 weeks and 6 weeks, and 3 months, 6 months, and 12 months after transplantation. Additional diagnostic bronchoscopies were performed to investigate clinical, radiographic, or spirometric abnormalities. All bronchoscopy specimens were submitted for fungal stains and cultures in all patients. Fungal smears and cultures from BAL, transbronchial biopsy, and surgical and autopsy specimens were reviewed for the presence of Aspergillus species.

Definitions of Cases and Antifungal Therapy
For the purposes of this study, we defined airway colonization as isolation of Aspergillus species from bronchial specimens in patients without clinical, endoscopic, radiographic, or histologic evidence of invasive disease. Isolated tracheobronchitis was defined as the isolation of Aspergillus species from endobronchial specimens, the presence of one or more endobronchial lesions without an alternative diagnosis, and without clinical, radiographic, or histologic evidence of invasive parenchymal disease. Invasive aspergillosis was defined as radiographic evidence of nodules, infiltrates, cavities, or pleural disease with characteristic histologic evidence of tissue invasion, and isolation of the organism from respiratory specimens, with or without evidence of dissemination to other organs.

Patients who met the criteria for airway colonization with Aspergillus species within a year of transplantation were treated with oral itraconazole, 200 mg bid, for 6 months. Patients with airway colonization beyond the first year were not treated. Patients with evidence of Aspergillus tracheobronchitis received itraconazole, 200 mg bid, for 6 to 12 months, depending on clinical response. Patients who met the criteria for invasive disease were treated with standard (nonlipid) formulation of IV amphotericin B, 1.0 to 1.5 mg/kg/d.

Review of the Literature
We searched the MEDLINE database (National Library of Medicine, Bethesda, MD) to identify all English-language articles published between 1966 and 1999, addressing aspergillosis in lung or heart-lung transplant recipients. Our search terms included "lung transplantation," "infection," "bronchitis," "anastomosis," "Aspergillus," and "aspergillosis." We reviewed all articles (including case reports, case series, and review articles) that included a reference to Aspergillus infection in lung or heart-lung transplant recipients. Studies that did not report the total number of transplantations performed were not used in the calculation of cumulative incidence, but were included in calculation of cumulative outcomes.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Incidence of Isolation of Aspergillus Species
Between November 1990 and August 1998, 130 patients (69 men) underwent 133 lung transplantations at our institution (111 single and 22 bilateral lung transplantations). The median age at the time of transplantation was 51 years (range, 18 to 63 years). Three patients underwent retransplantation for acute or chronic graft failure. Aspergillus species were isolated from 53 of our patients (40%; Table 1 ). The most common isolated species was Aspergillus fumigatus (58%), followed by Aspergillus niger (28%), Aspergillus flavus (11%), and Aspergillus versicolor (2%; one isolate). We found no correlation between the isolation of Aspergillus species and patients’ age, gender, smoking history, diagnosis leading to lung transplantation, episodes of acute rejection, or CMV disease.


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  		Table 1.. Incidence of Aspergillus Isolation in Lung Transplantation*

 
Review of all published series showed a cumulative incidence of isolation of Aspergillus from respiratory samples in 20% of lung transplant recipients (Table 1) .10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 Since this figure includes data from series in which routine surveillance bronchoscopies were not performed, it likely underestimates the number of asymptomatic airway colonizations and disproportionately represents symptomatic infections. Analysis of data from centers that performed surveillance bronchoscopies showed an airway colonization rate of 26%, which is consistent with our series.

Aspergillus Airway Colonization
Among the 53 patients from whom Aspergillus was isolated, 38 patients (72%) met the definition of airway colonization. In patients with Aspergillus airway colonization, 23 patients (61%) were identified within 1 year of transplantation. This group was treated with 6 months of oral itraconazole, 200 mg bid, which resulted in eradication of the organism in all; none developed invasive disease. Another 15 patients, who developed Aspergillus colonization > 1 year after transplantation, were monitored closely but were not treated. In this group, one patient developed invasive Aspergillus pneumonia that subsequently responded to therapy with systemic amphotericin B.

Most published series did not report on the timing of isolation of the organism in patients with airway colonization, but in the largest published series of patients in this category, 45% of isolates were found within 6 months of transplantation.11 Patients with cystic fibrosis, whose airways were colonized with Aspergillus species before transplantation, were not predisposed to development of posttransplantation colonization or infection with Aspergillus.14 20 22 Patients with Aspergillus airway colonization were uniformly asymptomatic in both our series and in the published literature,27 although case reports have identified three patients with recurrence of preexisting allergic bronchopulmonary aspergillosis after lung transplantation.38 39

Isolated Aspergillus Tracheobronchitis
Isolated Aspergillus tracheobronchitis was found in six patients in our series. All patients were asymptomatic, and isolated Aspergillus tracheobronchitis was diagnosed during surveillance bronchoscopy; all patients responded to therapy, with eradication of the organism and healing of endobronchial lesions. Isolated Aspergillus tracheobronchitis was diagnosed in all patients in the first 6 months after transplantation. All lesions occurred in the transplanted (and not native) lung, and invariably involved the anastomosis line. The bronchoscopic appearance of the airway lesions consisted of ulcerations that were extensive, with pseudomembrane formation in two patients and a black eschar in another patient. All six patients were treated with oral itraconazole, and two patients required additional surgical debridement via rigid bronchoscopy. None progressed to develop invasive pneumonia.

The incidence of isolated tracheobronchitis was highest in the first year after transplantation in both our series and the published literature (Fig 1 , top, A).11 12 13 16 17 18 19 21 22 23 25 26 29 30 31 32 33 34 35 36 37 40 41 42 43 In the published series, presentation of isolated tracheobronchitis has been variously reported as asymptomatic disease identified on surveillance bronchoscopy,25 36 symptomatic infection with fever and cough,27 wheezing due to airway compromise,17 and massive hemoptysis.40 41 The endoscopic appearance of the lesion in the literature also encompassed a wide spectrum, including mild bronchitis, endobronchial ulcerations with or without pseudomembranes, airway stenosis, and suture line dehiscence.10 17 36



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  		Figure 1.. Incidence of Aspergillus tracheobronchitis (top, A) and pneumonia or disseminated infection (bottom, B) after lung transplantation, from pooled data from our series and other studies.11 12 13 16 17 18 19 21 22 23 25 26 29 30 31 32 33 34 35 36 37 40 41 42 43

 
Invasive Aspergillus Pneumonia and Disseminated Disease
Invasive aspergillosis occurred in 10 patients in our series, 8 of whom presented within the first year after transplantation (Table 2 ). All patients presented with pneumonia. One patient had received a previous diagnosis of Aspergillus airway colonization > 1 year after lung transplantation. All patients presented with pulmonary infiltrates, and three patients had evidence of cavitation. In all but one case, infection involved the transplanted lung. The remaining patient received a diagnosis after undergoing an open lung biopsy for a cavitary pneumonia in the native lung. All patients were treated with systemic amphotericin B, and five patients survived the infection.


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  		Table 2.. Characteristics of Patients With Invasive Aspergillosis in this Series*

 
In both our series and the published literature, the majority of cases of invasive aspergillosis occurred in the first year after transplantation (Fig 1 , bottom, B), although cases were reported as long as 3 years after transplantation.22 23 The clinical features of invasive aspergillosis in lung transplant recipients were similar to that in other hosts: of the 79 patients with invasive aspergillosis after lung transplantation reported in the literature, 64 patients (81%) presented with pneumonia, 13 patients (16%) presented with disseminated disease, and 2 patients (3%) presented with wound infection (data compiled from our series and others10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 ). In our series, all of our 10 patients presented with pneumonia, and 5 patients survived. In series that reported mortality statistics (including ours), 26 of 64 patients (41%) responded to therapy and survived.10 11 12 13 17 19 20 21 23 24 25 26 27 28 29 30 31 35 36

Therapy of Colonization and Isolated Tracheobronchitis
The role of antifungal therapy for Aspergillus airway colonization in lung transplant recipients is unclear and unproven. In our series, 23 patients received a diagnosis of Aspergillus colonization within a year after transplantation; all were treated with 6 months of itraconazole, and none developed invasive disease. Another 15 patients, who developed Aspergillus colonization > 1 year after transplantation, were monitored closely but were not treated. In this group, one patient developed invasive Aspergillus pneumonia that subsequently responded to therapy. In some series, the majority of patients with colonization were treated,19 20 27 while others11 28 limited treatment to patients with early isolation of Aspergillus (Table 3 ). Treatment regimens also varied in the literature, and included oral itraconazole, inhaled amphotericin B, and systemic amphotericin B.11 19 27 28 33


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  		Table 3.. Therapy and Outcome of Aspergillus Airway Colonization*

 
Ten published series reported on the incidence of progression from previously recognized Aspergillus airway colonization to infection.11 19 20 22 27 28 32 33 In pooling the data from these series and ours, we found that 3 of 97 patients progressed from colonization to infection: 2 patients developed invasive pneumonia (1 each in our series and the study by Cahill et al11 ), and another patient developed isolated tracheobronchial infection.27 None of the patients who progressed from colonization to infection had received antifungal therapy.

In our series, isolated Aspergillus tracheobronchitis was found in six patients during surveillance bronchoscopy and was successfully treated in all patients with oral itraconazole; two patients required additional surgical debridement via rigid bronchoscopy. Other centers have used standard preparation of amphotericin B,10 28 34 liposomal amphotericin B,17 40 or itraconazole27 28 33 35 36 as mainstays of therapy (Table 4 ). Some centers have used terbinafine43 and aerosolized amphotericin B22 27 40 as adjunctive treatment. Additional surgical intervention was performed in two series.16 17 With appropriate treatment, isolated Aspergillus tracheobronchitis had a favorable outcome; in pooled data from all series that reported on outcome of therapy (including ours), the infection was successfully treated in 41 of 50 patients (82%).10 22 25 27 28 32 33 34 35 36 37 40 41 42 43 Data on outcome were not provided in three patients.16 17 18


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  		Table 4.. Therapy and Outcome of Isolated Aspergillus Tracheobronchitis*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Invasive aspergillosis is a potentially fatal complication of immunosuppression. While the disease has been studied in other immunocompromised hosts, its optimal management in lung transplant recipients has not been systematically investigated. Given that the number of patients who develop invasive aspergillosis in any given lung transplantation center is limited, randomized studies to evaluate the optimal diagnostic or preventative approach are difficult to perform. We therefore summarized the published data pertaining to Aspergillus infection in lung transplant recipients.

Given the high mortality rate of established invasive aspergillosis, evaluation of strategies aimed at prevention of infection, early diagnosis, and early treatment are of particular interest. One approach aimed at the early diagnosis of invasive aspergillosis is identification of patients at highest risk for the infection. The association of CMV infection with invasive aspergillosis, noted by two series,18 28 has been attributed to the immunomodulatory effects of CMV infection. Conversely, several series have convincingly shown that pretransplantation colonization with Aspergillus, a frequent finding in patients with cystic fibrosis, is not a risk factor for development of Aspergillus pneumonia after transplantation.14 20 22

Another approach to the early diagnosis of invasive aspergillosis is regular surveillance mycologic cultures during bronchoscopy, aimed at early recognition of patients with Aspergillus airway colonization or Aspergillus tracheobronchitis. This strategy assumes that a subset of patients with these conditions progress to develop invasive aspergillosis. Surveillance bronchoscopy with fungal cultures has been performed in 11 series, including ours.11 19 20 22 23 25 27 28 32 33 While these series detected and treated a larger number of patients with Aspergillus airway colonization, the incidence and mortality of invasive pneumonia or disseminated disease in their patients was similar to that in series that did not perform surveillance fungal cultures. As such, the optimal management of patients with Aspergillus airway colonization is unclear, since only a small proportion (3%) progressed to develop invasive disease, and the long-term outcome of untreated patients with Aspergillus airway colonization is unknown. In contrast, the available data support an aggressive approach to the diagnosis and treatment of Aspergillus tracheobronchitis in lung transplant recipients, since this condition may progress to invasive pneumonia if management is delayed, and it is effectively treated with systemic amphotericin B or oral itraconazole.

Several studies have reported on the use of antifungal prophylaxis in lung transplant recipients. Administration of aerosolized amphotericin B has been shown to be safe and feasible.44 45 46 47 Three observational studies have reported a reduced incidence of invasive aspergillosis in lung transplant recipients who were treated with prophylactic postoperative aerosolized amphotericin, as compared to historical control subjects.15 48 49 Other investigators have reported using aerosolized25 or low-dose systemic16 amphotericin, without clear benefit. One study has demonstrated that (despite the potential for drug interactions) itraconazole, 400 mg/d, is bioavailable in lung transplant recipients,50 but its impact as a prophylactic measure has not been addressed. Thus, the data addressing prophylactic therapy against Aspergillus infection in lung transplant recipients are limited by their uncontrolled design and comparison to historical control subjects. In addition to possible differences in baseline characteristics between the treatment and control groups in these studies, the possible occurrence of Aspergillus infections in clusters related to environmental exposure weakens their conclusions. As such, the value of routine antifungal prophylaxis in lung transplant recipients awaits further studies.

Several considerations limit the conclusions that can be drawn from the present study. The definitions of Aspergillus colonization and tracheobronchitis may have differed among some of the reviewed series. In addition, the frequency of Aspergillus airway colonization and tracheobronchitis were likely underestimated in series that did not perform surveillance mycologic cultures. The diagnosis of invasive aspergillosis was also likely underestimated, since a variable proportion of fatalities in different series did not undergo necropsy. Finally, another limitation of interpretation of cumulative published data is bias in favor of publication of successful treatments and lower mortality rates.

Given the paucity of prospective, randomized, controlled trials in this area, however, these data define the spectrum of Aspergillus infection in lung transplant recipients, and support an aggressive approach aimed at early diagnosis and treatment of isolated Aspergillus tracheobronchitis. Future trials are warranted to address the optimal management of Aspergillus airway colonization, the value of antifungal prophylaxis in lung transplant recipients, and the relative benefit of itraconazole and amphotericin B as therapy in patients with isolated tracheobronchitis.


   Footnotes
 
Abbreviation: CMV = cytomegalovirus

Supported in part by National Institutes of Health grants 1P50HL46487 and 1K08HL04220–01.

Received for publication December 28, 1999. Accepted for publication August 1, 2000.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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Invasive fungal infections: a review of epidemiology and management options.
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 Clin. Microbiol. Rev.Home page
N. Singh and D. L. Paterson
Aspergillus Infections in Transplant Recipients
Clin. Microbiol. Rev., January 1, 2005; 18(1): 44 - 69.
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R. M. Kotloff, V. N. Ahya, and S. W. Crawford
Pulmonary Complications of Solid Organ and Hematopoietic Stem Cell Transplantation
Am. J. Respir. Crit. Care Med., July 1, 2004; 170(1): 22 - 48.
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 J Med MicrobiolHome page
E. Dannaoui, J. Meletiadis, A.-M. Tortorano, F. Symoens, N. Nolard, M.-A. Viviani, M.-A. Piens, B. Lebeau, P. E. Verweij, and R. Grillot
Susceptibility testing of sequential isolates of Aspergillus fumigatus recovered from treated patients
J. Med. Microbiol., February 1, 2004; 53(2): 129 - 134.
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 ChestHome page
P. Lee, O. A. Minai, A. C. Mehta, M. M. DeCamp, and S. Murthy
Pulmonary Nodules in Lung Transplant Recipients: Etiology and Outcome
Chest, January 1, 2004; 125(1): 165 - 172.
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 Am. J. Roentgenol.Home page
E. Konen, G. L. Weisbrod, S. Pakhale, T. Chung, N. S. Paul, and M. A. Hutcheon
Fibrosis of the Upper Lobes: A Newly Identified Late-Onset Complication After Lung Transplantation?
Am. J. Roentgenol., December 1, 2003; 181(6): 1539 - 1543.
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 ChestHome page
M. Helmi, R. B. Love, D. Welter, R. D. Cornwell, and K. C. Meyer
Aspergillus Infection in Lung Transplant Recipients With Cystic Fibrosis: Risk Factors and Outcomes Comparison to Other Types of Transplant Recipients
Chest, March 1, 2003; 123(3): 800 - 808.
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 ChestHome page
D. R. Nunley, A. A. Gal, J. D. Vega, C. Perlino, P. Smith, and E. C. Lawrence
Saprophytic Fungal Infections and Complications Involving the Bronchial Anastomosis Following Human Lung Transplantation
Chest, October 1, 2002; 122(4): 1185 - 1191.
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