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The Clinical Spectrum of Pulmonary Aspergillosis Chris Kosmidis, David W Denning

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The Clinical Spectrum of Pulmonary Aspergillosis Chris Kosmidis, David W Denning Thorax Online First, published on October 29, 2014 as 10.1136/thoraxjnl-2014-206291 Review Thorax: first published as 10.1136/thoraxjnl-2014-206291 on 29 October 2014. Downloaded from The clinical spectrum of pulmonary aspergillosis Chris Kosmidis, David W Denning The National Aspergillosis ABSTRACT a more indolent fashion, usually affecting patients Centre, University Hospital of The clinical presentation of Aspergillus lung disease is with underlying lung disease, but with no or only South Manchester, The University of Manchester, determined by the interaction between fungus and host. subtle generalised immune compromise. Recently Manchester Academic Health Invasive aspergillosis develops in severely rediscovered is Aspergillus bronchitis in those with Science Centre, Manchester, immunocompromised patients, including those with cystic fibrosis (CF), bronchiectasis especially, as well UK neutropenia, and increasingly in the non-neutropenic as lung transplant recipients and those ventilated in host, including lung transplant recipients, the critically ill intensive therapy units. Finally, an allergic response Correspondence to Dr Chris Kosmidis, patients and patients on steroids. A high index of to inhaled Aspergillus results in allergic broncho- The National Aspergillosis suspicion is required in patients without the classical risk pulmonary aspergillosis (ABPA) and severe asthma Centre, University Hospital factors as early presentation is usually silent and non- with fungal sensitisation. of South Manchester, specific, pyrexia uncommon and timely treatment is Aspergillus fumigatus is the most common The University of Manchester, Manchester Academic Health crucial for survival. Invasive aspergillosis has also been species implicated in all pulmonary syndromes, Science Centre, Manchester diagnosed in normal hosts after massive exposure to although Aspergillus flavus is a more common M23 9LT, UK; fungal spores. Chronic pulmonary aspergillosis affects cause of various forms of allergic rhinosinusitis, [email protected]. patients without obvious immune compromise, but with postoperative aspergillosis and fungal keratitis. uk an underlying lung condition such as COPD or Aspergillus terreus is a common cause of IA in some Received 8 September 2014 sarcoidosis, prior or concurrent TB or non-tuberculous institutions and is amphotericin B resistant. Revised 2 October 2014 mycobacterial disease. Aspergillus bronchitis may be Aspergillus niger is an occasional cause of IA or Accepted 9 October 2014 responsible for persistent respiratory symptoms in Aspergillus bronchitis, but is also a proportionately patients with Aspergillus detected repeatedly in sputum more common coloniser of the respiratory tract. without evidence of parenchymal Aspergillus disease, Several advances have been recently made especially in patients with bronchiectasis and cystic towards understanding the clinical spectrum of fibrosis. Allergic bronchopulmonary aspergillosis affects Aspergillus infection, with improved diagnostic cap- patients with asthma and cystic fibrosis, and is important ability. In this review, we present the clinical syn- to recognise as permanent lung or airways damage may dromes of pulmonary disease caused by Aspergillus accrue if untreated. Changes in the classification of and discuss the most important issues on their Aspergillus allergic lung disease have been proposed management. recently. Cases of extrinsic allergic alveolitis and chronic pulmonary aspergillosis have been observed after INVASIVE ASPERGILLOSIS Aspergillus exposure. Asymptomatic colonisation of the IA implies invasion of lung tissue by hyphae as http://thorax.bmj.com/ respiratory tract needs close monitoring as it can lead to demonstrated on histology. The clinical presenta- clinical disease especially with ongoing tion is relatively rapid, ranging from days to a few immunosuppression. The various syndromes should be weeks. It has been studied extensively in the neu- viewed as a semicontinuous spectrum of disease and tropenic host; however, it has also become increas- one form may evolve into another depending on the ingly recognised in patients without neutropenia. degree of ongoing immunosuppression. Neutropenic host The classic risk factor for IA is neutropenia, and on September 24, 2021 by guest. Protected copyright. INTRODUCTION the likelihood of IA correlates with its duration and Aspergillus is a ubiquitous fungus that causes a depth. Platelets may also be important in defence variety of clinical syndromes. Although exposure to against IA, and thrombocytopenia tends to parallel Aspergillus conidia through inhalation is common, neutropenia. Angioinvasion is involved in the only a minority of those exposed will develop lung pathogenesis in neutropenic hosts and is respon- disease. The clinical features, course and prognosis sible for the higher frequency of dissemination to 1 of Aspergillus infections largely depend on the other organs such as skin, brain or eyes (figure 2). degree of immune compromise of the host, At higher risk for IA are patients undergoing allo- although there is increasing recognition of the geneic HSCT and patients with prolonged neutro- importance of genetics. The interplay between the penia following chemotherapy. IA in patients with 23 pathogen and host immune dysfunction or hyper- neutropenia has been extensively reviewed. activity determines which clinical syndrome is more likely to develop (figure 1). Non-neutropenic host On one end of the spectrum, invasive aspergil- IA occurs in a wide range of non-neutropenic losis (IA) predominantly affects patients with pro- hosts. The most common unifying risk factor is cor- To cite: Kosmidis C, found defects in immune function, such as ticosteroid use, often prior to hospital admission. Denning DW. Thorax Published Online First: haematopoietic stem cell transplant (HSCT) or IA has been recognised in solid organ transplant [please include Day Month solid organ transplant recipients, and patients recipients (particularly lung and heart-lung trans- Year] doi:10.1136/thoraxjnl- undergoing chemotherapy or taking corticosteroids. plant recipients), patients with AIDS, COPD, the 2014-206291 Chronic pulmonary aspergillosis (CPA) presents in critically ill intensive care unit (ICU) patients, Kosmidis C, et al. Thorax 2014;0:1–8. doi:10.1136/thoraxjnl-2014-206291 1 Copyright Article author (or their employer) 2014. Produced by BMJ Publishing Group Ltd (& BTS) under licence. Review Thorax: first published as 10.1136/thoraxjnl-2014-206291 on 29 October 2014. Downloaded from Invasive lung disease tends to occur later after transplant, and may be associated with dissemination to other organs. Prophylaxis consisting of inhaled amphotericin or oral vorico- nazole or itraconazole is employed routinely for lung transplant patients with risk factors for development of IA. The most important factor is pre-transplant or post-transplant colonisa- tion; the latter was an independent factor for mortality in a retrospective study.89Other risk factors are induction with alemtuzumab or thymoglobulin, single lung transplant, cyto- megalovirus infection, hypogammaglobulinaemia and rejection with use of monoclonal antibody.8 In a study of patients with CF undergoing transplantation, a positive intraoperative culture was associated with a fourfold higher risk of IA.10 Figure 1 Interaction of Aspergillus with host. ABPA, allergic bronchopulmonary aspergillosis; IA, invasive aspergillosis. The critically ill IA is being increasingly described in the ICU setting, carries high patients with liver failure and those with chronic granulomatous inhospital mortality and is associated with significant costs.11 The disease. In these hosts, in contrast to patients with neutropenia, majority of patients with IA in the ICU do not have neutropenia fi 1 angioinvasion is not a common feature ( gure 2). Fever is and have non-specific risk factors such as COPD, steroid use, uncommon, and symptoms often absent until late in the course. multiple previous antibiotic regimens, renal or hepatic failure fl The time course usually re ects total net immunosuppression. and diabetes. Many cases follow an episode of sepsis, probably Many cases are relatively indolent and the condition progresses due to so-called ‘immunoparalysis’. The widespread use of ster- over weeks rather than over days. Lack of angioinvasion on oids for COPD exacerbations may contribute to the increased imaging was associated with more protracted clinical course and 4 rate of IA. In a multicentre study from the USA that excluded delayed diagnosis in heart transplant recipients. Consequently, patients with the classical risk factors, 77% of critically ill fi diagnosis is often not suspected because of the non-speci c patients with IA had received high-dose steroids during their hos- symptoms and imaging. As an example, more than half of pitalisation.11 Recently, cases occurring after severe H1N1 infec- patients with liver cirrhosis and IA where diagnosed post- 5 tion and after extracorporeal membrane oxygenation use have mortem. IA is the most common infection-related missed diag- 12 13 6 been reported. In some cases, IA in patients admitted to the nosis at autopsy in ICU patients. ICU has been attributed to Aspergillus contamination of air filters.14 With better supportive care that prolongs survival in Lung transplant recipients critically ill patients, the incidence of IA is likely to increase. Aspergillosis is the most common fungal infection in lung trans- Diagnosis of IA in the
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