Review of influenza-associated pulmonary aspergillosis in ICU patients and proposal for a case definition: an expert opinion

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Abstract

Purpose

Invasive pulmonary aspergillosis is increasingly reported in patients with influenza admitted to the intensive care unit (ICU). Classification of patients with influenza-associated pulmonary aspergillosis (IAPA) using the current definitions for invasive fungal diseases has proven difficult, and our aim was to develop case definitions for IAPA that can facilitate clinical studies.

Methods

A group of 29 international experts reviewed current insights into the epidemiology, diagnosis and management of IAPA and proposed a case definition of IAPA through a process of informal consensus.

Results

Since IAPA may develop in a wide range of hosts, an entry criterion was proposed and not host factors. The entry criterion was defined as a patient requiring ICU admission for respiratory distress with a positive influenza test temporally related to ICU admission. In addition, proven IAPA required histological evidence of invasive septate hyphae and mycological evidence for Aspergillus. Probable IAPA required the detection of galactomannan or positive Aspergillus culture in bronchoalveolar lavage (BAL) or serum with pulmonary infiltrates or a positive culture in upper respiratory samples with bronchoscopic evidence for tracheobronchitis or cavitating pulmonary infiltrates of recent onset. The IAPA case definitions may be useful to classify patients with COVID-19-associated pulmonary aspergillosis (CAPA), while awaiting further studies that provide more insight into the interaction between Aspergillus and the SARS-CoV-2-infected lung.

Conclusion

A consensus case definition of IAPA is proposed, which will facilitate research into the epidemiology, diagnosis and management of this emerging acute and severe Aspergillus disease, and may be of use to study CAPA.

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Most cited references 42

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Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China

Chaolin Huang, Yeming Wang, Xingwang Li … (2020)

Summary Background A recent cluster of pneumonia cases in Wuhan, China, was caused by a novel betacoronavirus, the 2019 novel coronavirus (2019-nCoV). We report the epidemiological, clinical, laboratory, and radiological characteristics and treatment and clinical outcomes of these patients. Methods All patients with suspected 2019-nCoV were admitted to a designated hospital in Wuhan. We prospectively collected and analysed data on patients with laboratory-confirmed 2019-nCoV infection by real-time RT-PCR and next-generation sequencing. Data were obtained with standardised data collection forms shared by WHO and the International Severe Acute Respiratory and Emerging Infection Consortium from electronic medical records. Researchers also directly communicated with patients or their families to ascertain epidemiological and symptom data. Outcomes were also compared between patients who had been admitted to the intensive care unit (ICU) and those who had not. Findings By Jan 2, 2020, 41 admitted hospital patients had been identified as having laboratory-confirmed 2019-nCoV infection. Most of the infected patients were men (30 [73%] of 41); less than half had underlying diseases (13 [32%]), including diabetes (eight [20%]), hypertension (six [15%]), and cardiovascular disease (six [15%]). Median age was 49·0 years (IQR 41·0–58·0). 27 (66%) of 41 patients had been exposed to Huanan seafood market. One family cluster was found. Common symptoms at onset of illness were fever (40 [98%] of 41 patients), cough (31 [76%]), and myalgia or fatigue (18 [44%]); less common symptoms were sputum production (11 [28%] of 39), headache (three [8%] of 38), haemoptysis (two [5%] of 39), and diarrhoea (one [3%] of 38). Dyspnoea developed in 22 (55%) of 40 patients (median time from illness onset to dyspnoea 8·0 days [IQR 5·0–13·0]). 26 (63%) of 41 patients had lymphopenia. All 41 patients had pneumonia with abnormal findings on chest CT. Complications included acute respiratory distress syndrome (12 [29%]), RNAaemia (six [15%]), acute cardiac injury (five [12%]) and secondary infection (four [10%]). 13 (32%) patients were admitted to an ICU and six (15%) died. Compared with non-ICU patients, ICU patients had higher plasma levels of IL2, IL7, IL10, GSCF, IP10, MCP1, MIP1A, and TNFα. Interpretation The 2019-nCoV infection caused clusters of severe respiratory illness similar to severe acute respiratory syndrome coronavirus and was associated with ICU admission and high mortality. Major gaps in our knowledge of the origin, epidemiology, duration of human transmission, and clinical spectrum of disease need fulfilment by future studies. Funding Ministry of Science and Technology, Chinese Academy of Medical Sciences, National Natural Science Foundation of China, and Beijing Municipal Science and Technology Commission.

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Clinical and virological data of the first cases of COVID-19 in Europe: a case series

François-Xavier Lescure, Lila Bouadma, Duc Nguyên … (2020)

Summary Background On Dec 31, 2019, China reported a cluster of cases of pneumonia in people at Wuhan, Hubei Province. The responsible pathogen is a novel coronavirus, named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). We report the relevant features of the first cases in Europe of confirmed infection, named coronavirus disease 2019 (COVID-19), with the first patient diagnosed with the disease on Jan 24, 2020. Methods In this case series, we followed five patients admitted to Bichat-Claude Bernard University Hospital (Paris, France) and Pellegrin University Hospital (Bordeaux, France) and diagnosed with COVID-19 by semi-quantitative RT-PCR on nasopharyngeal swabs. We assessed patterns of clinical disease and viral load from different samples (nasopharyngeal and blood, urine, and stool samples), which were obtained once daily for 3 days from hospital admission, and once every 2 or 3 days until patient discharge. All samples were refrigerated and shipped to laboratories in the National Reference Center for Respiratory Viruses (The Institut Pasteur, Paris, and Hospices Civils de Lyon, Lyon, France), where RNA extraction, real-time RT-PCR, and virus isolation and titration procedures were done. Findings The patients were three men (aged 31 years, 48 years, and 80 years) and two women (aged 30 years and 46 years), all of Chinese origin, who had travelled to France from China around mid-January, 2020. Three different clinical evolutions are described: (1) two paucisymptomatic women diagnosed within a day of exhibiting symptoms, with high nasopharyngeal titres of SARS-CoV-2 within the first 24 h of the illness onset (5·2 and 7·4 log10 copies per 1000 cells, respectively) and viral RNA detection in stools; (2) a two-step disease progression in two young men, with a secondary worsening around 10 days after disease onset despite a decreasing viral load in nasopharyngeal samples; and (3) an 80-year-old man with a rapid evolution towards multiple organ failure and a persistent high viral load in lower and upper respiratory tract with systemic virus dissemination and virus detection in plasma. The 80-year-old patient died on day 14 of illness (Feb 14, 2020); all other patients had recovered and been discharged by Feb 19, 2020. Interpretation We illustrated three different clinical and biological types of evolution in five patients infected with SARS-CoV-2 with detailed and comprehensive viral sampling strategy. We believe that these findings will contribute to a better understanding of the natural history of the disease and will contribute to advances in the implementation of more efficient infection control strategies. Funding REACTing (Research & Action Emerging Infectious Diseases).

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Avian flu: influenza virus receptors in the human airway.

Kyoko Shinya, Masahito Ebina, Shinya Yamada … (2006)

Although more than 100 people have been infected by H5N1 influenza A viruses, human-to-human transmission is rare. What are the molecular barriers limiting human-to-human transmission? Here we demonstrate an anatomical difference in the distribution in the human airway of the different binding molecules preferred by the avian and human influenza viruses. The respective molecules are sialic acid linked to galactose by an alpha-2,3 linkage (SAalpha2,3Gal) and by an alpha-2,6 linkage (SAalpha2,6Gal). Our findings may provide a rational explanation for why H5N1 viruses at present rarely infect and spread between humans although they can replicate efficiently in the lungs.

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Author and article information

Contributors

Paul E. Verweij:

ORCID: http://orcid.org/0000-0002-8600-9860

paul.verweij@radboudumc.nl

Journal

Journal ID (nlm-ta): Intensive Care Med

Journal ID (iso-abbrev): Intensive Care Med

Title: Intensive Care Medicine

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 0342-4642

ISSN (Electronic): 1432-1238

Publication date (Electronic): 22 June 2020

Publication date PMC-release: 22 June 2020

Pages: 1-12

Affiliations

[1 ]GRID grid.10417.33, ISNI 0000 0004 0444 9382, Department of Medical Microbiology, , Radboud University Medical Center, ; PO box 9101, 6500 HB Nijmegen, The Netherlands

[2 ]GRID grid.413327.0, ISNI 0000 0004 0444 9008, Centre of Expertise in Mycology Radboudumc/CWZ, , Radboudumc Center for Infectious Diseases (RCI), ; Nijmegen, The Netherlands

[3 ]GRID grid.5645.2, ISNI 000000040459992X, Department of Internal Medicine and Infectious Diseases, , Erasmus MC, University Medical Center, ; Rotterdam, The Netherlands

[4 ]GRID grid.10417.33, ISNI 0000 0004 0444 9382, Department of Pharmacy and Radboud Institute of Health Sciences, , Radboud University Medical Centre, ; Nijmegen, The Netherlands

[5 ]GRID grid.413328.f, ISNI 0000 0001 2300 6614, Medical Intensive Care Unit, , Saint-Louis Hospital, APHP, ; Paris, France

[6 ]Clinica Malattie Infettive, Ospedale Policlinico San Martino - IRCCS, Genoa, Italy

[7 ]GRID grid.5606.5, ISNI 0000 0001 2151 3065, Department of Health Sciences, DISSAL, , University of Genoa, ; Genoa, Italy

[8 ]GRID grid.5342.0, ISNI 0000 0001 2069 7798, Department of Internal Medicine and Paediatrics, Faculty of Medicine and Health Sciences, , Ghent University, ; Ghent, Belgium

[9 ]GRID grid.1003.2, ISNI 0000 0000 9320 7537, Burns, Trauma, and Critical Care Research Centre, Centre for Clinical Research, Faculty of Medicine, , The University of Queensland, ; Brisbane, QLD Australia

[10 ]GRID grid.8515.9, ISNI 0000 0001 0423 4662, Infectious Diseases Service, Department of Medicine, , Lausanne University Hospital and University of Lausanne, ; 1011 Lausanne, Switzerland

[11 ]GRID grid.21925.3d, ISNI 0000 0004 1936 9000, Division of Infectious Diseases, , University of Pittsburgh, ; Pittsburgh, PA USA

[12 ]GRID grid.413935.9, ISNI 0000 0004 0420 3665, Infectious Diseases Section, , VA Pittsburgh Healthcare System, ; Pittsburgh, USA

[13 ]GRID grid.6190.e, ISNI 0000 0000 8580 3777, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), , University of Cologne, ; Cologne, Germany

[14 ]GRID grid.6190.e, ISNI 0000 0000 8580 3777, Department of Internal Medicine, ECMM Center of Excellence for Medical Mycology, German Centre for Infection Research, Partner Site Bonn-Cologne (DZIF), , University of Cologne, ; Cologne, Germany

[15 ]GRID grid.6190.e, ISNI 0000 0000 8580 3777, Clinical Trials Centre Cologne (ZKS Köln), , University of Cologne, ; Cologne, Germany

[16 ]GRID grid.416738.f, ISNI 0000 0001 2163 0069, Centers for Disease Control and Prevention, ; Atlanta, GA 30329 USA

[17 ]GRID grid.410566.0, ISNI 0000 0004 0626 3303, Department of Critical Care Medicine, , Ghent University Hospital, ; Ghent, Belgium

[18 ]GRID grid.5606.5, ISNI 0000 0001 2151 3065, Department of Health Sciences, , University of Genoa, ; Genoa, Italy

[19 ]GRID grid.10417.33, ISNI 0000 0004 0444 9382, Department of Medicine, , Radboud University Medical Center, ; Nijmegen, The Netherlands

[20 ]GRID grid.5596.f, ISNI 0000 0001 0668 7884, Department of Microbiology, Immunology and Transplantation, , KU Leuven, ; Leuven, Belgium

[21 ]GRID grid.410569.f, ISNI 0000 0004 0626 3338, Department of Laboratory Medicine and National Reference Centre for Mycosis, , University Hospitals Leuven, ; Leuven, Belgium

[22 ]GRID grid.5361.1, ISNI 0000 0000 8853 2677, Division of Hygiene and Medical Microbiology, , Medical University of Innsbruck, ; Innsbruck, Austria

[23 ]GRID grid.6292.f, ISNI 0000 0004 1757 1758, Infectious Diseases Hospital, S’Orsola-Malpighi, Department of Medical and Surgical Sciences, , University of Bologna, ; Bologna, Italy

[24 ]GRID grid.256105.5, ISNI 0000 0004 1937 1063, Department of Emergency and Critical Care Medicine, Fu Jen Catholic University Hospital, , Fu Jen Catholic University, ; New Taipei, Taiwan

[25 ]GRID grid.256105.5, ISNI 0000 0004 1937 1063, School of Medicine, College of Medicine, , Fu Jen Catholic University, ; New Taipei, Taiwan

[26 ]GRID grid.412134.1, ISNI 0000 0004 0593 9113, Necker - Pasteur Center for Infectious Diseases and Tropical Medicine, Necker-Enfants Malades Hospital, AP-HP, , Paris University, ; Paris, France

[27 ]GRID grid.428999.7, ISNI 0000 0001 2353 6535, Molecular Mycology Unit National Reference Center for Invasive Mycoses and Antifungals, CNRS, UMR 2000, , Institut Pasteur, ; Paris, France

[28 ]GRID grid.410569.f, ISNI 0000 0004 0626 3338, Department of Hematology, , University Hospitals Leuven, ; Leuven, Belgium

[29 ]GRID grid.416409.e, ISNI 0000 0004 0617 8280, Department of Intensive Care Medicine, Multidisciplinary Intensive Care Research Organization (MICRO), , St. James’s Hospital, ; Dublin, Ireland

[30 ]GRID grid.5841.8, ISNI 0000 0004 1937 0247, Hospital Clinic, IDIBAPS, , Universidad de Barcelona, Ciberes, ; Barcelona, Spain

[31 ]GRID grid.267309.9, ISNI 0000 0001 0629 5880, Department of Medicine, Division of Infectious Diseases, , University of Texas Health Science Center at San Antonio, ; San Antonio, TX USA

[32 ]South Texas Veterans Health Care Center, San Antonio, TX USA

[33 ]GRID grid.416409.e, ISNI 0000 0004 0617 8280, Department of Clinical Microbiology, Trinity College Dublin, , St. James’s Hospital, ; Dublin, Ireland

[34 ]GRID grid.10417.33, ISNI 0000 0004 0444 9382, Department of Intensive Care Medicine, , Radboud University Medical Center, ; Nijmegen, The Netherlands

[35 ]GRID grid.10417.33, ISNI 0000 0004 0444 9382, Scientific Center for Quality of Healthcare (IQ Healthcare), Radboud Institute for Health Sciences, , Radboud University Medical Center, ; Nijmegen, The Netherlands

[36 ]GRID grid.410569.f, ISNI 0000 0004 0626 3338, Pharmacy Department, , University Hospitals Leuven, ; Leuven, Belgium

[37 ]GRID grid.410569.f, ISNI 0000 0004 0626 3338, Department of General Internal Medicine, Medical Intensive Care Unit, , University Hospitals Leuven, ; Leuven, Belgium

Author information

Paul E. Verweij http://orcid.org/0000-0002-8600-9860

Bart J. A. Rijnders http://orcid.org/0000-0003-3343-9610

Roger J. M. Brüggemann http://orcid.org/0000-0002-7618-725X

Elie Azoulay http://orcid.org/0000-0002-8162-1508

Matteo Bassetti http://orcid.org/0000-0002-0145-9740

Stijn Blot http://orcid.org/0000-0003-2145-0345

Thierry Calandra http://orcid.org/0000-0003-3051-1285

Cornelius J. Clancy http://orcid.org/0000-0003-1505-4119

Oliver A. Cornely http://orcid.org/0000-0001-9599-3137

Tom Chiller http://orcid.org/0000-0002-2251-8033

Pieter Depuydt http://orcid.org/0000-0001-5164-5376

Daniele Roberto Giacobbe http://orcid.org/0000-0003-2385-1759

Nico A. F. Janssen http://orcid.org/0000-0002-9629-8627

Bart-Jan Kullberg http://orcid.org/0000-0002-6813-8167

Katrien Lagrou http://orcid.org/0000-0001-8668-1350

Cornelia Lass-Flörl http://orcid.org/0000-0002-2946-7785

Russell E. Lewis http://orcid.org/0000-0002-2002-4339

Peter Wei-Lun Liu http://orcid.org/0000-0001-8593-8492

Olivier Lortholary http://orcid.org/0000-0002-8325-8060

Johan Maertens http://orcid.org/0000-0003-4257-5980

Ignacio Martin-Loeches http://orcid.org/0000-0002-5834-4063

M. Hong Nguyen http://orcid.org/0000-0002-8564-7529

Thomas F. Patterson http://orcid.org/0000-0002-9513-7127

Thomas R. Rogers http://orcid.org/0000-0003-4336-7729

Jeroen A. Schouten http://orcid.org/0000-0001-9118-4420

Isabel Spriet http://orcid.org/0000-0001-6342-0676

Lore Vanderbeke http://orcid.org/0000-0002-3364-1213

Joost Wauters http://orcid.org/0000-0002-5983-3897

Frank L. van de Veerdonk http://orcid.org/0000-0002-1121-4894

Article

Publisher ID: 6091

DOI: 10.1007/s00134-020-06091-6

PMC ID: 7306567

PubMed ID: 32572532

SO-VID: de59557b-6b05-4a59-a5f6-795fe150d527

License:

Open AccessThis article is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License, which permits any non-commercial use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc/4.0/.

History

Date received : 28 February 2020

Date accepted : 7 May 2020

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100014476, Pfizer Pharmaceuticals;

Review of influenza-associated pulmonary aspergillosis in ICU patients and proposal for a case definition: an expert opinion

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Abstract

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Novel Coronavirus Disease COVID-19

Most cited references 42

Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China

Clinical and virological data of the first cases of COVID-19 in Europe: a case series

Avian flu: influenza virus receptors in the human airway.

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