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Factors for severe outcomes following SARS-CoV-2 infection in people with cystic fibrosis in Europe

Andreas Jung, Annalisa Orenti, Fiona Dunlevy, Elina Aleksejeva, Egil Bakkeheim, Vladimir Bobrovnichy, Siobhán B. Carr, Carla Colombo, Harriet Corvol, Rebecca Cosgriff, Géraldine Daneau, Deniz Dogru, Pavel Drevinek, Andrea Dugac Vukic, Isabelle Fajac, Alice Fox, Stojka Fustik, Vincent Gulmans, Satenik Harutyunyan, Elpis Hatziagorou, Irena Kasmi, Hana Kayserová, Elena Kondratyeva, Uroš Krivec, Halyna Makukh, Kestutis Malakauskas, Edward F. McKone, Meir Mei-Zahav, Isabelle de Monestrol, Hanne Vebert Olesen, Rita Padoan, Tsitsino Parulava, Maria Dolores Pastor-Vivero, Luísa Pereira, Guergana Petrova, Andreas Pfleger, Liviu Pop, Jacqui G. van Rens, Milan Rodić, Marc Schlesser, Valérie Storms, Oxana Turcu, Lukasz Woźniacki, Panayiotis Yiallouros, Anna Zolin, Damian G. Downey, Lutz Naehrlich
ERJ Open Research 2021; DOI: 10.1183/23120541.00411-2021
Andreas Jung
1Paediatric Pulmonology, University Children's Hospital Zurich, Zurich, Switzerland
48Contributed equally as first author
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  • For correspondence: Andreas.Jung@kispi.uzh.ch
Annalisa Orenti
2Department of Clinical Sciences and Community Health, Laboratory of Medical Statistics, Epidemiology and Biometry G. A. Maccacaro, University of Milan, Milan, Italy
48Contributed equally as first author
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Fiona Dunlevy
3European Cystic Fibrosis Society, Karup, Denmark
48Contributed equally as first author
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Elina Aleksejeva
4Department of Pneumology, Children's Clinical University Hospital, Rīga Stradinš University, Riga, Latvia
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Egil Bakkeheim
5Dep. of Paediatrics, Norwegian Cystic Fibrosis Registry, Oslo University Hospital, Oslo, Norway
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Vladimir Bobrovnichy
6Belarusian Republic Children's Center of Pulmonology and Cystic Fibrosis, Pulmonary Department, 3rd City Children's Clinical Hospital, Minsk, Belarus
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Siobhán B. Carr
7Department of Respiratory Paediatrics, Royal Brompton Hospital; NHLI, Imperial College, London, UK
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Carla Colombo
8Department of Pathophysiology and Transplantation, Cystic Fibrosis Reference Center of Lombardia Region, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, University of Milan, Milan, Italy
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Harriet Corvol
9Pediatric Pulmonology Department and Cystic Fibrosis Center, Sorbonne Université, Centre de Recherche Saint-Antoine, Inserm UMR_S938, Assistance Publique-Hôpitaux de Paris, Hôpital Trousseau, Paris, France
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Rebecca Cosgriff
10Cystic Fibrosis Trust, London, UK
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Géraldine Daneau
11Sciensano, Epidemiology and public health, Health services research, Brussels, Belgium
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Deniz Dogru
12Cystic Fibrosis Registry of Turkey, Ankara, Turkey
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Pavel Drevinek
13Department of Medical Microbiology, Second Faculty of Medicine, Charles University and Motol University Hospital, Prague, Czech Republic
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Andrea Dugac Vukic
14University Hospital Centre Zagreb, Cystic Fibrosis Centre - Paediatrics and Adults, Zagreb, Croatia
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Isabelle Fajac
15Université Paris Descartes, Sorbonne Paris Cité, Paris, France
1616AP-HP, Hôpital Cochin, Service de Physiologie et Explorations Fonctionnelles, Paris, France
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Alice Fox
3European Cystic Fibrosis Society, Karup, Denmark
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Stojka Fustik
17Centre for Cystic Fibrosis, University Children's Hospital, Skopje, North Macedonia
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Vincent Gulmans
18Dutch Cystic Fibrosis Foundation (NCFS), Baarn, The Netherlands
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Satenik Harutyunyan
19Yerevan University CF Centre, Muratsan Hospital, Yerevan, Armenia
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Elpis Hatziagorou
20Cystic Fibrosis Unit, Hippokration General Hospital, Aristotle University of Thessaloniki, Thessaloniki, Greece
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Irena Kasmi
21Department of Paediatrics, “Mother Thereza” Hospital Center, Tirana, Albania
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Hana Kayserová
22Cystic Fibrosis Centre, University Hospital of Bratislava, Bratislava, Slovakia
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Elena Kondratyeva
23Clinical research department of cystic fibrosis “Research Centre for Medical Genetics”, Moscow, Russian Federation
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Uroš Krivec
24Department of Paediatric Pulmonology, University Children's Hospital, Ljubljana University Medical Centre, Ljubljana, Slovenia
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Halyna Makukh
25Institute of Hereditary Pathology Ukrainian National Academy of Medical Sciences, Lviv, Ukraine
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Kestutis Malakauskas
26Adult Cystic Fibrosis center, Department of Pulmonology, Lithuanian University of Health Sciences, Kaunas, Lithuania
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Edward F. McKone
27St. Vincent's University Hospital & University College Dublin School of Medicine, Dublin, Ireland
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Meir Mei-Zahav
28Pulmonary Institute, Schneider Children's Medical Center of Israel, Petah Tikva, Israel
29Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
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Isabelle de Monestrol
30Stockholm CF centre, Karolinska University Hospital, Karolinska Institutet, Stockholm, Sweden
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Hanne Vebert Olesen
31Department of Pediatrics and Adolescent Medicine, Cystic Fibrosis Center, Aarhus University Hospital, Aarhus, Denmark
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Rita Padoan
32Department of Paediatrics, Cystic Fibrosis Regional Support Centre, University of Brescia, Brescia
33Scientific Board of Italian CF Registry, Rome, Italy
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Tsitsino Parulava
34I. Tsitsishvili Children's Clinic, CF Centre, Tblisi, Georgia
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Maria Dolores Pastor-Vivero
35Pediatric Pneumology and Cystic Fibrosis Unit, Osakidetza, Hospital Universitario Cruces, Bizkaia, Spain
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Luísa Pereira
36Centre for Cystic Fibrosis, Hospital de Santa Maria, Lisbon, Portugal
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Guergana Petrova
37Pediatric Clinic, Alexandrovska University Hospital, Medical University, Sofia, Bulgaria
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Andreas Pfleger
38Department of Pediatrics and Adolescent Medicine, Division of Pediatric Pulmonology and Allergology, Medical University of Graz, Graz, Austria
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Liviu Pop
39Victor Babes University of Medicine and Pharmacy Timisoara, National Cystic Fibrosis Centre Timisoara, Romania
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Jacqui G. van Rens
3European Cystic Fibrosis Society, Karup, Denmark
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Milan Rodić
40National Centre for Cystic Fibrosis, Mother and Child Health Institute of Serbia “Dr Vukan Čupić”, Belgrade, Serbia
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Marc Schlesser
41Department of Pulmonology, Hôpital Robert Schuman, Luxembourg, Luxembourg
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Valérie Storms
42Cystic Fibrosis Europe, Brussels, Belgium
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Oxana Turcu
43Department of Pediatrics, Ambulatory Cystic Fibrosis and Other Rare Diseases Center, Institute for Maternal and Child Healthcare, State University of Medicine and Pharmacy “Nicolae Testemitanu”, Chisinau, Republic of Moldova
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Lukasz Woźniacki
44Dziekanow Paediatric Hospital, Cystic Fibrosis Centre, Institute of Mother and Child, Warsaw, Poland
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Panayiotis Yiallouros
45Medical School, University of Cyprus, Nicosia, Cyprus
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Anna Zolin
2Department of Clinical Sciences and Community Health, Laboratory of Medical Statistics, Epidemiology and Biometry G. A. Maccacaro, University of Milan, Milan, Italy
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Damian G. Downey
46Wellcome-Wolfson Institute for Experimental Medicine, Queen's University Belfast; Regional Respiratory Centre Belfast City Hospital, Belfast, Northern Ireland
49Contributed equally as last author
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Lutz Naehrlich
47Universities of Giessen and Marburg Lung Center, German Center of Lung Research, Justus-Liebig-University Giessen, Giessen, Germany
49Contributed equally as last author
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Abstract

Background SARS-Co-V-2 infection in people with CF (pwCF) can lead to severe outcomes.

Methods In this observational study, the European Cystic Fibrosis Society Patient Registry collected data on pwCF and SARS-CoV-2 infection to estimate incidence, describe clinical presentation and investigate factors associated with severe outcomes using multivariable analysis.

Results Up to 31 December 2020, 26 countries reported information on 828 pwCF and SARS-CoV-2 infection. Incidence was 17.2 per 1000 pwCF (95% CI: 16.0–18.4). Median age was 24 years, 48.4% were male and 9.4% had lung transplants. SARS-CoV-2 incidence was higher in lung-transplanted (28.6 [95% CI: 22.7–35.5]) versus non-lung transplanted pwCF (16.6 [95% CI: 15.4–17.8]) (p=<0.001).

SARS-CoV-2 infection caused symptomatic illness in 75.7%. Factors associated with symptomatic SARS-CoV-2 infection were age >40 years, at least one F508del mutation, and pancreatic insufficiency.

Overall, 23.7% were admitted to hospital, 2.5% to intensive care. Regretfully 11 pwCF (1.4%) died. Hospitalisation, oxygen therapy, intensive care, respiratory support and death were 2–6-fold more frequent in lung-transplanted versus non-lung transplanted pwCF.

Factors associated with hospitalisation and oxygen therapy were lung transplantation, CF-related diabetes (CFRD), moderate or severe lung disease and azithromycin use (often considered a surrogate marker for Pseudomonas aeruginosa infection and poorer lung function).

Conclusion SARS-CoV-2 infection yielded high morbidity and hospitalisation in pwCF. PwCF with forced expiratory volume in one second (FEV1) <70% predicted, CFRD and those with lung transplants are at particular risk of more severe outcomes.

Footnotes

This manuscript has recently been accepted for publication in the ERJ Open Research. It is published here in its accepted form prior to copyediting and typesetting by our production team. After these production processes are complete and the authors have approved the resulting proofs, the article will move to the latest issue of the ERJOR online. Please open or download the PDF to view this article.

Conflict of interest: Andreas Jung has nothing to disclose.

Conflict of interest: Annalisa Orenti has nothing to disclose.

Conflict of interest: Fiona Dunlevy reports support for the present manuscript from Chiesi Farmaceutici SpA.

Conflict of interest: Elina Aleksejeva has nothing to disclose.

Conflict of interest: Egil Bakkeheim has nothing to disclose.

Conflict of interest: Vladimir Bobrovnichy has nothing to disclose.

Conflict of interest: Siobhán B. Carr reports receiving speaker honoraria from Vertex and Chiesi, outside the submitted work. Participation on a Data Safety Monitoring Board or Advisory Board for Vertex, Profile Pharma and Chiesi, outside the submitted work. Leadership or fiduciary role in other board, society, committee or advocacy group, paid or unpaid from UK CF Trust. PI for Pharmacovigilance study, payment to institution from Pharmaxis, outside the submitted work.

Conflict of interest: Carla Colombo has nothing to disclose.

Conflict of interest: Harriet Corvol has nothing to disclose.

Conflict of interest: Rebecca Cosgrif declares outside the submitted work to be the director of the Cystic Fibrosis Trust.

Conflict of interest: Géraldine Daneau has nothing to disclose.

Conflict of interest: Deniz Dogru has nothing to disclose.

Conflict of interest: Pavel Drevinek reports grants or contracts from Ministry of Health, Czech Republic, outside the submitted work. Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Vertex Pharmaceuticals and Actelion Pharmaceuticals, outside the submitted work. Participation on a Data Safety Monitoring Board or Advisory Board for Vertex Pharmaceuticals, outside the submitted work. Leadership or fiduciary role in other board, society, committee or advocacy group, paid or unpaid from Society for Medical Microbiology, outside the submitted work.

Conflict of interest: Andrea Dugac Vukic has nothing to disclose.

Conflict of interest: Isabelle Fajac reports grants or contracts from Boehringer Ingelheim, Celtaxsys, Corbus Pharmaceuticals, and Vertex Pharmaceuticals, outside the submitted work. Consulting fees from Boehringer Ingelheim and Vertex Pharmaceuticals, outside the submitted work. Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Vertex Pharmaceuticals and Boehringer Ingelheim, outside the submitted work. Leadership or fiduciary role in other board, society, committee or advocacy group, paid or unpaid for European Cystic Fibrosis Society.

Conflict of interest: Alice Fox support for the present manuscript from Chiesi Farmaceutici SpA.

Conflict of interest: Stojka Fustik has nothing to disclose.

Conflict of interest: Vincent Gulmans has nothing to disclose.

Conflict of interest: Satenik Harutyunyan has nothing to disclose.

Conflict of interest: Elpis Hatziagorou has nothing to disclose.

Conflict of interest: Irena Kasmi has nothing to disclose.

Conflict of interest: Hana Kayserová has nothing to disclose.

Conflict of interest: Elena Kondratyeva reports payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from All-Russian online school with international participation, outside the submitted work.

Conflict of interest: Uroš Krivec has nothing to disclose.

Conflict of interest: Halyna Makukh has nothing to disclose.

Conflict of interest: Kestutis Malakauskas has nothing to disclose.

Conflict of interest: Edward F. McKone reports grants or contracts from vertex, outside the submitted work. Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Vertex Pharmaceuticals and Roche Pharmaceuticals, outside the submitted work. Support for attending meetings and/or travel from A Menarini, outside the submitted work. Participation on a Data Safety Monitoring Board or Advisory Board for Insmed and Janssen Pharmaceuticals, outside the submitted work.

Conflict of interest: Meir Mei-Zahav has nothing to disclose.

Conflict of interest: Isabelle de Monestrol reports grant from Vertex for an academic research study regarding gastrointestinal outcome in CF patients taking Orkambi medication, outside the submitted work. Leadership or fiduciary role in other board, society, committee or advocacy group, paid or unpaid from Swedish CF Registry and the Swedish Society of Medicine's CF working group.

Conflict of interest: Hanne Vebert Olesen has nothing to disclose.

Conflict of interest: Rita Padoan has nothing to disclose.

Conflict of interest: Tsitsino Parulava has nothing to disclose.

Conflict of interest: Maria Dolores Pastor-Vivero has nothing to disclose.

Conflict of interest: Luísa Pereira has nothing to disclose.

Conflict of interest: Guergana Petrova Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from TEVA Pharmaceuticals, Mylan and Alvogen, outside the submitted work.

Conflict of interest: Andreas Pfleger has nothing to disclose.

Conflict of interest: Liviu Pop has nothing to disclose.

Conflict of interest: Jacqui G. van Rens has nothing to disclose.

Conflict of interest: Milan Rodić has nothing to disclose.

Conflict of interest: Marc Schlesser has nothing to disclose.

Conflict of interest: Valérie Storms has nothing to disclose.

Conflict of interest: Oxana Turcu has nothing to disclose.

Conflict of interest: Lukasz Woźniacki has nothing to disclose.

Conflict of interest: Panayiotis Yiallouros has nothing to disclose.

Conflict of interest: Anna Zolin has nothing to disclose.

Conflict of interest: Damian G. Downey has nothing to disclose.

Conflict of interest: Lutz Naehrlich reports support for the present manuscript from Chiesi Farmaceutici SpA. Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from ArticulateScience LLC, outside the submitted work. Participation on a Data Safety Monitoring Board or Advisory Board for Trial Steering committee of CF Storm, outside the submitted work. Leadership or fiduciary role in other board, society, committee or advocacy group, paid or unpaid from Society for German CF Registry European CF Patient Registry, outside the submitted work. Other financial or nonfinancial interests from Vertex Pharmaceuticals and Boehringer Ingelheim; Institutional fees for site participation (PI) in clinical trials from Vertex Pharmaceuticals and Boehringer Ingelheim.

This is a PDF-only article. Please click on the PDF link above to read it.

  • Received June 21, 2021.
  • Accepted September 12, 2021.
  • Copyright ©The authors 2021
http://creativecommons.org/licenses/by-nc/4.0/

This version is distributed under the terms of the Creative Commons Attribution Non-Commercial Licence 4.0. For commercial reproduction rights and permissions contact permissions{at}ersnet.org

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Factors for severe outcomes following SARS-CoV-2 infection in people with cystic fibrosis in Europe
Andreas Jung, Annalisa Orenti, Fiona Dunlevy, Elina Aleksejeva, Egil Bakkeheim, Vladimir Bobrovnichy, Siobhán B. Carr, Carla Colombo, Harriet Corvol, Rebecca Cosgriff, Géraldine Daneau, Deniz Dogru, Pavel Drevinek, Andrea Dugac Vukic, Isabelle Fajac, Alice Fox, Stojka Fustik, Vincent Gulmans, Satenik Harutyunyan, Elpis Hatziagorou, Irena Kasmi, Hana Kayserová, Elena Kondratyeva, Uroš Krivec, Halyna Makukh, Kestutis Malakauskas, Edward F. McKone, Meir Mei-Zahav, Isabelle de Monestrol, Hanne Vebert Olesen, Rita Padoan, Tsitsino Parulava, Maria Dolores Pastor-Vivero, Luísa Pereira, Guergana Petrova, Andreas Pfleger, Liviu Pop, Jacqui G. van Rens, Milan Rodić, Marc Schlesser, Valérie Storms, Oxana Turcu, Lukasz Woźniacki, Panayiotis Yiallouros, Anna Zolin, Damian G. Downey, Lutz Naehrlich
ERJ Open Research Jan 2021, 00411-2021; DOI: 10.1183/23120541.00411-2021

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Factors for severe outcomes following SARS-CoV-2 infection in people with cystic fibrosis in Europe
Andreas Jung, Annalisa Orenti, Fiona Dunlevy, Elina Aleksejeva, Egil Bakkeheim, Vladimir Bobrovnichy, Siobhán B. Carr, Carla Colombo, Harriet Corvol, Rebecca Cosgriff, Géraldine Daneau, Deniz Dogru, Pavel Drevinek, Andrea Dugac Vukic, Isabelle Fajac, Alice Fox, Stojka Fustik, Vincent Gulmans, Satenik Harutyunyan, Elpis Hatziagorou, Irena Kasmi, Hana Kayserová, Elena Kondratyeva, Uroš Krivec, Halyna Makukh, Kestutis Malakauskas, Edward F. McKone, Meir Mei-Zahav, Isabelle de Monestrol, Hanne Vebert Olesen, Rita Padoan, Tsitsino Parulava, Maria Dolores Pastor-Vivero, Luísa Pereira, Guergana Petrova, Andreas Pfleger, Liviu Pop, Jacqui G. van Rens, Milan Rodić, Marc Schlesser, Valérie Storms, Oxana Turcu, Lukasz Woźniacki, Panayiotis Yiallouros, Anna Zolin, Damian G. Downey, Lutz Naehrlich
ERJ Open Research Jan 2021, 00411-2021; DOI: 10.1183/23120541.00411-2021
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