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

Andreas Jung^{1

2}, Annalisa Orenti^{3

2}, Fiona Dunlevy^{4

2}, Elina Aleksejeva⁵, Egil Bakkeheim⁶, Vladimir Bobrovnichy⁷, Siobhán B Carr^{8

9}, Carla Colombo¹⁰, Harriet Corvol¹¹, Rebecca Cosgriff¹², Géraldine Daneau¹³, Deniz Dogru¹⁴, Pavel Drevinek¹⁵, Andrea Dugac Vukic¹⁶, Isabelle Fajac^{17

18}, Alice Fox⁴, Stojka Fustik¹⁹, Vincent Gulmans²⁰, Satenik Harutyunyan²¹, Elpis Hatziagorou²², Irena Kasmi²³, Hana Kayserová²⁴, Elena Kondratyeva²⁵, Uroš Krivec²⁶, Halyna Makukh²⁷, Kestutis Malakauskas²⁸, Edward F McKone²⁹, Meir Mei-Zahav^{30

31}, Isabelle de Monestrol³², Hanne Vebert Olesen³³, Rita Padoan^{34

35}, Tsitsino Parulava³⁶, Maria Dolores Pastor-Vivero³⁷, Luísa Pereira³⁸, Guergana Petrova³⁹, Andreas Pfleger⁴⁰, Liviu Pop⁴¹, Jacqui G van Rens⁴, Milan Rodic⁴², Marc Schlesser⁴³, Valérie Storms⁴⁴, Oxana Turcu⁴⁵, Lukasz Woz Niacki⁴⁶, Panayiotis Yiallouros⁴⁷, Anna Zolin³, Damian G Downey^{48

49

50}, Lutz Naehrlich^{3

51

50}

Affiliations

¹ Paediatric Pulmonology, University Children's Hospital Zurich, Zurich, Switzerland.
² Co-first authors.
³ Dept of Clinical Sciences and Community Health, Laboratory of Medical Statistics, Epidemiology and Biometry G.A. Maccacaro, University of Milan, Milan, Italy.
⁴ European Cystic Fibrosis Society, Karup, Denmark.
⁵ Dept of Pneumology, Children's Clinical University Hospital, Rīga Stradinš University, Riga, Latvia.
⁶ Dept of Paediatrics, Norwegian Cystic Fibrosis Registry, Oslo University Hospital, Oslo, Norway.
⁷ Belarusian Republic Children's Center of Pulmonology and Cystic Fibrosis, Pulmonary Department, 3rd City Children's Clinical Hospital, Minsk, Belarus.
⁸ Dept of Respiratory Paediatrics, Royal Brompton Hospital, London, UK.
⁹ NHLI, Imperial College, London, UK.
¹⁰ Dept of Pathophysiology and Transplantation, Cystic Fibrosis Reference Center of Lombardia Region, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, University of Milan, Milan, Italy.
¹¹ Pediatric Pulmonology Dept and Cystic Fibrosis Center, Sorbonne Université, Centre de Recherche Saint-Antoine, Inserm UMR_S938, Assistance Publique-Hôpitaux de Paris, Hôpital Trousseau, Paris, France.
¹² Cystic Fibrosis Trust, London, UK.
¹³ Sciensano, Epidemiology and Public Health, Health Services Research, Brussels, Belgium.
¹⁴ Cystic Fibrosis Registry of Turkey, Ankara, Turkey.
¹⁵ Dept of Medical Microbiology, Second Faculty of Medicine, Charles University and Motol University Hospital, Prague, Czech Republic.
¹⁶ University Hospital Centre Zagreb, Cystic Fibrosis Centre - Paediatrics and Adults, Zagreb, Croatia.
¹⁷ Université Paris Descartes, Sorbonne Paris Cité, Paris, France.
¹⁸ AP-HP, Hôpital Cochin, Service de Physiologie et Explorations Fonctionnelles, Paris, France.
¹⁹ Centre for Cystic Fibrosis, University Children's Hospital, Skopje, North Macedonia.
²⁰ Dutch Cystic Fibrosis Foundation (NCFS), Baarn, The Netherlands.
²¹ Yerevan University CF Centre, Muratsan Hospital, Yerevan, Armenia.
²² Cystic Fibrosis Unit, Hippokration General Hospital, Aristotle University of Thessaloniki, Thessaloniki, Greece.
²³ Dept of Paediatrics, "Mother Thereza" Hospital Center, Tirana, Albania.
²⁴ Cystic Fibrosis Centre, University Hospital of Bratislava, Bratislava, Slovakia.
²⁵ Clinical Research Dept of Cystic Fibrosis "Research Centre for Medical Genetics", Moscow, Russian Federation.
²⁶ Dept of Paediatric Pulmonology, University Children's Hospital, Ljubljana University Medical Centre, Ljubljana, Slovenia.
²⁷ Institute of Hereditary Pathology, Ukrainian National Academy of Medical Sciences, Lviv, Ukraine.
²⁸ Adult Cystic Fibrosis Center, Dept of Pulmonology, Lithuanian University of Health Sciences, Kaunas, Lithuania.
²⁹ St Vincent's University Hospital & University College Dublin School of Medicine, Dublin, Ireland.
³⁰ Pulmonary Institute, Schneider Children's Medical Center of Israel, Petah Tikva, Israel.
³¹ Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
³² Stockholm CF Centre, Karolinska University Hospital, Karolinska Institutet, Stockholm, Sweden.
³³ Dept of Pediatrics and Adolescent Medicine, Cystic Fibrosis Center, Aarhus University Hospital, Aarhus, Denmark.
³⁴ Dept of Paediatrics, Cystic Fibrosis Regional Support Centre, University of Brescia, Brescia.
³⁵ Scientific Board of Italian CF Registry, Rome, Italy.
³⁶ I. Tsitsishvili Children's Clinic, CF Centre, Tblisi, Georgia.
³⁷ Pediatric Pneumology and Cystic Fibrosis Unit, Osakidetza, Hospital Universitario Cruces, Bizkaia, Spain.
³⁸ Centre for Cystic Fibrosis, Hospital de Santa Maria, Lisbon, Portugal.
³⁹ Pediatric Clinic, Alexandrovska University Hospital, Medical University, Sofia, Bulgaria.
⁴⁰ Dept of Pediatrics and Adolescent Medicine, Division of Pediatric Pulmonology and Allergology, Medical University of Graz, Graz, Austria.
⁴¹ Victor Babes University of Medicine and Pharmacy Timisoara, National Cystic Fibrosis Centre, Timisoara, Romania.
⁴² National Centre for Cystic Fibrosis, Mother and Child Health Institute of Serbia "Dr Vukan Čupić", Belgrade, Serbia.
⁴³ Dept of Pulmonology, Hôpital Robert Schuman, Luxembourg, Luxembourg.
⁴⁴ Cystic Fibrosis Europe, Brussels, Belgium.
⁴⁵ Dept 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.
⁴⁶ Dziekanow Paediatric Hospital, Cystic Fibrosis Centre, Institute of Mother and Child, Warsaw, Poland.
⁴⁷ Medical School, University of Cyprus, Nicosia, Cyprus.
⁴⁸ Wellcome-Wolfson Institute for Experimental Medicine, Queen's University Belfast, Belfast, UK.
⁴⁹ Regional Respiratory Centre, Belfast City Hospital, Belfast, UK.
⁵⁰ Co-senior authors.
⁵¹ Universities of Giessen and Marburg Lung Center, German Center of Lung Research, Justus-Liebig-University Giessen, Giessen, Germany.

PMID: 34984210
PMCID: PMC8557394
DOI: 10.1183/23120541.00411-2021

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

Andreas Jung et al. ERJ Open Res. 2021.

. 2021 Dec 27;7(4):00411-2021.

doi: 10.1183/23120541.00411-2021. eCollection 2021 Oct.

Authors

Affiliations

¹ Paediatric Pulmonology, University Children's Hospital Zurich, Zurich, Switzerland.
² Co-first authors.
³ Dept of Clinical Sciences and Community Health, Laboratory of Medical Statistics, Epidemiology and Biometry G.A. Maccacaro, University of Milan, Milan, Italy.
⁴ European Cystic Fibrosis Society, Karup, Denmark.
⁵ Dept of Pneumology, Children's Clinical University Hospital, Rīga Stradinš University, Riga, Latvia.
⁶ Dept of Paediatrics, Norwegian Cystic Fibrosis Registry, Oslo University Hospital, Oslo, Norway.
⁷ Belarusian Republic Children's Center of Pulmonology and Cystic Fibrosis, Pulmonary Department, 3rd City Children's Clinical Hospital, Minsk, Belarus.
⁸ Dept of Respiratory Paediatrics, Royal Brompton Hospital, London, UK.
⁹ NHLI, Imperial College, London, UK.
¹⁰ Dept of Pathophysiology and Transplantation, Cystic Fibrosis Reference Center of Lombardia Region, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, University of Milan, Milan, Italy.
¹¹ Pediatric Pulmonology Dept and Cystic Fibrosis Center, Sorbonne Université, Centre de Recherche Saint-Antoine, Inserm UMR_S938, Assistance Publique-Hôpitaux de Paris, Hôpital Trousseau, Paris, France.
¹² Cystic Fibrosis Trust, London, UK.
¹³ Sciensano, Epidemiology and Public Health, Health Services Research, Brussels, Belgium.
¹⁴ Cystic Fibrosis Registry of Turkey, Ankara, Turkey.
¹⁵ Dept of Medical Microbiology, Second Faculty of Medicine, Charles University and Motol University Hospital, Prague, Czech Republic.
¹⁶ University Hospital Centre Zagreb, Cystic Fibrosis Centre - Paediatrics and Adults, Zagreb, Croatia.
¹⁷ Université Paris Descartes, Sorbonne Paris Cité, Paris, France.
¹⁸ AP-HP, Hôpital Cochin, Service de Physiologie et Explorations Fonctionnelles, Paris, France.
¹⁹ Centre for Cystic Fibrosis, University Children's Hospital, Skopje, North Macedonia.
²⁰ Dutch Cystic Fibrosis Foundation (NCFS), Baarn, The Netherlands.
²¹ Yerevan University CF Centre, Muratsan Hospital, Yerevan, Armenia.
²² Cystic Fibrosis Unit, Hippokration General Hospital, Aristotle University of Thessaloniki, Thessaloniki, Greece.
²³ Dept of Paediatrics, "Mother Thereza" Hospital Center, Tirana, Albania.
²⁴ Cystic Fibrosis Centre, University Hospital of Bratislava, Bratislava, Slovakia.
²⁵ Clinical Research Dept of Cystic Fibrosis "Research Centre for Medical Genetics", Moscow, Russian Federation.
²⁶ Dept of Paediatric Pulmonology, University Children's Hospital, Ljubljana University Medical Centre, Ljubljana, Slovenia.
²⁷ Institute of Hereditary Pathology, Ukrainian National Academy of Medical Sciences, Lviv, Ukraine.
²⁸ Adult Cystic Fibrosis Center, Dept of Pulmonology, Lithuanian University of Health Sciences, Kaunas, Lithuania.
²⁹ St Vincent's University Hospital & University College Dublin School of Medicine, Dublin, Ireland.
³⁰ Pulmonary Institute, Schneider Children's Medical Center of Israel, Petah Tikva, Israel.
³¹ Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
³² Stockholm CF Centre, Karolinska University Hospital, Karolinska Institutet, Stockholm, Sweden.
³³ Dept of Pediatrics and Adolescent Medicine, Cystic Fibrosis Center, Aarhus University Hospital, Aarhus, Denmark.
³⁴ Dept of Paediatrics, Cystic Fibrosis Regional Support Centre, University of Brescia, Brescia.
³⁵ Scientific Board of Italian CF Registry, Rome, Italy.
³⁶ I. Tsitsishvili Children's Clinic, CF Centre, Tblisi, Georgia.
³⁷ Pediatric Pneumology and Cystic Fibrosis Unit, Osakidetza, Hospital Universitario Cruces, Bizkaia, Spain.
³⁸ Centre for Cystic Fibrosis, Hospital de Santa Maria, Lisbon, Portugal.
³⁹ Pediatric Clinic, Alexandrovska University Hospital, Medical University, Sofia, Bulgaria.
⁴⁰ Dept of Pediatrics and Adolescent Medicine, Division of Pediatric Pulmonology and Allergology, Medical University of Graz, Graz, Austria.
⁴¹ Victor Babes University of Medicine and Pharmacy Timisoara, National Cystic Fibrosis Centre, Timisoara, Romania.
⁴² National Centre for Cystic Fibrosis, Mother and Child Health Institute of Serbia "Dr Vukan Čupić", Belgrade, Serbia.
⁴³ Dept of Pulmonology, Hôpital Robert Schuman, Luxembourg, Luxembourg.
⁴⁴ Cystic Fibrosis Europe, Brussels, Belgium.
⁴⁵ Dept 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.
⁴⁶ Dziekanow Paediatric Hospital, Cystic Fibrosis Centre, Institute of Mother and Child, Warsaw, Poland.
⁴⁷ Medical School, University of Cyprus, Nicosia, Cyprus.
⁴⁸ Wellcome-Wolfson Institute for Experimental Medicine, Queen's University Belfast, Belfast, UK.
⁴⁹ Regional Respiratory Centre, Belfast City Hospital, Belfast, UK.
⁵⁰ Co-senior authors.
⁵¹ Universities of Giessen and Marburg Lung Center, German Center of Lung Research, Justus-Liebig-University Giessen, Giessen, Germany.

PMID: 34984210
PMCID: PMC8557394
DOI: 10.1183/23120541.00411-2021

Abstract

Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in people with cystic fibrosis (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 December 31, 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% of pwCF were admitted to hospital, 2.5% of those to intensive care, and regretfully 11 (1.4%) died. Hospitalisation, oxygen therapy, intensive care, respiratory support and death were 2- to 6-fold more frequent in lung-transplanted versus non-lung-transplanted pwCF.Factors associated with hospitalisation and oxygen therapy were lung transplantation, cystic fibrosis-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 1 s <70% predicted, CFRD and those with lung transplants are at particular risk of more severe outcomes.

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Conflict of interest statement

Conflict of interest: A. Jung has nothing to disclose. Conflict of interest: A. Orenti has nothing to disclose. Conflict of interest: F. Dunlevy reports support for the present manuscript from Chiesi Farmaceutici SpA. Conflict of interest: E. Aleksejeva has nothing to disclose. Conflict of interest: E. Bakkeheim has nothing to disclose. Conflict of interest: V. Bobrovnichy has nothing to disclose. Conflict of interest: S.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: C. Colombo has nothing to disclose. Conflict of interest: H. Corvol has nothing to disclose. Conflict of interest: R. Cosgrif declares outside the submitted work to be the director of the Cystic Fibrosis Trust. Conflict of interest: G. Daneau has nothing to disclose. Conflict of interest: D. Dogru has nothing to disclose. Conflict of interest: P. 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: A.D. Vukic has nothing to disclose. Conflict of interest: I. 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: A. Fox support for the present manuscript from Chiesi Farmaceutici SpA. Conflict of interest: S. Fustik has nothing to disclose. Conflict of interest: V. Gulmans has nothing to disclose. Conflict of interest: S. Harutyunyan has nothing to disclose. Conflict of interest: E. Hatziagorou has nothing to disclose. Conflict of interest: I. Kasmi has nothing to disclose. Conflict of interest: H. Kayserová has nothing to disclose. Conflict of interest: E. 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: U. Krivec has nothing to disclose. Conflict of interest: H. Makukh has nothing to disclose. Conflict of interest: K. Malakauskas has nothing to disclose. Conflict of interest: E.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: M. Mei-Zahav has nothing to disclose. Conflict of interest: I. 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: H.V. Olesen has nothing to disclose. Conflict of interest: R. Padoan has nothing to disclose. Conflict of interest: T. Parulava has nothing to disclose. Conflict of interest: M.D. Pastor-Vivero has nothing to disclose. Conflict of interest: L. Pereira has nothing to disclose. Conflict of interest: G. Petrova reports 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: A. Pfleger has nothing to disclose. Conflict of interest: L. Pop has nothing to disclose. Conflict of interest: J.G. van Rens has nothing to disclose. Conflict of interest: M. Rodić has nothing to disclose. Conflict of interest: M. Schlesser has nothing to disclose. Conflict of interest: V. Storms has nothing to disclose. Conflict of interest: O. Turcu has nothing to disclose. Conflict of interest: L. Woźniacki has nothing to disclose. Conflict of interest: P. Yiallouros has nothing to disclose. Conflict of interest: A. Zolin has nothing to disclose. Conflict of interest: D.G. Downey has nothing to disclose. Conflict of interest: L. 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.

Figures

**FIGURE 1**
Data collection for people with cystic fibrosis (pwCF) and SARS-CoV-2 infection. ^#: Albania, Belarus, Bulgaria, Cyprus, Georgia, Lithuania, Luxembourg, Republic of Moldova, Romania, Serbia and Ukraine. Hungary did not report information to ECFSPR. ^¶: Armenia, Austria, Belgium, Croatia, Czech Republic, Denmark, France, Germany, Greece, Israel, Ireland, Italy, Latvia, Netherlands, Norway, North Macedonia, Portugal, Poland, Russia, Slovak Republic, Slovenia, Spain, Sweden, Switzerland, Turkey and UK. ⁺: these cases were diagnosed by antibody test, antigen test, CT scan or medical team opinion without PCR confirmation. ^§: this group included 10 people with non-lung solid organ transplants (seven liver, two kidney, one unspecified).

**FIGURE 2**
Diagnosis of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in people with cystic fibrosis (pwCF) (n=828) in 2020, by month.

**FIGURE 3**
SARS-CoV-2 incidence per 1000 people with cystic fibrosis in 2020, by country.

**FIGURE 4**
Factors positively (+) and negatively (−) associated with SARS-CoV-2 infection symptoms and outcomes. ABPA: allergic bronchopulmonary aspergillosis; BMI: body mass index; CFTR: cystic fibrosis transmembrane conductance regulator; GI: gastrointestinal; MRSA: methicillin-resistant *Staphylococcus aureus*; FEV₁ % pred: per cent predicted forced expiratory volume in 1 s. A person was considered underweight if their BMI z-score was ≤2, using Centers for Disease Control and Prevention reference values [40].

**FIGURE 5**
Multivariable analysis of factors associated with symptoms and outcomes of SARS-CoV-2 infection in people with cystic fibrosis (CF). BMI: body mass index; CFTR: cystic fibrosis transmembrane conductance regulator; FEV₁ % pred: per cent predicted forced expiratory volume in 1 s; *P. aeruginosa*: *Pseudomonas aeruginosa*.

See this image and copyright information in PMC

References

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

Affiliations

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

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

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