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The effect of the COVID-19 pandemic on severe asthma care in Europe: will care change for good?

Katrien Eger, Dora Paroczai, Alison Bacon, Florence Schleich, Svetlana Sergejeva, Arnaud Bourdin, Isabelle Vachier, Eleftherios Zervas, Konstantinos Katsoulis, Dimosthenis Papapetrou, Konstantinos Kostikas, Zsuzsanna Csoma, Enrico Heffler, Giorgio Walter Canonica, Ineta Grisle, Kristina Bieksiene, Jolita Palacionyte, Anneke ten Brinke, Simone Hashimoto, Frank W.J.M. Smeenk, Gert-Jan Braunstahl, Simone van der Sar, Florin Mihălţan, Natalia Nenasheva, Marina Peredelskaya, Biljana Zvezdin, Ivan Čekerevac, Sanja Hromiš, Vojislav Ćupurdija, Zorica Lazic, Branislava Milenkovic, Sanja Dimic-Janjic, Valentyna Yasinska, Barbro Dahlén, Apostolos Bossios, Nikolaos Lazarinis, David Aronsson, Arne Egesten, Abul Kashem Mohammad Munir, Lars Ahlbeck, Christer Janson, Sabina Škrgat, Natalija Edelbaher, Joerg Leuppi, Fabienne Jaun, Jochen Rüdiger, Nikolay Pavlov, Pietro Gianella, Reta Fischer, Florian Charbonnier, Rekha Chaudhuri, Steven James Smith, Simon Doe, Michelle Fawdon, Matthew Masoli, Liam Heaney, Hans Michael Haitchi, Ramesh Kurukulaaratchy, Olivia Fulton, Betty Frankemölle, Toni Gibson, Karen Needham, Peter Howarth, Ratko Djukanovic, Elisabeth Bel, Michael Hyland
ERJ Open Research 2022 8: 00065-2022; DOI: 10.1183/23120541.00065-2022
Katrien Eger
1Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands
47Co-first authors
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  • For correspondence: k.a.eger@amsterdamumc.nl
Dora Paroczai
2Csongrad County Hospital and Dept of Pulmonology, University of Szeged, Szeged, Hungary
47Co-first authors
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Alison Bacon
3School of Psychology, University of Plymouth, Plymouth, UK
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Florence Schleich
4CHU of Liege, Liege, Belgium
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Svetlana Sergejeva
5The North Estonian Medical Centre, Tallinn, Estonia
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Arnaud Bourdin
6PhyMedExp, CHU Montpellier, University of Montpellier, Montpellier, France
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  • ORCID record for Arnaud Bourdin
Isabelle Vachier
6PhyMedExp, CHU Montpellier, University of Montpellier, Montpellier, France
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Eleftherios Zervas
77th Respiratory Dept, Athens Chest Hospital, Athens, Greece
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Konstantinos Katsoulis
8Pulmonary Dept, 424 Army General Hospital, Thessaloniki, Greece
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Dimosthenis Papapetrou
9Medical Group of Athens (Paleo Faliro Clinic), Athens, Greece
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Konstantinos Kostikas
10Respiratory Medicine Dept, University Hospital of Ioannina, Ioannina, Greece
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Zsuzsanna Csoma
11National Koranyi Institute for Pulmonology, Budapest, Hungary
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Enrico Heffler
12Personalized Medicine, Asthma and Allergy - IRCCS Humanitas Research Hospital - Rozzano (MI), Italy
13Departmento of Biomedical Sciences - Humanitas University - Pieve Emanuele (MI), Italy
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Giorgio Walter Canonica
12Personalized Medicine, Asthma and Allergy - IRCCS Humanitas Research Hospital - Rozzano (MI), Italy
13Departmento of Biomedical Sciences - Humanitas University - Pieve Emanuele (MI), Italy
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Ineta Grisle
14Riga East University Hospital, Riga, Latvia
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Kristina Bieksiene
15Lithuanian University of Health Science, Kaunas, Lithuania
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Jolita Palacionyte
15Lithuanian University of Health Science, Kaunas, Lithuania
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Anneke ten Brinke
16Medical Centre Leeuwarden, Leeuwarden, The Netherlands
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Simone Hashimoto
1Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands
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Frank W.J.M. Smeenk
17Catharina Ziekenhuis Eindhoven, Eindhoven, The Netherlands
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Gert-Jan Braunstahl
18Franciscus Gasthuis en Vlietland, Rotterdam, The Netherlands
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Simone van der Sar
19Amphia Ziekenhuis, Breda, The Netherlands
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Florin Mihălţan
20National Institute of Pneumology, Bucharest, Romania
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Natalia Nenasheva
21Russian Medical Academy of Continuous Professional Education of the Ministry of Healthcare of the Russian Federation, Moscow, Russian Federation
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Marina Peredelskaya
21Russian Medical Academy of Continuous Professional Education of the Ministry of Healthcare of the Russian Federation, Moscow, Russian Federation
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Biljana Zvezdin
22Institute for Pulmonary Diseases of Vojvodina, Sremska Kamenica, Serbia
23Medical Faculty Novi Sad, University of Novi Sad, Bucharest, Romania
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Ivan Čekerevac
24Clinic for Pulmonology, University Clinical Center Kragujevac, Kragujevac, Serbia
25Dept of Internal Medicine, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia
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Sanja Hromiš
22Institute for Pulmonary Diseases of Vojvodina, Sremska Kamenica, Serbia
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Vojislav Ćupurdija
24Clinic for Pulmonology, University Clinical Center Kragujevac, Kragujevac, Serbia
25Dept of Internal Medicine, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia
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Zorica Lazic
24Clinic for Pulmonology, University Clinical Center Kragujevac, Kragujevac, Serbia
25Dept of Internal Medicine, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia
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Branislava Milenkovic
26Clinic for Pulmonology, University Clinical Center of Serbia, Belgrade Medical faculty, Belgrade, Serbia
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Sanja Dimic-Janjic
26Clinic for Pulmonology, University Clinical Center of Serbia, Belgrade Medical faculty, Belgrade, Serbia
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Valentyna Yasinska
27Karolinska Severe Asthma Center, Dept of Respiratory Medicine and Allergy, Karolinska University Hospital, Huddinge and Dept of Medicine, Huddinge, Karolinska Institutet, Stockholm, Sweden
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Barbro Dahlén
27Karolinska Severe Asthma Center, Dept of Respiratory Medicine and Allergy, Karolinska University Hospital, Huddinge and Dept of Medicine, Huddinge, Karolinska Institutet, Stockholm, Sweden
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Apostolos Bossios
27Karolinska Severe Asthma Center, Dept of Respiratory Medicine and Allergy, Karolinska University Hospital, Huddinge and Dept of Medicine, Huddinge, Karolinska Institutet, Stockholm, Sweden
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Nikolaos Lazarinis
27Karolinska Severe Asthma Center, Dept of Respiratory Medicine and Allergy, Karolinska University Hospital, Huddinge and Dept of Medicine, Huddinge, Karolinska Institutet, Stockholm, Sweden
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David Aronsson
28Respiratory Medicine and Allergology, Dept of Clinical Sciences Lund, Lund University and Skåne University Hospital, Lund, Sweden
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Arne Egesten
28Respiratory Medicine and Allergology, Dept of Clinical Sciences Lund, Lund University and Skåne University Hospital, Lund, Sweden
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Abul Kashem Mohammad Munir
28Respiratory Medicine and Allergology, Dept of Clinical Sciences Lund, Lund University and Skåne University Hospital, Lund, Sweden
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Lars Ahlbeck
29Allergy Center, Linköping, Sweden
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Christer Janson
30Dept of Medical Sciences, Uppsala University, Uppsala, Sweden
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Sabina Škrgat
31Dept for Pulmonary Diseases, University Medical Centre Ljubljana, Medical Faculty, University of Ljubljana, Ljubljana, Slovenia
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Natalija Edelbaher
32Pulmonary Dept, University Medical Centre Maribor, Maribor, Slovenia
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Joerg Leuppi
33Medical Faculty University of Basel and Cantonal Hospital Baselland, Liestal, Switzerland
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Fabienne Jaun
33Medical Faculty University of Basel and Cantonal Hospital Baselland, Liestal, Switzerland
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Jochen Rüdiger
34Medizin Stollturm, Basel, Switzerland
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Nikolay Pavlov
35Dept of Pulmonary Medicine, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
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Pietro Gianella
36EOC Lugano, Lugano, Switzerland
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Reta Fischer
37Quartier Bleu, Bern, Switzerland
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Florian Charbonnier
38HUG Geneve, Geneva, Switzerland
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Rekha Chaudhuri
39Gartnavel General Hospital, Glasgow, UK
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Steven James Smith
39Gartnavel General Hospital, Glasgow, UK
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Simon Doe
40Royal Victoria Infirmary, Newcastle, UK
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Michelle Fawdon
40Royal Victoria Infirmary, Newcastle, UK
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Matthew Masoli
41The Royal Devon & Exeter Hospital, Exeter, UK
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Liam Heaney
42Wellcome-Wolfson Centre for Experimental Medicine, Queens University Belfast, Belfast, UK
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Hans Michael Haitchi
43University Hospital Southampton, Southampton, UK
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Ramesh Kurukulaaratchy
43University Hospital Southampton, Southampton, UK
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Olivia Fulton
44European Lung Foundation, Sheffield, UK
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Betty Frankemölle
44European Lung Foundation, Sheffield, UK
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Toni Gibson
44European Lung Foundation, Sheffield, UK
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Karen Needham
44European Lung Foundation, Sheffield, UK
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Peter Howarth
45Global Medical Affairs, Specialty Medicine TA, GSK, Brentford, UK
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Ratko Djukanovic
43University Hospital Southampton, Southampton, UK
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Elisabeth Bel
1Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands
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Michael Hyland
46Plymouth Marjon University, Plymouth, UK
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  • Article
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  • FIGURE 1
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    FIGURE 1

    Satisfaction with change to video/phone consultations. A change to video/phone consultations was reported by 212 patients, of whom 207 indicated their satisfaction level with this change.

  • FIGURE  2
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    FIGURE  2

    Satisfaction with change to home-administered biologics. Satisfaction with change to home-administered biologics in patients reporting this change in their biologic care (n=153).

  • FIGURE 3
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    FIGURE 3

    Physicians’ expected changes to future severe asthma care. Physicians’ beliefs about how asthma care will change following the pandemic (n=268).

Tables

  • Figures
  • Supplementary Materials
  • TABLE 1

    Country breakdown of physician and patient respondents to questionnaires

    CountryPhysicians nPatients
    nFemale
    n (%)
    Use of biologics
    n (%)
    Daily OCS
    n (%)
    Belgium1310257 (56)86 (84)9 (9)
    Estonia81413 (93)6 (43)5 (36)
    France281510 (67)13 (87)5 (33)
    Greece1812282 (67)74 (60)35 (29)
    Hungary4011071 (65)71 (65)22 (20)
    Italy315238 (73)28 (54)13 (25)
    Latvia45433 (61)24 (44)19 (35)
    Lithuania155335 (66)41 (77)8 (15)
    The Netherlands211469 (61)79 (69)27 (24)
    Romania31125 (42)9 (75)3 (25)
    Russian Federation135534 (62)11 (20)9 (16)
    Serbia157450 (68)45 (60)30 (41)
    Slovenia27051 (73)64 (91)12 (17)
    Sweden912260 (49)67 (55)34 (28)
    Switzerland195725 (44)46 (81)19 (33)
    UK207543 (57)45 (60)31 (41)
    Total2681101676 (61)709 (64)281 (26)

    Number of returned physician surveys per country, and number and characteristics of participating patients per country. OCS: oral corticosteroids.

    • TABLE 2

      Physician-reported changes in delivery of care

      Change in caren (%)
      Reorganisation of care by physicians (i.e. voluntary)
       Change to video/phone consultations122 (46)
       Outpatient clinic continued with social distancing142 (53)
       Urgent consultations only44 (16)
       New patients postponed32 (12)
       Switch to home-administered biologics102 (38)
      Changes induced by the pandemic (i.e. involuntary)
       Reduced capacity outpatient clinic109 (41)
       Reduced capacity lung function lab159 (59)
       Fewer physicians available115 (43)
       Fewer nurses available76 (28)

      Changes in severe asthma care during the coronavirus disease 2019 (COVID-19) pandemic as reported by the participating severe asthma specialists (n=268).

      • TABLE 3

        Satisfaction scores with types of change in care and asthma control

        n (%)Satisfaction with careSatisfaction with changes in careEffect on asthma control attributed to changes in care
        All patients (n=1101)
         No change607 (55)4.42±0.61#
         Change494 (45)3.85±0.72#3.68±0.931.90±0.84
        Type of change reported (n=467)
         Phone/video consultations212 (45)3.96±0.673.81±0.871.80±0.78
         Monitored my asthma at home24 (5)3.55±0.763.65±0.862.24±0.70
         The location of my appointments was changed43 (9)3.90±0.683.78±0.911.86±0.87
         Attended alternative unit (e.g. ED)10 (2)3.66±0.923.55±1.282.50±1.25
         I chose to cancel appointments61 (13)3.60±0.743.30±1.002.07±0.96
         Cancelled or postponed by clinic117 (25)3.79±0.743.55±0.971.91±0.85

        Data presented as mean±sd, unless otherwise stated. Patient-reported changes in severe asthma care during the coronavirus disease 2019 (COVID-19) pandemic and associated levels of satisfaction with care and changes in care, and patient-perceived effect on asthma control. Higher satisfaction scores indicate better satisfaction (range 1–5, 1=very low satisfaction and 5=very high satisfaction); higher asthma control scores indicate greater agreement with statements that changes in care induced worsening of asthma control (range 1–5, 1=strongly disagree and 5=strongly agree). ED: emergency department. #: t (1068)=15.82, p<0.001, d=0.96.

        • TABLE 4

          Satisfaction scores with types of change in biologic care and asthma control

          n (%)Satisfaction with careSatisfaction with changes in careEffect on asthma control attributed to changes in biologic treatment
          All patients on biologics (n=709)
           No change542 (76)4.40±0.59#
           Change167 (24)3.93±0.68#3.72±1.081.90±0.88
          Type of change reported (n=167)
           Switch to home administration153 (92)3.96±0.673.90±0.871.76±0.74
           Treatment less frequent4 (2)4.05±0.463.83±0.532.22±1.57
           Treatment postponed7 (4)3.63±0.843.92±1.022.05±0.83
           Treatment stopped3 (2)3.04±0.333.17±0.293.22±0.69

          Data presented as mean±sd, unless otherwise stated. Patient-reported changes in biologic care during the coronavirus disease 2019 (COVID-19) pandemic and associated levels of satisfaction with care and changes in care, and patient-perceived effect on asthma control. Higher satisfaction scores indicate better satisfaction (range 1–5, 1=very low satisfaction and 5=very high satisfaction); higher asthma control scores indicate greater agreement with a statement that changes in biologic care induced worsening of asthma control (range 1–5, 1=strongly disagree and 5=strongly agree). Data of 709 patients on biologics; 26 did not complete the questions concerning satisfaction with care. #: t (674)=8.47, p<0.001, d=0.72.

          Supplementary Materials

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          • Supplementary Material

            Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.

            Guidance for Reporting Involvement of Patients and the Public (GRIPP)-2 form 00065-2022.SUPPLEMENT

            Patient survey 00065-2022.SUPPLEMENT2

            Physician survey 00065-2022.SUPPLEMENT3

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          The effect of the COVID-19 pandemic on severe asthma care in Europe: will care change for good?
          Katrien Eger, Dora Paroczai, Alison Bacon, Florence Schleich, Svetlana Sergejeva, Arnaud Bourdin, Isabelle Vachier, Eleftherios Zervas, Konstantinos Katsoulis, Dimosthenis Papapetrou, Konstantinos Kostikas, Zsuzsanna Csoma, Enrico Heffler, Giorgio Walter Canonica, Ineta Grisle, Kristina Bieksiene, Jolita Palacionyte, Anneke ten Brinke, Simone Hashimoto, Frank W.J.M. Smeenk, Gert-Jan Braunstahl, Simone van der Sar, Florin Mihălţan, Natalia Nenasheva, Marina Peredelskaya, Biljana Zvezdin, Ivan Čekerevac, Sanja Hromiš, Vojislav Ćupurdija, Zorica Lazic, Branislava Milenkovic, Sanja Dimic-Janjic, Valentyna Yasinska, Barbro Dahlén, Apostolos Bossios, Nikolaos Lazarinis, David Aronsson, Arne Egesten, Abul Kashem Mohammad Munir, Lars Ahlbeck, Christer Janson, Sabina Škrgat, Natalija Edelbaher, Joerg Leuppi, Fabienne Jaun, Jochen Rüdiger, Nikolay Pavlov, Pietro Gianella, Reta Fischer, Florian Charbonnier, Rekha Chaudhuri, Steven James Smith, Simon Doe, Michelle Fawdon, Matthew Masoli, Liam Heaney, Hans Michael Haitchi, Ramesh Kurukulaaratchy, Olivia Fulton, Betty Frankemölle, Toni Gibson, Karen Needham, Peter Howarth, Ratko Djukanovic, Elisabeth Bel, Michael Hyland
          ERJ Open Research Apr 2022, 8 (2) 00065-2022; DOI: 10.1183/23120541.00065-2022

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          The effect of the COVID-19 pandemic on severe asthma care in Europe: will care change for good?
          Katrien Eger, Dora Paroczai, Alison Bacon, Florence Schleich, Svetlana Sergejeva, Arnaud Bourdin, Isabelle Vachier, Eleftherios Zervas, Konstantinos Katsoulis, Dimosthenis Papapetrou, Konstantinos Kostikas, Zsuzsanna Csoma, Enrico Heffler, Giorgio Walter Canonica, Ineta Grisle, Kristina Bieksiene, Jolita Palacionyte, Anneke ten Brinke, Simone Hashimoto, Frank W.J.M. Smeenk, Gert-Jan Braunstahl, Simone van der Sar, Florin Mihălţan, Natalia Nenasheva, Marina Peredelskaya, Biljana Zvezdin, Ivan Čekerevac, Sanja Hromiš, Vojislav Ćupurdija, Zorica Lazic, Branislava Milenkovic, Sanja Dimic-Janjic, Valentyna Yasinska, Barbro Dahlén, Apostolos Bossios, Nikolaos Lazarinis, David Aronsson, Arne Egesten, Abul Kashem Mohammad Munir, Lars Ahlbeck, Christer Janson, Sabina Škrgat, Natalija Edelbaher, Joerg Leuppi, Fabienne Jaun, Jochen Rüdiger, Nikolay Pavlov, Pietro Gianella, Reta Fischer, Florian Charbonnier, Rekha Chaudhuri, Steven James Smith, Simon Doe, Michelle Fawdon, Matthew Masoli, Liam Heaney, Hans Michael Haitchi, Ramesh Kurukulaaratchy, Olivia Fulton, Betty Frankemölle, Toni Gibson, Karen Needham, Peter Howarth, Ratko Djukanovic, Elisabeth Bel, Michael Hyland
          ERJ Open Research Apr 2022, 8 (2) 00065-2022; DOI: 10.1183/23120541.00065-2022
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