International consensus on lung function testing during the COVID-19 pandemic and beyond

doi:10.1183/23120541.00602-2021

Review

. 2022 Mar 7;8(1):00602-2021.

doi: 10.1183/23120541.00602-2021. eCollection 2022 Jan.

International consensus on lung function testing during the COVID-19 pandemic and beyond

Aisling McGowan^{1

2}, Pierantonio Laveneziana^{3

4}, Sam Bayat^{5

6}, Nicole Beydon⁷, P W Boros⁸, Felip Burgos⁹, Matjaž Fležar^{10

11}, Monika Franczuk⁸, Maria-Alejandra Galarza^{3

4}, Adrian H Kendrick^{12

13

14}, Enrico Lombardi¹⁵, Jellien Makonga-Braaksma¹⁶, Meredith C McCormack¹⁷, Laurent Plantier^{18

19}, Sanja Stanojevic²⁰, Irene Steenbruggen²¹, Bruce Thompson²², Allan L Coates²³, Jack Wanger²⁴, Donald W Cockcroft²⁵, Bruce Culver²⁶, Karl Sylvester^{27

28}, Frans De Jongh²⁹

Affiliations

¹ Dept of Respiratory and Sleep Diagnostics, Connolly Hospital, Dublin, Ireland.
² School of Physics, Clinical and Optometric Sciences, Technological University Dublin, Dublin, Ireland.
³ Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale et Clinique, Paris, France.
⁴ AP-HP, Groupe Hospitalier Universitaire APHP-Sorbonne Université, Service des Explorations Fonctionnelles de la Respiration, de l'Exercice et de la Dyspnée (Département R3S), Paris, France.
⁵ Centre Hospitalier Universitaire de Grenoble Alpes, Unité d'Explorations Fonctionnelles, Cardiorespiratoires, Grenoble, France.
⁶ Université Grenoble Alpes - INSERM UA7, Rayonnement Synchrotron pour la Recherche Biomédicale (STROBE), Grenoble, France.
⁷ Unité Fonctionnelle de Physiologie-Explorations Fonctionnelles Respiratoires, AP-HP Sorbonne Université, Hôpital Armand-Trousseau, Paris, France.
⁸ Lung Pathophysiology Dept, National Tuberculosis and Lung Diseases Research Institute, Warsaw, Poland.
⁹ Department of Pulmonary Medicine, Hospital Clínic, Institut d'Investigacions Biomèdiques August Pi I Sunyer, Universitat de Barcelona, CIBERES, Barcelona, Spain.
¹⁰ University Clinic of Respiratory and Allergic Diseases, Golnik, Slovenia.
¹¹ Medical Faculty, University of Ljubljana, Ljubljana, Slovenia.
¹² Dept of Respiratory Medicine, University Hospitals Bristol & Weston NHS Trust, Bristol, UK.
¹³ University of West of England, Bristol, UK.
¹⁴ School of Physiology, Pharmacology and Neurophysiology, University of Bristol, Bristol, UK.
¹⁵ Pediatric Pulmonary Unit, Anna Meyer Pediatric University Hospital, Florence, Italy.
¹⁶ Lung Function Dept, Meander Medisch Centrum, Amersfoort, The Netherlands.
¹⁷ Pulmonary Function Laboratory, Pulmonary and Critical Care Medicine, Johns Hopkins University, Baltimore, MD, USA.
¹⁸ Pulmonology and Lung Function Testing, CHRU de Tours, Tours, France.
¹⁹ University of Tours, CEPR/Inserm UMR1100, Tours, France.
²⁰ Dept of Community Health and Epidemiology, Dalhousie University, New Brunswick, NS, Canada.
²¹ Pulmonary Function Dept, Isala Hospital, Zwolle, The Netherlands.
²² Faculty of Health, Arts and Design, Swinburne University of Technology, Victoria, Australia.
²³ Division of Respiratory Medicine, Dept of Pediatrics, Physiology and Environmental Medicine, Research Institute, Hospital for Sick Children, University of Toronto, Toronto, ON, Canada.
²⁴ Pulmonary Function Testing and Clinical Trial Consultant, Rochester, MN, USA.
²⁵ Division of Respirology, Critical Care and Sleep Medicine, Dept of Medicine, University of Saskatchewan, Saskatoon, SK, Canada.
²⁶ Pulmonary, Critical Care and Sleep Medicine, University of Washington, Seattle, WA, USA.
²⁷ Cambridge Respiratory Physiology, Cambridge University Hospital, Cambridge, UK.
²⁸ Royal Papworth Hospital, Cambridge, UK.
²⁹ Lung Function Lab, Medisch Spectrum Twente, Enschede, The Netherlands.

PMID: 35261912
PMCID: PMC8607240
DOI: 10.1183/23120541.00602-2021

Review

International consensus on lung function testing during the COVID-19 pandemic and beyond

Aisling McGowan et al. ERJ Open Res. 2022.

. 2022 Mar 7;8(1):00602-2021.

doi: 10.1183/23120541.00602-2021. eCollection 2022 Jan.

Authors

Affiliations

¹ Dept of Respiratory and Sleep Diagnostics, Connolly Hospital, Dublin, Ireland.
² School of Physics, Clinical and Optometric Sciences, Technological University Dublin, Dublin, Ireland.
³ Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale et Clinique, Paris, France.
⁴ AP-HP, Groupe Hospitalier Universitaire APHP-Sorbonne Université, Service des Explorations Fonctionnelles de la Respiration, de l'Exercice et de la Dyspnée (Département R3S), Paris, France.
⁵ Centre Hospitalier Universitaire de Grenoble Alpes, Unité d'Explorations Fonctionnelles, Cardiorespiratoires, Grenoble, France.
⁶ Université Grenoble Alpes - INSERM UA7, Rayonnement Synchrotron pour la Recherche Biomédicale (STROBE), Grenoble, France.
⁷ Unité Fonctionnelle de Physiologie-Explorations Fonctionnelles Respiratoires, AP-HP Sorbonne Université, Hôpital Armand-Trousseau, Paris, France.
⁸ Lung Pathophysiology Dept, National Tuberculosis and Lung Diseases Research Institute, Warsaw, Poland.
⁹ Department of Pulmonary Medicine, Hospital Clínic, Institut d'Investigacions Biomèdiques August Pi I Sunyer, Universitat de Barcelona, CIBERES, Barcelona, Spain.
¹⁰ University Clinic of Respiratory and Allergic Diseases, Golnik, Slovenia.
¹¹ Medical Faculty, University of Ljubljana, Ljubljana, Slovenia.
¹² Dept of Respiratory Medicine, University Hospitals Bristol & Weston NHS Trust, Bristol, UK.
¹³ University of West of England, Bristol, UK.
¹⁴ School of Physiology, Pharmacology and Neurophysiology, University of Bristol, Bristol, UK.
¹⁵ Pediatric Pulmonary Unit, Anna Meyer Pediatric University Hospital, Florence, Italy.
¹⁶ Lung Function Dept, Meander Medisch Centrum, Amersfoort, The Netherlands.
¹⁷ Pulmonary Function Laboratory, Pulmonary and Critical Care Medicine, Johns Hopkins University, Baltimore, MD, USA.
¹⁸ Pulmonology and Lung Function Testing, CHRU de Tours, Tours, France.
¹⁹ University of Tours, CEPR/Inserm UMR1100, Tours, France.
²⁰ Dept of Community Health and Epidemiology, Dalhousie University, New Brunswick, NS, Canada.
²¹ Pulmonary Function Dept, Isala Hospital, Zwolle, The Netherlands.
²² Faculty of Health, Arts and Design, Swinburne University of Technology, Victoria, Australia.
²³ Division of Respiratory Medicine, Dept of Pediatrics, Physiology and Environmental Medicine, Research Institute, Hospital for Sick Children, University of Toronto, Toronto, ON, Canada.
²⁴ Pulmonary Function Testing and Clinical Trial Consultant, Rochester, MN, USA.
²⁵ Division of Respirology, Critical Care and Sleep Medicine, Dept of Medicine, University of Saskatchewan, Saskatoon, SK, Canada.
²⁶ Pulmonary, Critical Care and Sleep Medicine, University of Washington, Seattle, WA, USA.
²⁷ Cambridge Respiratory Physiology, Cambridge University Hospital, Cambridge, UK.
²⁸ Royal Papworth Hospital, Cambridge, UK.
²⁹ Lung Function Lab, Medisch Spectrum Twente, Enschede, The Netherlands.

PMID: 35261912
PMCID: PMC8607240
DOI: 10.1183/23120541.00602-2021

Abstract

Coronavirus disease 2019 (COVID-19) has negatively affected the delivery of respiratory diagnostic services across the world due to the potential risk of disease transmission during lung function testing. Community prevalence, reoccurrence of COVID-19 surges and the emergence of different variants of SARS-CoV-2 have impeded attempts to restore services. Finding consensus on how to deliver safe lung function services for both patients attending and for staff performing the tests are of paramount importance. This international statement presents the consensus opinion of 23 experts in the field of lung function and respiratory physiology balanced with evidence from the reviewed literature. It describes a robust roadmap for restoration and continuity of lung function testing services during the COVID-19 pandemic and beyond. Important strategies presented in this consensus statement relate to the patient journey when attending for lung function tests. We discuss appointment preparation, operational and environmental issues, testing room requirements including mitigation strategies for transmission risk, requirement for improved ventilation, maintaining physical distance and use of personal protection equipment. We also provide consensus opinion on precautions relating to specific tests, filters, management of special patient groups and alternative options to testing in hospitals. The pandemic has highlighted how vulnerable lung function services are and forces us to re-think how long-term mitigation strategies can protect our services during this and any possible future pandemic. This statement aspires to address the safety concerns that exist and provide strategies to make lung function tests and the testing environment safer when tests are required.

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Conflict of interest statement

Conflict of interest: A. McGowan has nothing to disclose. Conflict of interest: P. Laveneziana reports personal fees from Novartis France, Chiesi France and Boehringer France, outside the submitted work. Conflict of interest: S. Bayat has nothing to disclose. Conflict of interest: N. Beydon has nothing to disclose. Conflict of interest: P.W. Boros has nothing to disclose. Conflict of interest: F. Burgos reports participation on a scientific advisory board for Medical Graphics Coorporation Diagnostics. Conflict of interest: M. Fležar has nothing to disclose. Conflict of interest: M. Franczuk reports personal fees from AstraZeneca, Boehringer Ingelheim and Chiesi, outside the submitted work. Conflict of interest: M-A. Galarza has nothing to disclose. Conflict of interest: A.H. Kendrick has nothing to disclose. Conflict of interest: E. Lombardi reports nonfinancial support from AbbVie, personal fees from Angelini and Boehringer, personal fees and nonfinancial support from Chiesi, personal fees from GSK, nonfinancial support from Lusofarmaco, personal fees and nonfinancial support from Novartis, personal fees from Omron, grants and nonfinancial support from Restech, grants and personal fees from Sanofi, personal fees and nonfinancial support from Vertex, and personal fees from Vifor, outside the submitted work. Conflict of interest: J. Makonga-Braaksma has nothing to disclose. Conflict of interest: M.C. McCormack reports royalties from UpToDate, and personal fees from Vera Med, GlaxoSmithKline and Celgene, outside the submitted work. Conflict of interest: L. Plantier has nothing to disclose. Conflict of interest: S. Stanojevic has nothing to disclose. Conflict of interest: I. Steenbruggen has nothing to disclose. Conflict of interest: B. Thompson has nothing to disclose. Conflict of interest: A.L. Coates has nothing to disclose. Conflict of interest: J. Wanger has nothing to disclose. Conflict of interest: D.W. Cockcroft reports participation on a medical advisory board for Pharmaxis. Conflict of interest: B. Culver has nothing to disclose. Conflict of interest: K. Sylvester has nothing to disclose. Conflict of interest: F. de Jongh has nothing to disclose.

Figures

**FIGURE 1**
The consensus statement process and timeline. ERS: European Respiratory Society.

**FIGURE 2**
Workflow for spirometry during COVID-19 era. PPE: personal protective equipment; MDI: metered-dose inhaler.

**FIGURE 3**
a) An extraction hood positioned immediately over the dosimeter/nebuliser. b) Large protective screen on casters, separating patient from staff, providing some droplet protection if the patient coughs.

**FIGURE 4**
Lung function testing (LFT) pathway with precautions during coronavirus disease 2019 (COVID-19) pandemic. BCT: bronchial challenge test; CPET: cardiopulmonary exercise testing; S_pO₂: oxygen saturation measured by pulse oximetry; PPE: personal protective equipment; HEPA: high-efficiency particulate air; ACH: air changes per hour.

See this image and copyright information in PMC

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References

1. Helgeson SA, Lim KG, Lee AS, et al. . Aerosol generation during spirometry. Ann Am Thorac Soc 2020; 17: 1637–1639. doi:10.1513/AnnalsATS.202005-569RL - DOI - PMC - PubMed
1. Wilson, NM, Marks, GB, Eckhardt, A, et al. . The effect of respiratory activity, non-invasive respiratory support and facemasks on aerosol generation and its relevance to COVID-19. Anaesthesia 2021; 76: 1465–1474. 10.1111/anae.15475 - DOI - PMC - PubMed
1. McGowan A, Sylvester K,et al. . Lung function testing during COVID-19 pandemic and beyond. Recommendation from ERS Group 9.1 [Respiratory function technologists/scientists] ERS Group 9.1, May 2020. https://ers.app.box.com/s/zs1uu88wy51monr0ewd990itoz4tsn2h
1. Thompson B, Warner J. P eak Respiratory Bodies recommend suspension of lung function testing. The Thoracic Society of Australia & New Zealand and Australian and New Zealand Society of Respiratory Science Ltd, 2020. https://nwmphn.org.au/wp-content/uploads/2020/10/peak_respiratory_bodies.... Accessed June 2020
1. ARTP COVID-19 Group. Respiratory function testing during endemic COVID-19. www.artp.org.uk/write/MediaUploads/Standards/COVID19/Respiratory_Functio... Date last updated: 26 May 2020.

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[1] Helgeson SA, Lim KG, Lee AS, et al. . Aerosol generation during spirometry. Ann Am Thorac Soc 2020; 17: 1637–1639. doi:10.1513/AnnalsATS.202005-569RL - DOI - PMC - PubMed

[2] Helgeson SA, Lim KG, Lee AS, et al. . Aerosol generation during spirometry. Ann Am Thorac Soc 2020; 17: 1637–1639. doi:10.1513/AnnalsATS.202005-569RL - DOI - PMC - PubMed

[3] Wilson, NM, Marks, GB, Eckhardt, A, et al. . The effect of respiratory activity, non-invasive respiratory support and facemasks on aerosol generation and its relevance to COVID-19. Anaesthesia 2021; 76: 1465–1474. 10.1111/anae.15475 - DOI - PMC - PubMed

[4] Wilson, NM, Marks, GB, Eckhardt, A, et al. . The effect of respiratory activity, non-invasive respiratory support and facemasks on aerosol generation and its relevance to COVID-19. Anaesthesia 2021; 76: 1465–1474. 10.1111/anae.15475 - DOI - PMC - PubMed

[5] McGowan A, Sylvester K,et al. . Lung function testing during COVID-19 pandemic and beyond. Recommendation from ERS Group 9.1 [Respiratory function technologists/scientists] ERS Group 9.1, May 2020. https://ers.app.box.com/s/zs1uu88wy51monr0ewd990itoz4tsn2h

[6] McGowan A, Sylvester K,et al. . Lung function testing during COVID-19 pandemic and beyond. Recommendation from ERS Group 9.1 [Respiratory function technologists/scientists] ERS Group 9.1, May 2020. https://ers.app.box.com/s/zs1uu88wy51monr0ewd990itoz4tsn2h

[7] Thompson B, Warner J. P eak Respiratory Bodies recommend suspension of lung function testing. The Thoracic Society of Australia & New Zealand and Australian and New Zealand Society of Respiratory Science Ltd, 2020. https://nwmphn.org.au/wp-content/uploads/2020/10/peak_respiratory_bodies.... Accessed June 2020

[8] Thompson B, Warner J. P eak Respiratory Bodies recommend suspension of lung function testing. The Thoracic Society of Australia & New Zealand and Australian and New Zealand Society of Respiratory Science Ltd, 2020. https://nwmphn.org.au/wp-content/uploads/2020/10/peak_respiratory_bodies.... Accessed June 2020

[9] ARTP COVID-19 Group. Respiratory function testing during endemic COVID-19. www.artp.org.uk/write/MediaUploads/Standards/COVID19/Respiratory_Functio... Date last updated: 26 May 2020.

[10] ARTP COVID-19 Group. Respiratory function testing during endemic COVID-19. www.artp.org.uk/write/MediaUploads/Standards/COVID19/Respiratory_Functio... Date last updated: 26 May 2020.

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International consensus on lung function testing during the COVID-19 pandemic and beyond

Affiliations

International consensus on lung function testing during the COVID-19 pandemic and beyond

Authors

Affiliations

Abstract

Conflict of interest statement

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