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

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. International expert consensus statement describing the infection protection control strategies for restoration and continuity of lung function testing services during #COVID19 pandemic and beyond https://bit.ly/3kn47Gy

[1]  G. Evans,et al.  Aerosol generation during pulmonary function testing: Monitoring during different testing modalities , 2021, Canadian Journal of Respiratory, Critical Care, and Sleep Medicine.

[2]  A. Nagy,et al.  Real-life measurement of size-fractionated aerosol concentration in a plethysmography box during the COVID-19 pandemic and estimation of the associated viral load , 2021, Journal of Hospital Infection.

[3]  I. Ladeira,et al.  Effect of a viral filter on cardiopulmonary exercise testing , 2021, Pulmonology.

[4]  O. Pybus,et al.  Viral infection and transmission in a large, well-traced outbreak caused by the SARS-CoV-2 Delta variant , 2021, Nature communications.

[5]  Tham Kwok Wai,et al.  Viral Load of SARS-CoV-2 in Respiratory Aerosols Emitted by COVID-19 Patients while Breathing, Talking, and Singing , 2021, medRxiv.

[6]  Jaesung Jang,et al.  Recent advancements in the measurement of pathogenic airborne viruses , 2021, Journal of Hazardous Materials.

[7]  M. V. Van Kerkhove,et al.  Increased transmissibility and global spread of SARS-CoV-2 variants of concern as at June 2021 , 2021, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[8]  S. Stanojevic,et al.  How Local SARS-CoV-2 Prevalence Shapes Pulmonary Function Testing Laboratory Protocols and Practices During the COVID-19 Pandemic , 2021, Chest.

[9]  N. Maskell,et al.  Aerosol generating procedures: are they of relevance for transmission of SARS-CoV-2? , 2021, The Lancet Respiratory Medicine.

[10]  R. Schooley,et al.  Ten scientific reasons in support of airborne transmission of SARS-CoV-2 , 2021, The Lancet.

[11]  M. Suchard,et al.  Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil , 2021, Science.

[12]  F. Garden,et al.  The effect of respiratory activity, non‐invasive respiratory support and facemasks on aerosol generation and its relevance to COVID‐19 , 2021, Anaesthesia.

[13]  Graham W. Taylor,et al.  Assessing transmissibility of SARS-CoV-2 lineage B.1.1.7 in England , 2021, Nature.

[14]  J. Reid,et al.  Aerosol emission from the respiratory tract: an analysis of relative risks from oxygen delivery systems , 2021, medRxiv.

[15]  I. Balfour‐Lynn,et al.  Initiating home spirometry for children during the COVID-19 pandemic – A practical guide , 2021, Paediatric Respiratory Reviews.

[16]  J. Swan,et al.  P36 Cough provoked by lung function testing – should lung function testing be treated as an aerosol generating procedure post COVID-19? , 2021 .

[17]  Nicole M. Bouvier,et al.  Expiratory aerosol particle escape from surgical masks due to imperfect sealing , 2021, Scientific Reports.

[18]  M. M. van der Eerden,et al.  Duration and key determinants of infectious virus shedding in hospitalized patients with coronavirus disease-2019 (COVID-19) , 2021, Nature communications.

[19]  Carl A. B. Pearson,et al.  Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England , 2021, Science.

[20]  C. Rhee,et al.  What Is an Aerosol-Generating Procedure? , 2020, JAMA surgery.

[21]  A. Abramowicz,et al.  A quantitative evaluation of aerosol generation during tracheal intubation and extubation , 2020, Anaesthesia.

[22]  J. Pórszász,et al.  Airborne Particulate Concentrations During and After Pulmonary Function Testing , 2020, Chest.

[23]  Chenyu Sun,et al.  Face masks to prevent transmission of COVID-19: A systematic review and meta-analysis , 2020, American Journal of Infection Control.

[24]  M. Rosenfeld,et al.  Pediatric lung function testing during a pandemic: An international perspective , 2020, Paediatric Respiratory Reviews.

[25]  J. Reid,et al.  A quantitative evaluation of aerosol generation during tracheal intubation and extubation , 2020, Anaesthesia.

[26]  N. Papadopoulos,et al.  Face masks, respiratory patients and COVID-19 , 2020, European Respiratory Journal.

[27]  A. Olin,et al.  Small droplet emission in exhaled breath during different breathing manoeuvres: Implications for clinical lung function testing during COVID‐19 , 2020, Allergy.

[28]  Augustine S. Lee,et al.  Aerosol Generation during Spirometry , 2020, Annals of the American Thoracic Society.

[29]  T. Yeo,et al.  Viral dynamics and immune correlates of COVID-19 disease severity , 2020, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[30]  T. Greenhalgh,et al.  Two metres or one: what is the evidence for physical distancing in covid-19? , 2020, BMJ.

[31]  T. Troosters,et al.  COVID-19: interim guidance on rehabilitation in the hospital and post-hospital phase from a European Respiratory Society- and American Thoracic Society-coordinated international task force , 2020, European Respiratory Journal.

[32]  R. Vijayakumar,et al.  High-Efficiency Particulate Air Filters in the Era of COVID-19: Function and Efficacy , 2020, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[33]  S. Stanojevic,et al.  Restoring Pulmonary and Sleep Services as the COVID-19 Pandemic Lessens. From an Association of Pulmonary, Critical Care, and Sleep Division Directors and American Thoracic Society–coordinated Task Force , 2020, Annals of the American Thoracic Society.

[34]  C. Vancheri,et al.  Resumption of respiratory outpatient services in the COVID-19 era: Experience from Southern Italy , 2020, American Journal of Infection Control.

[35]  R. Dhand,et al.  Coughs and Sneezes: Their Role in Transmission of Respiratory Viral Infections, Including SARS-CoV-2 , 2020, American journal of respiratory and critical care medicine.

[36]  B. Prunet,et al.  Prehospital pulse oximetry: a red flag for early detection of silent hypoxemia in COVID-19 patients , 2020, Critical Care.

[37]  F. Costes,et al.  [Lung function testing under COVID-19: A position paper]. , 2020, Revue des maladies respiratoires.

[38]  A. Turchetta,et al.  Italian pediatric respiratory society recommendations on pediatric pulmonary function testing during COVID-19 pandemic , 2020, Italian Journal of Pediatrics.

[39]  Zachary Schiffman,et al.  Predicting infectious SARS-CoV-2 from diagnostic samples , 2020, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[40]  D. Patrick,et al.  High SARS-CoV-2 Attack Rate Following Exposure at a Choir Practice - Skagit County, Washington, March 2020. , 2020, MMWR. Morbidity and mortality weekly report.

[41]  John P. Thomas,et al.  Evaluating the national PPE guidance for NHS healthcare workers during the COVID-19 pandemic. , 2020, Clinical medicine.

[42]  B. Gemicioğlu,et al.  Turkish Thoracic Society Experts Consensus Report: Recommendations for Pulmonary Function Tests During and After COVID 19 Pandemic. , 2020, Turkish thoracic journal.

[43]  Sheng Zhang,et al.  Profile of RT-PCR for SARS-CoV-2: A Preliminary Study From 56 COVID-19 Patients , 2020, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[44]  A. Chughtai,et al.  Airborne or Droplet Precautions for Health Workers Treating Coronavirus Disease 2019? , 2020, The Journal of infectious diseases.

[45]  Yuguo Li,et al.  Indoor transmission of SARS-CoV-2 , 2020, medRxiv.

[46]  P. Vollmar,et al.  Virological assessment of hospitalized patients with COVID-2019 , 2020, Nature.

[47]  G. Joynt,et al.  Understanding COVID-19: what does viral RNA load really mean? , 2020, The Lancet Infectious Diseases.

[48]  G. Onder,et al.  Case-Fatality Rate and Characteristics of Patients Dying in Relation to COVID-19 in Italy. , 2020, JAMA.

[49]  Beijing China. Prevention,et al.  Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China , 2020 .

[50]  Dylan H. Morris,et al.  Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1 , 2020, The New England journal of medicine.

[51]  Hannah R. Meredith,et al.  The Incubation Period of Coronavirus Disease 2019 (COVID-19) From Publicly Reported Confirmed Cases: Estimation and Application , 2020, Annals of Internal Medicine.

[52]  Zunyou Wu,et al.  Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. , 2020, JAMA.

[53]  Kevin McCarthy,et al.  Standardization of Spirometry 2019 Update. An Official American Thoracic Society and European Respiratory Society Technical Statement , 2019, American journal of respiratory and critical care medicine.

[54]  A. Wexler,et al.  Aerosol emission and superemission during human speech increase with voice loudness , 2019, Scientific Reports.

[55]  A. Coates,et al.  ERS technical standard on bronchial challenge testing: pathophysiology and methodology of indirect airway challenge testing , 2018, European Respiratory Journal.

[56]  D. Cockcroft,et al.  Methacholine Challenge Testing: A Novel Method for Measuring PD20 , 2017, Chest.

[57]  E. Mirgorodskaya,et al.  The effect of exhalation flow on endogenous particle emission and phospholipid composition , 2017, Respiratory Physiology & Neurobiology.

[58]  V. Brusasco,et al.  Executive Summary: 2017 ERS/ATS standards for single-breath carbon monoxide uptake in the lung , 2017, European Respiratory Journal.

[59]  V. Brusasco,et al.  2017 ERS/ATS standards for single-breath carbon monoxide uptake in the lung , 2017, European Respiratory Journal.

[60]  G. Ruppel.  Aerosol Use in the Pulmonary Function Lab , 2015, Respiratory Care.

[61]  A. Coates,et al.  Developing alternative delivery systems for methacholine challenge tests. , 2014, Journal of aerosol medicine and pulmonary drug delivery.

[62]  Jonathan V. Szalajda,et al.  Dispersion and Exposure to a Cough-Generated Aerosol in a Simulated Medical Examination Room , 2012, Journal of occupational and environmental hygiene.

[63]  Kerrie Mengersen,et al.  Size distribution and sites of origin of droplets expelled from the human respiratory tract during expiratory activities , 2009 .

[64]  R. Wilson,et al.  An audit into the efficacy of single use bacterial/viral filters for the prevention of equipment contamination during lung function assessment. , 2006, Respiratory medicine.

[65]  R J Shaughnessy,et al.  What Is an Effective Portable Air Cleaning Device? A Review , 2006, Journal of occupational and environmental hygiene.

[66]  S. Anderson,et al.  The safety and efficacy of inhaled dry powder mannitol as a bronchial provocation test for airway hyperresponsiveness: a phase 3 comparison study with hypertonic (4.5%) saline , 2005, Respiratory research.

[67]  Y. Li,et al.  Role of air distribution in SARS transmission during the largest nosocomial outbreak in Hong Kong. , 2005, Indoor air.

[68]  A. Yassi,et al.  Research Gaps in Protecting Healthcare Workers From SARS and Other Respiratory Pathogens: An Interdisciplinary, Multi-Stakeholder, Evidence-Based Approach , 2005, Journal of occupational and environmental medicine.

[69]  L. Sehulster,et al.  Guidelines for environmental infection control in health-care facilities. Recommendations of CDC and the Healthcare Infection Control Practices Advisory Committee (HICPAC). , 2003, MMWR. Recommendations and reports : Morbidity and mortality weekly report. Recommendations and reports.

[70]  C C Coffey,et al.  Performance of N95 respirators: filtration efficiency for airborne microbial and inert particles. , 1998, American Industrial Hygiene Association journal.

[71]  Heating, ventilation and air-conditioning systems in the context of COVID-19 , 2020 .

[72]  Christopher W. Bach.  Effects of a Bacteriological Filter on VO2max Measured by a Computerized Metabolic System , 2012 .

[73]  Marco Perino,et al.  Natural Ventilation for Infection Control in Health-Care Settings , 2009 .

[74]  B. Crook,et al.  Evaluating the protection afforded by surgical masks against influenza bioaerosols Gross protection of surgical masks compared to filtering facepiece respirators , 2008 .

[75]  J. Clausen.  Lung volume equipment and infection control , 2002 .

[76]  A. Buist.  Standardization of spirometry. , 1987, The American review of respiratory disease.

[77]  Robert J. Jacobs,et al.  Infection control guidelines , 1986 .

[78]  B. Arsić,et al.  [Epidemiology of infectious diseases]. , 1979, Vojnosanitetski pregled.