Semin Respir Crit Care Med 2022; 43(02): 295-303
DOI: 10.1055/s-0041-1740582
Review Article

New Insights into the Prevention of Hospital-Acquired Pneumonia/Ventilator-Associated Pneumonia Caused by Viruses

Michael Klompas
1   Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Healthcare Institute, Boston, Massachusetts
2   Department of Medicine, Brigham and Women's Hospital, Boston, Massachusetts
› Author Affiliations

Abstract

A fifth or more of hospital-acquired pneumonias may be attributable to respiratory viruses. The SARS-CoV-2 pandemic has clearly demonstrated the potential morbidity and mortality of respiratory viruses and the constant threat of nosocomial transmission and hospital-based clusters. Data from before the pandemic suggest the same can be true of influenza, respiratory syncytial virus, and other respiratory viruses. The pandemic has also helped clarify the primary mechanisms and risk factors for viral transmission. Respiratory viruses are primarily transmitted by respiratory aerosols that are routinely emitted when people exhale, talk, and cough. Labored breathing and coughing increase aerosol generation to a much greater extent than intubation, extubation, positive pressure ventilation, and other so-called aerosol-generating procedures. Transmission risk is proportional to the amount of viral exposure. Most transmissions take place over short distances because respiratory emissions are densest immediately adjacent to the source but then rapidly dilute and diffuse with distance leading to less viral exposure. The primary risk factors for transmission then are high viral loads, proximity, sustained exposure, and poor ventilation as these all increase net viral exposure. Poor ventilation increases the risk of long-distance transmission by allowing aerosol-borne viruses to accumulate over time leading to higher levels of exposure throughout an enclosed space. Surgical and procedural masks reduce viral exposure but do not eradicate it and thus lower but do not eliminate transmission risk. Most hospital-based clusters have been attributed to delayed diagnoses, transmission between roommates, and staff-to-patient infections. Strategies to prevent nosocomial respiratory viral infections include testing all patients upon admission, preventing healthcare providers from working while sick, assuring adequate ventilation, universal masking, and vaccinating both patients and healthcare workers.



Publication History

Article published online:
18 January 2022

© 2022. Thieme. All rights reserved.

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  • References

  • 1 Magill SS, O'Leary E, Janelle SJ. et al; Emerging Infections Program Hospital Prevalence Survey Team. Changes in prevalence of health care-associated infections in U.S. hospitals. N Engl J Med 2018; 379 (18) 1732-1744
  • 2 Walter J, Haller S, Quinten C. et al; ECDC PPS Study Group. Healthcare-associated pneumonia in acute care hospitals in European Union/European Economic Area countries: an analysis of data from a point prevalence survey, 2011 to 2012. Euro Surveill 2018; 23 (32) 23
  • 3 Corrado RE, Lee D, Lucero DE, Varma JK, Vora NM. Burden of adult community-acquired, health-care-associated, hospital-acquired, and ventilator-associated pneumonia: New York City, 2010 to 2014. Chest 2017; 152 (05) 930-942
  • 4 Ji W, McKenna C, Ochoa A. et al; CDC Prevention Epicenters Program. Development and assessment of objective surveillance definitions for nonventilator hospital-acquired pneumonia. JAMA Netw Open 2019; 2 (10) e1913674
  • 5 Melsen WG, Rovers MM, Groenwold RH. et al. Attributable mortality of ventilator-associated pneumonia: a meta-analysis of individual patient data from randomised prevention studies. Lancet Infect Dis 2013; 13 (08) 665-671
  • 6 Steen J, Vansteelandt S, De Bus L. et al. Attributable mortality of ventilator-associated pneumonia. Replicating findings, revisiting methods. Ann Am Thorac Soc 2021; 18 (05) 830-837
  • 7 Klompas M, Branson R, Eichenwald EC. et al; Society for Healthcare Epidemiology of America (SHEA). Strategies to prevent ventilator-associated pneumonia in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol 2014; 35 (08) 915-936
  • 8 Torres A, Niederman MS, Chastre J. et al. International ERS/ESICM/ESCMID/ALAT guidelines for the management of hospital-acquired pneumonia and ventilator-associated pneumonia: Guidelines for the management of hospital-acquired pneumonia (HAP)/ventilator-associated pneumonia (VAP) of the European Respiratory Society (ERS), European Society of Intensive Care Medicine (ESICM), European Society of Clinical Microbiology and Infectious Diseases (ESCMID) and Asociación Latinoamericana del Tórax (ALAT). Eur Respir J 2017; 50 (03) 50
  • 9 Klompas M. Prevention of intensive care unit-acquired pneumonia. Semin Respir Crit Care Med 2019; 40 (04) 548-557
  • 10 Lyons PG, Kollef MH. Prevention of hospital-acquired pneumonia. Curr Opin Crit Care 2018; 24 (05) 370-378
  • 11 Jaillette E, Girault C, Brunin G. et al; BestCuff Study Group and the BoRéal Network. Impact of tapered-cuff tracheal tube on microaspiration of gastric contents in intubated critically ill patients: a multicenter cluster-randomized cross-over controlled trial. Intensive Care Med 2017; 43 (11) 1562-1571
  • 12 Saito M, Maruyama K, Mihara T, Hoshijima H, Hirabayashi G, Andoh T. Comparison of polyurethane tracheal tube cuffs and conventional polyvinyl chloride tube cuff for prevention of ventilator-associated pneumonia: a systematic review with meta-analysis. Medicine (Baltimore) 2021; 100 (09) e24906
  • 13 Dat VQ, Yen LM, Loan HT. et al. Effectiveness of continuous endotracheal cuff pressure control for the prevention of ventilator associated respiratory infections: an open-label randomised, controlled trial. Clin Infect Dis 2021; ciab724 (epub ahead of print) DOI: 10.1093/cid/ciab724.
  • 14 Marjanovic N, Boisson M, Asehnoune K. et al; AGATE Study Group. Continuous pneumatic regulation of tracheal cuff pressure to decrease ventilator-associated pneumonia in trauma patients who were mechanically ventilated: the AGATE multicenter randomized controlled study. Chest 2021; 160 (02) 499-508
  • 15 Pozuelo-Carrascosa DP, Torres-Costoso A, Alvarez-Bueno C, Cavero-Redondo I, López Muñoz P, Martínez-Vizcaíno V. Multimodality respiratory physiotherapy reduces mortality but may not prevent ventilator-associated pneumonia or reduce length of stay in the intensive care unit: a systematic review. J Physiother 2018; 64 (04) 222-228
  • 16 Caroff DA, Li L, Muscedere J, Klompas M. Subglottic secretion drainage and objective outcomes: a systematic review and meta-analysis. Crit Care Med 2016; 44 (04) 830-840
  • 17 Björling G, Johansson D, Bergström L. et al. Tolerability and performance of BIP endotracheal tubes with noble metal alloy coating – a randomized clinical evaluation study. BMC Anesthesiol 2015; 15: 174
  • 18 Klompas M, Berra L, Branson R. Beware the siren's song of novel endotracheal tube designs. Intensive Care Med 2017; 43 (11) 1708-1711
  • 19 Johnstone J, Meade M, Lauzier F. et al; Prevention of Severe Pneumonia and Endotracheal Colonization Trial (PROSPECT) Investigators and the Canadian Critical Care Trials Group. Effect of probiotics on incident ventilator-associated pneumonia in critically ill patients: a randomized clinical trial. JAMA 2021; 326 (11) 1024-1033
  • 20 Dale CM, Rose L, Carbone S. et al. Effect of oral chlorhexidine de-adoption and implementation of an oral care bundle on mortality for mechanically ventilated patients in the intensive care unit (CHORAL): a multi-center stepped wedge cluster-randomized controlled trial. Intensive Care Med 2021; 47 (11) 1295-1302
  • 21 Shorr AF, Fisher K, Micek ST, Kollef MH. The burden of viruses in pneumonia associated with acute respiratory failure: an underappreciated issue. Chest 2018; 154 (01) 84-90
  • 22 Choi SH, Hong SB, Ko GB. et al. Viral infection in patients with severe pneumonia requiring intensive care unit admission. Am J Respir Crit Care Med 2012; 186 (04) 325-332
  • 23 Micek ST, Chew B, Hampton N, Kollef MH. A case-control study assessing the impact of nonventilated hospital-acquired pneumonia on patient outcomes. Chest 2016; 150 (05) 1008-1014
  • 24 Hong HL, Hong SB, Ko GB. et al. Viral infection is not uncommon in adult patients with severe hospital-acquired pneumonia. PLoS One 2014; 9 (04) e95865
  • 25 Chow EJ, Mermel LA. Hospital-acquired respiratory viral infections: incidence, morbidity, and mortality in pediatric and adult patients. Open Forum Infect Dis 2017; 4 (01) ofx006
  • 26 Honda H, Iwahashi J, Kashiwagi T. et al. Outbreak of human metapneumovirus infection in elderly inpatients in Japan. J Am Geriatr Soc 2006; 54 (01) 177-180
  • 27 Kim T, Jin CE, Sung H. et al. Molecular epidemiology and environmental contamination during an outbreak of parainfluenza virus 3 in a haematology ward. J Hosp Infect 2017; 97 (04) 403-413
  • 28 Javaid W, Ehni J, Gonzalez-Reiche AS. et al. Real-time investigation of a large nosocomial influenza A outbreak informed by genomic epidemiology. Clin Infect Dis 2021; 73 (11) e4375-e4383
  • 29 Wilson KE, Wood SM, Schaecher KE. et al. Nosocomial outbreak of influenza A H3N2 in an inpatient oncology unit related to health care workers presenting to work while ill. Am J Infect Control 2019; 47 (06) 683-687
  • 30 Hababou Y, Taleb A, Recoing A. et al. Molecular investigation of a RSV outbreak in a geriatric hospital. BMC Geriatr 2021; 21 (01) 120
  • 31 van Someren Gréve F, Juffermans NP, Bos LDJ. et al. Respiratory viruses in invasively ventilated critically ill patients - a prospective multicenter observational study. Crit Care Med 2018; 46 (01) 29-36
  • 32 Kwong JC, Schwartz KL, Campitelli MA. et al. Acute myocardial infarction after laboratory-confirmed influenza infection. N Engl J Med 2018; 378 (04) 345-353
  • 33 Chow EJ, Rolfes MA, O'Halloran A. et al. Acute cardiovascular events associated with influenza in hospitalized adults: a cross-sectional study. Ann Intern Med 2020; 173 (08) 605-613
  • 34 Blackburn R, Zhao H, Pebody R, Hayward A, Warren-Gash C. Laboratory-confirmed respiratory infections as predictors of hospital admission for myocardial infarction and stroke: time-series analysis of English data for 2004-2015. Clin Infect Dis 2018; 67 (01) 8-17
  • 35 Legoff J, Zucman N, Lemiale V. et al. Clinical significance of upper airway virus detection in critically ill hematology patients. Am J Respir Crit Care Med 2019; 199 (04) 518-528
  • 36 Piroth L, Cottenet J, Mariet AS. et al. Comparison of the characteristics, morbidity, and mortality of COVID-19 and seasonal influenza: a nationwide, population-based retrospective cohort study. Lancet Respir Med 2021; 9 (03) 251-259
  • 37 Ludwig M, Jacob J, Basedow F, Andersohn F, Walker J. Clinical outcomes and characteristics of patients hospitalized for influenza or COVID-19 in Germany. Int J Infect Dis 2021; 103: 316-322
  • 38 Cobb NL, Sathe NA, Duan KI. et al. Comparison of clinical features and outcomes in critically ill patients hospitalized with COVID-19 versus influenza. Ann Am Thorac Soc 2021; 18 (04) 632-640
  • 39 Read JM, Green CA, Harrison EM. et al; ISARIC4C Investigators. Hospital-acquired SARS-CoV-2 infection in the UK's first COVID-19 pandemic wave. Lancet 2021; 398 (10305): 1037-1038
  • 40 Chow K, Aslam A, McClure T. et al. Risk of healthcare-associated transmission of SARS-CoV-2 in hospitalized cancer patients. Clin Infect Dis 2021; DOI: 10.1093/cid/ciab670.
  • 41 Meredith LW, Hamilton WL, Warne B. et al. Rapid implementation of SARS-CoV-2 sequencing to investigate cases of health-care associated COVID-19: a prospective genomic surveillance study. Lancet Infect Dis 2020; 20 (11) 1263-1271
  • 42 Lumley SF, Constantinides B, Sanderson N. et al; OUH Microbiology Laboratory, OUH Infection Prevention and Control team. Epidemiological data and genome sequencing reveals that nosocomial transmission of SARS-CoV-2 is underestimated and mostly mediated by a small number of highly infectious individuals. J Infect 2021; 83 (04) 473-482
  • 43 Blackburn RM, Frampton D, Smith CM. et al; ICONIC Group. Nosocomial transmission of influenza: a retrospective cross-sectional study using next generation sequencing at a hospital in England (2012-2014). Influenza Other Respir Viruses 2019; 13 (06) 556-563
  • 44 Coleman BL, Ng W, Mahesh V. et al. Active surveillance for influenza reduces but does not eliminate hospital exposure to patients with influenza. Infect Control Hosp Epidemiol 2017; 38 (04) 387-392
  • 45 Ambrosch A, Rockmann F. Effect of two-step hygiene management on the prevention of nosocomial influenza in a season with high influenza activity. J Hosp Infect 2016; 94 (02) 143-149
  • 46 Ellingford JM, George R, McDermott JH. et al. Genomic and healthcare dynamics of nosocomial SARS-CoV-2 transmission. eLife 2021; 10: 10
  • 47 Klompas M, Baker MA, Griesbach D. et al. Transmission of SARS-CoV-2 from asymptomatic and presymptomatic individuals in healthcare settings despite medical masks and eye protection. Clin Infect Dis 2021; 73 (09) 1693-1699
  • 48 Lucey M, Macori G, Mullane N. et al. Whole-genome sequencing to track severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission in nosocomial outbreaks. Clin Infect Dis 2021; 72 (11) e727-e735
  • 49 Cheng VC, Fung KS, Siu GK. et al. Nosocomial outbreak of coronavirus disease 2019 by possible airborne transmission leading to a superspreading event. Clin Infect Dis 2021; 73 (06) e1356-e1364
  • 50 Klompas M, Baker MA, Rhee C. et al. A SARS-CoV-2 cluster in an acute care hospital. Ann Intern Med 2021; 174 (06) 794-802
  • 51 Jung J, Lee J, Jo S. et al. Nosocomial outbreak of COVID-19 in a hematologic ward. Infect Chemother 2021; 53 (02) 332-341
  • 52 Cheng VC, Fung KS, Siu GK. et al. Nosocomial outbreak of COVID-19 by possible airborne transmission leading to a superspreading event. Clin Infect Dis 2021; 73 (06) e1356-e1364
  • 53 Shitrit P, Zuckerman NS, Mor O, Gottesman BS, Chowers M. Nosocomial outbreak caused by the SARS-CoV-2 delta variant in a highly vaccinated population, Israel, July 2021. Euro Surveill 2021; 26 (39) 26
  • 54 Abbas M, Robalo Nunes T, Cori A. et al. Explosive nosocomial outbreak of SARS-CoV-2 in a rehabilitation clinic: the limits of genomics for outbreak reconstruction. J Hosp Infect 2021; 117: 124-134
  • 55 Rhee C, Baker M, Vaidya V. et al; CDC Prevention Epicenters Program. Incidence of nosocomial COVID-19 in patients hospitalized at a large US Academic Medical Center. JAMA Netw Open 2020; 3 (09) e2020498
  • 56 Morawska L, Johnson GR, Ristovski ZD. et al. Size distribution and sites of origin of droplets expelled from the human respiratory tract during expiratory activities. J Aerosol Sci 2009; 40: 256-259
  • 57 Adenaiye OO, Lai J, de Mesquita PJB. et al; University of Maryland StopCOVID Research Group. Infectious SARS-CoV-2 in exhaled aerosols and efficacy of masks during early mild infection. Clin Infect Dis 2021; ciab797 (epub ahead of print) DOI: 10.1093/cid/ciab797.
  • 58 Wenzhao Chen, Nan Zhang, Jianjian Wei, Hui-Ling Yen, Yuguo Li. Short-range airborne route dominates exposure of respiratory infection during close contact. Building and Environment 176 2020; 106859 ISSN 0360-1323, https://doi.org/10.1016/j.buildenv.2020.106859 https://www.sciencedirect.com/science/article/pii/S0360132320302183
  • 59 Coleman KK, Tay DJW, Sen Tan K. et al. Viral load of SARS-CoV-2 in respiratory aerosols emitted by COVID-19 patients while breathing, talking, and singing. Clin Infect Dis 2021; ciab691 (epub ahead of print) DOI: 10.1093/cid/ciab691.
  • 60 Sajgalik P, Garzona-Navas A, Csécs I. et al. Characterization of aerosol generation during various intensities of exercise. Chest 2021; 160 (04) 1377-1387
  • 61 Asadi S, Wexler AS, Cappa CD, Barreda S, Bouvier NM, Ristenpart WD. Aerosol emission and superemission during human speech increase with voice loudness. Sci Rep 2019; 9 (01) 2348
  • 62 Sickbert-Bennett EE, Samet JM, Clapp PW. et al. Filtration efficiency of hospital face mask alternatives available for use during the COVID-19 pandemic. JAMA Intern Med 2020; 180 (12) 1607-1612
  • 63 Jones LD, Chan ER, Zabarsky TF. et al. Transmission of SARS-CoV-2 on a patient transport van. Clin Infect Dis 2021; ciab347 (epub ahead of print) DOI: 10.1093/cid/ciab347.
  • 64 Hetemäki I, Kääriäinen S, Alho P. et al. An outbreak caused by the SARS-CoV-2 Delta variant (B.1.617.2) in a secondary care hospital in Finland, May 2021. Euro Surveill 2021; 26 (30) 26
  • 65 Marks M, Millat-Martinez P, Ouchi D. et al. Transmission of COVID-19 in 282 clusters in Catalonia, Spain: a cohort study. Lancet Infect Dis 2021; 21 (05) 629-636
  • 66 Kawasuji H, Takegoshi Y, Kaneda M. et al. Transmissibility of COVID-19 depends on the viral load around onset in adult and symptomatic patients. PLoS One 2020; 15 (12) e0243597
  • 67 Cheng HY, Jian SW, Liu DP, Ng TC, Huang WT, Lin HH. Taiwan COVID-19 Outbreak Investigation Team. Contact tracing assessment of COVID-19 transmission dynamics in Taiwan and risk at different exposure periods before and after symptom onset. JAMA Intern Med 2020; 180 (09) 1156-1163
  • 68 Ang AX, Luhung I, Ahidjo BA. et al. Airborne SARS-CoV-2 surveillance in hospital environment using high-flow rate air samplers and its comparison to surface sampling. Indoor Air 2022; 32 (01) e12930
  • 69 Hu M, Lin H, Wang J. et al. Risk of coronavirus disease 2019 transmission in train passengers: an epidemiological and modeling study. Clin Infect Dis 2021; 72 (04) 604-610
  • 70 Miller SL, Nazaroff WW, Jimenez JL. et al. Transmission of SARS-CoV-2 by inhalation of respiratory aerosol in the Skagit Valley Chorale superspreading event. Indoor Air 2021; 31 (02) 314-323
  • 71 Li Y, Qian H, Hang J. et al. Probable airborne transmission of SARS-CoV-2 in a poorly ventilated restaurant. Build Environ 2021; 196: 107788
  • 72 Shah ASV, Gribben C, Bishop J. et al. Effect of vaccination on transmission of SARS-CoV-2. N Engl J Med 2021; 385 (18) 1718-1720
  • 73 Harris RJ, Hall JA, Zaidi A, Andrews NJ, Dunbar JK, Dabrera G. Effect of vaccination on household transmission of SARS-CoV-2 in England. N Engl J Med 2021; 385 (08) 759-760
  • 74 Chan VW, Ng HH, Rahman L. et al. Transmission of severe acute respiratory syndrome coronavirus 1 and severe acute respiratory syndrome coronavirus 2 during aerosol-generating procedures in critical care: a systematic review and meta-analysis of observational studies. Crit Care Med 2021; 49 (07) 1159-1168
  • 75 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 (11) 1465-1474
  • 76 Brown J, Gregson FKA, Shrimpton A. et al. A quantitative evaluation of aerosol generation during tracheal intubation and extubation. Anaesthesia 2021; 76 (02) 174-181
  • 77 Gaeckle NT, Lee J, Park Y, Kreykes G, Evans MD, Hogan Jr CJ. Aerosol generation from the respiratory tract with various modes of oxygen delivery. Am J Respir Crit Care Med 2020; 202 (08) 1115-1124
  • 78 O'Neil CA, Li J, Leavey A. et al; Centers for Disease Control and Prevention Epicenters Program. Characterization of aerosols generated during patient care activities. Clin Infect Dis 2017; 65 (08) 1335-1341
  • 79 Klompas M, Baker M, Rhee C. What is an aerosol-generating procedure?. JAMA Surg 2021; 156 (02) 113-114
  • 80 Baier C, Linderkamp C, Beilken A. et al. Influenza and respiratory syncytial virus screening for the detection of asymptomatically infected patients in hematology and oncology. GMS Hyg Infect Control 2018; 13: Doc08
  • 81 Clark TW, Beard KR, Brendish NJ. et al. Clinical impact of a routine, molecular, point-of-care, test-and-treat strategy for influenza in adults admitted to hospital (FluPOC): a multicentre, open-label, randomised controlled trial. Lancet Respir Med 2021; 9 (04) 419-429
  • 82 Nesher L, Tsaban G, Dreiher J. et al. The impact of incorporating early rapid influenza diagnosis on hospital occupancy and hospital acquired influenza. Infect Control Hosp Epidemiol 2019; 40 (08) 897-903
  • 83 Egbuonu K, Hyle EP, Hurtado RM. et al. Yield of severe acute respiratory syndrome coronavirus 2 lower respiratory tract testing after a negative nasopharyngeal test among hospitalized persons under investigation for coronavirus disease 2019. Open Forum Infect Dis 2021; 8 (06) b257
  • 84 Karan A, Klompas M, Tucker R, Baker M, Vaidya V, Rhee C. CDC Prevention Epicenters Program. The risk of SARS-CoV-2 transmission from patients with undiagnosed COVID-19 to roommates in a large academic medical center. Clin Infect Dis 2021; ciab564 (epub ahead of print) DOI: 10.1093/cid/ciab564.
  • 85 Trannel AM, Kobayashi T, Dains A. et al. Coronavirus disease 2019 (COVID-19) incidence after exposures in shared patient rooms in a tertiary-care center in Iowa, July 2020-May 2021. Infect Control Hosp Epidemiol 2021; (epub ahead of print) DOI: 10.1017/ice.2021.313.
  • 86 He X, Lau EHY, Wu P. et al. Temporal dynamics in viral shedding and transmissibility of COVID-19. Nat Med 2020; 26 (05) 672-675
  • 87 Ip DKM, Lau LLH, Chan KH. et al. The dynamic relationship between clinical symptomatology and viral shedding in naturally acquired seasonal and pandemic influenza virus infections. Clin Infect Dis 2016; 62 (04) 431-437
  • 88 Braun KM, Moreno GK, Buys A. et al. Viral sequencing to investigate sources of SARS-CoV-2 infection in US healthcare personnel. Clin Infect Dis 2021; 73 (06) e1329-e1336
  • 89 Shah ASV, Wood R, Gribben C. et al. Risk of hospital admission with coronavirus disease 2019 in healthcare workers and their households: nationwide linkage cohort study. BMJ 2020; 371: m3582
  • 90 Jinadatha C, Jones LD, Choi H. et al. Transmission of SARS-CoV-2 in inpatient and outpatient settings in a Veterans Affairs health care system. Open Forum Infect Dis 2021; 8 (08) b328
  • 91 Tartari E, Saris K, Kenters N. et al; International Society of Antimicrobial Chemotherapy Infection and Prevention Control (ISAC-IPC) Working Group. Not sick enough to worry? “Influenza-like” symptoms and work-related behavior among healthcare workers and other professionals: results of a global survey. PLoS One 2020; 15 (05) e0232168
  • 92 Ip DK, Lau LL, Leung NH. et al. Viral shedding and transmission potential of asymptomatic and paucisymptomatic influenza virus infections in the community. Clin Infect Dis 2017; 64 (06) 736-742
  • 93 Eyre DW, Taylor D, Purver M. et al. The impact of SARS-CoV-2 vaccination on Alpha and Delta variant transmission. Medrxiv 2021
  • 94 Vanhems P, Voirin N, Roche S. et al. Risk of influenza-like illness in an acute health care setting during community influenza epidemics in 2004-2005, 2005-2006, and 2006-2007: a prospective study. Arch Intern Med 2011; 171 (02) 151-157
  • 95 Menzies D, Fanning A, Yuan L, FitzGerald JM. Canadian Collaborative Group in Nosocomial Transmission of TB. Hospital ventilation and risk for tuberculous infection in Canadian health care workers. Ann Intern Med 2000; 133 (10) 779-789
  • 96 Klompas M, Ye S, Vaidya V. et al. Association between airborne infection isolation room utilization rates and healthcare worker COVID-19 infections in two academic hospitals. Clin Infect Dis 2021; ciab849 (epub ahead of print) DOI: 10.1093/cid/ciab849.
  • 97 Rhee C, Baker MA, Tucker R, Klompas M. Absence of long-range severe acute respiratory coronavirus virus 2 (SARS-CoV-2) transmission from a highly infectious patient with undiagnosed coronavirus disease 2019 (COVID-19) in a positive-pressure room. Infect Control Hosp Epidemiol 2021; 1–2 (epub ahead of print) DOI: 10.1017/ice.2021.327.
  • 98 Tsui BCH, Pan S. Are aerosol-generating procedures safer in an airborne infection isolation room or operating room?. Br J Anaesth 2020; 125 (06) e485-e487
  • 99 Conway-Morris A, Sharrocks K, Bousfield R. et al. The removal of airborne SARS-CoV-2 and other microbial bioaerosols by air filtration on COVID-19 surge units. Medrxiv 2021
  • 100 Garzona-Navas A, Sajgalik P, Csécs I. et al. Mitigation of aerosols generated during exercise testing with a portable high-efficiency particulate air filter with fume hood. Chest 2021; 160 (04) 1388-1396
  • 101 Lindsley WG, Derk RC, Coyle JP. et al. Efficacy of portable air cleaners and masking for reducing indoor exposure to simulated exhaled SARS-CoV-2 aerosols - United States, 2021. Morb Mortal Wkly Rep 2021; 70 (27) 972-976
  • 102 Buonanno M, Welch D, Shuryak I, Brenner DJ. Far-UVC light (222 nm) efficiently and safely inactivates airborne human coronaviruses. Sci Rep 2020; 10 (01) 10285
  • 103 Nardell EA, Nathavitharana RR. Airborne spread of SARS-CoV-2 and a potential role for air disinfection. JAMA 2020; 324 (02) 141-142
  • 104 Riley J, Huntley JM, Miller JA. et al. Mask effectiveness for preventing secondary cases of COVID-19, Johnson County, Iowa, USA. Emerg Infect Dis 2022; (epub ahead of print) DOI: 10.3201/eid2801.211591.
  • 105 Wang X, Ferro EG, Zhou G, Hashimoto D, Bhatt DL. Association between universal masking in a health care system and SARS-CoV-2 positivity among health care workers. JAMA 2020; 324 (07) 703-704
  • 106 Kociolek LK, Patel AB, Hultquist JF. et al. Viral whole-genome sequencing to assess impact of universal masking on SARS-CoV-2 transmission among pediatric healthcare workers. Infect Control Hosp Epidemiol 2021; (epub ahead of print) DOI: 10.1017/ice.2021.415.
  • 107 Arulsundaram V, Houston K, Vicencio E. et al. Universal masking to prevent nosocomial respiratory viral infections in malignant hematology inpatient units. Infect Control Hosp Epidemiol 2020; 41: S501-S502
  • 108 Ambrosch A, Klawonn FA. “Masks Save Lives” Campaign Effectively Prevents Nosocomial Influenza A/B. ASM Microbe. San Francisco, CA: ; June 21, 2019
  • 109 Klompas M, Rhee C, Baker M. Universal use of N95s in healthcare settings when community COVID-19 rates are high. Clin Infect Dis 2021; (epub ahead of print) DOI: 10.1093/cid/ciab539.
  • 110 Kim MC, Bae S, Kim JY. et al. Effectiveness of surgical, KF94, and N95 respirator masks in blocking SARS-CoV-2: a controlled comparison in 7 patients. Infect Dis (Lond) 2020; 52 (12) 908-912
  • 111 Elliott P, Haw D, Wang H. et al. Exponential growth, high prevalence of SARS-CoV-2, and vaccine effectiveness associated with the Delta variant. Science 2021; DOI: 10.1126/science.abl9551.
  • 112 Thompson MG, Burgess JL, Naleway AL. et al. Prevention and attenuation of COVID-19 with the BNT162b2 and mRNA-1273 vaccines. N Engl J Med 2021; 385 (04) 320-329
  • 113 Chia PY, Xiang Ong SW, Chiew CJ. et al. Virological and serological kinetics of SARS-CoV-2 Delta variant vaccine-breakthrough infections: a multi-center cohort study. Clin Microbiol Infect 2021; DOI: 10.1016/j.cmi.2021.11.010.
  • 114 Ke R, Martinez PP, Smith RL. et al. Longitudinal analysis of SARS-CoV-2 vaccine breakthrough infections reveal limited infectious virus shedding and restricted tissue distribution. Medrxiv 2021. Doi: 10.1101/2021.08.30.21262701
  • 115 Ahmed F, Lindley MC, Allred N, Weinbaum CM, Grohskopf L. Effect of influenza vaccination of healthcare personnel on morbidity and mortality among patients: systematic review and grading of evidence. Clin Infect Dis 2014; 58 (01) 50-57
  • 116 Riphagen-Dalhuisen J, Burgerhof JG, Frijstein G. et al. Hospital-based cluster randomised controlled trial to assess effects of a multi-faceted programme on influenza vaccine coverage among hospital healthcare workers and nosocomial influenza in the Netherlands, 2009 to 2011. Euro Surveill 2013; 18 (26) 20512
  • 117 Klompas M, Pearson M, Morris C. The case for mandating COVID-19 vaccines for health care workers. Ann Intern Med 2021; 174 (09) 1305-1307
  • 118 Lawton T, Butler M, Peters C. Airborne protection for staff is associated with reduced hospital-acquired COVID-19 in English NHS Trusts. J Hosp Infect 2021; DOI: 10.1016/j.jhin.2021.11.018.