Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community
Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenz...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 115; no. 5; pp. 1081 - 1086 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
30.01.2018
|
| Series | From the Cover |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-minute breath samples (coarse >5-μm and fine ≤5-μm fractions) on days 1–3 after symptom onset. We assessed viral RNA copy number for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy numbers were 3.8 × 10⁴/30-minutes fine-, 1.2 × 10⁴/30-minutes coarse-aerosol sample, and 8.2 × 10⁸ per NP swab. Fine- and coarse-aerosol viral RNA were positively associated with body mass index and number of coughs and negatively associated with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also positively associated with having influenza vaccination for both the current and prior season. NP swab viral RNA was positively associated with upper respiratory symptoms and negatively associated with age but was not significantly associated with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent. |
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| AbstractList | Lack of human data on influenza virus aerosol shedding fuels debate over the importance of airborne transmission. We provide overwhelming evidence that humans generate infectious aerosols and quantitative data to improve mathematical models of transmission and public health interventions. We show that sneezing is rare and not important for—and that coughing is not required for—influenza virus aerosolization. Our findings, that upper and lower airway infection are independent and that fine-particle exhaled aerosols reflect infection in the lung, opened a pathway for a deeper understanding of the human biology of influenza infection and transmission. Our observation of an association between repeated vaccination and increased viral aerosol generation demonstrated the power of our method, but needs confirmation.
Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-minute breath samples (coarse >5-µm and fine ≤5-µm fractions) on days 1–3 after symptom onset. We assessed viral RNA copy number for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy numbers were 3.8 × 10
4
/30-minutes fine-, 1.2 × 10
4
/30-minutes coarse-aerosol sample, and 8.2 × 10
8
per NP swab. Fine- and coarse-aerosol viral RNA were positively associated with body mass index and number of coughs and negatively associated with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also positively associated with having influenza vaccination for both the current and prior season. NP swab viral RNA was positively associated with upper respiratory symptoms and negatively associated with age but was not significantly associated with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent. Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-minute breath samples (coarse >5-μm and fine ≤5-μm fractions) on days 1-3 after symptom onset. We assessed viral RNA copy number for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy numbers were 3.8 x 104/30-minutes fine-, 1.2 x 104/30-minutes coarse-aerosol sample, and 8.2 x 108 per NP swab. Fine- and coarse-aerosol viral RNA were positively associated with body mass index and number of coughs and negatively associated with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also positively associated with having influenza vaccination for both the current and prior season. NP swab viral RNA was positively associated with upper respiratory symptoms and negatively associated with age but was not significantly associated with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent. Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-minute breath samples (coarse >5-µm and fine ≤5-µm fractions) on days 1-3 after symptom onset. We assessed viral RNA copy number for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy numbers were 3.8 × 104/30-minutes fine-, 1.2 × 104/30-minutes coarse-aerosol sample, and 8.2 × 108 per NP swab. Fine- and coarse-aerosol viral RNA were positively associated with body mass index and number of coughs and negatively associated with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also positively associated with having influenza vaccination for both the current and prior season. NP swab viral RNA was positively associated with upper respiratory symptoms and negatively associated with age but was not significantly associated with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent.Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-minute breath samples (coarse >5-µm and fine ≤5-µm fractions) on days 1-3 after symptom onset. We assessed viral RNA copy number for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy numbers were 3.8 × 104/30-minutes fine-, 1.2 × 104/30-minutes coarse-aerosol sample, and 8.2 × 108 per NP swab. Fine- and coarse-aerosol viral RNA were positively associated with body mass index and number of coughs and negatively associated with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also positively associated with having influenza vaccination for both the current and prior season. NP swab viral RNA was positively associated with upper respiratory symptoms and negatively associated with age but was not significantly associated with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent. Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-minute breath samples (coarse >5-μm and fine ≤5-μm fractions) on days 1–3 after symptom onset. We assessed viral RNA copy number for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy numbers were 3.8 × 10⁴/30-minutes fine-, 1.2 × 10⁴/30-minutes coarse-aerosol sample, and 8.2 × 10⁸ per NP swab. Fine- and coarse-aerosol viral RNA were positively associated with body mass index and number of coughs and negatively associated with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also positively associated with having influenza vaccination for both the current and prior season. NP swab viral RNA was positively associated with upper respiratory symptoms and negatively associated with age but was not significantly associated with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent. Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-minute breath samples (coarse >5-µm and fine ≤5-µm fractions) on days 1-3 after symptom onset. We assessed viral RNA copy number for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy numbers were 3.8 × 10 /30-minutes fine-, 1.2 × 10 /30-minutes coarse-aerosol sample, and 8.2 × 10 per NP swab. Fine- and coarse-aerosol viral RNA were positively associated with body mass index and number of coughs and negatively associated with increasing days since symptom onset in adjusted models. Fine-aerosol viral RNA was also positively associated with having influenza vaccination for both the current and prior season. NP swab viral RNA was positively associated with upper respiratory symptoms and negatively associated with age but was not significantly associated with fine- or coarse-aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent. |
| Author | Pantelic, Jovan Yan, Jing Milton, Donald K. Grantham, Michael de Mesquita, P. Jacob Bueno Ehrman, Sheryl Liu, Fengjie Albert, Barbara |
| Author_xml | – sequence: 1 givenname: Jing surname: Yan fullname: Yan, Jing organization: Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD 20742 – sequence: 2 givenname: Michael surname: Grantham fullname: Grantham, Michael organization: Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD 20742 – sequence: 3 givenname: Jovan surname: Pantelic fullname: Pantelic, Jovan organization: Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD 20742 – sequence: 4 givenname: P. Jacob Bueno surname: de Mesquita fullname: de Mesquita, P. Jacob Bueno organization: Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD 20742 – sequence: 5 givenname: Barbara surname: Albert fullname: Albert, Barbara organization: Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD 20742 – sequence: 6 givenname: Fengjie surname: Liu fullname: Liu, Fengjie organization: Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD 20742 – sequence: 7 givenname: Sheryl surname: Ehrman fullname: Ehrman, Sheryl organization: Department of Chemical and Biomolecular Engineering, Clark School of Engineering, University of Maryland, College Park, MD 20742 – sequence: 8 givenname: Donald K. surname: Milton fullname: Milton, Donald K. organization: Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD 20742 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29348203$$D View this record in MEDLINE/PubMed |
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| Copyright | Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles Copyright © 2018 the Author(s). Published by PNAS. Copyright National Academy of Sciences Jan 30, 2018 Copyright © 2018 the Author(s). Published by PNAS. 2018 |
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| Keywords | influenza virus vaccination effects airborne infection viral shedding aerosol |
| Language | English |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 2Present address: Center for the Built Environment, University of California, Berkeley, CA 94720. 1Present address: Department of Biology, Missouri Western State University, St. Joseph, MO 64507. Edited by Peter Palese, Icahn School of Medicine at Mount Sinai, New York, NY, and approved December 15, 2017 (received for review September 19, 2017) 4Present address: Davidson College of Engineering, San José State University, San José, CA 95192. Author contributions: S.E., D.K.M., and E.C. designed research; J.Y., M.G., J.P., P.J.B.d.M., B.A., F.L., S.E., and D.K.M. performed research; D.K.M. contributed new reagents/analytic tools; J.Y. and D.K.M. analyzed data; and J.Y., M.G., and D.K.M. wrote the paper. 3Present address: Division of Viral Products, Center for Biologics Evaluation and Research, Food and Drug Administration, Silver Spring, MD 20903. |
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| Snippet | Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of... Lack of human data on influenza virus aerosol shedding fuels debate over the importance of airborne transmission. We provide overwhelming evidence that humans... |
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| SubjectTerms | Aerosols Air Microbiology Biological Sciences Body Mass Index Body size Copy number Cough Exhalation Female Humans Influenza Influenza, Human - transmission Influenza, Human - virology Male Models, Theoretical Prevalence Respiratory diseases Respiratory System Respiratory Tract Infections - virology Ribonucleic acid RNA RNA, Viral - genetics Seasons Sneezing Students Temperature Universities Vaccination Viruses Young Adult |
| Title | Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community |
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