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The hygiene hypothesis, the COVID pandemic, and consequences for the human microbiome

B. Brett Finlay, View ORCID ProfileKatherine R. Amato, View ORCID ProfileMeghan Azad, Martin J. Blaser, View ORCID ProfileThomas C. G. Bosch, Hiutung Chu, View ORCID ProfileMaria Gloria Dominguez-Bello, Stanislav Dusko Ehrlich, View ORCID ProfileEran Elinav, View ORCID ProfileNaama Geva-Zatorsky, View ORCID ProfilePhilippe Gros, View ORCID ProfileKaren Guillemin, View ORCID ProfileFrédéric Keck, View ORCID ProfileTal Korem, View ORCID ProfileMargaret J. McFall-Ngai, View ORCID ProfileMelissa K. Melby, Mark Nichter, View ORCID ProfileSven Pettersson, View ORCID ProfileHendrik Poinar, View ORCID ProfileTobias Rees, View ORCID ProfileCarolina Tropini, Liping Zhao, and View ORCID ProfileTamara Giles-Vernick
PNAS February 9, 2021 118 (6) e2010217118; https://doi.org/10.1073/pnas.2010217118
B. Brett Finlay
aMichael Smith Laboratories, University of British Columbia, Vancouver, BC V6T 1Z4, Canada;
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
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  • For correspondence: bfinlay@msl.ubc.ca tamara.giles-vernick@pasteur.fr
Katherine R. Amato
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
cDepartment of Anthropology, Northwestern University, Evanston, IL 60208;
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  • ORCID record for Katherine R. Amato
Meghan Azad
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
dManitoba Interdisciplinary Lactation Centre, Children’s Hospital Research Institute of Manitoba, Winnipeg, MB R3E 3P4, Canada;
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  • ORCID record for Meghan Azad
Martin J. Blaser
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
eCenter for Advanced Biotechnology and Medicine at Rutgers Biomedical and Health Sciences, Rutgers University, Piscataway, NJ 08854-8021;
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Thomas C. G. Bosch
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
fZoologisches Institut, University of Kiel, 24118 Kiel, Germany;
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  • ORCID record for Thomas C. G. Bosch
Hiutung Chu
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
gDepartment of Pathology, University of California San Diego, La Jolla, CA 92093;
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Maria Gloria Dominguez-Bello
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
hDepartment of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ 08901;
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Stanislav Dusko Ehrlich
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
iMetagenopolis Unit, French National Institute for Agricultural Research, 78350 Jouy-en-Josas, France;
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Eran Elinav
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
jDepartment of Immunology, Weizmann Institute of Science, Rehovot 761000, Israel;
kCancer-Microbiome Division, Deutsches Krebsforschungszentrum, 69120 Heidelberg, Germany;
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  • ORCID record for Eran Elinav
Naama Geva-Zatorsky
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
lTechnion Integrated Cancer Center, Department of Cell Biology and Cancer Science, Technion−Israel Institute of Technology, Haifa 3525433, Israel;
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  • ORCID record for Naama Geva-Zatorsky
Philippe Gros
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
mDepartment of Biochemistry, McGill University, Montreal, QC H3G 1Y6, Canada;
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Karen Guillemin
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
nInstitute of Molecular Biology, University of Oregon, Eugene, OR 97403;
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Frédéric Keck
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
oCentre National de la Recherche Scientifique, 75016 Paris, France;
pLaboratoire d’Anthropologie Sociale, Collège de France, 75005 Paris, France;
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  • ORCID record for Frédéric Keck
Tal Korem
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
qDepartment of Systems Biology, Irving Cancer Research Center, Columbia University, New York, NY 10032;
rDepartment of Obstetrics and Gynecology, Irving Cancer Research Center, Columbia University, New York, NY 10032;
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  • ORCID record for Tal Korem
Margaret J. McFall-Ngai
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
sPacific Biosciences Research Center, University of Hawai’i at Manoa, Honolulu, HI 96822;
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  • ORCID record for Margaret J. McFall-Ngai
Melissa K. Melby
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
tDepartment of Anthropology, University of Delaware, Newark, DE 19711;
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  • ORCID record for Melissa K. Melby
Mark Nichter
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
uDepartment of Anthropology, University of Arizona, Tucson, AZ 85721;
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Sven Pettersson
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
vLee Kong Chian School of Medicine, Nanyang Technological University, 637715 Singapore;
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Hendrik Poinar
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
wDepartment of Anthropology, McMaster University, Hamilton, ON L8S 4M4, Canada;
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Tobias Rees
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
xTransformations of the Human Program, Berggruen Institute, Los Angeles, CA 90013;
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Carolina Tropini
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
ySchool of Biomedical Engineering, University of British Columbia, Vancouver, BC V6T 1Z3, Canada;
zDepartment of Microbiology & Immunology, University of British Columbia, Vancouver, BC V6T 1Z3, Canada;
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Liping Zhao
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
hDepartment of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ 08901;
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Tamara Giles-Vernick
bHumans and the Microbiome Program, Canadian Institute for Advanced Research, Toronto, ON M5G 1M1, Canada;
aaAnthropology & Ecology of Disease Emergence, Institut Pasteur, 75015 Paris, France
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  • ORCID record for Tamara Giles-Vernick
  • For correspondence: bfinlay@msl.ubc.ca tamara.giles-vernick@pasteur.fr
  1. Edited by Lora V. Hooper, University of Texas Southwestern Medical Center, Dallas, TX, and approved December 14, 2020 (received for review August 3, 2020)

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Abstract

The COVID-19 pandemic has the potential to affect the human microbiome in infected and uninfected individuals, having a substantial impact on human health over the long term. This pandemic intersects with a decades-long decline in microbial diversity and ancestral microbes due to hygiene, antibiotics, and urban living (the hygiene hypothesis). High-risk groups succumbing to COVID-19 include those with preexisting conditions, such as diabetes and obesity, which are also associated with microbiome abnormalities. Current pandemic control measures and practices will have broad, uneven, and potentially long-term effects for the human microbiome across the planet, given the implementation of physical separation, extensive hygiene, travel barriers, and other measures that influence overall microbial loss and inability for reinoculation. Although much remains uncertain or unknown about the virus and its consequences, implementing pandemic control practices could significantly affect the microbiome. In this Perspective, we explore many facets of COVID-19−induced societal changes and their possible effects on the microbiome, and discuss current and future challenges regarding the interplay between this pandemic and the microbiome. Recent recognition of the microbiome’s influence on human health makes it critical to consider both how the microbiome, shaped by biosocial processes, affects susceptibility to the coronavirus and, conversely, how COVID-19 disease and prevention measures may affect the microbiome. This knowledge may prove key in prevention and treatment, and long-term biological and social outcomes of this pandemic.

  • COVID-19
  • microbiome
  • hygiene hypothesis

Footnotes

  • ↵1To whom correspondence may be addressed. Email: bfinlay{at}msl.ubc.ca or tamara.giles-vernick{at}pasteur.fr.
  • Author contributions: B.B.F., K.R.A., M.A., M.J.B., T.C.G.B., H.C., M.G.D.-B., S.D.E., E.E., N.G.-Z., P.G., K.G., F.K., T.K., M.J.M.-N., M.K.M., M.N., S.P., H.P., T.R., C.T., L.Z., and T.G.-V. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

Data Availability.

All study data are included in the article.

Published under the PNAS license.

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The hygiene hypothesis, the COVID pandemic, and consequences for the human microbiome
B. Brett Finlay, Katherine R. Amato, Meghan Azad, Martin J. Blaser, Thomas C. G. Bosch, Hiutung Chu, Maria Gloria Dominguez-Bello, Stanislav Dusko Ehrlich, Eran Elinav, Naama Geva-Zatorsky, Philippe Gros, Karen Guillemin, Frédéric Keck, Tal Korem, Margaret J. McFall-Ngai, Melissa K. Melby, Mark Nichter, Sven Pettersson, Hendrik Poinar, Tobias Rees, Carolina Tropini, Liping Zhao, Tamara Giles-Vernick
Proceedings of the National Academy of Sciences Feb 2021, 118 (6) e2010217118; DOI: 10.1073/pnas.2010217118

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The hygiene hypothesis, the COVID pandemic, and consequences for the human microbiome
B. Brett Finlay, Katherine R. Amato, Meghan Azad, Martin J. Blaser, Thomas C. G. Bosch, Hiutung Chu, Maria Gloria Dominguez-Bello, Stanislav Dusko Ehrlich, Eran Elinav, Naama Geva-Zatorsky, Philippe Gros, Karen Guillemin, Frédéric Keck, Tal Korem, Margaret J. McFall-Ngai, Melissa K. Melby, Mark Nichter, Sven Pettersson, Hendrik Poinar, Tobias Rees, Carolina Tropini, Liping Zhao, Tamara Giles-Vernick
Proceedings of the National Academy of Sciences Feb 2021, 118 (6) e2010217118; DOI: 10.1073/pnas.2010217118
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Proceedings of the National Academy of Sciences: 118 (6)
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  • Biological Sciences
  • Microbiology

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  • Article
    • Abstract
    • COVID-19 and the Microbiome
    • Hygienic Measures during a Pandemic and Their Effects on Microbiome Acquisition, Loss, and Reinoculation
    • Feeding Ourselves and Our Microbiome during a Pandemic
    • Social Microbiomes
    • Impacts of Hygiene on Microbiomes of the Young and the Old
    • The Communal Microbiome
    • Conclusion
    • Data Availability.
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