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

doi:10.1073/pnas.2010217118

New Research In

Edited by Lora V. Hooper, University of Texas Southwestern Medical Center, Dallas, TX, and approved December 14, 2020 (received for review August 3, 2020)

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.

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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Proceedings of the National Academy of Sciences: 118 (6)

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Article Classifications

Biological Sciences
Microbiology

[1] 1.↵
B. B. Finlay; CIFAR Humans; Microbiome
, Are noncommunicable diseases communicable? Science 367, 250–251 (2020).
OpenUrl Abstract/FREE Full Text

[2] B. B. Finlay; CIFAR Humans; Microbiome

[3] 2.↵
D. P. Strachan
, Hay fever, hygiene, and household size. BMJ 299, 1259–1260 (1989).
OpenUrl FREE Full Text

[4] D. P. Strachan

[5] 3.↵
M. Scudellari
, News feature: Cleaning up the hygiene hypothesis. Proc. Natl. Acad. Sci. U.S.A. 114, 1433–1436 (2017).
OpenUrl FREE Full Text

[6] M. Scudellari

[7] 4.↵
L. T. Stiemsma,
L. A. Reynolds,
S. E. Turvey,
B. B. Finlay
, The hygiene hypothesis: Current perspectives and future therapies. ImmunoTargets Ther. 4, 143–157 (2015).
OpenUrl CrossRef PubMed

[8] L. T. Stiemsma,

[9] L. A. Reynolds,

[10] S. E. Turvey,

[11] B. B. Finlay

[12] 5.↵
Q. Le Bastard et al
., Systematic review: Human gut dysbiosis induced by non-antibiotic prescription medications. Aliment. Pharmacol. Ther. 47, 332–345 (2018).
OpenUrl CrossRef PubMed

[13] Q. Le Bastard et al

[14] 6.↵
J. L. Sonnenburg,
E. D. Sonnenburg
, Vulnerability of the industrialized microbiota. Science 366, eaaw9255 (2019).
OpenUrl Abstract/FREE Full Text

[15] J. L. Sonnenburg,

[16] E. D. Sonnenburg

[17] 7.↵
N. A. Bokulich et al
., Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci. Transl. Med. 8, 343ra382 (2016).
OpenUrl

[18] N. A. Bokulich et al

[19] 8.↵
M. J. Blaser,
S. Falkow
, What are the consequences of the disappearing human microbiota? Nat. Rev. Microbiol. 7, 887–894 (2009).
OpenUrl CrossRef PubMed

[20] M. J. Blaser,

[21] S. Falkow

[22] 9.↵
G. A. Rook
, Hygiene and other early childhood influences on the subsequent function of the immune system. Dig. Dis. 29, 144–153 (2011).
OpenUrl CrossRef PubMed

[23] G. A. Rook

[24] 10.↵
T. W. Buford
, (Dis)trust your gut: The gut microbiome in age-related inflammation, health, and disease. Microbiome 5, 80 (2017).
OpenUrl CrossRef

[25] T. W. Buford

[26] 11.↵
J. Cahenzli,
Y. Köller,
M. Wyss,
M. B. Geuking,
K. D. McCoy
, Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe 14, 559–570 (2013).
OpenUrl CrossRef PubMed

[27] J. Cahenzli,

[28] Y. Köller,

[29] M. Wyss,

[30] M. B. Geuking,

[31] K. D. McCoy

[32] 12.↵
C. Ohnmacht et al
., MUCOSAL IMMUNOLOGY. The microbiota regulates type 2 immunity through RORγt⁺ T cells. Science 349, 989–993 (2015).
OpenUrl Abstract/FREE Full Text

[33] C. Ohnmacht et al

[34] 13.↵
S. Illi et al.; GABRIELA Study Group
, Protection from childhood asthma and allergy in Alpine farm environments—The GABRIEL Advanced Studies. J. Allergy Clin. Immunol. 129, 1470–7.e6 (2012).
OpenUrl CrossRef PubMed

[35] S. Illi et al.; GABRIELA Study Group

[36] 14.↵
A. A. Aguirre
, Changing patterns of emerging zoonotic diseases in wildlife, domestic animals, and humans linked to biodiversity loss and globalization. ILAR J. 58, 315–318 (2017).
OpenUrl CrossRef PubMed

[37] A. A. Aguirre

[38] 15.↵
L. Denyer Willis,
C. Chandler
, Quick fix for care, productivity, hygiene and inequality: Reframing the entrenched problem of antibiotic overuse. BMJ Glob. Health 4, e001590 (2019).
OpenUrl Abstract/FREE Full Text

[39] L. Denyer Willis,

[40] C. Chandler

[41] 16.↵
T. Giles-Vernick,
L. Bainilago,
M. Fofana,
P. Bata,
M. Vray
, Home care of children with diarrhea in Bangui’s therapeutic landscape (Central African Republic). Qual. Health Res. 26, 164–175 (2016).
OpenUrl CrossRef PubMed

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