Microbiomes of the

Built Environment

A RESEARCH AGENDA FOR INDOOR MICROBIOLOGY,
HUMAN HEALTH, AND BUILDINGS

Committee on Microbiomes of the Built Environment:
From Research to Application

Board on Life Sciences

Board on Environmental Studies and Toxicology

Board on Infrastructure and the Constructed Environment

Division on Earth and Life Studies

Health and Medicine Division

Division on Engineering and Physical Sciences

National Academy of Engineering

A Consensus Study Report of

THE NATIONAL ACADEMIES PRESS
Washington, DC
www.nap.edu

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This activity was supported by Grant No. 2014-13628 from the Alfred P. Sloan Foundation, a grant from the Gordon and Betty Moore Foundation, Grant No. NNX16AC85G from the National Aeronautics and Space Administration, Contract No. HHSN263201200074I with the National Institutes of Health, Contract No. EP-C-14-005/0007 with the U.S. Environmental Protection Agency, and with additional support from the National Academy of Sciences Cecil and Ida Green Fund. Any opinions, findings, conclusions, or recommendations expressed in this publication do not necessarily reflect the views of any organization or agency that provided support for the project.

International Standard Book Number-13: 978-0-309-44980-9
International Standard Book Number-10: 0-309-44980-4
Digital Object Identifier: https://doi.org/10.17226/23647
Library of Congress Control Number: 2017952589

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Suggested citation: National Academies of Sciences, Engineering, and Medicine. 2017. Microbiomes of the Built Environment: A Research Agenda for Indoor Microbiology, Human Health, and Buildings. Washington, DC: The National Academies Press. doi: https://doi.org/10.17226/23647.

COMMITTEE ON MICROBIOMES OF THE BUILT ENVIRONMENT: FROM RESEARCH TO APPLICATION

Committee Members

JOAN WENNSTROM BENNETT (Chair), Rutgers University

JONATHAN ALLEN, Lawrence Livermore National Laboratory

JEAN COX-GANSER, National Institute for Occupational Safety and Health

JACK GILBERT, University of Chicago

DIANE GOLD, Brigham and Women’s Hospital, Harvard Medical School, and Harvard T.H. Chan School of Public Health

JESSICA GREEN, University of Oregon

CHARLES HAAS, Drexel University

MARK HERNANDEZ, University of Colorado Boulder

ROBERT HOLT, University of Florida

RONALD LATANISION, Exponent, Inc.

HAL LEVIN, Building Ecology Research Group

VIVIAN LOFTNESS, Carnegie Mellon University

KAREN NELSON, J. Craig Venter Institute

JORDAN PECCIA, Yale University

ANDREW PERSILY, National Institute of Standards and Technology

JIZHONG ZHOU, University of Oklahoma

Project Staff

KATHERINE BOWMAN, Study Director and Senior Program Officer, Board on Life Sciences

ELIZABETH BOYLE, Program Officer, Board on Environmental Studies and Toxicology

DAVID A. BUTLER, Scholar, Health and Medicine Division

ANDREA HODGSON, Postdoctoral Fellow, Board on Life Sciences

JENNA OGILVIE, Research Associate, Board on Life Sciences

CAMERON OSKVIG, Director, Board on Infrastructure and the Constructed Environment

PROCTOR REID, Director, National Academy of Engineering Program Office

FRANCES SHARPLES, Director, Board on Life Sciences

Consultants

RONA BRIERE, Editor

HELAINE RESNICK, Editor

Acknowledgments

This Consensus Study Report was reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise. The purpose of this independent review is to provide candid and critical comments that will assist the National Academies of Sciences, Engineering, and Medicine in making each published report as sound as possible and to ensure that it meets the institutional standards for quality, objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process.

We thank the following individuals for their review of this report:

William P. Bahnfleth, The Pennsylvania State University

Rita R. Colwell, University of Maryland, College Park

Richard Corsi, The University of Texas at Austin

Pieter C. Dorrestein, University of California, San Diego

Peter B. Hutt, Covington & Burling LLP

Susan Lynch, University of California, San Francisco

Janet Macher, California Department of Public Health (retired)

Mihai Pop, University of Maryland, College Park

Joan B. Rose, Michigan State University

Sarah Slaughter, Built Environment Coalition

Martin Täubel, National Institute for Health and Welfare, Finland

Mary E. Wilson, Harvard T.H. Chan School of Public Health

Although the reviewers listed above provided many constructive comments and suggestions, they were not asked to endorse the conclusions or

recommendations of this report, nor did they see the final draft before its release. The review of this report was overseen by Michael R. Ladisch, Purdue University, and William W. Nazaroff, University of California, Berkeley. They were responsible for making certain that an independent examination of this report was carried out in accordance with the standards of the National Academies and that all review comments were carefully considered. Responsibility for the final content rests entirely with the authoring committee and the National Academies.

Preface

Ours is a microbial world. Although we cannot see microbes with the naked eye, we all live with microbial consortia. The microbes that are indigenous to our bodies are an essential component of our biology. Moreover, the indoor environments in which we live also harbor a complicated constellation of microbial types. The levels of microbial diversity, and the sheer numbers of organisms, are incongruous with our visual experience, but current microbiome research is changing the way we look not only at ourselves but also at the built environments we have created. DNA sequencing technologies provide a new view of the ubiquity and diversity of microbes in our lives. In looking back on centuries of human experience with buildings, we can see that people have developed many systems that support human comfort and convenience. The vision articulated in this report is that microbiome research can guide improvements to future buildings to enhance human healthfulness.

Do we know enough to rationally manage the microbial communities around us in built environments? The answer is “no.” However, there are provocative hints that in the future, coherent management of the indoor microbiome can help prevent the spread of disease and contribute to human longevity, health, and well-being.

To produce this Consensus Study Report, the National Academies of Sciences, Engineering, and Medicine brought together a group of experts to discuss the microbial communities inside our built environments and their potential effects on human health. The committee sought to understand indoor microbiome research, a discipline that is dedicated to studying build-

ings, the microbial communities found inside of buildings, and the complex interactions that impact human health and well-being. Of necessity, this report touches on a number of extremely dissimilar areas of research and therefore required a committee with diverse expertise. I am grateful to the informed and insightful group of professionals who so generously shared their time and knowledge during the process of writing this report. Their collective expertise was reflective of the range of subject matter covered during our deliberations. The report also was informed by a number of excellent speakers and other participants who came to our open sessions. We thank all of these contributors for sharing their perspectives and research with us. Their contributions were invaluable in further developing our ideas and filling gaps in our expertise. In addition, we thank the report reviewers who provided insightful and instrumental feedback.

On behalf of the committee, I extend our greatest appreciation to the staff of the National Academies who worked with us throughout the process of creating this report. Without their time and guidance, this report would not have been possible. Finally, we thank the sponsors of the study for their financial support and for their astute vision of what this report could accomplish.

Joan Wennstrom Bennett, Chair
Committee on Microbiomes of the Built Environment:
From Research to Application

Contents

ACRONYMS AND ABBREVIATIONS

SUMMARY

1 INTRODUCTION

Study Charge

Study Focus and Scope

Emerging Tools That Facilitate Analysis

Studying the Intersection of Microbial Communities, Built Environments, and Human Occupants

Prior Efforts on Which This Report Builds

Organization of the Report

References

2 MICROORGANISMS IN BUILT ENVIRONMENTS: IMPACTS ON HUMAN HEALTH

Influence of Building Microbiomes on Human Health: Ecologic and Biologic Plausibility

Transmission of Infection in Indoor Environments

Damp Indoor Environments, Indoor Microbial Exposures, and Respiratory or Allergic Disease Outcomes

Nonairway and Nonallergy Effects

Beneficial Effects of Microbes

Summary Observations and Knowledge Gaps

References

3 THE BUILT ENVIRONMENT AND MICROBIAL COMMUNITIES

Introduction to Microbial Reservoirs in Commercial and Residential Buildings

The Diversity of Buildings and Its Impact on Their Microbiomes

Indoor Air Sources and Reservoirs of Microbes

Indoor Water Sources and Reservoirs of Microbes

Building Surfaces and Reservoirs of Microbes

Impacts of Microbes on Degradation of Building Materials and Energy Usage

Building Codes and Standards That May Affect the Microbiome

The Influence of Climate and Climate Change on the Built Environment and Microbial Communities

Summary Observations and Knowledge Gaps

References

4 TOOLS FOR CHARACTERIZING MICROBIOME–BUILT ENVIRONMENT INTERACTIONS

The Built Environment as a Complex Experimental Environment

Characterizing Buildings

Characterizing Indoor Microbial Communities

Linking Analysis of Microbial Communities to Building Characteristics and Human Health Impacts

Needs for Future Progress

Moving from Research Toward Practice

Summary Observations and Knowledge Gaps

References

5 INTERVENTIONS IN THE BUILT ENVIRONMENT

Physical Interventions to Reduce Exposure to Hazardous Microbes

Chemical Interventions to Reduce Exposure to Hazardous Microbes

Interventions to Encourage Exposure to Beneficial Microbes

A Framework for Assessing Built Environment Interventions

Summary Observations and Knowledge Gaps

References

6 MOVING FORWARD: A VISION FOR THE FUTURE AND RESEARCH AGENDA

A Vision for the Future of the Field: Microbiome-Informed Built Environments

A Research Agenda for Achieving the Vision

References

APPENDIXES

A An Assessment of Molecular Characterization Tools

B Study Methods

C Committee Member Biographies

D Glossary

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Boxes, Figures, and Tables

BOXES

S-1 Key Terms Used in This Report

S-2 Knowledge Gaps Identified in This Report

S-3 A Research Agenda for Moving to Practical Application

1-1 Statement of Task

1-2 Modeling Built Environment Ecology

2-1 Transmission of Infectious and Noninfectious Organisms in Hospital Neonates

2-2 Flint, Michigan: An Exemplar of the Role of the Municipal Water Supply in Triggering a Legionnaires’ Disease Outbreak

2-3 Asthma, Early-Life Exposures, and Farm-Type Environments

3-1 Concealed Spaces

3-2 Challenges for the Management of Microbes: The International Space Station

4-1 Design and Use of Longitudinal Building Studies to Understand Microbiome–Built Environment–Human Interactions

FIGURES

1-1 The complex interactions among human occupants, built environments, and associated microbial communities

1-2 Transport and life cycle of indoor microbes

2-1 Modes of transmission of microorganisms from the airborne environment

3-1 The influence of water chemistry and flow on the microbiome of bulk water pipes

5-1 Physical processes govern the assembly of indoor microbial communities

TABLES

2-1 Mode of Transmission for Selected Pathogens Implicated in Infections Due to Inhalation or Fomite Interactions

2-2 Associations Between Health Outcomes and Exposure to Damp Indoor Environments

Annex Table 2-1: Selected Studies on Building/Home-Based Exposure Reduction and Asthma Outcomes in Children (2000–2017)

Annex Table 2-2: Beneficial Associations of Indoor Microbiota with Asthma or Allergy Outcomes in Selected Studies Using Metagenomics, Molecular Biologic, or Culture Methods to Measure Indoor Environmental Microbiota

3-1 Buildings and Surfaces Where Viruses Have Been Detected or Survived

3-2 Home High-Touch Surfaces and Bacterial Reservoirs

3-3 Hospital High-Touch Surfaces and Bacterial Reservoirs

3-4 Environmental, Location, and Surface Parameters That May Influence Microbial Populations and Communities

3-5 Sustainable, Green, and Healthy Codes, Standards, Guidelines, and Certifications That Address Microbiome-Related Issues

3-6 WELL Building Standard Features That Address Microbiome-Related Issues

4-1 Selected Building Simulation Tools

A-1 Overview of Molecular Characterization Tools

Acronyms and Abbreviations