The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research

Abstract

Reproducible science requires transparent reporting. The ARRIVE guidelines (Animal Research: Reporting of In Vivo Experiments) were originally developed in 2010 to improve the reporting of animal research. They consist of a checklist of information to include in publications describing in vivo experiments to enable others to scrutinise the work adequately, evaluate its methodological rigour, and reproduce the methods and results. Despite considerable levels of endorsement by funders and journals over the years, adherence to the guidelines has been inconsistent, and the anticipated improvements in the quality of reporting in animal research publications have not been achieved. Here, we introduce ARRIVE 2.0. The guidelines have been updated and information reorganised to facilitate their use in practice. We used a Delphi exercise to prioritise and divide the items of the guidelines into 2 sets, the “ARRIVE Essential 10,” which constitutes the minimum requirement, and the “Recommended Set,” which describes the research context. This division facilitates improved reporting of animal research by supporting a stepwise approach to implementation. This helps journal editors and reviewers verify that the most important items are being reported in manuscripts. We have also developed the accompanying Explanation and Elaboration (E&E) document, which serves (1) to explain the rationale behind each item in the guidelines, (2) to clarify key concepts, and (3) to provide illustrative examples. We aim, through these changes, to help ensure that researchers, reviewers, and journal editors are better equipped to improve the rigour and transparency of the scientific process and thus reproducibility.

About the Authors:

Nathalie Percie du Sert

Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Visualization, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliation: NC3Rs, London, United Kingdom

ORCID logo http://orcid.org/0000-0002-9478-0540

Viki Hurst

Roles Data curation, Investigation, Methodology, Project administration, Resources, Writing – original draft

Affiliation: NC3Rs, London, United Kingdom

Amrita Ahluwalia

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliations The William Harvey Research Institute, London, United Kingdom, Barts Cardiovascular CTU, Queen Mary University of London, London, United Kingdom

ORCID logo http://orcid.org/0000-0001-7626-6399

Sabina Alam

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Taylor & Francis Group, London, United Kingdom

ORCID logo http://orcid.org/0000-0002-8615-9658

Marc T. Avey

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Health Science Practice, ICF, Durham, North Carolina, United States of America

ORCID logo http://orcid.org/0000-0002-8696-3232

Monya Baker

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Nature, San Francisco, California, United States of America

William J. Browne

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: School of Education, University of Bristol, Bristol, United Kingdom

ORCID logo http://orcid.org/0000-0002-6659-6885

Alejandra Clark

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: PLOS ONE, Cambridge, United Kingdom

ORCID logo http://orcid.org/0000-0002-1292-0408

Innes C. Cuthill

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: School of Biological Sciences, University of Bristol, Bristol, United Kingdom

ORCID logo http://orcid.org/0000-0002-5007-8856

Ulrich Dirnagl

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: QUEST Center for Transforming Biomedical Research, Berlin Institute of Health & Department of Experimental Neurology, Charite Universitätsmedizin Berlin, Berlin, Germany

ORCID logo http://orcid.org/0000-0003-0755-6119

Michael Emerson

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: National Heart and Lung Institute, Imperial College London, London, United Kingdom

Paul Garner

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Centre for Evidence Synthesis in Global Health, Clinical Sciences Department, Liverpool School of Tropical Medicine, Liverpool, United Kingdom

ORCID logo http://orcid.org/0000-0002-0607-6941

Stephen T. Holgate

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Clinical and Experimental Sciences, University of Southampton, Southampton, United Kingdom

David W. Howells

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Tasmanian School of Medicine, University of Tasmania, Hobart, Australia

ORCID logo http://orcid.org/0000-0002-2512-7724

Natasha A. Karp

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Data Sciences & Quantitative Biology, Discovery Sciences, R&D, AstraZeneca, Cambridge, United Kingdom

ORCID logo http://orcid.org/0000-0002-8404-2907

Stanley E. Lazic

Roles Writing – review & editing

Affiliation: Prioris.ai Inc, Ottawa, Canada

Katie Lidster

Roles Investigation, Project administration, Writing – review & editing

Affiliation: NC3Rs, London, United Kingdom

Catriona J. MacCallum

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Hindawi Ltd, London, United Kingdom

ORCID logo http://orcid.org/0000-0001-9623-2225

Malcolm Macleod

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom

ORCID logo http://orcid.org/0000-0001-9187-9839

Esther J. Pearl

Roles Writing – review & editing

Affiliation: NC3Rs, London, United Kingdom

ORCID logo http://orcid.org/0000-0001-6510-0959

Ole H. Petersen

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Academia Europaea Knowledge Hub, Cardiff University, Cardiff, United Kingdom

ORCID logo http://orcid.org/0000-0002-6998-0380

Frances Rawle

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Medical Research Council, London, United Kingdom

ORCID logo http://orcid.org/0000-0002-8877-6262

Penny Reynolds

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Statistics in Anesthesiology Research (STAR) Core, Department of Anesthesiology, College of Medicine, University of Florida, Gainesville, Florida, United States of America

ORCID logo http://orcid.org/0000-0001-7480-6275

Kieron Rooney

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Discipline of Exercise and Sport Science, Faculty of Medicine and Health, University of Sydney, Sydney, Australia

ORCID logo http://orcid.org/0000-0001-6563-7617

Emily S. Sena

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom

ORCID logo http://orcid.org/0000-0002-3282-8502

Shai D. Silberberg

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: National Institute of Neurological Disorders and Stroke, Bethesda, Maryland, United States of America

Thomas Steckler

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Janssen Pharmaceutica NV, Beerse, Belgium

ORCID logo http://orcid.org/0000-0002-9927-5121

Hanno Würbel

Roles Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing

Affiliation: Veterinary Public Health Institute, Vetsuisse Faculty, University of Bern, Bern, Switzerland

ORCID logo http://orcid.org/0000-0002-2934-3010

Abstract

Reproducible science requires transparent reporting. The ARRIVE guidelines (Animal Research: Reporting of In Vivo Experiments) were originally developed in 2010 to improve the reporting of animal research. They consist of a checklist of information to include in publications describing in vivo experiments to enable others to scrutinise the work adequately, evaluate its methodological rigour, and reproduce the methods and results. Despite considerable levels of endorsement by funders and journals over the years, adherence to the guidelines has been inconsistent, and the anticipated improvements in the quality of reporting in animal research publications have not been achieved. Here, we introduce ARRIVE 2.0. The guidelines have been updated and information reorganised to facilitate their use in practice. We used a Delphi exercise to prioritise and divide the items of the guidelines into 2 sets, the “ARRIVE Essential 10,” which constitutes the minimum requirement, and the “Recommended Set,” which describes the research context. This division facilitates improved reporting of animal research by supporting a stepwise approach to implementation. This helps journal editors and reviewers verify that the most important items are being reported in manuscripts. We have also developed the accompanying Explanation and Elaboration (E&E) document, which serves (1) to explain the rationale behind each item in the guidelines, (2) to clarify key concepts, and (3) to provide illustrative examples. We aim, through these changes, to help ensure that researchers, reviewers, and journal editors are better equipped to improve the rigour and transparency of the scientific process and thus reproducibility.

Citation: Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, et al. (2020) The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol 18(7): e3000410. https://doi.org/10.1371/journal.pbio.3000410

Academic Editor: Isabelle Boutron, University Paris Descartes, FRANCE

Published: July 14, 2020

This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Funding: This work was supported by the National Centre of the Replacement, Refinement and Reduction on Animals in Research (NC3Rs, https://www.nc3rs.org.uk/). NPdS, KL, VH, and EJP are employees of the NC3Rs.

Competing interests: I have read the journal’s policy and the authors of this manuscript have the following competing interests: AA is the editor in chief of the British Journal of Pharmacology. WJB, ICC, and ME are authors of the original ARRIVE guidelines. WJB serves on the Independent Statistical Standing Committee of the funder CHDI foundation. AC is a Senior Editor for PLOS ONE. AC, CJM, MM, and ESS were involved in the IICARus trial. ME, MM, and ESS have received funding from NC3Rs. ME sits on the MRC ERPIC panel. STH is chair of the NC3Rs board; trusteeship of the BLF, Kennedy Trust, DSRU, and CRUK; member of Governing Board, Nuffield Council of Bioethics, member Science Panel for Health (EU H2020); founder and NEB Director Synairgen; consultant Novartis, Teva, and AZ; and chair MRC/GSK EMINENT Collaboration. VH, KL, EJP, and NPdS are NC3Rs staff; role includes promoting the ARRIVE guidelines. SEL and UD are on the advisory board of the UK Reproducibility Network. CJM has shareholdings in Hindawi, is on the publishing board of the Royal Society, and on the EU Open Science policy platform. UD, MM, NPdS, CJM, ESS, TS, and HW are members of EQIPD. MM is a member of the Animals in Science Committee and on the steering group of the UK Reproducibility Network. NPdS and TS are associate editors of BMJ Open Science. OHP is vice president of Academia Europaea, editor in chief of Function, senior executive editor of the Journal of Physiology, and member of the Board of the European Commission’s SAPEA (Science Advice for Policy by European Academies). FR is an NC3Rs board member and has shareholdings in GSK. FR and NAK have shareholdings in AstraZeneca. PR is a member of the University of Florida Institutional Animal Care and Use Committee and editorial board member of Shock. ESS is editor in chief of BMJ Open Science. SDS’s role is to provide expertise and does not represent the opinion of the NIH. TS has shareholdings in Johnson & Johnson. SA, MTA, MB, PG, DWH, and KR declared no conflict of interest.

Abbreviations: ARRIVE, Animal Research: Reporting of In Vivo Experiments; E&E, Explanation and Elaboration; FAIR, Findable, Accessible, Interoperable, Reusable; MDAR, Materials, Design, Analysis and Reporting; NIH, National Institutes of Health

See S1 Annotated Byline for individual authors’ positions at the time this article was submitted.

Why good reporting is important

In recent years, concerns about the reproducibility of research findings have been raised by scientists, funders, research users, and policy makers [1, 2]. Factors that contribute to poor reproducibility include flawed study design and analysis, variability and inadequate validation of reagents and other biological materials, insufficient reporting of methodology and results, and barriers to accessing data [3]. The bioscience community has introduced a range of initiatives to address the problem, from open access and open practices to enable the scrutiny of all aspects of the research [4, 5] through to study preregistration to shift the focus towards robust methods rather than the novelty of the results [6, 7], as well as resources to improve experimental design and statistical analysis [8–10].

Transparent reporting of research methods and findings is an essential component of reproducibility. Without this, the methodological rigour of the studies cannot be adequately scrutinised, the reliability of the findings cannot be assessed, and the work cannot be repeated or built upon by others. Despite the development of specific reporting guidelines for preclinical and clinical research, evidence suggests that scientific publications often lack key information and that there continues to be considerable scope for improvement [11–18]. Animal research is a good case in point, where poor reporting impacts on the development of therapeutics and irreproducible findings can spawn an entire field of research, or trigger clinical studies, subjecting patients to interventions unlikely to be effective [2, 19, 20].

In an attempt to improve the reporting of animal research, the Animal Research: Reporting of In Vivo Experiments (ARRIVE) guidelines were published in 2010. The guidelines consist of a checklist of the items that should be included in any manuscript that reports in vivo experiments, to ensure a comprehensive and transparent description [21–30]. They apply to any area of research using live animal species and are especially pertinent to describe comparative research in the laboratory or other formal test setting. The guidelines are also relevant in a wider context, for example, for observational research, studies conducted in the field, and where animal tissues are used. In the 10 years since publication, the ARRIVE guidelines have been endorsed by more than a thousand journals from across the life sciences. Endorsement typically includes advocating their use in guidance to authors and reviewers. However, despite this level of support, recent studies have shown that important information as set out in the ARRIVE guidelines is still missing from most publications sampled. This includes details on randomisation (reported in only 30%–40% of publications), blinding (reported in only approximately 20% of publications), sample size justification (reported in less than 10% of publications), and animal characteristics (all basic characteristics reported in less than 10% of publications) [11, 31, 32].

Evidence suggests that 2 main factors limit the impact of the ARRIVE guidelines. The first is the extent to which editorial and journal staff are actively involved in enforcing reporting standards. This is illustrated by a randomised controlled trial at PLOS ONE, designed to test the effect of requesting a completed ARRIVE checklist in the manuscript submission process. This single editorial intervention, which did not include further verification from journal staff, failed to improve the disclosure of information in published papers [33]. In contrast, other studies using shorter checklists (primarily focused on experimental design) with more editorial follow-up have shown a marked improvement in the nature and detail of the information included in publications [34–36]. It is likely that the level of resource required from journals and editors currently prohibits the implementation of all the items of the ARRIVE guidelines.

The second issue is that researchers and other individuals and organisations responsible for the integrity of the research process are not sufficiently aware of the consequences of incomplete reporting. There is some evidence that awareness of ARRIVE is linked to the use of more rigorous experimental design standards [37]; however, researchers are often unfamiliar with the much larger systemic bias in the publication of research and in the reliability of certain findings and even of entire fields [33, 38–40]. This lack of understanding affects how experiments are designed and grant proposals prepared, how animals are used and data recorded in the laboratory, and how manuscripts are written by authors or assessed by journal staff, editors, and reviewers.

Approval for experiments involving animals is generally based on a harm–benefit analysis, weighing the harms to the animals involved against the benefits of the research to society. If the research is not reported in enough detail, even when conducted rigorously, the benefits may not be realised, and the harm–benefit analysis and public trust in the research are undermined [41]. As a community, we must do better to ensure that, where animals are used, the research is both well designed and analysed as well as transparently reported. Here, we introduce the revised ARRIVE guidelines, referred to as ARRIVE 2.0. The information included has been updated, extended, and reorganised to facilitate the use of the guidelines, helping to ensure that researchers, editors, and reviewers—as well as other relevant journal staff—are better equipped to improve the rigour and reproducibility of animal research.

Introducing ARRIVE 2.0

In ARRIVE 2.0, we have improved the clarity of the guidelines, prioritised the items, added new information, and generated the accompanying Explanation and Elaboration (E&E) document to provide context and rationale for each item [42] (also available at https://www.arriveguidelines.org). New additions comprise inclusion and exclusion criteria, which are a key aspect of data handling and prevent the ad hoc exclusion of data [43]; protocol registration, a recently emerged approach that promotes scientific rigour and encourages researchers to carefully consider the experimental design and analysis plan before any data are collected [44]; and data access, in line with the FAIR Data Principles [45] (Findable, Accessible, Interoperable, and Reusable). S1 Table summarises the changes.

The most significant departure from the original guidelines is the classification of items into 2 prioritised groups, as shown in Tables 1 and 2. There is no ranking of the items within each group. The first group is the “ARRIVE Essential 10,” which describes information that is the basic minimum to include in a manuscript, as without this information, reviewers and readers cannot confidently assess the reliability of the findings presented. It includes details on the study design, the sample size, measures to reduce subjective bias, outcome measures, statistical methods, the animals, experimental procedures, and results. The second group, referred to as the “Recommended Set,” adds context to the study described. This includes the ethical statement, declaration of interest, protocol registration, and data access, as well as more detailed information on the methodology such as animal housing, husbandry, care, and monitoring. Items on the abstract, background, objectives, interpretation, and generalisability also describe what to include in the more narrative parts of a manuscript.

[Figure omitted. See PDF.]

Table 1. ARRIVE Essential 10.

https://doi.org/10.1371/journal.pbio.3000410.t001

[Figure omitted. See PDF.]

Table 2. ARRIVE Recommended Set.

https://doi.org/10.1371/journal.pbio.3000410.t002

Revising the guidelines has been an extensive and collaborative effort, with input from the scientific community carefully built into the process. The revision of the ARRIVE guidelines has been undertaken by an international working group—the authors of this publication—with expertise from across the life sciences community, including funders, journal editors, statisticians, methodologists, and researchers from academia and industry. We used a Delphi exercise [46] with external stakeholders to maximise diversity in fields of expertise and geographical location, with experts from 19 countries providing feedback on each item, suggesting new items, and ranking items according to their relative importance for assessing the reliability of research findings. This ranking resulted in the prioritisation of the items of the guidelines into the 2 sets. Demographics of the Delphi panel and full methods and results are presented in Supporting Information S1 Delphi and S1 Data. Following their publication on BioRxiv, the revised guidelines and the E&E were also road tested with researchers preparing manuscripts describing in vivo studies, to ensure that these documents were well understood and useful to the intended users. This study is presented in Supporting Information S1 Road Testing and S2 Data.

While reporting animal research in adherence to all 21 items of ARRIVE 2.0 represents best practice, the classification of the items into 2 groups is intended to facilitate the improved reporting of animal research by allowing an initial focus on the most critical issues. This better allows journal staff, editors, and reviewers to verify that the items have been adequately reported in manuscripts. The first step should be to ensure compliance with the ARRIVE Essential 10 as a minimum requirement. Items from the Recommended Set can then be added over time and in line with specific editorial policies until all the items are routinely reported in all manuscripts. ARRIVE 2.0 are fully compatible with and complementary to other guidelines that have been published in recent years. By providing a comprehensive set of recommendations that are specifically tailored to the description of in vivo research, they help authors reporting animal experiments adhere to the National Institutes of Health (NIH) standards [43] and the minimum standards framework and checklist (Materials, Design, Analysis and Reporting [MDAR] [47]). The revised guidelines are also in line with many journals’ policies and will assist authors in complying with information requirements on the ethical review of the research [48, 49], data presentation and access [50–52], statistical methods [51, 52], and conflicts of interest [53, 54].

Although the guidelines are written with researchers and journal editorial policies in mind, it is important to stress that researchers alone should not have to carry the responsibility for transparent reporting. Funders, institutions, and publishers’ endorsement of ARRIVE has been instrumental in raising awareness to date; they now have a key role to play in building capacity and championing the behavioural changes required to improve reporting practices. This includes embedding ARRIVE 2.0 in appropriate training, workflows, and processes to support researchers in their different roles. While the primary focus of the guidelines has been on the reporting of animal studies, ARRIVE also has other applications earlier in the research process, including in the planning and design of in vivo experiments. For example, requesting a description of the study design in line with the guidelines in funding or ethical review applications ensures that steps to minimise experimental bias are considered at the beginning of the research cycle [55].

Conclusion

Transparent reporting is clearly essential if animal studies are to add to the knowledge base and inform future research, policy, and clinical practice. ARRIVE 2.0 prioritises the reporting of information related to study reliability. This enables research users to assess how much weight to ascribe to the findings and, in parallel, promotes the use of rigorous methodology in the planning and conduct of in vivo experiments [37], thus increasing the likelihood that the findings are reliable and, ultimately, reproducible.

The intention of ARRIVE 2.0 is not to supersede individual journal requirements but to promote a harmonised approach across journals to ensure that all manuscripts contain the essential information needed to appraise the research. Journals usually share a common objective of improving the methodological rigour and reproducibility of the research they publish, but different journals emphasise different pieces of information [56–58]. Here, we propose an expert consensus on information to prioritise. This will provide clarity for authors, facilitate transfer of manuscripts between journals, and accelerate an improvement of reporting standards.

Concentrating the efforts of the research and publishing communities on the ARRIVE Essential 10 items provides a manageable approach to evaluate reporting quality efficiently and assess the effect of interventions and policies designed to improve the reporting of animal experiments. It provides a starting point for the development of operationalised checklists to assess reporting, ultimately leading to the build of automated or semi-automated artificial intelligence tools that can detect missing information rapidly [59].

Improving reporting is a collaborative endeavour, and concerted effort from the biomedical research community is required to ensure maximum impact. We welcome collaboration with other groups operating in this area, as well as feedback on ARRIVE 2.0 and our implementation strategy.

Supporting information

S1 Table. Noteworthy changes in ARRIVE 2.0.

This table recapitulates noteworthy changes in the ARRIVE guidelines 2.0, compared to the original ARRIVE guidelines published in 2010.

https://doi.org/10.1371/journal.pbio.3000410.s001

(PDF)

S1 Delphi. Delphi methods and results.

Methodology and results of the Delphi study that was used to prioritise the items of the guidelines into the ARRIVE Essential 10 and Recommended Set.

https://doi.org/10.1371/journal.pbio.3000410.s002

(PDF)

S1 Data. Delphi data.

Tabs 1, 2, and 3: Panel members’ scores for each of the ARRIVE items during rounds 1, 2, and 3, along with descriptive statistics. Tab 4: Qualitative feedback, collected from panel members during round 1, on the importance and the wording of each item. Tab 5: Additional items suggested for consideration in ARRIVE 2.0; similar suggestions were grouped together before processing. Tab 6: Justifications provided by panel members for changing an item’s score between round 1 and round 2.

https://doi.org/10.1371/journal.pbio.3000410.s003

(XLSX)

S2 Data. Road testing data.

Tab 1: Participants’ demographics and general feedback on the guidelines and the E&E preprints. Tab 2: Outcome of each manuscript’s assessment and justifications provided by participants for not including information covered in the ARRIVE guidelines.

https://doi.org/10.1371/journal.pbio.3000410.s004

(XLSX)

S1 Road Testing. Road testing methods and results.

Methodology used to road test the revised ARRIVE guidelines and E&E (as published in preprint) and how this information was used in the development of ARRIVE 2.0.

https://doi.org/10.1371/journal.pbio.3000410.s005

(PDF)

S1 Annotated Byline. Individual authors’ positions at the time this article was submitted.

https://doi.org/10.1371/journal.pbio.3000410.s006

(DOCX)

Acknowledgments

We would like to thank the members of the expert panel for the Delphi exercise and the participants of the road testing for their time and feedback. We are grateful to the DelphiManager team for advice and use of their software. We would like to acknowledge the late Doug Altman’s contribution to this project; Doug was a dedicated member of the working group and his input to the guidelines’ revision has been invaluable.

Citation: Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, et al. (2020) The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol 18(7): e3000410. https://doi.org/10.1371/journal.pbio.3000410

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