Precision epidemiology for infectious disease control

Advances in genomics and computing are transforming the capacity for the characterization of biological systems, and researchers are now poised for a precision-focused transformation in the way they prepare for, and respond to, infectious diseases. This includes the use of genome-based approaches to inform molecular diagnosis and individual-level treatment regimens. In addition, advances in the speed and granularity of pathogen genome generation have improved the capability to track and understand pathogen transmission, leading to potential improvements in the design and implementation of population-level public health interventions. In this Perspective, we outline several trends that are driving the development of precision epidemiology of infectious disease and their implications for scientists’ ability to respond to outbreaks.The emerging field of precision epidemiology allows the personalized diagnosis, tracking and treatment of infectious diseases.

[1]  Gregory S Turenchalk,et al.  Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. , 2009, The Journal of infectious diseases.

[2]  Julian Parkhill,et al.  Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study , 2013, The Lancet. Infectious Diseases.

[3]  Jennifer L. Gardy,et al.  Towards a genomics-informed, real-time, global pathogen surveillance system , 2017, Nature Reviews Genetics.

[4]  Yi Chen,et al.  Implementation of Nationwide Real-time Whole-genome Sequencing to Enhance Listeriosis Outbreak Detection and Investigation. , 2016, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[5]  Ruth Timme,et al.  The Public Health Impact of a Publically Available, Environmental Database of Microbial Genomes , 2017, Front. Microbiol..

[6]  Jeffrey R. Kugelman,et al.  Emergence of Ebola Virus Escape Variants in Infected Nonhuman Primates Treated with the MB-003 Antibody Cocktail. , 2015, Cell reports.

[7]  N. Khardori Emergence of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans , 2009 .

[8]  Lawrence O Gostin,et al.  Will Ebola change the game? Ten essential reforms before the next pandemic. The report of the Harvard-LSHTM Independent Panel on the Global Response to Ebola , 2015, The Lancet.

[9]  Art F. Y. Poon,et al.  Near real-time monitoring of HIV transmission hotspots from routine HIV genotyping: an implementation case study , 2016, The lancet. HIV.

[10]  Kristine M Wylie,et al.  Enhanced virome sequencing using targeted sequence capture , 2015, Genome research.

[11]  J. A. Comer,et al.  A novel coronavirus associated with severe acute respiratory syndrome. , 2003, The New England journal of medicine.

[12]  D. Butler What first case of sexually transmitted Ebola means for public health , 2015, Nature.

[13]  S. Zola,et al.  A Behavioral Task Predicts Conversion to Mild Cognitive Impairment and Alzheimer’s Disease , 2013, American journal of Alzheimer's disease and other dementias.

[14]  Caleb Webber,et al.  Large‐scale objective association of mouse phenotypes with human symptoms through structural variation identified in patients with developmental disorders , 2012, Human mutation.

[15]  A. Osterhaus,et al.  Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. , 2012, The New England journal of medicine.

[16]  Trevor Bedford,et al.  Virus genomes reveal factors that spread and sustained the Ebola epidemic , 2017, Nature.

[17]  W. Bolosky,et al.  Laboratory validation of a clinical metagenomic sequencing assay for pathogen detection in cerebrospinal fluid , 2018, bioRxiv.

[18]  Kenneth D. Mandl,et al.  Research Paper: The Value of Patient Self-report for Disease Surveillance , 2007, J. Am. Medical Informatics Assoc..

[19]  T. Kozel,et al.  Point-of-Care Testing for Infectious Diseases: Past, Present, and Future , 2017, Journal of Clinical Microbiology.

[20]  D. Cummings,et al.  The Role of Viral Introductions in Sustaining Community-Based HIV Epidemics in Rural Uganda: Evidence from Spatial Clustering, Phylogenetics, and Egocentric Transmission Models , 2014, PLoS medicine.

[21]  Rachel S. G. Sealfon,et al.  Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak , 2014, Science.

[22]  U. Obolski,et al.  Genomic and epidemiological monitoring of yellow fever virus transmission potential , 2018, Science.

[23]  L. du Plessis,et al.  Getting to the root of epidemic spread with phylodynamic analysis of genomic data. , 2015, Trends in microbiology.

[24]  Elissa J. Chesler,et al.  Mouse Phenome Database: an integrative database and analysis suite for curated empirical phenotype data from laboratory mice , 2017, Nucleic Acids Res..

[25]  Yoshihiro Kawaoka,et al.  oseltamivir: descriptive study , 2022 .

[26]  Hanlee P. Ji,et al.  Next-generation DNA sequencing , 2008, Nature Biotechnology.

[27]  F. Collins,et al.  A new initiative on precision medicine. , 2015, The New England journal of medicine.

[28]  Pardis C. Sabeti,et al.  Data sharing: Make outbreak research open access , 2015, Nature.

[29]  A. Walker,et al.  A Candida auris Outbreak and Its Control in an Intensive Care Setting , 2018, The New England journal of medicine.

[30]  Catherine A. Freije,et al.  Genomic analysis of Lassa virus from the 2018 surge in Nigeria , 2018, The New England journal of medicine.

[31]  E. Lyons,et al.  Pandemic Potential of a Strain of Influenza A (H1N1): Early Findings , 2009, Science.

[32]  Tanja Stadler,et al.  Insights into the Early Epidemic Spread of Ebola in Sierra Leone Provided by Viral Sequence Data , 2014, PLoS currents.

[33]  Trevor Bedford,et al.  Multiplex PCR method for MinION and Illumina sequencing of Zika and other virus genomes directly from clinical samples , 2017, Nature Protocols.

[34]  Rachel S. G. Sealfon,et al.  Evaluation of the Potential Impact of Ebola Virus Genomic Drift on the Efficacy of Sequence-Based Candidate Therapeutics , 2015, mBio.

[35]  A. Telenti,et al.  HIV treatment failure: testing for HIV resistance in clinical practice. , 1998, Science.

[36]  Adrienne T. Hall,et al.  Evaluation of Signature Erosion in Ebola Virus Due to Genomic Drift and Its Impact on the Performance of Diagnostic Assays , 2015, Viruses.

[37]  Shilu Tong,et al.  Using internet search queries for infectious disease surveillance: screening diseases for suitability , 2014, BMC Infectious Diseases.

[38]  Eric S. Lander,et al.  Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011 , 2012, Proceedings of the National Academy of Sciences.

[39]  Elizabeth M. Ryan,et al.  Clinical Sequencing Uncovers Origins and Evolution of Lassa Virus , 2015, Cell.

[40]  Uzma Bashir,et al.  Strengthening the influenza vaccine virus selection and development process: Report of the 3rd WHO Informal Consultation for Improving Influenza Vaccine Virus Selection held at WHO headquarters, Geneva, Switzerland, 1-3 April 2014. , 2015, Vaccine.

[41]  N. R. Faria,et al.  Establishment and cryptic transmission of Zika virus in Brazil and the Americas , 2017, Nature.

[42]  Doug Stryke,et al.  Rapid metagenomic identification of viral pathogens in clinical samples by real-time nanopore sequencing analysis , 2015, Genome Medicine.

[43]  Edward C. Holmes,et al.  The evolution of Ebola virus: Insights from the 2013–2016 epidemic , 2016, Nature.

[44]  Huaqin Pan,et al.  Using PhenX measures to identify opportunities for cross‐study analysis , 2012, Human mutation.

[45]  †The International HapMap Consortium The International HapMap Project , 2003, Nature.

[46]  C. E. Pearson,et al.  Table S2: Trans-factors and trinucleotide repeat instability Trans-factor , 2010 .

[47]  J. Brownstein,et al.  Digital disease detection--harnessing the Web for public health surveillance. , 2009, The New England journal of medicine.

[48]  Pardis C Sabeti,et al.  Roots, Not Parachutes: Research Collaborations Combat Outbreaks , 2016, Cell.

[49]  Trevor Bedford,et al.  Nextstrain: real-time tracking of pathogen evolution , 2017, bioRxiv.

[50]  Policy statement on data sharing by WHO in the context of public health emergencies (as of 13 April 2016. , 2016, Releve epidemiologique hebdomadaire.

[51]  Stephan Günther,et al.  Emergence of Zaire Ebola virus disease in Guinea. , 2014, The New England journal of medicine.

[52]  A. Cann,et al.  Reversion to neurovirulence of the live-attenuated Sabin type 3 oral poliovirus vaccine. , 1984, Nucleic acids research.

[53]  W. Ian Lipkin,et al.  Genetic Detection and Characterization of Lujo Virus, a New Hemorrhagic Fever–Associated Arenavirus from Southern Africa , 2009, PLoS pathogens.

[54]  Trevor Bedford,et al.  nextflu: real-time tracking of seasonal influenza virus evolution in humans , 2015, Bioinform..

[55]  C. Köser,et al.  Mycobacterium tuberculosis drug-resistance testing: challenges, recent developments and perspectives. , 2017, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[56]  P. Robinson,et al.  The Human Phenotype Ontology: a tool for annotating and analyzing human hereditary disease. , 2008, American journal of human genetics.

[57]  J. V. Moran,et al.  Initial sequencing and analysis of the human genome. , 2001, Nature.

[58]  Padmini Ramachandran,et al.  Genomics of foodborne pathogens for microbial food safety. , 2018, Current opinion in biotechnology.

[59]  Trevor Bedford,et al.  Prediction, dynamics, and visualization of antigenic phenotypes of seasonal influenza viruses , 2015, Proceedings of the National Academy of Sciences.

[60]  Tanja Stadler,et al.  Phylodynamics with Migration: A Computational Framework to Quantify Population Structure from Genomic Data , 2016, Molecular biology and evolution.

[61]  Ruth E. Timme,et al.  GenomeTrakr proficiency testing for foodborne pathogen surveillance: an exercise from 2015 , 2018, Microbial genomics.

[62]  Jens H Kuhn,et al.  Molecular Evidence of Sexual Transmission of Ebola Virus. , 2015, The New England journal of medicine.

[63]  O. Pybus,et al.  Measurably evolving pathogens in the genomic era. , 2015, Trends in ecology & evolution.

[64]  O. Pybus,et al.  Genomic Insights into Zika Virus Emergence and Spread , 2018, Cell.

[65]  Charles R. Davies,et al.  An electrocardiogram-based analysis evaluating sleep quality in patients with obstructive sleep apnea , 2013, Sleep and Breathing.

[66]  Darin P Clark,et al.  Whole-animal imaging, gene function, and the Zebrafish Phenome Project. , 2011, Current opinion in genetics & development.

[67]  D. Dassey Outbreak , 1995, The Lancet.

[68]  R. Nielsen,et al.  The Evolutionary Pathway to Virulence of an RNA Virus , 2017, Cell.

[69]  S. Steinhubl,et al.  High-Definition Medicine , 2017, Cell.

[70]  E. Snitkin,et al.  Whole Genome Sequencing—Implications for Infection Prevention and Outbreak Investigations , 2017, Current Infectious Disease Reports.

[71]  Joel O. Wertheim,et al.  Using HIV Networks to Inform Real Time Prevention Interventions , 2014, PloS one.

[72]  Adyasha Maharana,et al.  Social Media as a Sentinel for Disease Surveillance: What Does Sociodemographic Status Have to Do with It? , 2016, PLoS currents.

[73]  J S Brownstein,et al.  HealthMap: the development of automated real-time internet surveillance for epidemic intelligence. , 2007, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[74]  M. Shigematsu,et al.  Using Social Media for Actionable Disease Surveillance and Outbreak Management: A Systematic Literature Review , 2015, PloS one.

[75]  Michael B. Doud,et al.  Complete mapping of viral escape from neutralizing antibodies , 2016, bioRxiv.

[76]  Tarjei S Mikkelsen,et al.  Enhanced methods for unbiased deep sequencing of Lassa and Ebola RNA viruses from clinical and biological samples , 2014, Genome Biology.

[77]  Lauren Ancel Meyers,et al.  Preprints: An underutilized mechanism to accelerate outbreak science , 2018, PLoS Medicine.

[78]  D. Altshuler,et al.  A map of human genome variation from population-scale sequencing , 2010, Nature.

[79]  Toshihiro Tanaka The International HapMap Project , 2003, Nature.

[80]  Timothy B. Stockwell,et al.  The Sequence of the Human Genome , 2001, Science.

[81]  M. McCarthy,et al.  Research Capacity: Enabling African Scientists to Engage Fully in the Genomic Revolution , 2014 .

[82]  M. MacDonald,et al.  Large-scale phenome analysis defines a behavioral signature for Huntington's disease genotype in mice , 2016, Nature Biotechnology.

[83]  Hayden C. Metsky,et al.  Genomic epidemiology reveals multiple introductions of Zika virus into the United States , 2017, Nature.

[84]  Faisal M. Fadlelmola,et al.  Enabling Genomic Revolution in Africa , 2019, The Genetics of African Populations in Health and Disease.

[85]  L. Finelli,et al.  Emergence of a novel swine-origin influenza A (H1N1) virus in humans. , 2009, The New England journal of medicine.

[86]  Peter N. Robinson,et al.  Deep phenotyping for precision medicine , 2012, Human mutation.

[87]  Luc Bissonnette,et al.  Infectious Disease Management through Point-of-Care Personalized Medicine Molecular Diagnostic Technologies , 2012, Journal of personalized medicine.

[88]  C. V. van Dolleweerd,et al.  Monoclonal antibodies for prophylactic and therapeutic use against viral infections , 2013, Vaccine.