Using Combined Diagnostic Test Results to Hindcast Trends of Infection from Cross-Sectional Data

Infectious disease surveillance is key to limiting the consequences from infectious pathogens and maintaining animal and public health. Following the detection of a disease outbreak, a response in proportion to the severity of the outbreak is required. It is thus critical to obtain accurate information concerning the origin of the outbreak and its forward trajectory. However, there is often a lack of situational awareness that may lead to over- or under-reaction. There is a widening range of tests available for detecting pathogens, with typically different temporal characteristics, e.g. in terms of when peak test response occurs relative to time of exposure. We have developed a statistical framework that combines response level data from multiple diagnostic tests and is able to ‘hindcast’ (infer the historical trend of) an infectious disease epidemic. Assuming diagnostic test data from a cross-sectional sample of individuals infected with a pathogen during an outbreak, we use a Bayesian Markov Chain Monte Carlo (MCMC) approach to estimate time of exposure, and the overall epidemic trend in the population prior to the time of sampling. We evaluate the performance of this statistical framework on simulated data from epidemic trend curves and show that we can recover the parameter values of those trends. We also apply the framework to epidemic trend curves taken from two historical outbreaks: a bluetongue outbreak in cattle, and a whooping cough outbreak in humans. Together, these results show that hindcasting can estimate the time since infection for individuals and provide accurate estimates of epidemic trends, and can be used to distinguish whether an outbreak is increasing or past its peak. We conclude that if temporal characteristics of diagnostics are known, it is possible to recover epidemic trends of both human and animal pathogens from cross-sectional data collected at a single point in time.

[1]  M. Artois,et al.  Surveillance and monitoring of wildlife diseases. , 2002, Revue scientifique et technique.

[2]  Samuel Soubeyrand,et al.  A Bayesian Inference Framework to Reconstruct Transmission Trees Using Epidemiological and Genetic Data , 2012, PLoS Comput. Biol..

[3]  David A. Rasmussen,et al.  Phylodynamic Inference for Structured Epidemiological Models , 2014, PLoS Comput. Biol..

[4]  Benjamin J Cowling,et al.  Methods for monitoring influenza surveillance data. , 2006, International journal of epidemiology.

[5]  Thibaut Jombart,et al.  outbreaker2: Bayesian Reconstruction of Disease Outbreaks by Combining Epidemiologic and Genomic Data , 2018 .

[6]  R. Colwell,et al.  Temporal and Spatial Variability in the Distribution of Vibrio vulnificus in the Chesapeake Bay: A Hindcast Study , 2011, EcoHealth.

[7]  B. Althouse,et al.  Asymptomatic transmission and the resurgence of Bordetella pertussis , 2015, BMC Medicine.

[8]  Sergei L. Kosakovsky Pond,et al.  Phylodynamics of Infectious Disease Epidemics , 2009, Genetics.

[9]  L. Matthews,et al.  The construction and analysis of epidemic trees with reference to the 2001 UK foot–and–mouth outbreak , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  E. Nsoesie,et al.  A Simulation Optimization Approach to Epidemic Forecasting , 2013, PloS one.

[11]  G. Casella,et al.  Explaining the Gibbs Sampler , 1992 .

[12]  Arturo Casadevall,et al.  Host-Pathogen Interactions: Basic Concepts of Microbial Commensalism, Colonization, Infection, and Disease , 2000, Infection and Immunity.

[13]  G. Leung,et al.  Reflections on Pandemic (H1N1) 2009 and the International Response , 2010, PLoS medicine.

[14]  A Charlett,et al.  Changes in severity of 2009 pandemic A/H1N1 influenza in England: a Bayesian evidence synthesis , 2011, BMJ : British Medical Journal.

[15]  J. Shaman,et al.  Forecasting seasonal outbreaks of influenza , 2012, Proceedings of the National Academy of Sciences.

[16]  Gavin J. D. Smith,et al.  Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic , 2009, Nature.

[17]  A. L. Koch,et al.  The logarithm in biology. 1. Mechanisms generating the log-normal distribution exactly. , 1966, Journal of theoretical biology.

[18]  David S. Wethey,et al.  Ecological hindcasting of biogeographic responses to climate change in the European intertidal zone , 2008, Hydrobiologia.

[19]  J. Coetzer,et al.  Infectious diseases of livestock , 2004 .

[20]  P. Teunis,et al.  Estimation of incidences of infectious diseases based on antibody measurements , 2009, Statistics in medicine.

[21]  J. Sánchez-Vizcaíno,et al.  Experimental infection of European red deer (Cervus elaphus) with bluetongue virus serotypes 1 and 8. , 2010, Veterinary microbiology.

[22]  Nedialko B. Dimitrov,et al.  Optimizing Provider Recruitment for Influenza Surveillance Networks , 2012, PLoS Comput. Biol..

[23]  K. Stärk,et al.  Evaluation and optimization of surveillance systems for rare and emerging infectious diseases , 2008 .

[24]  W. Cleveland,et al.  Locally Weighted Regression: An Approach to Regression Analysis by Local Fitting , 1988 .

[25]  Gavin J. Gibson,et al.  A Systematic Bayesian Integration of Epidemiological and Genetic Data , 2015, PLoS Comput. Biol..

[26]  W. Stahel,et al.  Log-normal Distributions across the Sciences: Keys and Clues , 2001 .

[27]  Louise Matthews,et al.  New approaches to quantifying the spread of infection , 2005, Nature Reviews Microbiology.

[28]  F. Mooi,et al.  Seroprevalence of Pertussis in the Netherlands: Evidence for Increased Circulation of Bordetella pertussis , 2010, PloS one.

[29]  P. Gustafson,et al.  Conservative prior distributions for variance parameters in hierarchical models , 2006 .

[30]  C. Gilligan,et al.  Parameter estimation and prediction for the course of a single epidemic outbreak of a plant disease , 2007, Journal of The Royal Society Interface.

[31]  Rowland R Kao,et al.  Supersize me: how whole-genome sequencing and big data are transforming epidemiology , 2014, Trends in Microbiology.

[32]  J. Schellekens,et al.  Kinetics of the IgG antibody response to pertussis toxin after infection with B. pertussis , 2002, Epidemiology and Infection.

[33]  J. P. Davis,et al.  A countywide outbreak of pertussis: initial transmission in a high school weight room with subsequent substantial impact on adolescents and adults. , 2008, Archives of pediatrics & adolescent medicine.

[34]  P. Teunis,et al.  Sero-epidemiology as a tool to study the incidence of Salmonella infections in humans , 2007, Epidemiology and Infection.

[35]  J. Schellekens,et al.  Age-specific long-term course of IgG antibodies to pertussis toxin after symptomatic infection with Bordetella pertussis , 2005, Epidemiology and Infection.

[36]  Declan Butler,et al.  Disease surveillance needs a revolution , 2006, Nature.

[37]  K. Stärk,et al.  Evaluation and optimization of surveillance systems for rare and emerging infectious diseases. , 2008, Veterinary research.

[38]  Paul H. Garthwaite,et al.  Statistical methods for the prospective detection of infectious disease outbreaks: a review , 2012 .

[39]  Martyn Plummer,et al.  JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling , 2003 .

[40]  N G Becker,et al.  Effective reproduction numbers are commonly overestimated early in a disease outbreak , 2011, Statistics in medicine.

[41]  Carsten O. Daub,et al.  Transcriptional Dynamics Reveal Critical Roles for Non-coding RNAs in the Immediate-Early Response , 2015, PLoS Comput. Biol..

[42]  A. Gelman Prior distributions for variance parameters in hierarchical models (comment on article by Browne and Draper) , 2004 .

[43]  H W Saatkamp,et al.  Financial consequences of the Dutch bluetongue serotype 8 epidemics of 2006 and 2007. , 2010, Preventive veterinary medicine.

[44]  J. Zipprich,et al.  California pertussis epidemic, 2010. , 2012, The Journal of pediatrics.

[45]  A Perez,et al.  Global animal disease surveillance , 2011, Spatial and Spatio-temporal Epidemiology.

[46]  E. Bingen,et al.  Real-Time PCR Measurement of Persistence of Bordetella pertussis DNA in Nasopharyngeal Secretions during Antibiotic Treatment of Young Children with Pertussis , 2008, Journal of Clinical Microbiology.

[47]  Nick Andrews,et al.  A Statistical Algorithm for the Early Detection of Outbreaks of Infectious Disease , 1996 .

[48]  Pia Hardelid,et al.  Age-Specific Incidence of A/H1N1 2009 Influenza Infection in England from Sequential Antibody Prevalence Data Using Likelihood-Based Estimation , 2011, PloS one.

[49]  Víctor Hugo Borja-Aburto,et al.  Infection and death from influenza A H1N1 virus in Mexico: a retrospective analysis , 2009, The Lancet.

[50]  A. King,et al.  The pertussis enigma: reconciling epidemiology, immunology and evolution , 2016, Proceedings of the Royal Society B: Biological Sciences.

[51]  A. Cook,et al.  Real-Time Epidemic Monitoring and Forecasting of H1N1-2009 Using Influenza-Like Illness from General Practice and Family Doctor Clinics in Singapore , 2010, PloS one.

[52]  Maia Martcheva,et al.  Optimal Sampling Strategies for Detecting Zoonotic Disease Epidemics , 2014, PLoS Comput. Biol..

[53]  Alan S. Perelson,et al.  Estimating time since infection in early homogeneous HIV-1 samples using a poisson model , 2010, BMC Bioinformatics.

[54]  Lauren Ancel Meyers,et al.  Epidemiological and viral genomic sequence analysis of the 2014 ebola outbreak reveals clustered transmission. , 2015, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[55]  P. Rohani,et al.  Perplexities of pertussis: recent global epidemiological trends and their potential causes , 2013, Epidemiology and Infection.

[56]  Gertraud Regula,et al.  Concepts for risk-based surveillance in the field of veterinary medicine and veterinary public health: Review of current approaches , 2006, BMC Health Services Research.

[57]  N. Toft,et al.  Bayesian estimation of true between-herd and within-herd prevalence of Salmonella in Danish veal calves. , 2011, Preventive veterinary medicine.