Metagenomic analysis of viruses in toilet waste from long distance flights—A new procedure for global infectious disease surveillance

Human viral pathogens are a major public health threat. Reliable information that accurately describes and characterizes the global occurrence and transmission of human viruses is essential to support national and global priority setting, public health actions, and treatment decisions. However, large areas of the globe are currently without surveillance due to limited health care infrastructure and lack of international cooperation. We propose a novel surveillance strategy, using metagenomic analysis of toilet material from international air flights as a method for worldwide viral disease surveillance. The aim of this study was to design, implement, and evaluate a method for viral analysis of airplane toilet waste enabling simultaneous detection and quantification of a wide range of human viral pathogens. Toilet waste from 19 international airplanes was analyzed for viral content, using viral capture probes followed by high-throughput sequencing. Numerous human pathogens were detected including enteric and respiratory viruses. Several geographic trends were observed with samples originating from South Asia having significantly higher viral species richness as well as higher abundances of salivirus A, aichivirus A and enterovirus B, compared to samples originating from North Asia and North America. In addition, certain city specific trends were observed, including high numbers of rotaviruses in airplanes departing from Islamabad. Based on this study we believe that central sampling and analysis at international airports could be a useful supplement for global viral surveillance, valuable for outbreak detection and for guiding public health resources.

[1]  Subarna Roy,et al.  Salivirus in children with diarrhoea, western India. , 2016, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[2]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[3]  K. Eilbeck,et al.  Unbiased Detection of Respiratory Viruses by Use of RNA Sequencing-Based Metagenomics: a Systematic Comparison to a Commercial PCR Panel , 2016, Journal of Clinical Microbiology.

[4]  Søren Brunak,et al.  Investigation of Human Cancers for Retrovirus by Low-Stringency Target Enrichment and High-Throughput Sequencing , 2015, Scientific Reports.

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

[6]  Adam D. Wier,et al.  Raw Sewage Harbors Diverse Viral Populations , 2011, mBio.

[7]  Andrew J. Davison,et al.  Consensus statement: Virus taxonomy in the age of metagenomics , 2017, Nature Reviews Microbiology.

[8]  Z. Mladenova,et al.  Animal Picobirnavirus , 2014, VirusDisease.

[9]  David Wang,et al.  Extensive conservation of prokaryotic ribosomal binding sites in known and novel picobirnaviruses. , 2018, Virology.

[10]  P. Diggle,et al.  The spatiotemporal association of non-prescription retail sales with cases during the 2009 influenza pandemic in Great Britain , 2014, BMJ Open.

[11]  Lawrence O. Gostin,et al.  WHO’s Pandemic Influenza Preparedness Framework: A Milestone in Global Governance for Health , 2011, JAMA.

[12]  Kate E. Jones,et al.  Global trends in emerging infectious diseases , 2008, Nature.

[13]  Christian Drosten,et al.  Commentary: Middle East Respiratory Syndrome Coronavirus (MERS-CoV): Announcement of the Coronavirus Study Group , 2013, Journal of Virology.

[14]  Mikiko Senga,et al.  Ebola virus disease in West Africa--the first 9 months of the epidemic and forward projections. , 2014, The New England journal of medicine.

[15]  V. Erčulj,et al.  Early detection of influenza like illness through medication sales. , 2012, Central European journal of public health.

[16]  N. Speybroeck,et al.  World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010 , 2015, PLoS medicine.

[17]  M. Estes,et al.  Norovirus gastroenteritis. , 2009, The New England journal of medicine.

[18]  Richard Durbin,et al.  Fast and accurate long-read alignment with Burrows–Wheeler transform , 2010, Bioinform..

[19]  David A. Matthews,et al.  Real-time, portable genome sequencing for Ebola surveillance , 2016, Nature.

[20]  B. Bell,et al.  The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. , 2006, Journal of hepatology.

[21]  A. Mangili,et al.  Infectious Risks of Air Travel , 2015, Microbiology spectrum.

[22]  Kristy Deiner,et al.  Special Issue Article: Environmental DNA Choice of capture and extraction methods affect detection of freshwater biodiversity from environmental DNA , 2015 .

[23]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[24]  K. Shah,et al.  Polyomaviruses and human diseases. , 2006, Advances in experimental medicine and biology.

[25]  Clive Brown,et al.  First Confirmed Cases of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Infection in the United States, Updated Information on the Epidemiology of MERS-CoV Infection, and Guidance for the Public, Clinicians, and Public Health Authorities — May 2014 , 2014, American Journal of Transplantation.

[26]  J. Tate,et al.  Global, Regional, and National Estimates of Rotavirus Mortality in Children <5 Years of Age, 2000-2013. , 2016, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[27]  W. Knowles Discovery and epidemiology of the human polyomaviruses BK virus (BKV) and JC virus (JCV). , 2006, Advances in experimental medicine and biology.

[28]  Sandy Cairncross,et al.  Burden of disease from inadequate water, sanitation and hygiene in low- and middle-income settings: a retrospective analysis of data from 145 countries , 2014, Tropical medicine & international health : TM & IH.

[29]  E. Delwart,et al.  Picornavirus Salivirus/Klassevirus in Children with Diarrhea, China , 2010, Emerging infectious diseases.

[30]  S. Rasmussen,et al.  Ancient hepatitis B viruses from the Bronze Age to the Medieval period , 2018, Nature.

[31]  Heng Li Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[32]  Raymond Lo,et al.  Evaluation of shotgun metagenomics sequence classification methods using in silico and in vitro simulated communities , 2015, BMC Bioinformatics.

[33]  Reza Assadi,et al.  The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013 , 2016, The Lancet.

[34]  Raju V. Misra,et al.  Development of a candidate reference material for adventitious virus detection in vaccine and biologicals manufacturing by deep sequencing , 2015, Vaccine.

[35]  Jacqueline E Tate,et al.  estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes : a systematic review and meta-analysis , 2011 .

[36]  M. Al-Ahdal,et al.  Recommended advanced techniques for waterborne pathogen detection in developing countries. , 2015, Journal of infection in developing countries.

[37]  T. Yamashita,et al.  Isolation of Cytopathic Small Round Virus (Aichi Virus) from Pakistani Children and Japanese Travelers from Southeast Asia , 1995, Microbiology and immunology.

[38]  Jacqueline E Tate,et al.  2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. , 2011, The Lancet. Infectious diseases.

[39]  A. Tsakris,et al.  A case of imported Middle East Respiratory Syndrome coronavirus infection and public health response, Greece, April 2014. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[40]  E. Willerslev,et al.  Target-Dependent Enrichment of Virions Determines the Reduction of High-Throughput Sequencing in Virus Discovery , 2015, PloS one.

[41]  W. Team Ebola Virus Disease in West Africa — The First 9 Months of the Epidemic and Forward Projections , 2014 .

[42]  Elyse Stachler,et al.  Ebola Virus Persistence in the Environment: State of the Knowledge and Research Needs , 2015 .

[43]  N. Santos,et al.  Salivirus and aichivirus A infections in children with gastroenteritis in Brazil. , 2015, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[44]  Martin Kircher,et al.  Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform , 2011, Nucleic acids research.

[45]  Paul Turner,et al.  Reagent and laboratory contamination can critically impact sequence-based microbiome analyses , 2014, BMC Biology.

[46]  V. Chizhikov,et al.  Environmental surveillance of viruses by tangential flow filtration and metagenomic reconstruction. , 2016, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[47]  Giovanini Evelim Coelho,et al.  Zika virus in the Americas: Early epidemiological and genetic findings , 2016, Science.

[48]  P. Simmonds,et al.  Disease burden of the most commonly detected respiratory viruses in hospitalized patients calculated using the disability adjusted life year (DALY) model , 2011, Journal of Clinical Virology.

[49]  Rachel L. Marine,et al.  High Variety of Known and New RNA and DNA Viruses of Diverse Origins in Untreated Sewage , 2012, Journal of Virology.

[50]  M. Vicente,et al.  Monitoring influenza activity in Europe with Google Flu Trends: comparison with the findings of sentinel physician networks - results for 2009-10. , 2010, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[51]  A. Osterhaus,et al.  Identification of Multiple Novel Viruses, Including a Parvovirus and a Hepevirus, in Feces of Red Foxes , 2013, Journal of Virology.

[52]  S. Elledge,et al.  Comprehensive serological profiling of human populations using a synthetic human virome , 2015, Science.

[53]  B. Berger,et al.  Use of ion exchange resins in partial purification and concentration of poliomyelitis virus. , 1952, The Journal of laboratory and clinical medicine.

[54]  D. Lazer,et al.  The Parable of Google Flu: Traps in Big Data Analysis , 2014, Science.

[55]  Z. Duan,et al.  Salivirus in Children and Its Association with Childhood Acute Gastroenteritis: A Paired Case-Control Study , 2015, PloS one.

[56]  K. Bibby,et al.  Identification of viral pathogen diversity in sewage sludge by metagenome analysis. , 2013, Environmental science & technology.

[57]  P. Khamrin,et al.  Epidemiology of human and animal kobuviruses , 2014, VirusDisease.

[58]  Ashutosh Kumar Singh,et al.  Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015 , 2016, The Lancet.

[59]  Krzysztof Trzciński,et al.  Deep Sequencing Analyses of Low Density Microbial Communities: Working at the Boundary of Accurate Microbiota Detection , 2012, PloS one.

[60]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[61]  J. Abril,et al.  Evaluation of Methods for the Concentration and Extraction of Viruses from Sewage in the Context of Metagenomic Sequencing , 2017, PloS one.

[62]  X. Zhu,et al.  Concentration and detection of SARS coronavirus in sewage from Xiao Tang Shan Hospital and the 309th Hospital of the Chinese People's Liberation Army. , 2005, Water science and technology : a journal of the International Association on Water Pollution Research.

[63]  S. Rasmussen,et al.  Meta-genomic analysis of toilet waste from long distance flights; a step towards global surveillance of infectious diseases and antimicrobial resistance , 2015, Scientific Reports.

[64]  J. Nguyen-Van-Tam,et al.  The epidemiology and clinical impact of pandemic influenza. , 2003, Vaccine.

[65]  P. Chan,et al.  Tracing the SARS-coronavirus. , 2013, Journal of thoracic disease.

[66]  E. Delwart,et al.  Multiple divergent picobirnaviruses with functional prokaryotic Shine-Dalgarno ribosome binding sites present in cloacal sample of a diarrheic chicken. , 2018, Virology.