1887
  1. Home
  2. Eurosurveillance
  3. Volume 30, Issue 38, 25/Sep/2025
  4. Article
Research Open Access
Like 0
Download

Abstract

BACKGROUND

Hospital-based communicable disease surveillance may be costly during large outbreaks and often misses mild or asymptomatic infections. It can be enhanced by environmental surveillance, which monitors circulating pathogens, even from asymptomatic carriers.

AIM

We investigated if tracking viruses in indoor air could be used for their surveillance in a community setting. We also tested the value of untargeted metagenomics to identify viruses in air samples.

METHODS

Weekly indoor air samples were collected with active air samplers from January until December 2022 from a daycare centre in Leuven, Belgium. Samples were analysed using respiratory and enteric quantitative (q)PCR panels, as well as with untargeted metagenomics, enabling both targeted and agnostic viral detections.

RESULTS

Human-associated viruses were detected in 40 of 42 samples across the study period, with MW polyomavirus being most prevalent (33 samples). Respiratory agents such as rhinoviruses and RSV-B and enteric viruses including rotavirus A, astrovirus, and adenovirus appeared at epidemiologically expected times. Skin-associated viruses were also observed, notably Merkel cell polyomavirus and STL polyomavirus. Metagenomics enabled reconstructing multiple complete genomes, distinguishing viral subtypes and detecting copresence of closely related variants. Additionally, several animal, insect, fungal, and plant viruses were found, reflecting both indoor and outdoor environmental exposure.

CONCLUSION

Indoor air monitoring, combined with untargeted metagenomics, demonstrates a potential to support virus surveillance. This approach can allow monitoring circulation of viruses in community settings, including those causing asymptomatic or mild infections. By enabling to reconstruct complete viral genomes, it allows detailed variant tracking, facilitating adapted public health responses.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2025.30.38.2400711
2025-09-25
2026-04-19
/content/10.2807/1560-7917.ES.2025.30.38.2400711
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/30/38/eurosurv-30-38-2.html?itemId=/content/10.2807/1560-7917.ES.2025.30.38.2400711&mimeType=html&fmt=ahah

References

  1. Abat C, Chaudet H, Rolain JM, Colson P, Raoult D. Traditional and syndromic surveillance of infectious diseases and pathogens. Int J Infect Dis. 2016;48:22-8.  https://doi.org/10.1016/j.ijid.2016.04.021  PMID: 27143522 
  2. Leifels M, Khalilur Rahman O, Sam IC, Cheng D, Chua FJD, Nainani D, et al. The one health perspective to improve environmental surveillance of zoonotic viruses: lessons from COVID-19 and outlook beyond. ISME Commun. 2022;2(1):107.  https://doi.org/10.1038/s43705-022-00191-8  PMID: 36338866 
  3. Vieira CB, de Abreu Corrêa A, de Jesus MS, Luz SLB, Wyn-Jones P, Kay D, et al. Viruses Surveillance Under Different Season Scenarios of the Negro River Basin, Amazonia, Brazil. Food Environ Virol. 2016;8(1):57-69.  https://doi.org/10.1007/s12560-016-9226-8  PMID: 26783031 
  4. Iaconelli M, Muscillo M, Della Libera S, Fratini M, Meucci L, De Ceglia M, et al. One-year Surveillance of Human Enteric Viruses in Raw and Treated Wastewaters, Downstream River Waters, and Drinking Waters. Food Environ Virol. 2017;9(1):79-88.  https://doi.org/10.1007/s12560-016-9263-3  PMID: 27682315 
  5. Moresco V, Oliver DM, Weidmann M, Matallana-Surget S, Quilliam RS. Survival of human enteric and respiratory viruses on plastics in soil, freshwater, and marine environments. Environ Res. 2021;199:111367.  https://doi.org/10.1016/j.envres.2021.111367  PMID: 34029551 
  6. Kilaru P, Hill D, Anderson K, Collins MB, Green H, Kmush BL, et al. Wastewater Surveillance for Infectious Disease: A Systematic Review. Am J Epidemiol. 2023;192(2):305-22.  https://doi.org/10.1093/aje/kwac175  PMID: 36227259 
  7. Amman F, Markt R, Endler L, Hupfauf S, Agerer B, Schedl A, et al. Viral variant-resolved wastewater surveillance of SARS-CoV-2 at national scale. Nat Biotechnol. 2022;40(12):1814-22.  https://doi.org/10.1038/s41587-022-01387-y  PMID: 35851376 
  8. Jahn K, Dreifuss D, Topolsky I, Kull A, Ganesanandamoorthy P, Fernandez-Cassi X, et al. Early detection and surveillance of SARS-CoV-2 genomic variants in wastewater using COJAC. Nat Microbiol. 2022;7(8):1151-60.  https://doi.org/10.1038/s41564-022-01185-x  PMID: 35851854 
  9. Wastewater monitoring comes of age. Nat Microbiol. 2022;7(8):1101-2.  https://doi.org/10.1038/s41564-022-01201-0  PMID: 35918421 
  10. Dietz L, Constant DA, Fretz M, Horve PF, Olsen-Martinez A, Stenson J, et al. Exploring Integrated Environmental Viral Surveillance of Indoor Environments: A comparison of surface and bioaerosol environmental sampling in hospital rooms with COVID-19 patients. medRxiv. 2021. Preprint .  https://doi.org/10.1101/2021.03.26.21254416 
  11. Raymenants J, Geenen C, Budts L, Thibaut J, Thijssen M, De Mulder H, et al. Indoor air surveillance and factors associated with respiratory pathogen detection in community settings in Belgium. Nat Commun. 2023;14(1):1332.  https://doi.org/10.1038/s41467-023-36986-z  PMID: 36898982 
  12. Ramuta MD, Newman CM, Brakefield SF, Stauss MR, Wiseman RW, Kita-Yarbro A, et al. SARS-CoV-2 and other respiratory pathogens are detected in continuous air samples from congregate settings. Nat Commun. 2022;13(1):4717.  https://doi.org/10.1038/s41467-022-32406-w  PMID: 35953484 
  13. Raymenants J, Van Gestel L, Coppens J, De Block T, Bangwen E, Rutgers J, et al. Detection of mpox virus in ambient air in a sexual health clinic. Arch Virol. 2023;168(8):210.  https://doi.org/10.1007/s00705-023-05837-z  PMID: 37486383 
  14. Happaerts M, Geenen C, Michiels J, Gorissen S, Swinnen J, Beuselinck K, et al. Centralised Air Sampling From a Ventilation System for the Surveillance of Respiratory Pathogens. Indoor Air. 2024;1(1):5176619.  https://doi.org/10.1155/2024/5176619 
  15. Sinclair RG, Choi CY, Riley MR, Gerba CP. Pathogen surveillance through monitoring of sewer systems. Adv Appl Microbiol. 2008;65:249-69.  https://doi.org/10.1016/S0065-2164(08)00609-6  PMID: 19026868 
  16. Wang G, Li S, Yan Q, Guo R, Zhang Y, Chen F, et al. Optimization and evaluation of viral metagenomic amplification and sequencing procedures toward a genome-level resolution of the human fecal DNA virome. J Adv Res. 2023;48:75-86.  https://doi.org/10.1016/j.jare.2022.08.011  PMID: 35995413 
  17. Conceição-Neto N, Yinda KC, Van Ranst M, Matthijnssens J. NetoVIR: Modular Approach to Customize Sample Preparation Procedures for Viral Metagenomics. Methods Mol Biol. 2018;1838:85-95.  https://doi.org/10.1007/978-1-4939-8682-8_7  PMID: 30128991 
  18. Van Espen L, Bak EG, Beller L, Close L, Deboutte W, Juel HB, et al. A Previously Undescribed Highly Prevalent Phage Identified in a Danish Enteric Virome Catalog. mSystems. 2021;6(5):e0038221.  https://doi.org/10.1128/msystems.00382-21  PMID: 34665009 
  19. Yinda CK, Rector A, Zeller M, Conceição-Neto N, Heylen E, Maes P, et al. A single bat species in Cameroon harbors multiple highly divergent papillomaviruses in stool identified by metagenomics analysis. Virol Rep. 2016;6:74-80.  https://doi.org/10.1016/j.virep.2016.08.001  PMID: 32289018 
  20. Shi C, Beller L, Deboutte W, Yinda KC, Delang L, Vega-Rúa A, et al. Stable distinct core eukaryotic viromes in different mosquito species from Guadeloupe, using single mosquito viral metagenomics. Microbiome. 2019;7(1):121.  https://doi.org/10.1186/s40168-019-0734-2  PMID: 31462331 
  21. Deboutte W, Beller L, Yinda CK, Maes P, de Graaf DC, Matthijnssens J. Honey-bee-associated prokaryotic viral communities reveal wide viral diversity and a profound metabolic coding potential. Proc Natl Acad Sci USA. 2020;117(19):10511-9.  https://doi.org/10.1073/pnas.1921859117  PMID: 32341166 
  22. Ortega-Parra N, Zisi Z, Vogel E, Vos C, Hanssen I. First report of infections with isolates of the Asian genotype of Cucumber green mottle mosaic virus in cucumber crops in Belgium. Plant Dis. 2024;108(4):1121.  https://doi.org/10.1094/PDIS-11-23-2532-PDN 
  23. Gauthier NPG, Chorlton SD, Krajden M, Manges AR. Agnostic Sequencing for Detection of Viral Pathogens. Clin Microbiol Rev. 2023;36(1):e0011922.  https://doi.org/10.1128/cmr.00119-22  PMID: 36847515 
  24. Prussin AJ 2nd, Marr LC, Bibby KJ. Challenges of studying viral aerosol metagenomics and communities in comparison with bacterial and fungal aerosols. FEMS Microbiol Lett. 2014;357(1):1-9.  https://doi.org/10.1111/1574-6968.12487  PMID: 24891293 
  25. Minor NR, Ramuta MD, Stauss MR, Harwood OE, Brakefield SF, Alberts A, et al. Metagenomic sequencing detects human respiratory and enteric viruses in air samples collected from congregate settings. Sci Rep. 2023;13(1):21398.  https://doi.org/10.1038/s41598-023-48352-6  PMID: 38049453 
  26. Hannet I, Engsbro AL, Pareja J, Schneider UV, Lisby JG, Pružinec-Popović B, et al. Multicenter evaluation of the new QIAstat Gastrointestinal Panel for the rapid syndromic testing of acute gastroenteritis. Eur J Clin Microbiol Infect Dis. 2019;38(11):2103-12.  https://doi.org/10.1007/s10096-019-03646-4  PMID: 31352670 
  27. Conceição-Neto N, Zeller M, Lefrère H, De Bruyn P, Beller L, Deboutte W, et al. Modular approach to customise sample preparation procedures for viral metagenomics: a reproducible protocol for virome analysis. Sci Rep. 2015;5(1):16532.  https://doi.org/10.1038/srep16532  PMID: 26559140 
  28. Federale Overheidsdienst Sociale Zekerheid. Koninklijk besluit tot vaststelling van de financieringsvoorwaarden van de referentiecentra voor humane microbiologie. [Royal Decree establishing the financing conditions of the reference centres for human microbiology]. Brussels: Federale Overheidsdienst JUSTITIE; Feb 2011. Available from: https://www.ejustice.just.fgov.be/cgi/article_body.pl?language=nl&pub_date=2011-03-01&numac=2011022071
  29. Tisza M, Javornik Cregeen S, Avadhanula V, Zhang P, Ayvaz T, Feliz K, et al. Wastewater sequencing reveals community and variant dynamics of the collective human virome. Nat Commun. 2023;14(1):6878.  https://doi.org/10.1038/s41467-023-42064-1  PMID: 37898601 
  30. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10(2):giab008.  https://doi.org/10.1093/gigascience/giab008  PMID: 33590861 
  31. De Coninck L. ViPER. Zenodo; 2023. [Accessed 26 Sep 2023]. Available from: https://zenodo.org/record/5502203
  32. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes De Novo Assembler. Curr Protoc Bioinformatics. 2020;70(1):e102.  https://doi.org/10.1002/cpbi.102  PMID: 32559359 
  33. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12(1):59-60.  https://doi.org/10.1038/nmeth.3176  PMID: 25402007 
  34. Camargo AP, Roux S, Schulz F, Babinski M, Xu Y, Hu B, et al. You can move, but you can’t hide: identification of mobile genetic elements with geNomad. Bioinformatics; 2023.  https://doi.org/10.1101/2023.03.05.531206 
  35. Tregoning JS, Schwarze J. Respiratory viral infections in infants: causes, clinical symptoms, virology, and immunology. Clin Microbiol Rev. 2010;23(1):74-98.  https://doi.org/10.1128/CMR.00032-09  PMID: 20065326 
  36. Biscaro V, Piccinelli G, Gargiulo F, Ianiro G, Caruso A, Caccuri F, et al. Detection and molecular characterization of enteric viruses in children with acute gastroenteritis in Northern Italy. Infect Genet Evol. 2018;60:35-41.  https://doi.org/10.1016/j.meegid.2018.02.011  PMID: 29438743 
  37. Siebrasse EA, Reyes A, Lim ES, Zhao G, Mkakosya RS, Manary MJ, et al. Identification of MW polyomavirus, a novel polyomavirus in human stool. J Virol. 2012;86(19):10321-6.  https://doi.org/10.1128/JVI.01210-12  PMID: 22740408 
  38. Vanchiere JA, Abudayyeh S, Copeland CM, Lu LB, Graham DY, Butel JS. Polyomavirus shedding in the stool of healthy adults. J Clin Microbiol. 2009;47(8):2388-91.  https://doi.org/10.1128/JCM.02472-08  PMID: 19494079 
  39. Lim ES, Reyes A, Antonio M, Saha D, Ikumapayi UN, Adeyemi M, et al. Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology. 2013;436(2):295-303.  https://doi.org/10.1016/j.virol.2012.12.005  PMID: 23276405 
  40. Ong DSY, Schuurman R, Heikens E. Human bocavirus in stool: A true pathogen or an innocent bystander? J Clin Virol. 2016;74:45-9.  https://doi.org/10.1016/j.jcv.2015.11.027  PMID: 26655268 
  41. Kapusinszky B, Minor P, Delwart E. Nearly constant shedding of diverse enteric viruses by two healthy infants. J Clin Microbiol. 2012;50(11):3427-34.  https://doi.org/10.1128/JCM.01589-12  PMID: 22875894 
  42. Beller L, Deboutte W, Vieira-Silva S, Falony G, Tito RY, Rymenans L, et al. The virota and its transkingdom interactions in the healthy infant gut. Proc Natl Acad Sci USA. 2022;119(13):e2114619119.  https://doi.org/10.1073/pnas.2114619119  PMID: 35320047 
  43. Araujo NM. A dual role for adeno-associated virus in human health. Virol J. 2023;20(1):228.  https://doi.org/10.1186/s12985-023-02196-8  PMID: 37817259 
  44. Schowalter RM, Pastrana DV, Pumphrey KA, Moyer AL, Buck CB. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe. 2010;7(6):509-15.  https://doi.org/10.1016/j.chom.2010.05.006  PMID: 20542254 
  45. Bopp L, Wieland U, Hellmich M, Kreuter A, Pfister H, Silling S. Natural History of Cutaneous Human Polyomavirus Infection in Healthy Individuals. Front Microbiol. 2021;12:740947.  https://doi.org/10.3389/fmicb.2021.740947  PMID: 34733257 
  46. Aldridge RW, Lewer D, Beale S, Johnson AM, Zambon M, Hayward AC, et al. , Flu Watch Group. Seasonality and immunity to laboratory-confirmed seasonal coronaviruses (HCoV-NL63, HCoV-OC43, and HCoV-229E): results from the Flu Watch cohort study. Wellcome Open Res. 2020;5:52.  https://doi.org/10.12688/wellcomeopenres.15812.2  PMID: 33447664 
  47. Ramaekers K, Keyaerts E, Rector A, Borremans A, Beuselinck K, Lagrou K, et al. Prevalence and seasonality of six respiratory viruses during five consecutive epidemic seasons in Belgium. J Clin Virol. 2017;94:72-8.  https://doi.org/10.1016/j.jcv.2017.07.011  PMID: 28772168 
  48. Horvat C, Casalegno JS, Masson E, Benveniste C, Haesebaert J, Paget J, et al. Contribution of Infant Rhinovirus Bronchiolitis to Hospital Bed and Ventilation Use. JAMA Netw Open. 2024;7(2):e2355033.  https://doi.org/10.1001/jamanetworkopen.2023.55033  PMID: 38324316 
  49. Simpson S, Kaufmann MC, Glozman V, Chakrabarti A. Disease X: accelerating the development of medical countermeasures for the next pandemic. Lancet Infect Dis. 2020;20(5):e108-15.  https://doi.org/10.1016/S1473-3099(20)30123-7  PMID: 32197097 
  50. Rosario K, Fierer N, Miller S, Luongo J, Breitbart M. Diversity of DNA and RNA Viruses in Indoor Air As Assessed via Metagenomic Sequencing. Environ Sci Technol. 2018;52(3):1014-27.  https://doi.org/10.1021/acs.est.7b04203  PMID: 29298386 
  51. Uda K, Koyama-Wakai C, Shoji K, Iwase N, Motooka D, Nakamura S, et al. WU polyomavirus detected in children with severe respiratory failure. J Clin Virol. 2018;107:25-8.  https://doi.org/10.1016/j.jcv.2018.08.003  PMID: 30114678 
  52. Kuypers J, Campbell AP, Guthrie KA, Wright NL, Englund JA, Corey L, et al. WU and KI polyomaviruses in respiratory samples from allogeneic hematopoietic cell transplant recipients. Emerg Infect Dis. 2012;18(10):1580-8.  https://doi.org/10.3201/eid1810.120477  PMID: 23017213 
  53. Abed Y, Wang D, Boivin G. WU polyomavirus in children, Canada. Emerg Infect Dis. 2007;13(12):1939-41.  https://doi.org/10.3201/eid1312.070909  PMID: 18258053 
  54. Rockett RJ, Bialasiewicz S, Mhango L, Gaydon J, Holding R, Whiley DM, et al. Acquisition of human polyomaviruses in the first 18 months of life. Emerg Infect Dis. 2015;21(2):365-7.  https://doi.org/10.3201/eid2102.141429  PMID: 25626138 
  55. Borges JT, Nakada LYK, Maniero MG, Guimarães JR. SARS-CoV-2: a systematic review of indoor air sampling for virus detection. Environ Sci Pollut Res Int. 2021;28(30):40460-73.  https://doi.org/10.1007/s11356-021-13001-w  PMID: 33630259 
  56. Eren ZB, Vatansever C, Kabadayı B, Haykar B, Kuloğlu ZE, Ay S, et al. Surveillance of respiratory viruses by aerosol screening in indoor air as an early warning system for epidemics. Environ Microbiol Rep. 2024;16(4):e13303.  https://doi.org/10.1111/1758-2229.13303  PMID: 38982659 
  57. Hernaez B, Muñoz-Gómez A, Sanchiz A, Orviz E, Valls-Carbo A, Sagastagoitia I, et al. Monitoring monkeypox virus in saliva and air samples in Spain: a cross-sectional study. Lancet Microbe. 2023;4(1):e21-8.  https://doi.org/10.1016/S2666-5247(22)00291-9  PMID: 36436538 
  58. Geenen C, Traets S, Gorissen S, Happaerts M, Beuselinck K, Laenen L, et al. Interpretation of indoor air surveillance for respiratory infections: a prospective longitudinal observational study in a childcare setting. EBioMedicine. 2025;112:105512.  https://doi.org/10.1016/j.ebiom.2024.105512  PMID: 39884186 
  59. Kwok KTT, de Rooij MMT, Messink AB, Wouters IM, Smit LAM, Cotten M, et al. Establishing farm dust as a useful viral metagenomic surveillance matrix. Sci Rep. 2022;12(1):16308.  https://doi.org/10.1038/s41598-022-20701-x  PMID: 36175536 
  60. Justen L, Grimm S, Esvelt K, Bradshaw W. Indoor Air Sampling for Detection of Viral Nucleic Acids. SSRN Electron J. 2024 [Accessed 18 Jul 2024] .  https://doi.org/10.2139/ssrn.4823882 
  61. Prussin AJ 2nd, Torres PJ, Shimashita J, Head SR, Bibby KJ, Kelley ST, et al. Seasonal dynamics of DNA and RNA viral bioaerosol communities in a daycare center. Microbiome. 2019;7(1):53.  https://doi.org/10.1186/s40168-019-0672-z  PMID: 30935423 
Shotgun metagenomics on indoor air for surveillance of respiratory, enteric, and skin viruses in a Belgian daycare setting, January to December 2022
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Mustafa+Karatas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Karatas Mustafa</a>, <a href="/search?value1=Caspar+Geenen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Geenen Caspar</a>, <a href="/search?value1=Els+Keyaerts&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Keyaerts Els</a>, <a href="/search?value1=Lore+Budts&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Budts Lore</a>, <a href="/search?value1=Joren+Raymenants&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Raymenants Joren</a>, <a href="/search?value1=Charlotte+Eggers&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Eggers Charlotte</a>, <a href="/search?value1=Bastiaan+Craessaerts&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Craessaerts Bastiaan</a>, <a href="/search?value1=Emmanuel+Andr%C3%A9&option1=author&noRedirect=true" class="nonDisambigAuthorLink">André Emmanuel</a>, <a href="/search?value1=Jelle+Matthijnssens&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Matthijnssens Jelle</a></span>. Shotgun metagenomics on indoor air for surveillance of respiratory, enteric, and skin viruses in a Belgian daycare setting, January to December 2022. <a href="/content/ecdc">Euro Surveill.</a> 2025;30(38):pii=2400711. <a href="https://doi.org/10.2807/1560-7917.ES.2025.30.38.2400711" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2025.30.38.2400711</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 28 Oct 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 24 Feb 2025 </span> </p>
/content/10.2807/1560-7917.ES.2025.30.38.2400711
/content/10.2807/1560-7917.ES.2025.30.38.2400711
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error