{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T16:02:09Z","timestamp":1753891329864,"version":"3.41.2"},"reference-count":26,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,12,9]],"date-time":"2024-12-09T00:00:00Z","timestamp":1733702400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Med."],"abstract":"<jats:p>Rapid and sensitive diagnostic measures are a pre-requisite for the control of SARS-CoV-2 outbreaks. Dogs detect SARS-CoV-2-infected human individuals with high speed due to their extraordinary olfactory acuity. In the post-pandemic phase of SARS-CoV-2 it is difficult to obtain samples from infected humans for scent dog training. Established animal models for COVID-19 include hamsters and ferrets, which could overcome this shortcoming and have the advantage that samples are generated under controlled conditions. Respiratory samples from humans, hamsters and ferrets infected with SARS-CoV-2 and from ferrets infected with an H7-Influenza A virus were inactivated with <jats:italic>\u03b2<\/jats:italic>-propiolactone and presented via a device called \u201cDetection Dog Training System\u201d (DDTS). DDTS allows a fast, blinded, randomized, and automated sample presentation without trainer interference. Scent dogs generally showed a similar diagnostic sensitivity (DSe) and specificity (Dsp) for four tested scenarios (S1-4) and as reported previously for respiratory samples from humans. (S1) Human with COVID-19: DSe 88.1 [74.0\u2013100.0% CI<jats:sub>95%<\/jats:sub>] and DSp 89.6 [80.6\u201398.5% CI<jats:sub>95%<\/jats:sub>]. (S2) Hamster with COVID-19: DSe 82.4 [74.1\u201390.7% CI<jats:sub>95%<\/jats:sub>] and DSp 96.7 [93.7\u201399.7% CI<jats:sub>95%<\/jats:sub>]. (S3) Ferret with COVID-19: DSe 86.2 [69.8\u2013100.0% CI<jats:sub>95%<\/jats:sub>] and DSp 95.1 [89.5\u2013100.0% CI<jats:sub>95%<\/jats:sub>]. (S4) Ferrets infected with an H7 Influenza A-virus (IAV) as a distractor: DSe 96.9 [57.2\u2013100.0% CI<jats:sub>95%<\/jats:sub>] and DSp 89.86 [40.3\u2013100.0% CI<jats:sub>95%<\/jats:sub>]. We provide evidence that scent dogs detect samples from SARS-CoV-2-infected hamsters and ferrets with a similar accuracy as reported for humans. The study highlights that volatile organic compound odor patterns are similar in humans, hamsters, and ferrets after SARS-CoV-2 infection, but distinct after IAV-infection.<\/jats:p>","DOI":"10.3389\/fmed.2024.1476300","type":"journal-article","created":{"date-parts":[[2024,12,9]],"date-time":"2024-12-09T23:57:53Z","timestamp":1733788673000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Scent dogs identify SARS-CoV-2-infections in respiratory samples from experimentally infected ferrets and hamsters\u2014a pilot study"],"prefix":"10.3389","volume":"11","author":[{"given":"Claudia","family":"Schulz","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Friederike","family":"Twele","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sebastian","family":"Meller","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nele A.","family":"ten Hagen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Veronika","family":"Pilchov\u00e1","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katrin","family":"Wirz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sabrina","family":"Clever","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christian","family":"Meyer zu Natrup","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Asisa","family":"Volz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maren","family":"von K\u00f6ckritz-Blickwede","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Holger A.","family":"Volk","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2024,12,9]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"536","DOI":"10.1186\/s12879-020-05281-3","article-title":"Scent dog identification of samples from COVID-19 patients - A pilot study","volume":"20","author":"Jendrny","year":"2020","journal-title":"BMC Infect Dis"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1186\/s12879-021-06411-1","article-title":"Scent dog identification of SARS-CoV-2 infections in different body fluids","volume":"21","author":"Jendrny","year":"2021","journal-title":"BMC Infect Dis"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1824","DOI":"10.3389\/fmed.2022.877259","article-title":"Detection of post-COVID-19 patients using medical scent detection dogs\u2014a pilot study","volume":"9","author":"Twele","year":"2022","journal-title":"Front Med"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.annepidem.2023.05.002","article-title":"Canine olfactory detection of SARS-CoV-2-infected humans\u2014a systematic review","volume":"85","author":"Meller","year":"2023","journal-title":"Ann Epidemiol"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"661","DOI":"10.1177\/03009858211071012","article-title":"Ferrets are valuable models for SARS-CoV-2 research","volume":"59","author":"Ciurkiewicz","year":"2022","journal-title":"Vet Pathol"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"14","DOI":"10.3389\/fimmu.2023.1283595","article-title":"Characterization of young and aged ferrets as animal models for SARS-CoV-2 infection with focus on neutrophil extracellular traps","volume":"14","author":"Pilchov\u00e1","year":"2023","journal-title":"Front Immunol"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1165\/rcmb.2024-0005MA","article-title":"A new methodology for the oxygen measurement in lung tissue of an aged ferret model proves hypoxia during COVID-19","volume":"71","author":"Wirz","year":"2024","journal-title":"Am J Respir Cell Mol Biol"},{"key":"ref8","article-title":"Neutrophil extracellular traps-related host factors associated with acute respiratory distress syndrome (ARDS)-like disease in a ferret model of H7N7-influenza virus infection","volume-title":"Tagung der DVG-Fachgruppe Physiologie & Biochemie","author":"Schulz","year":"2024"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"20731","DOI":"10.2807\/1560-7917.ES2014.19.10.20731","article-title":"Nucleic acid-based detection of influenza A virus subtypes H7 and N9 with a special emphasis on the avian H7N9 virus","volume":"19","author":"Kalthoff","year":"2014","journal-title":"Eur Secur"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"114733","DOI":"10.1016\/j.jviromet.2023.114733","article-title":"\u03b2-Propiolactone (BPL)-inactivation of SARS-co-V-2: in vitro validation with focus on saliva from COVID-19 patients for scent dog training","volume":"317","author":"Pilchov\u00e1","year":"2023","journal-title":"J Virol Methods"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"3590","DOI":"10.3389\/FMED.2022.1015620\/BIBTEX","article-title":"Expert considerations and consensus for using dogs to detect human SARS-CoV-2-infections","volume":"9","author":"Meller","year":"2022","journal-title":"Front Med"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/J.JVEB.2017.05.002","article-title":"Animal olfactory detection of human diseases: guidelines and systematic review","volume":"20","author":"Edwards","year":"2017","journal-title":"J Vet Behav"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"2245","DOI":"10.3389\/fmed.2021.749588","article-title":"Discrimination of SARS-CoV-2 infections from other viral respiratory infections by scent detection dogs","volume":"8","author":"ten Hagen","year":"2021","journal-title":"Front Med"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"20143","DOI":"10.1038\/S41598-021-99742-7","article-title":"A proof of concept study for the differentiation of SARS-CoV-2, hCoV-NL63, and IAV-H1N1 in vitro cultures using ion mobility spectrometry","volume":"11","author":"Feuerherd","year":"2021","journal-title":"Sci Rep"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"13","DOI":"10.3390\/DIAGNOSTICS13040707","article-title":"Investigating the use of SARS-CoV-2 (COVID-19) odor expression as a non-invasive diagnostic tool\u2014pilot study","volume":"13","author":"Crespo-Cajigas","year":"2023","journal-title":"Diagnostics"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"102132","DOI":"10.1016\/J.LEGALMED.2022.102132","article-title":"Identification of volatile organic compounds in muscle tissues of different species based on headspace-gas-chromatography ion-mobility spectrometry","volume":"59","author":"Li","year":"2022","journal-title":"Legal Med"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1016\/J.FORSCIINT.2012.02.007","article-title":"Characterization of the volatile organic compounds present in the headspace of decomposing animal remains, and compared with human remains","volume":"220","author":"Cablk","year":"2012","journal-title":"Forensic Sci Int"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1163\/25889567-BJA10047","article-title":"Quality management and animal welfare as culture of Care for Animal Experiments under biosafety Level-3, taking COVID-19 as a practical example","volume":"1","author":"Richter","year":"2024","journal-title":"J App Animal Ethics Res"},{"year":"2024","key":"ref19","article-title":"Central COFONI technology platform | Universit\u00e4tsmedizin G\u00f6ttingen"},{"year":"2024","key":"ref20","article-title":"Medizinische Hochschule Hannover: Hannover Unified Biobank HUB"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1002\/9781119650836.ch4","article-title":"Basic virology","volume-title":"Veterinary Microbiology","author":"Abouelkhair","year":"2022"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"e218","DOI":"10.1016\/S2666-5247(20)30089-6","article-title":"SARS-CoV-2 in fruit bats, ferrets, pigs, and chickens: an experimental transmission study","volume":"1","author":"Schlottau","year":"2020","journal-title":"Lancet Microbe"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"3450","DOI":"10.1038\/s41467-024-47455-6","article-title":"Bat-borne H9N2 influenza virus evades MxA restriction and exhibits efficient replication and transmission in ferrets","volume":"15","author":"Halwe","year":"2024","journal-title":"Nat Commun"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.35248\/2167-0870.22.S16.002","article-title":"Screening for SARS-CoV-2 persistence in long COVID patients using sniffer dogs and scents from axillary sweats samples","author":"Grandjean","year":"2022","journal-title":"J Clin Trials"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"646022","DOI":"10.3389\/fvets.2021.646022","article-title":"Working dog training for the twenty-first century","volume":"8","author":"Hall","year":"2021","journal-title":"Front Vet Sci"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1007\/978-3-031-35159-4_22","article-title":"Canine Detection of Cancer in Humans: Expectations Versus Reality","volume":"15","author":"Jezierski","year":"2023","journal-title":"Chemical Signals in Vertebrates"}],"container-title":["Frontiers in Medicine"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmed.2024.1476300\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,9]],"date-time":"2024-12-09T23:57:55Z","timestamp":1733788675000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmed.2024.1476300\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,9]]},"references-count":26,"alternative-id":["10.3389\/fmed.2024.1476300"],"URL":"https:\/\/doi.org\/10.3389\/fmed.2024.1476300","relation":{},"ISSN":["2296-858X"],"issn-type":[{"type":"electronic","value":"2296-858X"}],"subject":[],"published":{"date-parts":[[2024,12,9]]},"article-number":"1476300"}}