{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,23]],"date-time":"2026-01-23T20:24:10Z","timestamp":1769199850030,"version":"3.49.0"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,7,1]],"date-time":"2025-07-01T00:00:00Z","timestamp":1751328000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2025,7,1]],"date-time":"2025-07-01T00:00:00Z","timestamp":1751328000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"DOI":"10.1038\/s41598-025-06730-2","type":"journal-article","created":{"date-parts":[[2025,7,1]],"date-time":"2025-07-01T18:35:15Z","timestamp":1751394915000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Evaluating the distribution and clustering of SARS-CoV-2 antibodies in dogs across the United States of America"],"prefix":"10.1038","volume":"15","author":[{"given":"Chi","family":"Chen","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mohammed","family":"Nooruzzaman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Csaba","family":"Varga","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Akhila","family":"Naru","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hannah Rose","family":"Cohen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mara S.","family":"Varvil","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nicolas","family":"Hernandez","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Diego G.","family":"Diel","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ying","family":"Fang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2025,7,1]]},"reference":[{"key":"6730_CR1","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1016\/S0140-6736(20)30251-8","volume":"395","author":"R Lu","year":"2020","unstructured":"Lu, R. et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: Implications for virus origins and receptor binding. The Lancet 395, 565\u2013574 (2020).","journal-title":"The Lancet"},{"key":"6730_CR2","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1038\/s41579-020-00459-7","volume":"19","author":"B Hu","year":"2021","unstructured":"Hu, B., Guo, H., Zhou, P. & Shi, Z.-L. Characteristics of SARS-CoV-2 and COVID-19. Nat. Rev. Microbiol. 19, 141\u2013154 (2021).","journal-title":"Nat. Rev. Microbiol."},{"key":"6730_CR3","doi-asserted-by":"publisher","first-page":"549","DOI":"10.3906\/sag-2004-127","volume":"50","author":"M Has\u00f6ks\u00fcz","year":"2020","unstructured":"Has\u00f6ks\u00fcz, M., Kilic, S. & Sara\u00e7, F. Coronaviruses and sars-cov-2. Turkish J. Med. Sci. 50, 549\u2013556 (2020).","journal-title":"Turkish J. Med. Sci."},{"key":"6730_CR4","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1038\/s41586-020-2008-3","volume":"579","author":"F Wu","year":"2020","unstructured":"Wu, F. et al. A new coronavirus associated with human respiratory disease in China. Nature 579, 265\u2013269. https:\/\/doi.org\/10.1038\/s41586-020-2008-3 (2020).","journal-title":"Nature"},{"key":"6730_CR5","doi-asserted-by":"publisher","DOI":"10.3389\/fvets.2020.596391","volume":"7","author":"MA Mahdy","year":"2020","unstructured":"Mahdy, M. A., Younis, W. & Ewaida, Z. An overview of SARS-CoV-2 and animal infection. Front. Vet. Sci. 7, 596391 (2020).","journal-title":"Front. Vet. Sci."},{"key":"6730_CR6","doi-asserted-by":"publisher","first-page":"2322","DOI":"10.1080\/22221751.2020.1833687","volume":"9","author":"NN Gaudreault","year":"2020","unstructured":"Gaudreault, N. N. et al. SARS-CoV-2 infection, disease and transmission in domestic cats. Emerg. Microbes Infect. 9, 2322\u20132332 (2020).","journal-title":"Emerg. Microbes Infect."},{"key":"6730_CR7","doi-asserted-by":"publisher","first-page":"e00961","DOI":"10.1128\/jvi.00961-22","volume":"96","author":"M Martins","year":"2022","unstructured":"Martins, M. et al. The omicron variant BA.1.1 presents a lower pathogenicity than B.1 D614G and delta variants in a feline model of SARS-CoV-2 infection. J. Virol. 96, e00961-e922. https:\/\/doi.org\/10.1128\/jvi.00961-22 (2022).","journal-title":"J. Virol."},{"key":"6730_CR8","doi-asserted-by":"publisher","first-page":"9970311","DOI":"10.1155\/2024\/9970311","volume":"2024","author":"BD Tomeo-Mart\u00edn","year":"2024","unstructured":"Tomeo-Mart\u00edn, B. D., Delgado-Bonet, P., Cejalvo, T., Herranz, S. & Peris\u00e9-Barrios, A. J. A comprehensive study of cellular and humoral immunity in dogs naturally exposed to SARS-CoV-2. Transbound Emerg. Dis. 2024, 9970311. https:\/\/doi.org\/10.1155\/2024\/9970311 (2024).","journal-title":"Transbound Emerg. Dis."},{"key":"6730_CR9","doi-asserted-by":"publisher","first-page":"3001","DOI":"10.1111\/tbed.14173","volume":"69","author":"AE van Aart","year":"2022","unstructured":"van Aart, A. E. et al. SARS-CoV-2 infection in cats and dogs in infected mink farms. Transbound Emerg. Dis. 69, 3001\u20133007. https:\/\/doi.org\/10.1111\/tbed.14173 (2022).","journal-title":"Transbound Emerg. Dis."},{"key":"6730_CR10","doi-asserted-by":"publisher","first-page":"1597","DOI":"10.1080\/21505594.2021.1936433","volume":"12","author":"M Dileepan","year":"2021","unstructured":"Dileepan, M. et al. Seroprevalence of SARS-CoV-2 (COVID-19) exposure in pet cats and dogs in Minnesota, USA. Virulence 12, 1597\u20131609. https:\/\/doi.org\/10.1080\/21505594.2021.1936433 (2021).","journal-title":"Virulence"},{"key":"6730_CR11","doi-asserted-by":"publisher","first-page":"26382","DOI":"10.1073\/pnas.2013102117","volume":"117","author":"AM Bosco-Lauth","year":"2020","unstructured":"Bosco-Lauth, A. M. et al. Experimental infection of domestic dogs and cats with SARS-CoV-2: Pathogenesis, transmission, and response to reexposure in cats. Proc. Natl. Acad. Sci. USA 117, 26382\u201326388. https:\/\/doi.org\/10.1073\/pnas.2013102117 (2020).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"6730_CR12","doi-asserted-by":"publisher","first-page":"1154","DOI":"10.3201\/eid2806.220423","volume":"28","author":"D Bienzle","year":"2022","unstructured":"Bienzle, D. et al. Risk FACTORS for SARS-CoV-2 infection and illness in cats and dogs. Emerg. Infect. Dis. 28, 1154\u20131162. https:\/\/doi.org\/10.3201\/eid2806.220423 (2022).","journal-title":"Emerg. Infect. Dis."},{"key":"6730_CR13","doi-asserted-by":"publisher","first-page":"1527","DOI":"10.3390\/v14071527","volume":"14","author":"S Cui","year":"2022","unstructured":"Cui, S. et al. An updated review on SARS-CoV-2 infection in animals. Viruses 14, 1527. https:\/\/doi.org\/10.3390\/v14071527 (2022).","journal-title":"Viruses"},{"key":"6730_CR14","doi-asserted-by":"publisher","first-page":"e823","DOI":"10.1111\/tbed.14359","volume":"69","author":"H Medkour","year":"2022","unstructured":"Medkour, H. et al. First evidence of human-to-dog transmission of SARS-CoV-2 B.1.160 variant in France. Transbound Emerg. Dis. 69, e823\u2013e830. https:\/\/doi.org\/10.1111\/tbed.14359 (2022).","journal-title":"Transbound Emerg. Dis."},{"key":"6730_CR15","doi-asserted-by":"publisher","first-page":"776","DOI":"10.1038\/s41586-020-2334-5","volume":"586","author":"TH Sit","year":"2020","unstructured":"Sit, T. H. et al. Infection of dogs with SARS-CoV-2. Nature 586, 776\u2013778 (2020).","journal-title":"Nature"},{"key":"6730_CR16","doi-asserted-by":"publisher","first-page":"e01058","DOI":"10.1128\/jcm.01058-22","volume":"60","author":"C Piewbang","year":"2022","unstructured":"Piewbang, C. et al. SARS-CoV-2 transmission from human to pet and suspected transmission from pet to human, Thailand. J. Clin. Microbiol. 60, e01058-e1022. https:\/\/doi.org\/10.1128\/jcm.01058-22 (2022).","journal-title":"J. Clin. Microbiol."},{"key":"6730_CR17","doi-asserted-by":"publisher","first-page":"5888","DOI":"10.4103\/jfmpc.jfmpc_1058_20","volume":"9","author":"P Jorwal","year":"2020","unstructured":"Jorwal, P., Bharadwaj, S. & Jorwal, P. One health approach and COVID-19: A perspective. J. Family Med. Prim. Care 9, 5888\u20135891. https:\/\/doi.org\/10.4103\/jfmpc.jfmpc_1058_20 (2020).","journal-title":"J. Family Med. Prim. Care"},{"key":"6730_CR18","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1186\/s12985-024-02505-9","volume":"21","author":"AP Castillo","year":"2024","unstructured":"Castillo, A. P. et al. SARS-CoV-2 surveillance in captive animals at the belo horizonte zoo, Minas Gerais. Brazil. Virol. J. 21, 297. https:\/\/doi.org\/10.1186\/s12985-024-02505-9 (2024).","journal-title":"Brazil. Virol. J."},{"key":"6730_CR19","doi-asserted-by":"publisher","first-page":"480","DOI":"10.2460\/javma.22.08.0375","volume":"261","author":"AY Liew","year":"2023","unstructured":"Liew, A. Y. et al. Clinical and epidemiologic features of SARS-CoV-2 in dogs and cats compiled through national surveillance in the United States. J. Am. Vet. Med. Assoc. 261, 480\u2013489. https:\/\/doi.org\/10.2460\/javma.22.08.0375 (2023).","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"6730_CR20","doi-asserted-by":"publisher","first-page":"1157","DOI":"10.3390\/v16071157","volume":"16","author":"AK Kimmerlein","year":"2024","unstructured":"Kimmerlein, A. K., McKee, T. S., Bergman, P. J., Sokolchik, I. & Leutenegger, C. M. The transmission of SARS-CoV-2 from COVID-19-diagnosed people to their pet dogs and cats in a multi-year surveillance project. Viruses 16, 1157. https:\/\/doi.org\/10.3390\/v16071157 (2024).","journal-title":"Viruses"},{"key":"6730_CR21","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0299388","volume":"19","author":"C Chen","year":"2024","unstructured":"Chen, C. et al. Spatial and temporal clustering of anti-SARS-CoV-2 antibodies in Illinois household cats, 2021\u20132023. PLoS ONE 19, e0299388 (2024).","journal-title":"PLoS ONE"},{"key":"6730_CR22","doi-asserted-by":"publisher","first-page":"2160","DOI":"10.1002\/jmv.27611","volume":"94","author":"SK Saxena","year":"2022","unstructured":"Saxena, S. K. et al. Transmission dynamics and mutational prevalence of the novel Severe acute respiratory syndrome coronavirus-2 Omicron Variant of Concern. J. Med. Virol. 94, 2160\u20132166. https:\/\/doi.org\/10.1002\/jmv.27611 (2022).","journal-title":"J. Med. Virol."},{"key":"6730_CR23","doi-asserted-by":"publisher","first-page":"782","DOI":"10.3201\/eid2904.221727","volume":"29","author":"KS Lyoo","year":"2023","unstructured":"Lyoo, K. S. et al. Experimental infection and transmission of SARS-CoV-2 delta and omicron variants among beagle dogs. Emerg. Infect. Dis. 29, 782\u2013785. https:\/\/doi.org\/10.3201\/eid2904.221727 (2023).","journal-title":"Emerg. Infect. Dis."},{"key":"6730_CR24","doi-asserted-by":"publisher","first-page":"940710","DOI":"10.3389\/fvets.2022.940710","volume":"9","author":"L S\u00e1nchez-Morales","year":"2022","unstructured":"S\u00e1nchez-Morales, L., S\u00e1nchez-Vizca\u00edno, J. M., P\u00e9rez-Sancho, M., Dom\u00ednguez, L. & Barroso-Ar\u00e9valo, S. The Omicron (B.1.1.529) SARS-CoV-2 variant of concern also affects companion animals. Front. Vet. Sci. 9, 940710. https:\/\/doi.org\/10.3389\/fvets.2022.940710 (2022).","journal-title":"Front. Vet. Sci."},{"key":"6730_CR25","doi-asserted-by":"publisher","first-page":"542","DOI":"10.3390\/antibiotics12030542","volume":"12","author":"S Yudhanto","year":"2023","unstructured":"Yudhanto, S. & Varga, C. Knowledge and attitudes of small animal veterinarians on antimicrobial use practices impacting the selection of antimicrobial resistance in dogs and cats in illinois, United States: A spatial epidemiological approach. Antibiotics (Basel) 12, 542. https:\/\/doi.org\/10.3390\/antibiotics12030542 (2023).","journal-title":"Antibiotics (Basel)"},{"key":"6730_CR26","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1111\/j.1538-4632.1995.tb00338.x","volume":"27","author":"L Anselin","year":"1995","unstructured":"Anselin, L. Local indicators of spatial association\u2014LISA. Geogr. Anal. 27, 93\u2013115 (1995).","journal-title":"Geogr. Anal."},{"key":"6730_CR27","unstructured":"Mitchel, A. The ESRI Guide to GIS analysis, Volume 2: Spartial measurements and statistics. ESRI Guide to GIS analysis 2 (2005)."},{"key":"6730_CR28","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0235291","volume":"15","author":"C Varga","year":"2020","unstructured":"Varga, C., John, P., Cooke, M. & Majowicz, S. E. Spatial and space-time clustering and demographic characteristics of human nontyphoidal Salmonella infections with major serotypes in Toronto, Canada. PLoS ONE 15, e0235291 (2020).","journal-title":"PLoS ONE"},{"key":"6730_CR29","unstructured":"Health, W. S. D. Respiratory Illness Data Dashboard, <https:\/\/doh.wa.gov\/data-and-statistical-reports\/diseases-and-chronic-conditions\/communicable-disease-surveillance-data\/respiratory-illness-data-dashboard> (2025)."},{"key":"6730_CR30","unstructured":"Health, F. D. Florida COVID-19 Data, <https:\/\/www.floridahealth.gov\/diseases-and-conditions\/respiratory-illness\/COVID-19\/> (2025)."},{"key":"6730_CR31","doi-asserted-by":"publisher","first-page":"e00067","DOI":"10.1128\/msphere.00067-23","volume":"8","author":"F Yuan","year":"2023","unstructured":"Yuan, F. et al. Development of monoclonal antibody-based blocking ELISA for detecting SARS-CoV-2 exposure in animals. mSphere 8, e00067-e23. https:\/\/doi.org\/10.1128\/msphere.00067-23 (2023).","journal-title":"mSphere"},{"key":"6730_CR32","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1186\/s12879-015-1106-6","volume":"15","author":"C Varga","year":"2015","unstructured":"Varga, C. et al. Area-level global and local clustering of human salmonella enteritidis infection rates in the city of Toronto, Canada, 2007\u20132009. BMC Infect. Dis. 15, 359. https:\/\/doi.org\/10.1186\/s12879-015-1106-6 (2015).","journal-title":"BMC Infect. Dis."},{"key":"6730_CR33","first-page":"1145","volume":"6","author":"K Krivoruchko","year":"2012","unstructured":"Krivoruchko, K. Empirical bayesian kriging. ArcUser Fall 6, 1145 (2012).","journal-title":"ArcUser Fall"},{"key":"6730_CR34","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1080\/14498596.2021.1955816","volume":"66","author":"A Thomas","year":"2021","unstructured":"Thomas, A. & Aryal, J. Spatial analysis methods and practice: Describe\u2013explore\u2013explain through GIS. J. Spatial Sci. 66, 533\u2013534. https:\/\/doi.org\/10.1080\/14498596.2021.1955816 (2021).","journal-title":"J. Spatial Sci."},{"key":"6730_CR35","doi-asserted-by":"publisher","DOI":"10.1017\/9781108614528","volume-title":"Spatial analysis methods and practice: Describe\u2013explore\u2013explain through GIS","author":"G Grekousis","year":"2020","unstructured":"Grekousis, G. Spatial analysis methods and practice: Describe\u2013explore\u2013explain through GIS (Cambridge University Press, 2020)."},{"key":"6730_CR36","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1111\/j.1538-4632.1992.tb00261.x","volume":"24","author":"A Getis","year":"1992","unstructured":"Getis, A. & Ord, J. K. The analysis of spatial association by use of distance statistics. Geogr. Anal. 24, 189\u2013206 (1992).","journal-title":"Geogr. Anal."},{"key":"6730_CR37","unstructured":"Kulldorff, M. SaTScan User Guide; 2018. Reference Source 505 (2022)."},{"key":"6730_CR38","doi-asserted-by":"publisher","first-page":"1481","DOI":"10.1080\/03610929708831995","volume":"26","author":"M Kulldorff","year":"1997","unstructured":"Kulldorff, M. A spatial scan statistic. Commun. Statist.-Theory Methods 26, 1481\u20131496 (1997).","journal-title":"Commun. Statist.-Theory Methods"},{"key":"6730_CR39","doi-asserted-by":"publisher","first-page":"1377","DOI":"10.2105\/AJPH.88.9.1377","volume":"88","author":"M Kulldorff","year":"1998","unstructured":"Kulldorff, M., Athas, W. F., Feurer, E. J., Miller, B. A. & Key, C. R. Evaluating cluster alarms: A space-time scan statistic and brain cancer in Los Alamos, New Mexico. Am. J. Public Health 88, 1377\u20131380 (1998).","journal-title":"Am. J. Public Health"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-06730-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-06730-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-06730-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,7,1]],"date-time":"2025-07-01T18:35:17Z","timestamp":1751394917000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-06730-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,1]]},"references-count":39,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["6730"],"URL":"https:\/\/doi.org\/10.1038\/s41598-025-06730-2","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,7,1]]},"assertion":[{"value":"9 April 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 June 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 July 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interest"}}],"article-number":"21758"}}