{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T17:02:02Z","timestamp":1786122122708,"version":"build-2736575974"},"reference-count":52,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T00:00:00Z","timestamp":1786060800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>SARS-CoV-2 transmission between humans and animals is an important One Health concern, particularly in settings where close human\u2013animal interactions are difficult to avoid. We developed and applied a qualitative likelihood ranking framework for SARS-CoV-2 transmission between people and captive lions (Panthera leo) in an urban zoological setting. Following a structured review, scenario trees were constructed to rank direct and indirect transmission pathways using five domains: activity duration, proximity and frequency, SARS-CoV-2 survival on fomites, and environmental conditions. The framework was applied to a case study of a lion exhibit at an urban zoo in Australia. Pathway ranking depended on the combined effects of baseline exposure attributes and subsequent modifiers reflecting exposure frequency and level of natural disinfection. Although direct pathways, such as veterinary procedures, had the highest likelihood of transmission, they were differentiated by interaction duration and proximity, with frequency modification distinguishing rare, high-intensity interactions from repeated lower-intensity activities. Therefore, routine husbandry or visitor-associated exposures could increase in relative importance. Environmental modification further differentiated pathway likelihood, in particular due to solar exposure and temperature. The framework provides a transparent, practical approach for ranking transmission likelihood when data are scarce, supports consistent prioritisation of biosecurity resources, and is applicable to other emerging infectious disease threats in zoological settings.<\/jats:p>","DOI":"10.3390\/ani16162450","type":"journal-article","created":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T08:01:36Z","timestamp":1786089696000},"page":"2450","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["A Qualitative Framework for Ranking the Relative Likelihood of SARS-CoV-2 Transmission Between People and Felids at Zoological Interfaces"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0009-0004-9529-5100","authenticated-orcid":false,"given":"Ricky","family":"Tang","sequence":"first","affiliation":[{"name":"Sydney School of Veterinary Science, The University of Sydney, Camperdown, Sydney, NSW 2006, Australia"},{"name":"Small Animal Specialist Hospital (SASH), Robina, Gold Coast, QLD 4226, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0003-6930","authenticated-orcid":false,"given":"Jacqueline M.","family":"Norris","sequence":"additional","affiliation":[{"name":"Sydney School of Veterinary Science, The University of Sydney, Camperdown, Sydney, NSW 2006, Australia"},{"name":"Sydney Infectious Disease Institute, The University of Sydney, Camperdown, Sydney, NSW 2006, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carol","family":"Bency","sequence":"additional","affiliation":[{"name":"Sydney School of Veterinary Science, The University of Sydney, Camperdown, Sydney, NSW 2006, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kimberly Vinette","family":"Herrin","sequence":"additional","affiliation":[{"name":"Taronga Wildlife Hospital, Taronga Zoo, Mosman, Sydney, NSW 2088, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0963-4926","authenticated-orcid":false,"given":"Victoria J.","family":"Brookes","sequence":"additional","affiliation":[{"name":"Sydney School of Veterinary Science, The University of Sydney, Camperdown, Sydney, NSW 2006, Australia"},{"name":"Sydney Infectious Disease Institute, The University of Sydney, Camperdown, Sydney, NSW 2006, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1038\/s41431-023-01462-1","article-title":"A comprehensive SARS-CoV-2 and COVID-19 review, Part 2: Host extracellular to systemic effects of SARS-CoV-2 infection","volume":"32","author":"Narayanan","year":"2024","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Mahdy, M.A.A., Younis, W., and Ewaida, Z. (2020). An Overview of SARS-CoV-2 and Animal Infection. Front. Vet. Sci., 7.","DOI":"10.3389\/fvets.2020.596391"},{"key":"ref_3","unstructured":"WHO (2026, July 12). Number of COVID-19 Cases Reported to WHO (Cumulative Total). Available online: https:\/\/data.who.int\/dashboards\/covid19\/cases?n=o."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1021\/acscentsci.1c00120","article-title":"A Comprehensive Review of the Global Efforts on COVID-19 Vaccine Development","volume":"7","author":"Li","year":"2021","journal-title":"ACS Cent. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"101365","DOI":"10.1016\/j.coviro.2023.101365","article-title":"Transmission of severe acute respiratory syndrome coronavirus 2 from humans to animals: Is there a risk of novel reservoirs?","volume":"63","year":"2023","journal-title":"Curr. Opin. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1126\/science.abe5901","article-title":"Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans","volume":"371","author":"Sikkema","year":"2021","journal-title":"Sci. (Am. Assoc. Adv. Sci.)"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Jahid, M.J., Bowman, A.S., and Nolting, J.M. (2024). SARS-CoV-2 Outbreaks on Mink Farms\u2014A Review of Current Knowledge on Virus Infection, Spread, Spillover, and Containment. Viruses, 16.","DOI":"10.3390\/v16010081"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.3201\/eid2906.230150","article-title":"Probable Transmission of SARS-CoV-2 from African Lion to Zoo Employees, Indiana, USA, 2021","volume":"29","author":"Siegrist","year":"2023","journal-title":"Emerg. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"6802","DOI":"10.1038\/s41467-021-27096-9","article-title":"Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands","volume":"12","author":"Lu","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"4078","DOI":"10.1038\/s41467-023-39782-x","article-title":"Transmission of SARS-CoV-2 in free-ranging white-tailed deer in the United States","volume":"14","author":"Feng","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Marques, A.D., Hogenauer, M., Bauer, N., Gibison, M., DeMarco, B., Sherrill-Mix, S., Merenstein, C., Collman, R.G., Gagne, R.B., and Bushman, F.D. (2025). Evolution of SARS-CoV-2 in white-tailed deer in Pennsylvania 2021\u20132024. PLoS Pathog., 21.","DOI":"10.1371\/journal.ppat.1012883"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"McAloose, D., Laverack, M., Wang, L., Killian, M.L., Caserta, L.C., Yuan, F., Mitchell, P.K., Queen, K., Mauldin, M.R., and Cronk, B.D. (2020). From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo. mBio, 11.","DOI":"10.1128\/mBio.02220-20"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"100133","DOI":"10.1016\/j.onehlt.2020.100133","article-title":"The risk of SARS-CoV-2 transmission to pets and other wild and domestic animals strongly mandates a one-health strategy to control the COVID-19 pandemic","volume":"10","author":"Leroy","year":"2020","journal-title":"One Health"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"6681","DOI":"10.1007\/s10668-020-00884-x","article-title":"Understanding COVID-19 transmission, health impacts and mitigation: Timely social distancing is the key","volume":"23","author":"Kaur","year":"2021","journal-title":"Environ. Dev. Sustain."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"100422","DOI":"10.1016\/j.onehlt.2022.100422","article-title":"A standardized instrument quantifying risk factors associated with bi-directional transmission of SARS-CoV-2 and other zoonotic pathogens: The COVID-19 human-animal interactions survey (CHAIS)","volume":"15","author":"Gass","year":"2022","journal-title":"One Health"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Agusi, E.R., Allendorf, V., Eze, E.A., Asala, O., Shittu, I., Dietze, K., Busch, F., Globig, A., and Meseko, C.A. (2022). SARS-CoV-2 at the Human-Animal Interface: Implication for Global Public Health from an African Perspective. Viruses, 14.","DOI":"10.3390\/v14112473"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1638\/2022-0141","article-title":"Global Retrospective Review of Severe Acute Respiratory Syndrome SARS CoV-2 Infections In Nondomestic Felids: March 2020\u2013February 2021","volume":"54","author":"Bartlett","year":"2023","journal-title":"J. Zoo Wildl. Med."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1111\/jvp.13429","article-title":"Safety and immunogenicity of an adjuvanted recombinant spike protein-based severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccine, SpikeVet\u2122, in selected Carnivora, Primates and Artiodactyla in Australian zoos","volume":"47","author":"McLelland","year":"2024","journal-title":"J. Vet. Pharmacol. Ther."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1224","DOI":"10.1638\/2021-0042","article-title":"Duration of Antigen Shedding and Development of Antibody Titers in Malayan Tigers (Panthera Tigris Jacksoni) Naturally Infected with SARS-CoV-2","volume":"52","author":"Cushing","year":"2021","journal-title":"J. Zoo Wildl. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"833","DOI":"10.3201\/eid2804.212219","article-title":"SARS-CoV-2 Outbreak among Malayan Tigers and Humans, Tennessee, USA, 2020","volume":"28","author":"Grome","year":"2022","journal-title":"Emerg. Infect. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1007\/s00705-022-05469-9","article-title":"Reverse-zoonotic transmission of SARS-CoV-2 lineage alpha (B.1.1.7) to great apes and exotic felids in a zoo in the Czech Republic","volume":"167","author":"Nagy","year":"2022","journal-title":"Arch. Virol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3047","DOI":"10.1111\/tbed.14290","article-title":"Natural infection of Delta mutant of SARS-CoV-2 in Asiatic lions of India","volume":"69","author":"Karikalan","year":"2022","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e3346","DOI":"10.1111\/tbed.14625","article-title":"Detection of SARS-CoV-2 clade B.1.2 in three snow leopards","volume":"69","author":"Wang","year":"2022","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1093\/emph\/eoaa021","article-title":"Lions, tigers and kittens too: ACE2 and susceptibility to COVID-19","volume":"2020","author":"Mathavarajah","year":"2020","journal-title":"Evol. Med. Public Health"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1007\/s13205-020-02471-3","article-title":"In silico analysis of ACE2 orthologues to predict animal host range with high susceptibility to SARS-CoV-2","volume":"10","author":"Bouricha","year":"2020","journal-title":"3 Biotech"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1126\/science.abc1669","article-title":"SARS-CoV-2 productively infects human gut enterocytes","volume":"369","author":"Lamers","year":"2020","journal-title":"Sci. (Am. Assoc. Adv. Sci.)"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1430","DOI":"10.1016\/j.ajic.2023.04.170","article-title":"Fecal-oral transmission of SARS-CoV-2: A systematic review of evidence from epidemiological and experimental studies","volume":"51","author":"Termansen","year":"2023","journal-title":"Am. J. Infect. Control"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2665","DOI":"10.1007\/s10096-021-04304-4","article-title":"Lack of evidence for infectious SARS-CoV-2 in feces and sewage","volume":"40","author":"Albert","year":"2021","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1186\/s12879-021-06222-4","article-title":"Modes of transmission of SARS-CoV-2 and evidence for preventive behavioral interventions","volume":"21","author":"Zhou","year":"2021","journal-title":"BMC Infect. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"101106","DOI":"10.1016\/j.cofs.2023.101106","article-title":"Survival of severe acute respiratory syndrome coronavirus 2 in foods and its inactivation by different methods","volume":"55","author":"Jung","year":"2024","journal-title":"Curr. Opin. Food Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1186\/s12985-020-01418-7","article-title":"The effect of temperature on persistence of SARS-CoV-2 on common surfaces","volume":"17","author":"Riddell","year":"2020","journal-title":"Virol. J."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1564","DOI":"10.1056\/NEJMc2004973","article-title":"Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1","volume":"382","author":"Bushmaker","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e10","DOI":"10.1016\/S2666-5247(20)30003-3","article-title":"Stability of SARS-CoV-2 in different environmental conditions","volume":"1","author":"Chin","year":"2020","journal-title":"Lancet Microbe"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Kwon, T., Gaudreault, N.N., and Richt, J.A. (2021). Environmental Stability of SARS-CoV-2 on Different Types of Surfaces under Indoor and Seasonal Climate Conditions. Pathogens, 10.","DOI":"10.3390\/pathogens10020227"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Jia, M., Taylor, T.M., Senger, S.M., Ovissipour, R., and Bertke, A.S. (2022). SARS-CoV-2 Remains Infectious on Refrigerated Deli Food, Meats, and Fresh Produce for up to 21 Days. Foods, 11.","DOI":"10.3390\/foods11030286"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1007\/s12250-021-00367-x","article-title":"Stability of SARS-CoV-2 on the Surfaces of Three Meats in the Setting That Simulates the Cold Chain Transportation","volume":"36","author":"Feng","year":"2021","journal-title":"Virol. Sin."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Gidari, A., Sabbatini, S., Bastianelli, S., Pierucci, S., Busti, C., Bartolini, D., Stabile, A.M., Monari, C., Galli, F., and Rende, M. (2021). SARS-CoV-2 Survival on Surfaces and the Effect of UV-C Light. Viruses, 13.","DOI":"10.3390\/v13030408"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"403","DOI":"10.12688\/f1000research.110305.1","article-title":"Effect of elevated temperature on SARS-CoV-2 viability","volume":"11","author":"Harapan","year":"2022","journal-title":"F1000Research"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Huang, S.-Y., Kung, Y.-A., Huang, P.-N., Chang, S.-Y., Gong, Y.-N., Han, Y.-J., Chiang, H.-J., Liu, K.-T., Lee, K.-M., and Chang, C.-Y. (2021). Stability of SARS-CoV-2 Spike G614 Variant Surpasses That of the D614 Variant after Cold Storage. mSphere, e00104-21.","DOI":"10.1128\/mSphere.00104-21"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1093\/infdis\/jiaa274","article-title":"Simulated Sunlight Rapidly Inactivates SARS-CoV-2 on Surfaces","volume":"222","author":"Williams","year":"2020","journal-title":"J. Infect. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1415","DOI":"10.1080\/22221751.2020.1777906","article-title":"Experimental aerosol survival of SARS-CoV-2 in artificial saliva and tissue culture media at medium and high humidity","volume":"9","author":"Smither","year":"2020","journal-title":"Emerg. Microbes Infect."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Biryukov, J., Boydston Jeremy, A., Dunning Rebecca, A., Yeager John, J., Wood, S., Reese Amy, L., Ferris, A., Miller, D., Weaver, W., and Zeitouni Nathalie, E. (2020). Increasing Temperature and Relative Humidity Accelerates Inactivation of SARS-CoV-2 on Surfaces. mSphere, e00441-20.","DOI":"10.1128\/msphere.00441-20"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e65902","DOI":"10.7554\/eLife.65902","article-title":"Mechanistic theory predicts the effects of temperature and humidity on inactivation of SARS-CoV-2 and other enveloped viruses","volume":"10","author":"Morris","year":"2021","journal-title":"eLife"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"148749","DOI":"10.1016\/j.scitotenv.2021.148749","article-title":"Close proximity risk assessment for SARS-CoV-2 infection","volume":"794","author":"Cortellessa","year":"2021","journal-title":"Sci. Total Environ."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1038\/s41586-023-06952-2","article-title":"Digital measurement of SARS-CoV-2 transmission risk from 7 million contacts","volume":"626","author":"Ferretti","year":"2024","journal-title":"Nature"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e0161022","DOI":"10.1128\/jcm.01610-22","article-title":"Role of Spillover and Spillback in SARS-CoV-2 Transmission and the Importance of One Health in Understanding the Dynamics of the COVID-19 Pandemic","volume":"61","author":"Sparrer","year":"2023","journal-title":"J. Clin. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Sehgal, N.J., and Milton, D.K. (2021). Applying the Hierarchy of Controls: What Occupational Safety Can Teach us About Safely Navigating the Next Phase of the Global COVID-19 Pandemic. Front. Public Health, 9.","DOI":"10.3389\/fpubh.2021.747894"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e13039","DOI":"10.1111\/sji.13039","article-title":"COVID-19: Risk Factors Associated with Infectivity and Severity","volume":"93","author":"Fadl","year":"2021","journal-title":"Scand. J. Immunol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"24224","DOI":"10.1038\/s41598-021-03632-x","article-title":"Finding of the factors affecting the severity of COVID-19 based on mathematical models","volume":"11","author":"Qu","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"105420","DOI":"10.1016\/j.jcv.2023.105420","article-title":"Duration of viral infectiousness and correlation with symptoms and diagnostic testing in non-hospitalized adults during acute SARS-CoV-2 infection: A longitudinal cohort study","volume":"161","author":"Drain","year":"2023","journal-title":"J. Clin. Virol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1136\/ebnurs-2024-104231","article-title":"Understanding sources of bias in research","volume":"28","author":"Smith","year":"2025","journal-title":"Evid. Based Nurs."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"100079","DOI":"10.1016\/j.anzjph.2023.100079","article-title":"Whose values, what bias, which subjectivity?: The need for reflexivity and positionality in epidemiological health equity scholarship","volume":"47","author":"Poirier","year":"2023","journal-title":"Aust. N. Z. J. Public Health"}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/16\/16\/2450\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T08:21:21Z","timestamp":1786090881000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/16\/16\/2450"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,7]]},"references-count":52,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["ani16162450"],"URL":"https:\/\/doi.org\/10.3390\/ani16162450","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,7]]}}}