SARS-CoV-2 delta variant in African lions (Panthera leo) and humans at Utah's Hogle Zoo, USA, 2021-22.

Ahead of Print

Publisher: Blackwell Verlag Country of Publication: Germany NLM ID: 101300786 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1863-2378 (Electronic) Linking ISSN: 18631959 NLM ISO Abbreviation: Zoonoses Public Health Subsets: MEDLINE

Original Publication: Berlin, Germany : Blackwell Verlag

Aims: We conducted a One Health investigation to assess the source and transmission dynamics of SARS-CoV-2 infection in African lions (Panthera leo) at Utah's Hogle Zoo in Salt Lake City from October 2021 to February 2022.
Methods and Results: Following observation of respiratory illness in the lions, zoo staff collected pooled faecal samples and individual nasal swabs from four lions. All specimens tested positive for SARS-CoV-2 by reverse transcription-polymerase chain reaction (RT-PCR). The resulting investigation included: lion observation; RT-PCR testing of lion faeces every 1-7 days; RT-PCR testing of lion respiratory specimens every 2-3 weeks; staff interviews and RT-PCR testing; whole-genome sequencing of viruses from lions and staff; and comparison with existing SARS-CoV-2 human community surveillance sequences. In addition to all five lions, three staff displayed respiratory symptoms. All lions recovered and no hospitalizations or deaths were reported among staff. Three staff reported close contact with the lions in the 10 days before lion illness onset, one of whom developed symptoms and tested positive for SARS-CoV-2 on days 3 and 4, respectively, after lion illness onset. The other two did not report symptoms or test positive. Two staff who did not have close contact with the lions were symptomatic and tested positive on days 5 and 8, respectively, after lion illness onset. We detected SARS-CoV-2 RNA in lion faeces for 33 days and in lion respiratory specimens for 14 weeks after illness onset. The viruses from lions were genetically highly related to those from staff and two contemporaneous surveillance specimens from Salt Lake County; all were delta variants (AY.44).
Conclusions: We did not determine the sources of these infections, although human-to-lion transmission likely occurred. The observed period of respiratory shedding was longer than in previously documented SARS-CoV-2 infections in large felids, indicating the need to further assess duration and potential implications of shedding.
(© 2024 Wiley‐VCH GmbH. Published by John Wiley & Sons Ltd.)

Allender, M. C., Adkesson, M. J., Langan, J. N., Delk, K. W., Meehan, T., Aitken‐Palmer, C., McEntire, M. M., Killian, M. L., Torchetti, M., Morales, S. A., Austin, C., Fredrickson, R., Olmstead, C., Ke, R., Smith, R., Hostnik, E. T., Terio, K., & Wang, L. (2022). Multi‐species outbreak of SARS‐CoV‐2 Delta variant in a zoological institution, with the detection in two new families of carnivores. Transboundary and Emerging Diseases, 69(5), e3060–e3075. https://doi.org/10.1111/tbed.14662.
Badiola, J. J., Otero, A., Sevilla, E., Marín, B., García Martínez, M., Betancor, M., Sola, D., Pérez Lázaro, S., Lozada, J., Velez, C., Chiner‐Oms, Á., Comas, I., Cancino‐Muñoz, I., Monleón, E., Monzón, M., Acín, C., Bolea, R., & Moreno, B. (2022). SARS‐CoV‐2 outbreak on a Spanish mink farm: Epidemiological, molecular, and pathological studies. Frontiers in Veterinary Science, 8, 805004. https://doi.org/10.3389/fvets.2021.805004.
Bartlett, S. L., Diel, D. G., Wang, L., Zec, S., Laverack, M., Martins, M., Caserta, L. C., Killian, M. L., Terio, K., Olmstead, C., Delaney, M. A., Stokol, T., Ivančić, M., Jenkins‐Moore, M., Ingerman, K., Teegan, T., McCann, C., Thomas, P., McAloose, D., … Calle, P. P. (2021). SARS‐CoV‐2 infection and longitudinal fecal screening in Malayan tigers (Panthera tigris jacksoni), Amur tigers (Panthera tigris altaica), and African lions (Panthera leo krugeri) at the Bronx zoo, New York, USA. Journal of Zoo and Wildlife Medicine, 51(4), 733–744. https://doi.org/10.1638/2020‐0171.
Barua, S., Hoque, M., Adekanmbi, F., Kelly, P., Jenkins‐Moore, M., Torchetti, M. K., Chenoweth, K., Wood, T., & Wang, C. (2021). Antibodies to SARS‐CoV‐2 in dogs and cats, USA. Emerging Microbes & Infections, 10(1), 1669–1674. https://doi.org/10.1080/22221751.2021.1967101.
Corman, V. M., Landt, O., Kaiser, M., Molenkamp, R., Meijer, A., Chu, D. K., Bleicker, T., Brünink, S., Schneider, J., Schmidt, M. L., Mulders, D. G., Haagmans, B. L., van der Veer, B., van den Brink, S., Wijsman, L., Goderski, G., Romette, J. L., Ellis, J., Zambon, M., … Drosten, C. (2020). Detection of 2019 novel coronavirus (2019‐nCoV) by real‐time RT‐PCR. Eurosurveillance, 25(3), 2000045. https://doi.org/10.2807/1560‐7917.ES.2020.25.3.2000045.
Cossaboom, C. M., Medley, A. M., Spengler, J. R., Kukielka, E. A., Goryoka, G. W., Baird, T., Bhavsar, S., Campbell, S., Campbell, T. S., Christensen, D., Condrey, J. A., Dawson, P., Doty, J. B., Feldpausch, A., Gabel, J., Jones, D., Lim, A., Loiacono, C. M., Jenkins‐Moore, M., … Barton Behravesh, C. (2021). Low SARS‐CoV‐2 seroprevalence and no active infections among dogs and cats in animal shelters with laboratory‐confirmed COVID‐19 human cases among employees. Biology, 10(9), 898. https://doi.org/10.3390/biology10090898.
Cossaboom, C. M., Wendling, N. M., Lewis, N. M., Rettler, H., Harvey, R. R., Amman, B. R., Towner, J. S., Spengler, J. R., Erickson, R., Burnett, C., Young, E. L., Oakeson, K., Carpenter, A., Kainulainen, M. H., Chatterjee, P., Flint, M., Uehara, A., Li, Y., Zhang, J., … Barton Behravesh, C. (2022). One health investigation of SARS‐CoV‐2 in people and animals on multiple mink farms in Utah. Viruses, 15(1), 96. https://doi.org/10.3390/v15010096.
Cushing, A. C., Sawatzki, K., Grome, H. N., Puryear, W. B., Kelly, N., & Runstadler, J. (2021). Duration of antigen shedding and development of antibody titers in Malayan tigers (Panthera tigris jacksoni) naturally infected with SARS‐CoV‐2. Journal of Zoo and Wildlife Medicine, 52(4), 1224–1228. https://doi.org/10.1638/2021‐0042.
Dileepan, M., Di, D., Huang, Q., Ahmed, S., Heinrich, D., Ly, H., & Liang, Y. (2021). Seroprevalence of SARS‐CoV‐2 (COVID‐19) exposure in pet cats and dogs in Minnesota, USA. Virulence, 12(1), 1597–1609. https://doi.org/10.1080/21505594.2021.1936433.
Fernández‐Bellon, H., Rodon, J., Fernández‐Bastit, L., Almagro, V., Padilla‐Solé, P., Lorca‐Oró, C., Valle, R., Roca, N., Grazioli, S., Trogu, T., Bensaid, A., Carrillo, J., Izquierdo‐Useros, N., Blanco, J., Parera, M., Noguera‐Julián, M., Clotet, B., Moreno, A., Segalés, J., & Vergara‐Alert, J. (2021). Monitoring natural SARS‐CoV‐2 infection in lions (Panthera leo) at the Barcelona zoo: Viral dynamics and host responses. Viruses, 13(9), 1683. https://doi.org/10.3390/v13091683.
Gaudreault, N. N., Trujillo, J. D., Carossino, M., Meekins, D. A., Morozov, I., Madden, D. W., Indran, S. V., Bold, D., Balaraman, V., Kwon, T., Artiaga, B. L., Cool, K., García‐Sastre, A., Ma, W., Wilson, W. C., Henningson, J., Balasuriya, U., & Richt, J. A. (2020). SARS‐CoV‐2 infection, disease and transmission in domestic cats. Emerging Microbes & Infections, 9(1), 2322–2332. https://doi.org/10.1080/22221751.2020.1833687.
Grome, H. N., Meyer, B., Read, E., Buchanan, M., Cushing, A., Sawatzki, K., Levinson, K. J., Thomas, L. S., Perry, Z., Uehara, A., Tao, Y., Queen, K., Tong, S., Ghai, R., Fill, M. M., Jones, T. F., Schaffner, W., & Dunn, J. (2022). SARS‐CoV‐2 outbreak among Malayan tigers and humans, Tennessee, USA, 2020. Emerging Infectious Diseases, 28(4), 833–836. https://doi.org/10.3201/eid2804.212219.
Hale, V. L., Dennis, P. M., McBride, D. S., Nolting, J. M., Madden, C., Huey, D., Ehrlich, M., Grieser, J., Winston, J., Lombardi, D., Gibson, S., Saif, L., Killian, M. L., Lantz, K., Tell, R. M., Torchetti, M., Robbe‐Austerman, S., Nelson, M. I., Faith, S. A., & Bowman, A. S. (2022). SARS‐CoV‐2 infection in free‐ranging white‐tailed deer. Nature, 602(7897), 481–486. https://doi.org/10.1038/s41586‐021‐04353‐x.
Hare, D., Meaney, C., Powell, J., Slevin, B., O' Brien, B., Power, L., O' Connell, N. H., De Gascun, C. F., Dunne, C. P., & Stapleton, P. J. (2022). Repeated transmission of SARS‐CoV‐2 in an overcrowded Irish emergency department elucidated by whole‐genome sequencing. The Journal of Hospital Infection, 126, 1–9. https://doi.org/10.1016/j.jhin.2022.04.015.
Kang, M., Xin, H., Yuan, J., Ali, S. T., Liang, Z., Zhang, J., Hu, T., Lau, E. H., Zhang, Y., Zhang, M., Cowling, B. J., Li, Y., & Wu, P. (2022). Transmission dynamics and epidemiological characteristics of SARS‐CoV‐2 Delta variant infections in Guangdong, China, may to June 2021. Eurosurveillance, 27(10), 2100815. https://doi.org/10.2807/1560‐7917.ES.2022.27.10.2100815.
Karikalan, M., Chander, V., Mahajan, S., Deol, P., Agrawal, R. K., Nandi, S., Rai, S. K., Mathur, A., Pawde, A., Singh, K. P., & Sharma, G. K. (2022). Natural infection of Delta mutant of SARS‐CoV‐2 in Asiatic lions of India. Transboundary and Emerging Diseases, 69(5), 3047–3055. https://doi.org/10.1111/tbed.14290.
Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14), 3059–3066. https://doi.org/10.1093/nar/gkf436.
Koeppel, K. N., Mendes, A., Strydom, A., Rotherham, L., Mulumba, M., & Venter, M. (2022). SARS‐CoV‐2 reverse zoonoses to pumas and lions, South Africa. Viruses, 14(1), 120. https://doi.org/10.3390/v14010120.
Krüger, N., Rocha, C., Runft, S., Krüger, J., Färber, I., Armando, F., Leitzen, E., Brogden, G., Gerold, G., Pöhlmann, S., Hoffmann, M., & Baumgärtner, W. (2021). The upper respiratory tract of felids is highly susceptible to SARS‐CoV‐2 infection. International Journal of Molecular Sciences, 22(19), 10636. https://doi.org/10.3390/ijms221910636.
Lumley, S. F., Constantinides, B., Sanderson, N., Rodger, G., Street, T. L., Swann, J., Chau, K. K., O'Donnell, D., Warren, F., Hoosdally, S., OUH Microbiology laboratory, OUH Infection Prevention and Control team, O'Donnell, A. M., Walker, T. M., Stoesser, N. E., Butcher, L., Peto, T. E., Crook, D. W., Jeffery, K., … Eyre, D. W. (2021). Epidemiological data and genome sequencing reveals that nosocomial transmission of SARS‐CoV‐2 is underestimated and mostly mediated by a small number of highly infectious individuals. The Journal of Infection, 83(4), 473–482. https://doi.org/10.1016/j.jinf.2021.07.034.
McAloose, D., Laverack, M., Wang, L., Killian, M. L., Caserta, L. C., Yuan, F., Mitchell, P. K., Queen, K., Mauldin, M. R., Cronk, B. D., Bartlett, S. L., Sykes, J. M., Zec, S., Stokol, T., Ingerman, K., Delaney, M. A., Fredrickson, R., Ivančić, M., Jenkins‐Moore, M., … Diel, D. G. (2020). From people to panthera: Natural SARS‐CoV‐2 infection in tigers and lions at the Bronx zoo. MBio, 11(5), e02220‐20. https://doi.org/10.1128/mBio.02220‐20.
Meredith, L. W., Hamilton, W. L., Warne, B., Houldcroft, C. J., Hosmillo, M., Jahun, A. S., Curran, M. D., Parmar, S., Caller, L. G., Caddy, S. L., Khokhar, F. A., Yakovleva, A., Hall, G., Feltwell, T., Forrest, S., Sridhar, S., Weekes, M. P., Baker, S., Brown, N., … Goodfellow, I. (2020). Rapid implementation of SARS‐CoV‐2 sequencing to investigate cases of health‐care associated COVID‐19: A prospective genomic surveillance study. The Lancet Infectious Diseases, 20(11), 1263–1272. https://doi.org/10.1016/S1473‐3099(20)30562‐4.
Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., von Haeseler, A., & Lanfear, R. (2020). IQ‐TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37(5), 1530–1534. https://doi.org/10.1093/molbev/msaa015.
Mishra, A., Kumar, N., Bhatia, S., Aasdev, A., Kanniappan, S., Sekhar, A. T., Gopinadhan, A., Silambarasan, R., Sreekumar, C., Dubey, C. K., Tripathi, M., Raut, A. A., & Singh, V. P. (2021). SARS‐CoV‐2 Delta variant among Asiatic lions, India. Emerging Infectious Diseases, 27(10), 2723–2725. https://doi.org/10.3201/eid2710.211500.
Mitchell, P. K., Martins, M., Reilly, T., Caserta, L. C., Anderson, R. R., Cronk, B. D., Murphy, J., Goodrich, E. L., & Diel, D. G. (2021). SARS‐CoV‐2 B.1.1.7 variant infection in Malayan tigers, Virginia, USA. Emerging Infectious Diseases, 27(12), 3171–3173. https://doi.org/10.3201/eid2712.211234.
Oude Munnink, B. B., Sikkema, R. S., Nieuwenhuijse, D. F., Molenaar, R. J., Munger, E., Molenkamp, R., van der Spek, A., Tolsma, P., Rietveld, A., Brouwer, M., Bouwmeester‐Vincken, N., Harders, F., Hakze‐van der Honing, R., Wegdam‐Blans, M., Bouwstra, R. J., GeurtsvanKessel, C., van der Eijk, A. A., Velkers, F. C., Smit, L., … Koopmans, M. (2021). Transmission of SARS‐CoV‐2 on mink farms between humans and mink and back to humans. Science, 371(6525), 172–177. https://doi.org/10.1126/science.abe5901.
Pickering, B., Lung, O., Maguire, F., Kruczkiewicz, P., Kotwa, J. D., Buchanan, T., Gagnier, M., Guthrie, J. L., Jardine, C. M., Marchand‐Austin, A., Massé, A., McClinchey, H., Nirmalarajah, K., Aftanas, P., Blais‐Savoie, J., Chee, H. Y., Chien, E., Yim, W., Banete, A., … Bowman, J. (2022). Divergent SARS‐CoV‐2 variant emerges in white‐tailed deer with deer‐to‐human transmission. Nature Microbiology, 7(12), 2011–2024. https://doi.org/10.1038/s41564‐022‐01268‐9.
Pomorska‐Mól, M., Turlewicz‐Podbielska, H., Gogulski, M., Ruszkowski, J. J., Kubiak, M., Kuriga, A., Barket, P., & Postrzech, M. (2021). A cross‐sectional retrospective study of SARS‐CoV‐2 seroprevalence in domestic cats, dogs and rabbits in Poland. BMC Veterinary Research, 17(1), 322. https://doi.org/10.1186/s12917‐021‐03033‐2.
Rambaut, A., Holmes, E. C., O'Toole, Á., Hill, V., McCrone, J. T., Ruis, C., du Plessis, L., & Pybus, O. G. (2020). A dynamic nomenclature proposal for SARS‐CoV‐2 lineages to assist genomic epidemiology. Nature Microbiology, 5(11), 1403–1407. https://doi.org/10.1038/s41564‐020‐0770‐5.
Seeman, T., Klötzl, F., & Page, A. (2017). Pairwise SNP distance matrix from a FASTA sequence alignment. https://github.com/tseemann/snp‐dists.
Sharun, K., Tiwari, R., Natesan, S., & Dhama, K. (2021). SARS‐CoV‐2 infection in farmed minks, associated zoonotic concerns, and importance of the one health approach during the ongoing COVID‐19 pandemic. The Veterinary Quarterly, 41(1), 50–60. https://doi.org/10.1080/01652176.2020.1867776.
Shi, J., Wen, Z., Zhong, G., Yang, H., Wang, C., Huang, B., Liu, R., He, X., Shuai, L., Sun, Z., Zhao, Y., Liu, P., Liang, L., Cui, P., Wang, J., Zhang, X., Guan, Y., Tan, W., Wu, G., … Bu, Z. (2020). Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS‐coronavirus 2. Science (New York, N.Y.), 368(6494), 1016–1020. https://doi.org/10.1126/science.abb7015.
Sila, T., Sunghan, J., Laochareonsuk, W., Surasombatpattana, S., Kongkamol, C., Ingviya, T., Siripaitoon, P., Kositpantawong, N., Kanchanasuwan, S., Hortiwakul, T., Charernmak, B., Nwabor, O. F., Silpapojakul, K., & Chusri, S. (2022). Suspected cat‐to‐human transmission of SARS‐CoV‐2, Thailand, July‐September 2021. Emerging Infectious Diseases, 28(7), 1485–1488. https://doi.org/10.3201/eid2807.212605.
Snell, L. B., Fisher, C. L., Taj, U., Stirrup, O., Merrick, B., Alcolea‐Medina, A., Charalampous, T., Signell, A. W., Wilson, H. D., Betancor, G., Kia Ik, M. T., Cunningham, E., Cliff, P. R., Pickering, S., Galao, R. P., Batra, R., Neil, S. J. D., Malim, M. H., Doores, K. J., … Awan, A. R. (2022). Combined epidemiological and genomic analysis of nosocomial SARS‐CoV‐2 infection early in the pandemic and the role of unidentified cases in transmission. Clinical Microbiology and Infection, 28(1), 93–100. https://doi.org/10.1016/j.cmi.2021.07.040.
Stevanovic, V., Vilibic‐Cavlek, T., Tabain, I., Benvin, I., Kovac, S., Hruskar, Z., Mauric, M., Milasincic, L., Antolasic, L., Skrinjaric, A., Staresina, V., & Barbic, L. (2021). Seroprevalence of SARS‐CoV‐2 infection among pet animals in Croatia and potential public health impact. Transboundary and Emerging Diseases, 68(4), 1767–1773. https://doi.org/10.1111/tbed.13924.
Stirrup, O., Hughes, J., Parker, M., Partridge, D. G., Shepherd, J. G., Blackstone, J., Coll, F., Keeley, A., Lindsey, B. B., Marek, A., Peters, C., Singer, J. B., COVID‐19 Genomics UK (COG‐UK) consortium, Tamuri, A., de Silva, T. I., Thomson, E. C., & Breuer, J. (2021). Rapid feedback on hospital onset SARS‐CoV‐2 infections combining epidemiological and sequencing data. eLife, 10, e65828. https://doi.org/10.7554/eLife.65828.
USDA APHIS. (2023). Confirmed Cases of SARS‐COV‐2 in Animals in the United States. https://www.aphis.usda.gov/aphis/dashboards/tableau/sars‐dashboard.
Utah Public Health Laboratory, Utah Department of Health and Human Services. (2020). Nextflow workflow for our analysis of SARS‐CoV‐2 – Cecret. https://github.com/UPHL‐BioNGS/Cecret.
Wang, L., Gyimesi, Z. S., Killian, M. L., Torchetti, M., Olmstead, C., Fredrickson, R., & Terio, K. A. (2022). Detection of SARS‐CoV‐2 clade B.1.2 in three snow leopards. Transboundary and Emerging Diseases, 69(5), e3346–e3351. https://doi.org/10.1111/tbed.14625.
Yen, H. L., Sit, T. H. C., Brackman, C. J., Chuk, S. S. Y., Gu, H., Tam, K. W. S., Law, P. Y. T., Leung, G. M., Peiris, M., Poon, L. L. M., & HKU‐SPH study team. (2022). Transmission of SARS‐CoV‐2 delta variant (AY.127) from pet hamsters to humans, leading to onward human‐to‐human transmission: A case study. Lancet, 399(10329), 1070–1078. https://doi.org/10.1016/S0140‐6736(22)00326‐9.
Yu, G., Smith, D. K., Zhu, H., Guan, Y., & Lam, T. T.‐Y. (2017). Ggtree: An r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution, 8(1), 28–36. https://doi.org/10.1111/2041‐210X.12628.

Keywords: Panthera leo; One Health; SARS‐CoV‐2 delta variant; lions; viral zoonotic disease

Date Created: 20240603 Latest Revision: 20240603

20240603

10.1111/zph.13156

38825749