Detection of neutralising antibodies against SARS-CoV-2 in companion animals in Istanbul

Yıl 2022, , 128 - 133, 31.12.2022

Hakan Enül , Fahriye Saraç , Cumhur Adıay , Serdar Uzar , Pelin Tuncer-göktuna , Seçkin Serdar Arun , Mustafa Hasöksüz

https://doi.org/10.30704/http-www-jivs-net.1198979

Öz

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged in late 2019 and rapidly spread throughout the world. After the susceptibility of various animals to SARS-CoV-2 infection was reported, the prevalence of COVID-19 infection in pet animals and their role in virus transmission became a source of concern. Seroprevalence of SARS-CoV-2 in pet animals has been reported from various parts of the world to date. In this study, 206 serum samples of household dogs and cats were obtained from a diagnostic laboratory in Istanbul. Ninety-nine of the samples were collected during the second wave (November and December 2020) of the pandemic, and 107 were collected between August and September 2021. Neutralizing antibodies against SARS-CoV-2 in companion animals was investigated by virus neutralization test. Among the 99 serum samples which were collected during the second wave (November and December 2020) of the pandemic, while no neutralizing antibodies were found in 61 sera of cats, one of 38 dogs was positive with a titer of 1/256. Similarly, 0/54 cats and 1/53 dogs were tested positive for the neutralizing antibodies among the samples collected between August and September 2021. This study is demonstrating the evidence of SARS-CoV-2 infection in dogs. 

Anahtar Kelimeler

COVID-19, Neutralising antibodies, cat, dog, SARS-CoV-2

Teşekkür

We would like to thank Görkem Çolak and Sedat Kılıç for their contributions.

Kaynakça

• Barua, S., Hoque, M., Adekanmbi, F., Kelly, C., 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 and Infections, 10, 1669-1674. DOI: 10.1080/22221751.2021.1967101.
• Bosco-Lauth, A.M., Hartwig, A.E., Porter, S.M., Gordy, P.W., Nehring, M., Byas, A.D., VandeWoude, S., Ragan, I.K., Maison, R.M., & Bowen R.A. (2020). Experimental infection of domestic dogs and cats with SARS-CoV-2: Pathogenesis, transmission, and response to reexposure in cats. Proceedings of the National Academy of Sciences of the United States of America, 117, 26382-26388. DOI:10.1073/pnas.2013102117.
• Calvet, G.A., Pereira, S.A., Ogrzewalska, M., Pauvolid-Corrêa, A., Resende, P.C., Tassinari, W de S., de Pina Costa, A., Keidel, L.O., da Rocha, A.S.B., da Silva, M.F.B., dos Santos, S.A., Lima, A.B.M., de Moraes, I.C.V., Mendes, A.A.V., das C Souza, T., Martins, E.B., Ornellas, R.O., Corrêa, M.L., da S Antonio, I.M., Guaraldo, L., do C Motta, F., Brasil, P., Siqueira, M.M., Gremião, I.D.F., & Menezes, R.C. (2021). Investigation of SARS-CoV-2 infection in dogs and cats of humans diagnosed with COVID-19 in Rio de Janeiro, Brazil. PLoS One, 16. DOI:10.1371/journal.pone.0250853.
• Davies, N.G., Abbott, S., Barnard, R.C., Jarvis, C.I., Kucharski, A.J., Munday, J.D., Pearson, C.A.B., Russell, T.W., Tully, D.C., Washburne, A.D., Wenseleers, T., Gimma, A., Waites, W., Wong, K.L.M., van Zandvoort, K., Silverman, J.D., Diaz-Ordaz, K., Keogh, R., Eggo, R.M., Funk, S., Jit, M., Atkins, K.E., & Edmunds, W.J. (2021). Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England. Science, 372. DOI:10.1126/science.abg3055.
• Fritz, M., Rosolen, B., Krafft, E., Becquart, P., Elguero, E., Vratskikh, O., Denolly, S., Boson, B., Vanhomwegen, J., Gouilh, M.A., Kodjo, A., Chirouze, C., Rosolen, S.G., Legros, V., & Leroy, E.M. (2020). High prevalence of SARS-CoV-2 antibodies in pets from COVID-19+ households. One Health, 11, 100192. DOI:10.1016/J.ONEHLT.2020.100192.
• Hamer, S.A., Pauvolid-Corrêa, A., Zecca, I.B., Davila, E., Auckland, L.D., Roundy, C.M., Tang, W., Torchetti, M., Killian, M.L., Jenkins-Moore, M., Mozingo, K., Akpalu, Y., Ghai, R.R., Spengler, J.R., Behravesh, C.B., Fischer, R.S.B., & Hamer, G.L. (2020). Natural SARS-CoV-2 infections, including virus isolation, among serially tested cats and dogs in households with confirmed human COVID-19 cases in Texas, USA. bioRxiv. DOI:10.1111/tbed.14122.
• Laidoudi, Y., Sereme, Y., Medkour, H., Watier-Grillot, S., Scandola, P., Ginesta, J., Andréo, V., Labarde, C., Comtet, L., Pourquier, P., Raoult, D., Lou Marié, J., & Davoust, B. (2021). SARS-CoV-2 antibodies seroprevalence in dogs from France using ELISA and an automated western blotting assay. One Health, 13. DOI:10.1016/j.onehlt.2021.100293.
• Michelitsch, A., Hoffmann, D., Wernike, K., & Beer, M. (2020). Occurrence of antibodies against SARS-CoV-2 in the domestic cat population of Germany. Vaccines, 8, 1–10. DOI:10.3390/vaccines8040772.
• Michelitsch, A., Schön, J., Hoffmann, D., Beer, M., & Wernike, K. (2021). The second wave of sars-cov-2 circulation—antibody detection in the domestic cat population in Germany. Viruses, 13, 1009. DOI:10.3390/v13061009.
• Munnink, B.B.O., 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., Van Der Honing, R.H., Wegdam-Blans, M.C.A., Bouwstra, R.J., GeurtsvanKessel, C., Van Der Eijk, A.A., Velkers, F.C., Smit, L.A.M., Stegeman, A., Van Der Poel, W.H.M., & Koopmans, M.P.G. (2021). Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans. Science, 371, 172-177. DOI: 10.1126/science.abe5901.
• Neira, V., Brito, B., Agüero, B., Berrios, F., Valdés, V., Gutierrez, A., Ariyama, N., Espinoza, P., Retamal, P., Holmes, E.C., Gonzalez-Reiche, A.S., Khan, Z., van de Guchte, A., Dutta, J., Miorin, L., Kehrer, T., Galarce, N., Almonacid, L.I., Levican, J., van Bakel, H., García-Sastre, A., & Medina, R.A.(2021). A household case evidences shorter shedding of SARS-CoV-2 in naturally infected cats compared to their human owners. Emerging Microbes and Infections, 10, 376-383. DOI:10.1080/22221751.2020.1863132.
• Palmer, M.V., Martins, M., Falkenberg, S., Buckley, A., Caserta, L.C., Mitchell, P.K., Cassmann, E.D., Rollins, A., Zylich, N.C., Renshaw, R.W., Guarino, C., Wagner, B., Lager, K., & Diel, D.G. (2021). Susceptibility of White-Tailed Deer (Odocoileus virginianus) to SARS-CoV-2. Journal of Virology, 95. DOI:10.1128/jvi.00083-21.
• Patterson, E.I., Elia, G., Grassi, A., Giordano, A., Desario, C., Medardo, M., Smith, S.L., Anderson, E.R., Prince, T., Patterson, G.T., Lorusso, E., Lucente, M.S., Lanave, G., Lauzi, S., Bonfanti, U., Stranieri, A., Martella, V., Solari Basano, F., Barrs, V.R., Radford, A.D., Agrimi, U., Hughes, G.L., Paltrinieri, S., & Decaro, N. (2020). Evidence of exposure to SARS-CoV-2 in cats and dogs from households in Italy. Nature Communications, 11, 6231. DOI:10.1038/s41467-020-20097-0.
• Public Health England, (2021). SARS-CoV-2 variants of concern and variants under investigation in England: technical briefing 10. Retrieved from : https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/984274/Variants_of_Concern_VOC_Technical_Briefing_10_England.pdf
• Ruiz-Arrondo, I., Portillo, A., Palomar, A.M., Santibáñez, S., Santibáñez, P., Cervera, C., & Oteo, J.A. (2021). Detection of SARS-CoV-2 in pets living with COVID-19 owners diagnosed during the COVID-19 lockdown in Spain: A case of an asymptomatic cat with SARS-CoV-2 in Europe. Transboundary and Emerging Diseases, 68, 973-976. DOI:10.1111/tbed.13803.
• Schlottau, K., Rissmann, M., Graaf, A., Schön, J., Sehl, J., Wylezich, C., Höper, D., Mettenleiter, T.C., Balkema-Buschmann, A., Harder, T., Grund, C., Hoffmann, D., Breithaupt, A., & Beer, M. (2020). SARS-CoV-2 in fruit bats, ferrets, pigs, and chickens: an experimental transmission study. The Lancet Microbe, 1, e218-e225. DOI:10.1016/S2666-5247(20)30089-6.
• Schulz, C., Martina, B., Mirolo, M., Müller, E., Klein, R., Volk, H., Egberink, H., Gonzalez-Hernandez, M., Kaiser, F., von Köckritz-Blickwede, M., & Osterhaus, A. (2021). SARS-CoV-2-specific antibodies in domestic cats during first COVID-19 Wave, Europe. Emerging Infectious Diseases, 27, 3115-3118. DOI:10.3201/eid2712.211252.
• Segalés, J., Puig, M., Rodon, J., Avila-Nieto, C., Carrillo, J., Cantero, G., Terrón, M.T., Cruz, S,, Parera, M., Noguera-Julián, M., Izquierdo-Useros, N., Guallar, V., Vidal, E., Valencia, A., Blanco, I., Blanco, J., Clotet, B., & Vergara-Alert, J. (2020). Detection of SARS-CoV-2 in a cat owned by a COVID-19-affected patient in Spain. Proceedings of the National Academy of Sciences of the United States of America, 117, 24790-24793. DOI:10.1073/pnas.2010817117.
• 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., & Chen, H., and Bu, Z.(2020). Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2. Science, 368, 1016-1020. DOI:10.1126/science.abb7015.
• Sia, S.F., Yan, L.M., Chin, A.W.H., Fung, K., Choy, K.T., Wong, A.Y.L., Kaewpreedee, P., Perera, R.A.P.M., Poon, L.L.M., Nicholls, J.M., Peiris, M., & Yen, H.L. (2020) Pathogenesis and transmission of SARS-CoV-2 in golden hamsters. Nature, 583, 834-838. DOI:10.1038/s41586-020-2342-5.
• 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, 1485-1488. DOI:10.3201/eid2807.212605
• Sit, T.H.C., Brackman, C.J., Ip, S.M., Tam, K.W.S., Law, P.Y.T., To, E.M.W., Yu, V.Y.T., Sims, L.D., Tsang, D.N.C., Chu, D.K.W., Perera, R.A.P.M., Poon, L.L.M., Peiris, M. (2020) Infection of dogs with SARS-CoV-2. Nature, 586, 776-778. DOI:10.1038/s41586-020-2334-5.
• Smith, S.L., Anderson, E.R., Cansado-Utrilla, C., Prince, T., Farrell, S., Brant, B., Smyth, S., Noble, P-J.M, Pinchbeck, G.L., Marshall, N., Roberts, L,, Hughes, G.L., Radford, A.D., Patterson, E.I. (2021). SARS-CoV-2 neutralising antibodies in dogs and cats in the United Kingdom. Current Research in Virology Science, 2, 100011. DOI:10.1016/j.crviro.2021.100011.
• 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, 1767-1773. DOI:10.1111/tbed.13924.
• Tan, C.W., Chia, W.N., Qin, X., Liu, P., Chen, M.I.C., Tiu, C., Hu, Z., Chen, V.C.W., Young , B.E., Sia, W.R., Tan, Y.J., Foo, R., Yi, Y., Lye, D.C., Anderson, D.E., & Wang, L.F. (2020). A SARS-CoV-2 surrogate virus neutralization test based on antibody-mediated blockage of ACE2–spike protein–protein interaction. Nature Biotechnology, 38, 1073-1078. DOI:10.1038/s41587-020-0631-z.
• Udom, K., Jairak, W., Chamsai, E., Charoenkul, K., Boonyapisitsopa, S., Bunpapong, N., Techakriengkrai, N., Amonsin, A. (2021). Serological survey of antibodies against SARS-CoV-2 in dogs and cats, Thailand. Transboundary and Emerging Diseases,1-8. DOI:10.1111/tbed.14208.
• Ulrich, L., Wernike, K., Hoffmann, D., Mettenleiter, T.C., & Beer, M. (2020). Experimental Infection of Cattle with SARS-CoV-2. Emerging Infectious Diseases, 26, 2979-2981. DOI:10.3201/eid2612.203799.
• WOAH, (2022). SARS-CoV-2 in Animals - Situation Report 11. Retrieved from: https://www.woah.org/app/uploads/2022/09/sars-cov-2-situation-report-16.pdf
• Yilmaz, A., Kayar, A., Turan, N., Iskefli, O., Bayrakal, A., Roman-Sosa, G., Or ,E., Tali, H.E., Kocazeybek, B., Karaali, R., Bold, D., Sadeyen, J.R., Lukosaityte, D., Chang, P., Iqbal, M., Richt, J.A., Yilmaz, H. (2021). Presence of Antibodies to SARS-CoV-2 in Domestic Cats in Istanbul, Turkey, Before and After COVID-19 Pandemic. Frontiers Veterinary Science, 8, 1123. DOI:10.3201/eid2612.203799.
• Zhang, Q., Zhang, H., Gao, J., Huang, K., Yang, Y., Hui, X., He, X., Li, C., Gong, W., Zhang, Y., Zhao, Y., Peng, C., Gao, X., Chen, H., Zou, Z., Shi, Z.L., Jin, M. (2020). A serological survey of SARS-CoV-2 in cat in Wuhan. Emerging Microbes and Infections, 9, 2013-2019. DOI:10.1080/22221751.2020.1817796.
• Zhao, S., Schuurman, N., Li, W., Wang, C., Smit, L.A.M., Broens, E.M., Wagenaar, J.A., van Kuppeveld, F.J.M., Bosch, B.J., Egberink, H. (2021). Serologic screening of severe acute respiratory syndrome coronavirus 2 infection in cats and dogs during first coronavirus disease wave, the Netherlands. Emerging Infectious Diseases, 27, 1362-1370. DOI:10.3201/eid2705.204055.
• Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., Niu, P., Zhan, F., Ma, X., Wang, D., Xu, W., Wu, G., Gao, G.F., & Tan, W. (2020). A Novel Coronavirus from Patients with Pneumonia in China, 2019. New England Journal of Medicine, 382, 727-733. DOI:10.1056/nejmoa2001017.