Serological Investigation on the Presence of Feline Coronavirus (FCoV) and Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) in Domestic Cats Living with COVID-19 Positive Owners in the UAE, 2022
Abstract
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethical Statement
2.2. Animals and Sampling
2.3. Detection of Feline Coronavirus Antibodies in Cats’ Sera
2.4. Detection of SARS-CoV-2 Antibodies in Cats’ Sera
2.5. Statistical Analysis
3. Results
3.1. Detection of Feline Coronavirus Antibodies in Cats’ Sera
3.2. Detection of SARS-CoV-2 in Cats’ Sera
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tekes, G.; Thiel, H.J. Feline Coronaviruses: Pathogenesis of Feline Infectious Peritonitis. Adv. Virus Res. 2016, 96, 193–218. [Google Scholar] [PubMed]
- Pedersen, N.C. A review of feline infectious peritonitis virus infection: 1963–2008. J. Feline Med. Surg. 2009, 11, 225–258. [Google Scholar] [CrossRef] [PubMed]
- Tasker, S. Diagnosis of feline infectious peritonitis: Update on evidence supporting available tests. J. Feline Med. Surg. 2018, 20, 228–243. [Google Scholar] [CrossRef]
- Addie, D.D.; Jarrett, O. Feline coronavirus infections. In Infectious Diseases of the Dog and the Cat, 3rd ed.; Greene, C.E., Ed.; Saunders Elsevier: St Louis, MO, USA, 2006; pp. 88–102. [Google Scholar]
- Addie, D.D.; Toth, S.; Murray, G.D.; Jarrett, O. Risk of feline infectious peritonitis in cats naturally infected with feline coronavirus. Am. J. Vet. Res. 1995, 56, 429–434. [Google Scholar] [PubMed]
- Foley, J.E.; Poland, A.; Carlson, J.; Pedersen, N.C. Risk factors for feline infectious peritonitis among cats in multiple-cat environments with endemic feline enteric coronavirus. J. Am. Vet. Med. Assoc. 1997, 210, 1313–1318. [Google Scholar]
- Herrewegh, A.A.; Mähler, M.; Hedrich, H.J.; Haagmans, B.L.; Egberink, H.F.; Horzinek, M.C.; Rottier, P.J.; de Groot, R.J. Persistence and evolution of feline coronavirus in a closed cat-breeding colony. Virology 1997, 234, 349–363. [Google Scholar] [CrossRef]
- Ritz, S.; Egberink, H.; Hartmann, K. Effect of feline interferon-omega on the survival time and quality of life of cats with feline infectious peritonitis. J. Vet. Intern. Med. 2007, 21, 1193–1197. [Google Scholar] [CrossRef]
- Addie, D.D.; Boucraut-Baralon, C.; Egberink, H.; Frymus, T.; Gruffydd-Jones, T.; Hartmann, K.; Horzinek, M.C.; Hosie, M.J.; Lloret, A.; Lutz, H.; et al. European Advisory Board on Cat Diseases. Disinfectant choices in veterinary practices, shelters and households: ABCD guidelines on safe and effective disinfection for feline environments. J. Feline Med. Surg. 2015, 17, 594–605. [Google Scholar] [CrossRef]
- Servat, A.; Picard-Meyer, E.; Robardet, E.; Muzniece, Z.; Must, K.; Cliquet, F. Evaluation of a Rapid Immunochromatographic Diagnostic Test for the detection of rabies from brain material of European mammals. Biologicals 2012, 40, 61–66. [Google Scholar] [CrossRef]
- Zhang, T.; Wu, Q.; Zhang, Z. Probable Pangolin Origin of SARS-CoV-2 Associated with the COVID-19 Outbreak. Curr. Biol. 2020, 30, 1346–1351. [Google Scholar] [CrossRef]
- Al-Rifai, R.H.; Acuna, J.; Al Hossany, F.I.; Aden, B.; Al Memari, S.A.; Al Mazrouei, S.K.; Ahmed, L.A. Epidemiological characterization of symptomatic and asymptomatic COVID-19 cases and positivity in subsequent RT-PCR tests in the United Arab Emirates. PLoS ONE 2021, 16, e0246903. [Google Scholar] [CrossRef]
- Al Hosany, F.; Ganesan, S.; Al Memari, S.; Al Mazrouei, S.; Ahamed, F.; Koshy, A.; Zaher, W. Response to COVID-19 pandemic in the UAE: A public health perspective. J. Glob. Health 2021, 11, 03050. [Google Scholar] [CrossRef]
- Al-Hosani, F.; Al-Mazrouei, S.; Al-Memari, S.; Al-Yafei, Z.; Paulo, M.S.; Koornneef, E. A Review of COVID-19 Mass Testing in the United Arab Emirates. Front. Public Health 2021, 9, 661134. [Google Scholar] [CrossRef]
- 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. Experimental infection of domestic dogs and cats with SARS-CoV-2: Pathogenesis, transmission, and response to reexposure in cats. Proc. Natl. Acad. Sci. USA 2020, 117, 26382–26388. [Google Scholar] [CrossRef]
- Shi, J.; Wen, Z.; Zhong, G.; Yang, H.; Wang, C.; Huang, B.; Liu, R.; He, X.; Shuai, L.; Sun, Z.; et al. Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2. Science 2020, 368, 1016–1020. [Google Scholar] [CrossRef]
- 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. Serologic screening of severe acute respiratory syndrome coronavirus 2 infection in cats and dogs during first coronavirus disease wave, The Netherlands. Emerg. Infect. Dis. 2021, 27, 1362–1370. [Google Scholar] [CrossRef]
- Sailleau, C.; Dumarest, M.; Vanhomwegen, J.; Delaplace, M.; Caro, V.; Kwasiborski, A.; Hourdel, V.; Chevaillier, P.; Barbarino, A.; Comtet, L.; et al. First detection and genome sequencing of SARS-CoV-2 in an infected cat in France. Transbound. Emerg. Dis. 2020, 67, 2324–2328. [Google Scholar] [CrossRef]
- Garigliany, M.; Van Laere, A.S.; Clercx, C.; Giet, D.; Escriou, N.; Huon, C.; van der Werf, S.; Eloit, M.; Desmecht, D. SARS-CoV-2 Natural Transmission from Human to Cat, Belgium, March 2020. Emerg. Infect. Dis. 2020, 26, 3069–3071. [Google Scholar] [CrossRef]
- Wu, L.; Chen, Q.; Liu, K.; Wang, J.; Han, P.; Zhang, Y.; Hu, Y.; Meng, Y.; Pan, X.; Qiao, C.; et al. Broad host range of SARS-CoV-2 and the molecular basis for SARS-CoV-2 binding to cat ACE2. Cell Discov. 2020, 6, 68. [Google Scholar] [CrossRef]
- Doliff, R.; Martens, P. Cats and SARS-CoV-2: A Scoping Review. Animals 2022, 12, 1413. [Google Scholar] [CrossRef]
- Jara, L.M.; Ferradas, C.; Schiaffino, F.; Sánchez-Carrión, C.; Martínez-Vela, A.; Ulloa, A.; Isasi-Rivas, G.; Montalván, A.; Sarmiento, L.G.; Fernández, M.; et al. Evidence of neutralizing antibodies against SARS-CoV-2 in domestic cats living with owners with a history of COVID-19 in Lima—Peru. One Health 2021, 13, 100318. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Zhang, H.; Gao, J.; Huang, K.; Yang, Y.; Hui, X.; He, X.; Li, C.; Gong, W.; Zhang, Y.; et al. A serological survey of SARS-CoV-2 in cat in Wuhan. Emerg. Microbes Infect. 2020, 9, 2013–2019. [Google Scholar] [CrossRef] [PubMed]
- Pomorska-Mól, M.; Turlewicz-Podbielska, H.; Gogulski, M.; Ruszkowski, J.J.; Kubiak, M.; Kuriga, A.; Barket, P.; Postrzech, M. A cross-sectional retrospective study of SARS-CoV-2 seroprevalence in domestic cats, dogs and rabbits in Poland. BMC Vet Res. 2021, 17, 322. [Google Scholar] [CrossRef] [PubMed]
- Hoskins, J.D.; Loar, A.S. Feline infectious diseases. Vet. Clin. N. Am. Small Anim. Pract. 1993, 23, 2–11. [Google Scholar]
- McNamara, T.; Richt, J.A.; Glickman, L.A. Critical needs assessment for research in companion animals and livestock following the pandemic of COVID-19 in humans. Vector Borne Zoonotic Dis. 2020, 20, 393–405. [Google Scholar] [CrossRef]
- Costagliola, A.; Liguori, G.; d’Angelo, D.; Costa, C.; Ciani, F.; Giordano, A. Do animals play a role in the transmission of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2)? A commentary. Animals 2020, 11, 16. [Google Scholar] [CrossRef]
- 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.; et al. SARS-CoV-2 infection, disease and transmission in domestic cats. Emerg. Microbes Infect. 2020, 9, 2322–2332. [Google Scholar] [CrossRef]
- Hosie, M.J.; Hofmann-Lehmann, R.; Hartmann, K.; Egberink, H.; Truyen, U.; Addie, D.D.; Belák, S.; Boucraut-Baralon, C.; Frymus, T.; Lloret, A.; et al. Anthropogenic infection of cats during the 2020 COVID-19 pandemic. Viruses 2021, 13, 185. [Google Scholar] [CrossRef]
- Bell, E.T.; Malik, R.; Norris, J.M. The relationship between the Feline Coronavirus antibody titre and the age, breed, gender and health status of Australian cats. Aust. Vet. J. 2006, 84, 2–7. [Google Scholar] [CrossRef]
- Bell, E.T.; Toribio, J.A.; White, J.D.; Malik, R.; Norris, J.M. Seroprevalence study of feline coronavirus in owned and feral cats in Sydney, Australia. Aust. Vet. J. 2006, 84, 74–81. [Google Scholar] [CrossRef]
- Brown, M.A.; Troyer, J.L.; Pecon-Slattery, J.; Roelke, M.E.; O’Brien, S.J. Genetics and pathogenesis of feline infectious peritonitis virus. Emerg. Infect. Dis. 2009, 15, 1445–1452. [Google Scholar] [CrossRef]
- Horzinek, M.C.; Osterhaus, A.D.M.E. Feline infectious peritonitis. A worldwide serosurvey. Am. J. Vet. Res. 1979, 40, 1487–1492. [Google Scholar]
- Pratelli, A.; Yesilbag, K.; Siniscalchi, M.; Yalçm, E.; Yilmaz, Z. Prevalence of feline coronavirus antibodies in cats in Bursa province, Turkey, by an enzyme-linked immunosorbent assay. J. Feline Med. Surg. 2009, 11, 881–884. [Google Scholar] [CrossRef]
- Sparkes, A.H.; Gruffydd-Jones, T.J.; Harbour, D.A. Feline coronavirus antibodies in UK cats. Vet. Rec. 1992, 131, 223–224. [Google Scholar] [CrossRef]
- Spada, E.; Canzi, I.; Baggiani, L.; Perego, R.; Vitale, F.; Migliazzo, A.; Proverbio, D. Prevalence of Leishmania infantum and co-infections in stray cats in northern Italy. Comp. Immunol. Microbiol. Infect. Dis. 2016, 45, 53–58. [Google Scholar] [CrossRef]
- Tekelioglu, B.K.; Berriatua, E.; Turan, N.; Helps, C.R.; Kocak, M.; Yilmaz, H.A. retrospective clinical and epidemiological study on feline coronavirus (FCoV) in cats in Istanbul, Turkey. Prev. Vet. Med. 2015, 119, 41–47. [Google Scholar] [CrossRef]
- Amoroso, M.G.; Serra, F.; Miletti, G.; Cardillo, L.; de Martinis, C.; Marati, L.; Alfano, F.; Ferrara, G.; Pagnini, U.; De Carlo, E.; et al. A Retrospective Study of Viral Molecular Prevalences in Cats in Southern Italy (Campania Region). Viruses 2022, 14, 2583. [Google Scholar] [CrossRef]
- Kiss, I.; Kecskeméti, S.; Tanyi, J.; Klingeborn, B.; Belák, S. Prevalence and genetic pattern of feline coronaviruses in urban cat populations. Vet. J. 2000, 159, 64–70. [Google Scholar] [CrossRef]
- Pesteanu-Somogyi, L.D.; Radzai, C.; Pressler, B.M. Prevalence of feline infectious peritonitis in specific cat breeds. J. Feline Med. Surg. 2006, 8, 1–5. [Google Scholar] [CrossRef]
- Worthing, K.A.; Wigney, D.I.; Dhand, N.K.; Fawcett, A.; McDonagh, P.; Malik, R.; Norris, J.M. Risk factors for feline infectious peritonitis in Australian cats. J. Feline Med. Surg. 2012, 14, 405–412. [Google Scholar] [CrossRef]
- Foley, J.E.; Pedersen, N.C. The inheritance of susceptibility to feline infectious peritonitis in purebred catteries. Feline Pract. 1996, 24, 14–22. [Google Scholar]
- Horzinek, M.; Addie, D.D.; Bélak, S.; Boucraut-Baralon, C.; Egberink, H.; Frymus, T.; Gruffydd-Jones, T.; Hartmann, K.; Hosie, M.J.; Lloret, A.; et al. ABCD guidelines on feline infectious perotinitis. Eur. Advis. Board Cat Dis. 2008, 1, 1–30. [Google Scholar]
- Almeida, A.; Galdino, M.V.; Araújo, J.P. Seroepidemiological study of feline coronavirus (FCoV) infection in domiciled cats from Botucatu, São Paulo, Brazil. Pesqui. Veterinária Bras. 2019, 39, 129–133. [Google Scholar] [CrossRef]
- Rohrbach, B.W.; Legendre, A.M.; Baldwin, C.A.; Lein, D.H.; Reed, W.M.; Wilson, R.B. Epidemiology of feline infectious peritonitis among cats examined at veterinary medical teaching hospitals. J. Am. Vet. Med. Assoc. 2001, 218, 1111–1115. [Google Scholar] [CrossRef]
- Barrs, V.R.; Peiris, M.; Tam, K.W.S.; Law, P.Y.T.; Brackman, C.J.; To, E.M.W.; Yu, V.Y.T.; Chu, D.K.W.; Perera, R.A.P.M.; Sit, T.H.C. SARS-CoV-2 in quarantined domestic cats from COVID-19 householdsor close contacts, Hong Kong, China. Emerg. Infect. Dis. 2020, 26, 3071–3074. [Google Scholar] [CrossRef]
- Newman, A.; Smith, D.; Ghai, R.R.; Wallace, R.M.; Torchetti, M.K.; Loiacono, C.; Murrell, L.S.; Carpenter, A.; Moroff, S.; Rooney, J.A.; et al. First reported cases of SARS-CoV-2 infection in companion animals—New York, March–April 2020. MMWR Morb. Mortal. Wkly. Rep. 2020, 69, 710–713. [Google Scholar] [CrossRef]
- Segalés, J.; Puig, M.; Rodon, J.; Avila-Nieto, C.; Carrillo, J.; Cantero, G.; Terrón, M.T.; Cruz, S.; Parera, M.; Noguera-Julián, M.; et al. Detection of SARS-CoV-2 in a cat owned by a COVID-19-affected patient in Spain. Proc. Natl. Acad. Sci. USA 2020, 117, 24790–24793. [Google Scholar] [CrossRef]
- Michelitsch, A.; Hoffmann, D.; Wernike, K.; Beer, M. Occurrence of antibodies against SARS-CoV-2 in the domestic cat population of Germany. Vaccines 2020, 8, 772. [Google Scholar] [CrossRef]
- Yilmaz, A.; Kayar, A.; Turan, N.; Iskefli, O.; Bayrakal, A.; Roman-Sosa, G.; Or, E.; Tali, H.E.; Kocazeybek, B.; Karaali, R.; et al. Presence of Antibodies to SARS-CoV-2 in Domestic Cats in Istanbul, Turkey, Before and After COVID-19 Pandemic. Front. Vet. Sci. 2021, 8, 707368. [Google Scholar] [CrossRef]
Regions | No. of Samples | Gender | Age Range | Breed | Access to the Outdoors | Reproductive Statues | Rearing Model | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Male | Female | <1 year | ≥1 year | Purebred | Mixed breed | Yes | No | Whole | Castrated or Spayed | Solitary | In Groups | ||
Al-Ain | 62 | 28 | 34 | 35 | 27 | 36 | 26 | 19 | 43 | 62 | 0 | 44 | 18 |
Abu-Dhabi | 21 | 12 | 9 | 12 | 9 | 9 | 12 | 8 | 13 | 19 | 2 | 18 | 3 |
Total | 83 | 40 | 43 | 47 | 36 | 45 | 38 | 27 | 56 | 81 | 2 | 62 | 21 |
Variables | FCoV Antibody Detection Rate | χ2 | p-Value a | ORs | 95% CIs | |
---|---|---|---|---|---|---|
Numbers (Infected/Total) | % | |||||
1—Geographic locations | ||||||
Al-Ain city | 39/62 | 63 | 0.501 | 0.479 | 0.329 | 0.128–1.20 |
Abu Dhabi city | 15/21 | 71 | ||||
2—Age | ||||||
<1 year | 32/47 | 68 | 0.436 | 0.509 | 1.18 | 0.382–3.66 |
≥1 year | 22/36 | 61 | ||||
3—Breed | ||||||
Purebred cats | 40/45 | 89 | 24.55 | <0.0001 a | 16.96 | 4.74–58.76 |
Mixed-breed cats | 14/38 | 37 | ||||
4—Gender | ||||||
Male | 25/40 | 62.5 | 0.223 | 0.637 | 0.402 | 0.130–1.24 |
Female | 29/43 | 67.4 | ||||
5—Reproductive status | ||||||
Castrated or spayed | 2/2 | 100 | * | * | * | * |
Whole | 52/81 | 64 | ||||
6—Rearing model | ||||||
Solitary | 39/62 | 63 | 0.502 | 0.479 | 0.562 | 0.191–1.56 |
Group | 15/21 | 71 | ||||
7—Outdoor access | ||||||
Yes | 13/27 | 48 | 5.03 | 0.02 a | 0.211 | 0.547−3.27 |
No | 41/56 | 73 |
Sample No. | Geographic Location | Breed | Gender | Age | Rearing Model | Outdoor Access | Reproductive Status |
---|---|---|---|---|---|---|---|
10 | Abu Dhabi | Himalayan | Female | ≥1 year | Group | No | Whole |
27 | Abu Dhabi | Mixed-breed | Female | ≥1 year | Group | No | Whole |
28 | Abu Dhabi | Mixed-breed | Female | ≥1 year | Group | No | Whole |
40 | Al-Ain | Mixed-breed | Female | <1 year | Solitary | No | Whole |
67 | Al-Ain | British short-hair | Female | <1 year | Solitary | No | Whole |
75 | Al-Ain | British short-hair | Female | ≥1 year | Solitary | No | Whole |
76 | Al-Ain | Scottish fold | Female | <1 year | Solitary | No | Whole |
79 | Al-Ain | Persian | Female | ≥1 year | Solitary | No | Whole |
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El-Tholoth, M.; Hussein, M.; Mohammed, D.; Al-Rasheedi, M.; Al-Qubaisi, H.; Al-Blooshi, A.; Al-Ahbabi, M.; Al-Dhaheri, Z.; Al-Blooshi, K.; Al-Herbawi, M.; et al. Serological Investigation on the Presence of Feline Coronavirus (FCoV) and Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) in Domestic Cats Living with COVID-19 Positive Owners in the UAE, 2022. Animals 2023, 13, 493. https://doi.org/10.3390/ani13030493
El-Tholoth M, Hussein M, Mohammed D, Al-Rasheedi M, Al-Qubaisi H, Al-Blooshi A, Al-Ahbabi M, Al-Dhaheri Z, Al-Blooshi K, Al-Herbawi M, et al. Serological Investigation on the Presence of Feline Coronavirus (FCoV) and Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) in Domestic Cats Living with COVID-19 Positive Owners in the UAE, 2022. Animals. 2023; 13(3):493. https://doi.org/10.3390/ani13030493
Chicago/Turabian StyleEl-Tholoth, Mohamed, Mahmoud Hussein, Dina Mohammed, Majed Al-Rasheedi, Hamad Al-Qubaisi, Abdullah Al-Blooshi, Mohammed Al-Ahbabi, Zayed Al-Dhaheri, Khalifa Al-Blooshi, Majd Al-Herbawi, and et al. 2023. "Serological Investigation on the Presence of Feline Coronavirus (FCoV) and Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) in Domestic Cats Living with COVID-19 Positive Owners in the UAE, 2022" Animals 13, no. 3: 493. https://doi.org/10.3390/ani13030493
APA StyleEl-Tholoth, M., Hussein, M., Mohammed, D., Al-Rasheedi, M., Al-Qubaisi, H., Al-Blooshi, A., Al-Ahbabi, M., Al-Dhaheri, Z., Al-Blooshi, K., Al-Herbawi, M., Abo Elfadl, E. A., & Seboussi, R. (2023). Serological Investigation on the Presence of Feline Coronavirus (FCoV) and Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) in Domestic Cats Living with COVID-19 Positive Owners in the UAE, 2022. Animals, 13(3), 493. https://doi.org/10.3390/ani13030493