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Volume 36 Issue 5
October 2021
    Citation: Hanna Turlewicz-Podbielska, Małgorzata Pomorska-Mól. Porcine Coronaviruses: Overview of the State of the Art .VIROLOGICA SINICA, 2021, 36(5) : 833-851.  http://dx.doi.org/10.1007/s12250-021-00364-0
    shu

    Porcine Coronaviruses: Overview of the State of the Art

    • 1.

      Department of Preclinical Sciences and Infectious Diseases, Faculty of Veterinary Medicine and Animal Sciences, Poznan University of Life Sciences, ul. Wołyńska 35, 60-637 Poznan, Poland

    • Corresponding author: Małgorzata Pomorska-Mól, mpomorska@up.poznan.pl, ORCID: http://orcid.org/0000-0003-2220-2730
    • Received Date: 26 May 2020
      Accepted Date: 19 November 2020
      Published Date: 15 March 2021
      Available online: 01 October 2021

    • Like RNA viruses in general, coronaviruses (CoV) exhibit high mutation rates which, in combination with their strong tendency to recombine, enable them to overcome the host species barrier and adapt to new hosts. It is currently known that six CoV are able to infect pigs. Four of them belong to the genus Alphacoronavirus [transmissible gastroenteritis coronavirus (TEGV), porcine respiratory coronavirus (PRCV), porcine epidemic diarrhea virus (PEDV), swine acute diarrhea syndrome coronavirus (SADS-CoV)], one of them to the genus Betacoronavirus [porcine hemagglutinating encephalomyelitis virus (PHEV)] and the last one to the genus Deltacoronavirus (PDCoV). PHEV was one of the first identified swine CoV and is still widespread, causing subclinical infections in pigs in several countries. PRCV, a spike deletion mutant of TGEV associated with respiratory tract infection, appeared in the 1980s. PRCV is considered non-pathogenic since its infection course is mild or subclinical. Since its appearance, pig populations have become immune to both PRCV and TGEV, leading to a significant reduction in the clinical and economic importance of TGEV. TGEV, PEDV and PDCoV are enteropathogenic CoV and cause clinically indistinguishable acute gastroenteritis in all age groups of pigs. PDCoV and SADS-CoV have emerged in 2014 (US) and in 2017 (China), respectively. Rapid diagnosis is crucial for controlling CoV infections and preventing them from spreading. Since vaccines are available only for some porcine CoV, prevention should focus mainly on a high level of biosecurity. In view of the diversity of CoV and the potential risk factors associated with zoonotic emergence, updating the knowledge concerning this area is essential.

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      1. Akimkin V, Beer M, Blome S, Hanke D, Höper D, Jenckel M, Pohlmann A (2016) New chimeric porcine coronavirus in swine feces, Germany, 2012. Emerg Infect Dis 22: 1314–1315
          doi: 10.3201/eid2207.160179

      2. Andries K, Pensaert MB (1980) Immunofluorescence studies on the pathogenesis of hemagglutinating encephalomyelitis virus infection in pigs after oronasal inoculation. Am J Vet Res 41: 1372–1378

      3. Andries K, Pensaert M, Callebaut P (1978) Pathogenicity of hemagglutinating encephalomyelitis (vomiting and wasting disease) virus of pigs, using different routes of inoculation. Zentralbl Veterinarmed B 25: 461–468

      4. Annamalai T, Saif LJ, Lu Z, Jung K (2015) Age-dependent variation in innate immune responses to porcine epidemic diarrhea virus infection in suckling versus weaned pigs. Vet Immunol Immunopathol 168: 193–202
          doi: 10.1016/j.vetimm.2015.09.006

      5. Appel M, Greig AS, Corner AH (1965) Encephalomyelitis of swine caused by a hemagglutinating virus. Ⅳ. Transmission studies. Res Vet Sci 6: 482–489
          doi: 10.1016/S0034-5288(18)34728-3

      6. Atanasova K, Van Gucht S, Barbé F, Lefebvre DJ, Chiers K, Van Reeth K (2008) Lung cell tropism and inflammatory cytokine-profile of porcine respiratory coronavirus infection. Open Vet Sci J 2: 117–126
          doi: 10.2174/1874318808002010117

      7. Bevins SN, Lutman M, Pedersen K, Barrett N, Gidlewski T, Deliberto TJ, Franklin AB (2018) Spillover of swine coronaviruses, United States. Emerg Infect Dis 24: 1390–1392
          doi: 10.3201/eid2407.172077

      8. Bjustrom-Kraft J, Woodard K, Gimenez-Lirola L, Setness B, Ji J, Lasley P, Nelson E, Zhang JQ, Baum D, Gauger P, Main R, Zimmerman J (2018) Serum and mammary secretion antibody responses in porcine epidemic diarrhea-immune gilts following porcine epidemic diarrhea vaccination. J Swine Health Prod 26: 34–40

      9. Bohl EH (1989) Transmissible gastroenteritis virus (classical enteric variant). In: Pensaert MB (ed.) Virus infections of vertebrates, vol 2, 2nd edn. Elsevier, Amsterdam, pp 139–153

      10. Boley PA, Alhamo MA, Lossie G, Yadav KK, Vasquez-Lee M, Saif LJ, Kenney SP (2020) Porcine deltacoronavirus infection and transmission in poultry, United States. Emerg Infect Dis 26: 255–265
          doi: 10.3201/eid2602.190346

      11. Boniotti MB, Papetti A, Lavazza A, Alborali G, Sozzi E, Chiapponi C, Faccini S, Bonilauri P, Cordioli P, Marthaler D (2016) Porcine epidemic diarrhea virus and discovery of a recombinant swine enteric coronavirus, Italy. Emerg Infect Dis 22: 83–87
          doi: 10.3201/eid2201.150544

      12. Bowman AS, Krogwold RA, Price T, Davis M, Moeller SJ (2015) Investigating the introduction of porcine epidemic Diarrhea virus into an Ohio swine operation. BMC Vet Res 11: 38
          doi: 10.1186/s12917-015-0348-2

      13. Bridgen A, Tobler K, Ackermann M (1993) Identification of coronaviral conserved sequences and application to viral genome amplification. Adv Exp Med Biol 342: 81–82

      14. Burlatschenko S, Arsenault C (2015) Elimination of porcine respiratory coronavirus by early weaning and segregation. J Swine Health Prod 23: 208–213

      15. Callebaut TP, Pensaert MB, Hooyberghs J (1989) A competitive inhibition ELISA for the differentiation of serum antibodies from pigs infected with transmissible gastroenteritis virus (TGEV) or with the TGEV-related porcine respiratory coronavirus. Vet Microbiol 20: 9–19
          doi: 10.1016/0378-1135(89)90003-5

      16. Callebaut P, Cox E, Pensaert M, Van Deun K (1990) Induction of milk IgA antibodies by porcine respiratory coronavirus infection. Adv Exp Med Biol 276: 421–428

      17. Callebaut P, Pensaert M (1995) Expression and immunogenicity of the spike glycoprotein of porcine respiratory coronavirus encoded in the E3 region of adenovirus. Adv Exp Med Biol 380: 65–270

      18. Cao L, Ge X, Gao Y, Ren Y, Ren X, Li G (2015) Porcine epidemic diarrhea virus infection induces NF-kappaB activation through the TLR2, TLR3 and TLR9 pathways in porcine intestinal epithelial cells. J Gen Virol 96: 1757–1767
          doi: 10.1099/vir.0.000133

      19. Carman S, Josephson G, McEwen B, Maxie G, Antochi M, Eernisse K, Nayar G, Halbur P, Erickson G, Nilsson E (2002) Field validation of a commercial blocking ELISA to differentiate antibody to transmissible gastroenteritis virus (TGEV) and porcine respiratory coronavirus and to identify TGEV-infected swine herds. J Vet Diagn Invest 14: 97–105
          doi: 10.1177/104063870201400202

      20. Cartwright SF, Lucas M (1970) Vomiting and wasting disease in piglets. Virological and epidemiological studies. Vet Rec 86: 278–280
          doi: 10.1136/vr.86.10.278

      21. Chan JF, To KK, Tse H, Jin DY, Yuen KY (2013) Interspecies transmission and emergence of novel viruses: lessons from bats and birds. Trends Microbiol 21: 544–555
          doi: 10.1016/j.tim.2013.05.005

      22. Chattha KS, Roth JA, Saif LJ (2015) Strategies for design and application of enteric viral vaccines. Annu Rev Anim Biosci 3: 375–395
          doi: 10.1146/annurev-animal-022114-111038

      23. Chen Q, Gauger P, Stafne M, Thomas J, Arruda P, Burrough E, Madson D, Brodie J, Magstadt D, Derscheid R, Welch M, Zhang J (2015) Pathogenicity and pathogenesis of a United States porcine deltacoronavirus cell culture isolate in 5-day-old neonatal piglets. Virology 482: 51–59
          doi: 10.1016/j.virol.2015.03.024

      24. Chen F, Knutson TP, Rossow S, Saif LJ, Marthaler DG (2019) Decline of transmissible gastroenteritis virus and its complex evolutionary relationship with porcine respiratory coronavirus in the United States. Sci Rep 9: 3953
          doi: 10.1038/s41598-019-40564-z

      25. Chen Y, Liu Q, Guo D (2020) Emerging coronaviruses: genome structure, replication, and pathogenesis. J Med Virol 92: 418–423
          doi: 10.1002/jmv.25681

      26. Cima G (2013) Viral disease affects US pigs: porcine epidemic diarrhea found in at least 11 states. J Am Vet Med Assoc 243: 30–31

      27. Crawford K, Lager KM, Kulshreshtha V, Miller LC, Faaberg KS (2016) Status of vaccines for porcine epidemic diarrhea virus in the United States and Canada. Virus Res 226: 108–116
          doi: 10.1016/j.virusres.2016.08.005

      28. Dastjerdi A, Carr J, Ellis RJ, Steinbach F, Williamson S (2015) Porcine epidemic diarrhea virus among farmed pigs, Ukraine. Emerg Infect Dis 21: 2235–2237
          doi: 10.3201/eid2112.150272

      29. De Arriba ML, Carvajal A, Pozo J, Rubio P (2002a) Mucosal and systemic isotype-specific antibody responses and protection in conventional pigs exposed to virulent or attenuated porcine epidemic diarrhoea virus. Vet Immunol Immunopathol 85: 85–97
          doi: 10.1016/S0165-2427(01)00417-2

      30. De Arriba ML, Carvajal A, Pozo J, Rubio P (2002b) Rubio Isotype-specific antibody-secreting cells in systemic and mucosal associated lymphoid tissues and antibody responses in serum of conventional pigs inoculated with PEDV. Vet Immunol Immunopathol 84: 1–16
          doi: 10.1016/S0165-2427(01)00386-5

      31. De Nova PJG, Cortey M, Díaz I, Puente H, Rubio P, Martín M, Carvajal A (2020) A retrospective study of porcine epidemic diarrhoea virus (PEDV) reveals the presence of swine enteric coronavirus (SeCoV) since 1993 and the recent introduction of a recombinant PEDV-SeCoV in Spain. Transbound Emerg Dis. https://doi.org/10.1111/tbed.13666

      32. Derbyshire JB, Jessett DM, Newman G (1969) An experimental epidemiological study of porcine transmissible gastroenteritis. J Comp Pathol 79: 445–452
          doi: 10.1016/0021-9975(69)90064-4

      33. Diel DG, Lawson S, Okda F, Singrey A, Clement T, Fernandes MHV, Christopher-Hennings J, Nelson EA (2016) Porcine epidemic diarrhea virus: an overview of current virological and serological diagnostic methods. Virus Res 226: 60–70
          doi: 10.1016/j.virusres.2016.05.013

      34. Doyle LP, Hutchings LM (1946) A transmissible gastroenteritis in pigs. J Am Vet Med Assoc 108: 257

      35. Duarte M, Laude H (1994) Sequence of the spike protein of the porcine epidemic diarrhoea virus. J Gen Virol 75: 1195–1200
          doi: 10.1099/0022-1317-75-5-1195

      36. Enjuanes L, van der Zeijst BAM (1995) Molecular basis of transmissible gastroenteritis virus epidemiology. Coronaviridae 337–376

      37. Enjuanes L, Sola I, Almazán F, Ortego J, Izeta A, González JM, Alonso S, Sánchez-Morgado JM, Escors D, Calvo E, Riquelme C, Sánchez CM (2001) Coronavirus derived expression systems. J Biotech 88: 183–204
          doi: 10.1016/S0168-1656(01)00281-4

      38. Fan H, Zhang J, Ye Y, Tong T, Xie K, Liao M (2012) Complete genome sequence of a novel porcine epidemic diarrhea virus in south China. J Virol 86: 10248–10249
          doi: 10.1128/JVI.01589-12

      39. Fang P, Fang L, Hong Y, Liu X, Dong N, Ma P, Bi J, Wang D, Xiao S (2017) Discovery of a novel accessory protein NS7a encoded by porcine deltacoronavirus. J Gen Virol 98: 173–178
          doi: 10.1099/jgv.0.000690

      40. Fenner F (2017) Chapter 24. Coronaviridae. In: Maclachlan NJ, Dubovi EJ (eds) Fenner's veterinary virology, 5th edn. Academic Press, New York, pp 435–461

      41. Fu J, Chen R, Hu J, Qu H, Zhao Y, Cao S, Wen X, Wen Y, Wu R, Zhao Q, Ma X, Huang X (2020) Identification of a novel linear B-cell epitope on the nucleocapsid protein of porcine deltacoronavirus. Int J Mol Sci 21: 648
          doi: 10.3390/ijms21020648

      42. Garwes DJ, Stewart F, Cartwright SF, Brown I (1988) Differentiation of porcine coronavirus from transmissible gastroenteritis virus. Vet Rec 122: 86–87
          doi: 10.1136/vr.122.4.86

      43. Gimenez-Lirola LG, Zhang J, Carrillo-Avila JA, Chen Q, Magtoto R, Poonsuk K, Baum DH, Pineyro P, Zimmerman J (2017) Reactivity of porcine epidemic diarrhea virus structural proteins to antibodies against porcine enteric coronaviruses: diagnostic implications. J Clin Microbiol 55: 1426–1436
          doi: 10.1128/JCM.02507-16

      44. Goede D, Murtaugh MP, Nerem J, Yeske P, Rossow K, Morrison R (2015) Previous infection of sows with a "mild" strain of porcine epidemic diarrhea virus confers protection against infection with a "severe" strain. Vet Microbiol 176: 161–164
          doi: 10.1016/j.vetmic.2014.12.019

      45. Gong L, Li J, Zhou Q, Xu Z, Chen L, Zhang Y, Xue C, Wen Z, Cao Y (2017) A new Bat-HKU2-like coronavirus in swine, China, 2017. Emerg Infect Dis 23: 1607–1609
          doi: 10.3201/eid2309.170915

      46. Grasland B, Bigault L, Bernard C, Quenault H, Toulouse O, Fablet C, Rose N, Touzain F, Blanchard Y (2015) Complete genome sequence of a porcine epidemic diarrhea s gene indel strain isolated in France in december 2014. Genome Announc 3: e00535-e615

      47. Greig AS, Mitchell D, Corner AH, Bannister GL, Meads EB, Julian RJ (1962) A hemagglutinating virus producing encephalomyelitis in baby pigs. Can J Comp Med Vet Sci 26: 49–56

      48. Halbur PG, Pallarés FJ, Opriessnig T, Vaughn EM, Paul PS (2003) Pathogenicity of three isolates of porcine respiratory coronavirus in the USA. Vet Rec 152: 358–361
          doi: 10.1136/vr.152.12.358

      49. Hammerberg C, Schurig GG, Ochs DL (1989) Immunodeficiency in young pigs. Am J Vet Res 50: 868–874

      50. Hanke D, Jenckel M, Petrov A, Ritzmann M, Stadler J, Akimkin V, Blome S, Pohlmann A, Schirrmeier H, Beer M, Höper D (2015) Comparison of porcine epidemic diarrhea viruses from Germany and the United States, 2014. Emerg Infect Dis 21: 493–496
          doi: 10.3201/eid2103.141165

      51. He WT, Ji X, He W, Dellicour S, Wang S, Li L, Zhang L, Gilbert M, Zhu H, Xing G, Veit M, Huang Z, Han G-Z, Huang Y, Suchard MA, Baele G, Lemey P, Su S (2020) Genomic epidemiology, evolution, and transmission dynamics of porcine deltacoronavirus. Mol Biol Evol 37: 2641–2654
          doi: 10.1093/molbev/msaa117

      52. Herrewegh AA, Smeenk I, Horzinek MC, Rottier PJ, de Groot RJ (1998) Feline coronavirus type Ⅱ strains 79–1683 and 79–1146 originate from a double recombination between feline coronavirus type Ⅰ and canine coronavirus. J Virol 72: 4508–4514
          doi: 10.1128/JVI.72.5.4508-4514.1998

      53. Hirano N, Ono K (1998) A serological survey of human coronavirus in pigs of the Tohoku District of Japan. Adv Exp Med Biol 440: 491–494

      54. Hirano N, Haga S, Fujiwara K (1993) The route of transmission of hemagglutinating encephalomyelitis virus (HEV) 67N strain in 4-week-old rats. Adv Exp Med Biol 342: 333–338

      55. Huang YW, Dickerman AW, Pineyro P, Li L, Fang L, Kiehne R, Opriessnig T, Meng XJ (2013) Origin, evolution, and genotyping of emergent porcine epidemic diarrhea virus strains in the United States. mBio 4: e00737–e1713

      56. Janetanakit T, Lumyai M, Bunpapong N, Boonyapisitsopa S, Chaiyawong S, Nonthabenjawan N, Kesdaengsakonwut S, Amonsin A (2016) Porcine deltacoronavirus, Thailand, 2015. Emerg Infect Dis 22: 757–759
          doi: 10.3201/eid2204.151852

      57. Jung K, Saif LJ (2015) Porcine epidemic diarrhea virus infection: etiology, epidemiology, pathogenesis and immunoprophylaxis. Vet J 204: 134–143
          doi: 10.1016/j.tvjl.2015.02.017

      58. Jung K, Renukaradhya GJ, Alekseev KP, Fang Y, Tang Y, Saif LJ (2009) Porcine reproductive and respiratory syndrome virus modifies innate immunity and alters disease outcome in pigs subsequently infected with porcine respiratory coronavirus: implications for respiratory viral co-infections. J Gen Virol 90: 2713–2723
          doi: 10.1099/vir.0.014001-0

      59. Jung K, Annamalai T, Lu Z, Saif LJ (2015) Comparative pathogenesis of US porcine epidemic diarrhea virus (PEDV) strain PC21A in conventional 9-day-old nursing piglets vs. 26-day-old weaned pigs. Vet Microbiol 178: 31–40
          doi: 10.1016/j.vetmic.2015.04.022

      60. Jung K, Hu H, Saif LJ (2016) Porcine deltacoronavirus infection: Etiology, cell culture for virus isolation and propagation, molecular epidemiology and pathogenesis. Virus Res 226: 50–59
          doi: 10.1016/j.virusres.2016.04.009

      61. Jung K, Miyazaki A, Saif LJ (2018) Immunohistochemical detection of the vomiting-inducing monoamine neurotransmitter serotonin and enterochromaffin cells in the intestines of conventional or gnotobiotic (Gn) pigs infected with porcine epidemic diarrhea virus (PEDV) and serum cytokine responses of Gn pigs to acute PEDV infection. Res Vet Sci 119: 99–108
          doi: 10.1016/j.rvsc.2018.06.009

      62. Killoran KE, Leedom-Larson KR (2016) Porcine respiratory coronavirus. Swine Health Information Center and Center for Food Security and Public Health. http://www.cfsph.iastate.edu/pdf/shic-factsheetporcine-respiratory-coronavirus

      63. Killoran KE, Leedom-Larson KR (2018) Porcine hemagglutinating encephalomyelitis virus. Swine Health Information Center and Center for Food Security and Public Health. http://www.cfsph.iastate.edu/pdf/shic-factsheet-porcine-hemagglutinating-encephalomyelitis-virus

      64. Kocherhans R, Bridgen A, Ackermann M, Tobler K (2001) Completion of the porcine epidemic diarrhoea coronavirus (PEDV) genome sequence. Virus Genes 23: 137–144
          doi: 10.1023/A:1011831902219

      65. Kochhar HS (2014) Canada: porcine epidemic diarrhea in Canada: an emerging disease case study. Can Vet J 5: 1048–1049

      66. Koonpaew S, Teeravechyan S, Frantz PN, Chailangkarn T, Jongkaewwattana A (2019) PEDV and PDCoV pathogenesis: the interplay between host innate immune responses and porcine enteric coronaviruses. Front Vet Sci 6: 34
          doi: 10.3389/fvets.2019.00034

      67. Krempl C, Schultze B, Laude H, Herrler G (1997) Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus. J Virol 71: 3285–3287
          doi: 10.1128/jvi.71.4.3285-3287.1997

      68. Krishna VD, Kim Y, Yang M, Vannucci F, Molitor T, Torremorell M, Cheeran MC-J (2020) Immune responses to porcine epidemic diarrhea virus (PEDV) in swine and protection against subsequent infection. PLoS ONE 15: e0231723
          doi: 10.1371/journal.pone.0231723

      69. Lara-Romero R, Gómez-Núñez L, Cerriteño-Sánchez JL, Márquez-Valdelamar L, Mendoza-Elvira S, Ramírez-Mendoza H, Rivera-Benítez J (2018) Molecular characterization of the spike gene of the porcine epidemic diarrhea virus in Mexico, 2013–2016. Virus Genes 54: 215–224. https://doi.org/10.1007/s11262-017-1528-x
          doi: 10.1007/s11262-017-1528-x

      70. Lee S, Lee C (2014) Complete genome characterization of korean porcine deltacoronavirus strain KOR/KNU14-04/2014. Genome Announc 2: e01191–e1214

      71. Lee DU, Kwon T, Je SH, Yoo SJ, Seo SW, Sunwoo SY, Lyoo YS (2016) Wild boars harboring porcine epidemic diarrhea virus (PEDV) may play an important role as a PEDV reservoir. Vet Microbiol 192: 90–94
          doi: 10.1016/j.vetmic.2016.07.003

      72. Li G, Chen Q, Harmon KM, Yoon KJ, Schwartz KJ, Hoogland MJ, Gauger PC, Main RG, Zhang J (2014) Full-length genome sequence of porcine deltacoronavirus strain USA/IA/2014/8734. Genome Announc 2: e00278–e314

      73. Li W, Hulswit RJG, Kenney SP, Widjaja I, Jung K, Alhamo MA, van Dieren B, van Kuppeveld FJM, Saif LJ, Bosch BJ (2018) Broad receptor engagement of an emerging global coronavirus may potentiate its diverse cross-species transmissibility. Proc Natl Acad Sci USA 115: E5135–E5143
          doi: 10.1073/pnas.1802879115

      74. Li HY, Li BX, Liang QQ, Jin XH, Tang L, Ding QW, Wang ZX, Wei ZY (2020) Porcine deltacoronavirus infection alters bacterial communities in the colon and feces of neonatal piglets. Microbiologyopen 9: e1036

      75. Lin CM, Annamalai T, Liu X, Gao X, Lu Z, El-Tholoth M, Hu H, Saif LJ, Wang Q (2015) Experimental infection of a US spike-insertion deletion porcine epidemic diarrhea virus in conventional nursing piglets and cross-protection to the original US PEDV infection. Vet Res 46: 134
          doi: 10.1186/s13567-015-0278-9

      76. Lin CM, Ghimire S, Hou Y, Langel SN, Vlasova AN, Saif LJ, Wang Q (2019) Pathogenicity and immunogenicity of attenuated porcine epidemic diarrhea virus PC22A strain in conventional weaned pigs. BMC Vet Res 15: 26
          doi: 10.1186/s12917-018-1756-x

      77. Liu C, Tang J, Ma Y, Liang X, Yang Y, Peng G, Qi Q, Jiang S, Li J, Du L (2015) Receptor usage and cell entry of porcine epidemic diarrhea coronavirus. J Virol 89: 6121–6125
          doi: 10.1128/JVI.00430-15

      78. Luo Y, Zhang J, Deng X, Ye Y, Liao M, Fan H (2012) Complete genome sequence of a highly prevalent isolate of porcine epidemic diarrhea virus in South China. J Virol 86: 9551
          doi: 10.1128/JVI.01455-12

      79. Ma Y, Zhang Y, Liang X, Lou F, Oglesbee M, Krakowka S, Li J (2015) Origin, evolution, and virulence of porcine deltacoronaviruses in the United States. MBio 6: e00064

      80. Ma Y, Zhang Y, Liang X, Oglesbee M, Krakowka S, Niehaus A, Wang G, Jia A, Song H, Li J (2016) Two-way antigenic cross-reactivity between porcine epidemic diarrhea virus and porcine deltacoronavirus. Vet Microbiol 186: 90–96
          doi: 10.1016/j.vetmic.2016.02.004

      81. Magtoto R, Poonsuk K, Baum D, Zhang J, Chen Q, Ji J, Piñeyro P, Zimmerman J, Giménez-Lirola LG (2019) Evaluation of the serologic cross-reactivity between transmissible gastroenteritis coronavirus and porcine respiratory coronavirus using commercial blocking enzyme-linked immunosorbent assay kits. mSphere 4: e00017–19

      82. Mandelik R, Sarvas M, Jackova A, Salamunova S, Novotny J, Vilcek S (2018) First outbreak with chimeric swine enteric coronavirus (SeCoV) on pig farms in Slovakia—lessons to learn. Acta Vet Hung 66: 488–492
          doi: 10.1556/004.2018.043

      83. Marthaler D, Raymond L, Jiang Y, Collins J, Rossow K, Rovira A (2014) Rapid detection, complete genome sequencing, and phylogenetic analysis of porcine deltacoronavirus. Emerg Infect Dis 20: 1347–1350

      84. Mayo KA (2017) Emerging swine enteric coronaviruses: comparison of pathogenicity and antibody response. Graduate Theses and Dissertations 16732

      85. Mengeling WL, Cutlip RC (1972) Experimentally induced infection of newborn pigs with hemagglutinating encephalomyelitis virus strain 67N. Am J Vet Res 33: 953–956

      86. Mole B (2013) Deadly pig virus slips through US borders. Nature 499: 388
          doi: 10.1038/499388a

      87. Moon HW, Kemeny LJ, Lambert G, Stark SL, Booth GD (1975) Age-dependent resistance to transmissible gastroenteritis of swine. Ⅲ. Effects of epithelial cell kinetics on coronavirus production and on atrophy of intestinal villi. Vet Pathol 12: 434–445
          doi: 10.1177/0300985875012005-00610

      88. Mora-Díaz JC, Piñeyro PE, Houston E, Zimmerman J, Giménez-Lirola LG (2019) Porcine hemagglutinating encephalomyelitis virus: a review. Front Vet Sci 6: 53
          doi: 10.3389/fvets.2019.00053

      89. Mora-Díaz JC, Magtoto R, Houston E, Baum D, Carrillo-Ávila JA, Temeeyasen G, Zimmerman J, Piñeyro P, Giménez-Lirola L (2020) Detecting and monitoring porcine hemagglutinating encephalomyelitis virus, an underresearched betacoronavirus. mSphere 5: e0019920

      90. Narita M, Kawamura H, Haritani M, Kobayashi M (1989a) Demonstration of viral antigen and immunoglobulin (IgG and IgM) in brain tissue of pigs experimentally infected with haemagglutinating encephalomyelitis virus. J Comp Pathol 100: 119–128
          doi: 10.1016/0021-9975(89)90122-9

      91. Narita M, Kawamura H, Tsuboi T, Haritani M, Kobayashi M (1989b) Immunopathological and ultrastructural studies on the tonsil of gnotobiotic pigs infected with strain 67N of haemagglutinating encephalomyelitis virus. J Comp Pathol 100: 305–312
          doi: 10.1016/0021-9975(89)90108-4

      92. Niederwerder MC, Hesse RA (2018) Swine enteric coronavirus disease: a review of 4 years with porcine epidemic diarrhoea virus and porcine deltacoronavirus in the United States and Canada. Transbound Emerg Dis 65: 660–675
          doi: 10.1111/tbed.12823

      93. Ojkic D, Hazlett M, Fairles J, Marom A, Slavic D, Maxie G, Alexandersen S, Pasick J, Alsop J, Burlatschenko S (2015) The first case of porcine epidemic diarrhea in Canada. Can Vet J 56: 149–152

      94. Ouyang K, Shyu DL, Dhakal S, Hiremath J, Binjawadagi B, Lakshmanappa YS, Guo R, Ransburgh R, Bondra KM, Gauger P, Zhang J, Specht T, Gilbertie A, Minton W, Fang Y, Renukaradhya GJ (2015) Evaluation of humoral immune status in porcine epidemic diarrhea virus (PEDV) infected sows under field conditions. Vet Res 46: 140
          doi: 10.1186/s13567-015-0285-x

      95. Pan Y, Tian X, Qin P, Wang B, Zhao P, Yang YL, Wang L, Wang D, Song Y, Zhang X, Huang YW (2017) Discovery of a novel swine enteric alphacoronavirus (seacov) in southern China. Vet Microbiol 211: 15–21
          doi: 10.1016/j.vetmic.2017.09.020

      96. Pasick J, Berhane Y, Ojkic D, Maxie G, Embury-Hyatt C, Swekla K, Handel K, Fairles J, Alexandersen S (2014) Investigation into the role of potentially contaminated feed as a source of the first-detected outbreaks of porcine epidemic diarrhea in Canada. Transbound Emerg Dis 61: 397–410
          doi: 10.1111/tbed.12269

      97. Paul PS, Mengeling WL (1984) Persistence of passively acquired antibodies to hemagglutinating encephalomyelitis virus in swine. Am J Vet Res 45: 932–934

      98. Pejsak Z (2007) Koronawirusowe zapalenie żołądka i jelit świń, in: Ochrona Zdrowia Świń, Państwowe Wyd. Rolnicze, pp, 223–224

      99. Peng JY, Punyadarsaniya D, Shin DL, Pavasutthipaisit S, Beineke A, Li G, Wu NH, Herrler G (2020) The cell tropism of porcine respiratory coronavirus for airway epithelial cells is determined by the expression of porcine aminopeptidase N. Viruses 23: 1211

      100. Pensaert MB, Callebaut PE (1974) Characteristics of a coronavirus causing vomition and wasting in pigs. Arch Gesamte Virusforsch 44: 35–50
          doi: 10.1007/BF01242179

      101. Pensaert MB, de Bouck P (1978) A new coronavirus-like particle associated with diarrhea in swine. Arch Virol 58: 243–247
          doi: 10.1007/BF01317606

      102. Pensaert MB, de Bouck P, Reynolds DJ (1981) An immunoelectron microscopic and immunofluorescent study on the antigenic relationship between the coronavirus-like agent, CV 777, and several coronaviruses. Arch Virol 68: 45–52
          doi: 10.1007/BF01315166

      103. Pilchard EI (1965) Experimental transmission of transmissible gastroenteritis virus by starlings. Am J Vet Res 26: 1177–1179

      104. Pillatzki A, Gauger P, Madson D, Burrough E, Zhang J, Chen Q, Magstadt D, Arruda P, Stevenson G, Yoon KJ (2015) Experimental inoculation of neonatal piglets with feed naturally contaminated with porcine epidemic diarrhea virus (PEDV). J Swine Health Prod 23: 317–320

      105. Putics A, Gorbalenya AE, Ziebuhr J (2006) Identification of protease and ADP-ribose 1''-monophosphatase activities associated with transmissible gastroenteritis virus non-structural protein 3. J Gen Virol 87: 651–656
          doi: 10.1099/vir.0.81596-0

      106. Qian S, Jia X, Gao Z, Zhang W, Xu Q, Li Z (2020) Isolation and identification of porcine deltacoronavirus and alteration of immunoglobulin transport receptors in the intestinal mucosa of PDCoV-infected piglets. Viruses 12: 79
          doi: 10.3390/v12010079

      107. Raihana RR, Hayakawa M, Sugiura E, Sugiura H, Hanaki K, Taniguchi T, Honda E (2009) Analysis of the properties of neutralizing monoclonal antibodies against the hemagglutinating encephalomyelitis virus and inhibition of HEV infection by specific MAb. J Vet Med Sci 71: 447–452
          doi: 10.1292/jvms.71.447

      108. Roe CK, Alexander TJA (1958) Disease of nursing pigs previously unreported in Ontario. Can J Comp Med Vet Sci 22: 305–307

      109. Saif LJ (1993) Coronavirus immunogens. Vet Microbiol 37: 285–297
          doi: 10.1016/0378-1135(93)90030-B

      110. Saif LJ, Sestak K (2006) Transmissible gastroenteritis virus and porcine respiratory coronavirus. In: Straw BE (ed) Diseases of swine, 9th edn. Blackwell Publishing, Ames, pp 489–516

      111. Saif LJ, Pensaert MB, Sestak K, Yeo S, Jung K (2012) Coronaviruses. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW (eds) Diseases of swine, 10th edn. Wiley, Ames, pp 501–524

      112. Sestak K, Lanza I, Park SK, Weilnau PA, Saif LJ (1996) Contribution of passive immunity to porcine respiratory coronavirus to protection against transmissible gastroenteritis virus challenge exposure in suckling pigs. Am J Vet Res 57: 664–671

      113. Shi J, Wen Z, Zhong G, Yang H, Wang C, Liu R, He X, Shuai L, Sun Z, Zhao Y, Liang L, Cui P, Wang J, Zhang X, Guan Y, Chen H, Bu Z (2020) Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS–coronavirus 2. BioRxiv: 2020.03.30.015347

      114. Song D, Park B (2012) Porcine epidemic diarrhoea virus: a comprehensive review of molecular epidemiology, diagnosis, and vaccines. Virus Genes 44: 167–175
          doi: 10.1007/s11262-012-0713-1

      115. Song D, Moon H, Kang B (2015) Porcine epidemic diarrhea: a review of current epidemiology and available vaccines. Clin Exp Vac Res 4: 166–176
          doi: 10.7774/cevr.2015.4.2.166

      116. Steinrigl A, Fernández SR, Stoiber F, Pikalo J, Sattler T, Schmoll F (2015) First detection, clinical presentation and phylogenetic characterization of Porcine epidemic diarrhea virus in Austria. BMC Vet Res 11: 310
          doi: 10.1186/s12917-015-0624-1

      117. Stevenson GW, Hoang H, Schwartz KJ, Burrough ER, Sun D, Madson D, Cooper VL, Pillatzki A, Gauger P, Schmitt BJ, Koster LG, Killian ML, Yoon KJ (2013) Emergence of porcine epidemic diarrhea virus in the United States: clinical signs, lesions, and viral genomic sequences. J Vet Diagn Invest 25: 649–654
          doi: 10.1177/1040638713501675

      118. Tan L, Li Y, He J, Hu Y, Cai X, Liu W, Liu T, Wang J, Li Z, Yuan X, Zhan Y, Yang L, Deng Z, Wang N, Yang Y, Wang A (2020) Epidemic and genetic characterization of porcine epidemic diarrhea virus strains circulating in the regions around Hunan, China, during 2017–2018. Arch Virol 165: 877–889
          doi: 10.1007/s00705-020-04532-7

      119. Tang XC, Zhang JX, Zhang SY, Wang P, Fan XH, Li LF, Li G, Dong BQ, Liu W, Cheung CL, Xu KM, Song WJ, Vijaykrishna D, Poon LL, Peiris JS, Smith GJ, Chen H, Guan Y (2006) Prevalence and genetic diversity of coronaviruses in bats from China. J Virol 80: 7481–7490
          doi: 10.1128/JVI.00697-06

      120. Teeravechyan S, Frantz PN, Wongthida P, Chailangkarn T, Jaru-Ampornpan P, Koonpaew S, Jongkaewwattana A (2016) Deciphering the biology of porcine epidemic diarrhea virus in the era of reverse genetics. Virus Res 226: 152–217
          doi: 10.1016/j.virusres.2016.05.003

      121. Theuns S, Conceição-Neto N, Christiaens I, Zeller M, Desmarets LM, Roukaerts ID, Acar DD, Heylen E, Matthijnssens J, Nauwynck HJ (2015) Complete genome sequence of a porcine epidemic diarrhea virus from a novel outbreak in Belgium, January 2015. Genome Announc 3: pii: e00506–15

      122. USDA (2017) Swine Enteric Coronavirus Disease (SECD) Situation Report. https://www.aphis.usda.gov/animal_health/animal_dis_spec/swine/downloads/secd_sit_rep_11_30_17.pdf. Animal and Plant Health Inspection Service

      123. Valkó A, Bálint Á, Bozsa Á, Cságola A (2019) Prevalence of antibodies against transmissible gastroenteritis virus (TGEV) in Hungary. Vet Anim Sci 7: 100042
          doi: 10.1016/j.vas.2018.11.003

      124. Van Deun K, Cox E, Cellebaut P, Pensaert MB (1990) Milk of sows infected with the porcine respiratory coronavirus: induction of IgA antibodies against transmissible gastroenteritis virus and protective capacity against intestinal infection in piglets. In: 11th Congres of the international pig veterinary society at: Lausanne

      125. Van Gucht S, Atanasova K, Barbé F, Cox E, Pensaert M, Van Reeth K (2006) Effect of porcine respiratory coronavirus infection on lipopolysaccharide recognition proteins and haptoglobin levels in the lungs. Microbes Infect 8: 1492–1501
          doi: 10.1016/j.micinf.2006.01.009

      126. Van Nieuwstadt AP, Zetstra T, Boonstra J (1989) Infection with porcine respiratory coronavirus does not fully protect pigs against intestinal transmissible gastroenteritis virus. Vet Rec 125: 58–60
          doi: 10.1136/vr.125.3.58

      127. Vannier P (1990) Disorders induced by the experimental infection of pigs with the porcine respiratory coronavirus (P.R.C.V.). Zentralbl Veterinarmed B 37: 177–180

      128. Vlasova AN, Marthaler D, Wang Q, Culhane MR, Rossow K, Rovira A, Collins J, Saif LJ (2014) Distinct characteristics and complex Evolution of PEDV strains, North America, May 2013–February 2014. Emerg Infect Dis 20: 1620–1628

      129. Vlasova AN, Saif LJ (2013) Biological aspects of the interspecies transmission of selected coronaviruses. In: Singh SK (ed) Viral infections and global change. Wiley, pp 393–418

      130. Wang L, Byrum B, Zhang Y (2014a) Detection and genetic characterization of deltacoronavirus in pigs, Ohio, USA, 2014. Emerg Infect Dis 20: 1227–1230

      131. Wang L, Byrum B, Zhang Y (2014b) Porcine coronavirus HKU15 detected in 9 US states, 2014. Emerg Infect Dis 20: 1594–1595
          doi: 10.3201/eid2009.140756

      132. Wang L, Byrum B, Zhang Y (2014c) New variant of porcine epidemic diarrhea virus, United States, 2014. Emerg Infect Dis 20: 917–919
          doi: 10.3201/eid2005.140195

      133. Wang L, Hu W, Fan C (2020) Structural and biochemical characterization of SADS-CoV papain-like protease 2. Protein Sci 29: 1228–1241
          doi: 10.1002/pro.3857

      134. Wang Q, Vlasova AN, Kenney SP, Saif LJ (2019) Emerging and re-emerging coronaviruses in pigs. Curr Opin Virol 34: 39–49
          doi: 10.1016/j.coviro.2018.12.001

      135. Wang YW, Yue H, Fang W, Huang YW (2015) Complete genome sequence of porcine deltacoronavirus strain CH/Sichuan/S27/2012 from Mainland China. Genome Announc 3: e00945–e1015

      136. Weingartl HM, Copps J, Drebot MA, Marszal P, Smith G, Gren J, Andonova M, Pasick J, Kitching P, Czub M (2004) Susceptibility of pigs and chickens to SARS coronavirus. Emerg Infect Dis 10: 179–184
          doi: 10.3201/eid1002.030677

      137. Wesley R (2002) Neutralizing antibody decay and lack of contact transmission after inoculation of 3- and 4-day-old piglets with porcine respiratory coronavirus. J Vet Diagn Invest 14: 525–527
          doi: 10.1177/104063870201400617

      138. Wesley RD, Woods RD (1996) Induction of protective immunity against transmissible gastroenteritis virus after exposure of neonatal pigs to porcine respiratory coronavirus. Am J Vet Res 57: 157–162

      139. Woo PC, Lau SK, Lam CS, Lau CC, Tsang AK, Lau JH, Bai R, Teng JL, Tsang CC, Wang M, Zheng BJ, Chan KH, Yuen KY (2012) Discovery of seven novel Mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus. J Virol 86: 3995–4008
          doi: 10.1128/JVI.06540-11

      140. Woo PC, Lau SK, Yip CC, Tsoi H, Chan K, Yuen K (2006) Comparative analysis of 22 coronavirus HKU1 genomes reveals a novel genotype and evidence of natural recombination in coronavirus HKU1. J Virol 80: 7136–7145
          doi: 10.1128/JVI.00509-06

      141. Wood EN (1977) An apparently new syndrome of porcine epidemic diarrhoea. Vet Rec 100: 243–244
          doi: 10.1136/vr.100.12.243

      142. Xu Z, Zhang Y, Gong L, Huang L, Lin Y, Qin J, Du Y, Zhou Q, Xue C, Cao Y (2019) Isolation and characterization of a highly pathogenic strain of Porcine enteric alphacoronavirus causing watery diarrhoea and high mortality in newborn piglets. Transbound Emerg Dis 66: 119–130
          doi: 10.1111/tbed.12992

      143. Yang YL, Qin P, Wang B, Liu Y, Xu GH, Peng L, Zhou J, Zhu SJ, Huang YW (2019) Broad cross-species infection of cultured cells by bat HKU2-related swine acute diarrhea syndrome coronavirus and identification of its replication in murine dendritic cells in vivo highlight its potential for diverse interspecies transmission. J Virol 93: e01448–e1519

      144. Yount B, Curtis KM, Baric RS (2000) Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. J Virol 74: 10600–10611
          doi: 10.1128/JVI.74.22.10600-10611.2000

      145. Zhang H, Liang Q, Li B, Cui X, Wei X, DING Q, Wang Y, Hu H, (2019) Prevalence, phylogenetic and evolutionary analysis of porcine deltacoronavirus in Henan province, China. Prev Vet Med 166: 8–15
          doi: 10.1016/j.prevetmed.2019.02.017

      146. Zhang M, Li W, Zhou P, Liu D, Luo R, Jongkaewwattana A, He Q (2019) Genetic manipulation of porcine deltacoronavirus reveals insights into NS6 and NS7 functions: a novel strategy for vaccine design. Emerg Microbes Infect 9: 20–31

      147. Zhang J, Han Y, Shi H, Chen J, Zhang X, Wang X, Zhou L, Liu J, Zhang J, Ji Z, Jing Z, Ma J, Shi D, Feng L (2020) Swine acute diarrhea syndrome coronavirus-induced apoptosis is caspase- and cyclophilin D-dependent. Emerg Microbes Infect 9: 439–456
          doi: 10.1080/22221751.2020.1722758

      148. Zhang Y, Han L, Xia L, Yuan Y, Hu H (2020) Assessment of hemagglutination activity of porcine deltacoronavirus. J Vet Sci 21: e12
          doi: 10.4142/jvs.2020.21.e12

      149. Zhou P, Fan H, Lan T, Yang XL, Shi WF, Zhang W, Zhu Y, Zhang YW, Xie QM, Mani S, Zheng XS, Li B, Li JM, Guo H, Pei GQ, An XP, Chen JW, Zhou L, Mai KJ, Wu ZX, Li D, Anderson DE, Zhang LB, Li SY, Mi ZQ, He TT, Cong F, Guo PJ, Huang R, Luo Y, Liu XL, Chen J, Huang Y, Sun Q, Zhang XLL, Wang YY, Xing SZ, Chen YS Sun Y, Li J, Daszak P, Wang LF, Shi ZL, Tong YG, Ma JY (2018) Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature 556: 255–258
          doi: 10.1038/s41586-018-0010-9

      150. Zhou L, Li QN, Su JN, Chen GH, Wu ZX, Luo Y, Wu RT, Sun Y, Lan T, Ma JY (2019a) The re-emerging of SADS-CoV infection in pig herds in Southern China. Transbound Emerg Dis 66: 2180–2183
          doi: 10.1111/tbed.13270

      151. Zhou L, Sun Y, Lan T, Wu R, Chen J, Wu Z, Xie Q, Zhang X, Ma J (2019b) Retrospective detection and phylogenetic analysis of swine acute diarrhoea syndrome coronavirus in pigs in southern China. Transbound Emerg Dis 66: 687–695
          doi: 10.1111/tbed.13008

      152. Zhao D, Gao X, Zhou P, Zhang L, Zhang Y, Wang Y, Liu X (2020) Evaluation of the immune response in conventionally weaned pigs infected with porcine deltacoronavirus. Arch Virol 12: 1–6
          doi: 10.1007/s00705-020-04590-x?utm_campaign=BSLB_AWA_SK01_GL_TrendMD2021&utm_content=null&utm_medium=cpc

      153. Zhou Z, Sun Y, Yan X, Tang X, Li Q, Tan Y, Lan T, Ma J (2020) Swine acute diarrhea syndrome coronavirus (SADS-CoV) antagonizes interferon- production via blocking IPS-1 and RIG-I. Virus Res 278: 197843
          doi: 10.1016/j.virusres.2019.197843

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      Porcine Coronaviruses: Overview of the State of the Art

        Corresponding author: Małgorzata Pomorska-Mól, mpomorska@up.poznan.pl
      • 1. Department of Preclinical Sciences and Infectious Diseases, Faculty of Veterinary Medicine and Animal Sciences, Poznan University of Life Sciences, ul. Wołyńska 35, 60-637 Poznan, Poland
      • Received Date: 26 May 2020
      • Accepted Date: 19 November 2020
      • Published Date: 15 March 2021

      Abstract: 

      Like RNA viruses in general, coronaviruses (CoV) exhibit high mutation rates which, in combination with their strong tendency to recombine, enable them to overcome the host species barrier and adapt to new hosts. It is currently known that six CoV are able to infect pigs. Four of them belong to the genus Alphacoronavirus [transmissible gastroenteritis coronavirus (TEGV), porcine respiratory coronavirus (PRCV), porcine epidemic diarrhea virus (PEDV), swine acute diarrhea syndrome coronavirus (SADS-CoV)], one of them to the genus Betacoronavirus [porcine hemagglutinating encephalomyelitis virus (PHEV)] and the last one to the genus Deltacoronavirus (PDCoV). PHEV was one of the first identified swine CoV and is still widespread, causing subclinical infections in pigs in several countries. PRCV, a spike deletion mutant of TGEV associated with respiratory tract infection, appeared in the 1980s. PRCV is considered non-pathogenic since its infection course is mild or subclinical. Since its appearance, pig populations have become immune to both PRCV and TGEV, leading to a significant reduction in the clinical and economic importance of TGEV. TGEV, PEDV and PDCoV are enteropathogenic CoV and cause clinically indistinguishable acute gastroenteritis in all age groups of pigs. PDCoV and SADS-CoV have emerged in 2014 (US) and in 2017 (China), respectively. Rapid diagnosis is crucial for controlling CoV infections and preventing them from spreading. Since vaccines are available only for some porcine CoV, prevention should focus mainly on a high level of biosecurity. In view of the diversity of CoV and the potential risk factors associated with zoonotic emergence, updating the knowledge concerning this area is essential.

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