Skip to main content
SpringerLink
Log in

Emergence of SARS and COVID-19 and preparedness for the next emerging disease X

  • Review
  • Published:
Frontiers of Medicine Aims and scope Submit manuscript

Abstract

Severe acute respiratory syndrome (SARS) and Coronavirus disease 2019 (COVID-19) are two human Coronavirus diseases emerging in this century, posing tremendous threats to public health and causing great loss to lives and economy. In this review, we retrospect the studies tracing the molecular evolution of SARS-CoV, and we sort out current research findings about the potential ancestor of SARS-CoV-2. Updated knowledge about SARS-CoV-2-like viruses found in wildlife, the animal susceptibility to SARS-CoV-2, as well as the interspecies transmission risk of SARS-related coronaviruses (SARSr-CoVs) are gathered here. Finally, we discuss the strategies of how to be prepared against future outbreaks of emerging or re-emerging coronaviruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Murray KA, Preston N, Allen T, Zambrana-Torrelio C, Hosseini PR, Daszak P. Global biogeography of human infectious diseases. Proc Natl Acad Sci USA 2015; 112(41): 12746–12751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Loh EH, Zambrana-Torrelio C, Olival KJ, Bogich TL, Johnson CK, Mazet JA, Karesh W, Daszak P. Targeting transmission pathways for emerging zoonotic disease surveillance and control. Vector Borne Zoonotic Dis 2015; 15(7): 432–437

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kreuder Johnson C, Hitchens PL, Smiley Evans T, Goldstein T, Thomas K, Clements A, Joly DO, Wolfe ND, Daszak P, Karesh WB, Mazet JK. Spillover and pandemic properties of zoonotic viruses with high host plasticity. Sci Rep 2015; 5(1): 14830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Woolhouse ME, Brierley L, McCaffery C, Lycett S. Assessing the epidemic potential of RNA and DNA viruses. Emerg Infect Dis 2016; 22(12): 2037–2044

    Article  PubMed  PubMed Central  Google Scholar 

  5. Adjemian J, Farnon EC, Tschioko F, Wamala JF, Byaruhanga E, Bwire GS, Kansiime E, Kagirita A, Ahimbisibwe S, Katunguka F, Jeffs B, Lutwama JJ, Downing R, Tappero JW, Formenty P, Amman B, Manning C, Towner J, Nichol ST, Rollin PE. Outbreak of Marburg hemorrhagic fever among miners in Kamwenge and Ibanda Districts, Uganda, 2007. J Infect Dis 2011; 204(Suppl 3): S796–S799

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kuzmin IV, Niezgoda M, Franka R, Agwanda B, Markotter W, Breiman RF, Shieh WJ, Zaki SR, Rupprecht CE. Marburg virus in fruit bat, Kenya. Emerg Infect Dis 2010; 16(2): 352–354

    Article  PubMed  PubMed Central  Google Scholar 

  7. Islam MS, Sazzad HM, Satter SM, Sultana S, Hossain MJ, Hasan M, Rahman M, Campbell S, Cannon DL, Ströher U, Daszak P, Luby SP, Gurley ES. Nipah virus transmission from bats to humans associated with drinking traditional liquor made from Date Palm Sap, Bangladesh, 2011–2014. Emerg Infect Dis 2016; 22(4): 664–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Zhong NS, Zheng BJ, Li YM, Poon LLM, Xie ZH, Chan KH, Li PH, Tan SY, Chang Q, Xie JP, Liu XQ, Xu J, Li DX, Yuen KY, Peiris JSM, Guan Y. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People’s Republic of China, in February, 2003. Lancet 2003; 362(9393): 1353–1358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 2012; 367(19): 1814–1820

    Article  CAS  PubMed  Google Scholar 

  10. Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, Si HR, Zhu Y, Li B, Huang CL, Chen HD, Chen J, Luo Y, Guo H, Jiang RD, Liu MQ, Chen Y, Shen XR, Wang X, Zheng XS, Zhao K, Chen QJ, Deng F, Liu LL, Yan B, Zhan FX, Wang YY, Xiao GF, Shi ZL. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020; 579(7798): 270–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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 GF, Tan W; China Novel Coronavirus Investigating and Research Team. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med 2020; 382(8): 727–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ren LL, Wang YM, Wu ZQ, Xiang ZC, Guo L, Xu T, Jiang YZ, Xiong Y, Li YJ, Li XW, Li H, Fan GH, Gu XY, Xiao Y, Gao H, Xu JY, Yang F, Wang XM, Wu C, Chen L, Liu YW, Liu B, Yang J, Wang XR, Dong J, Li L, Huang CL, Zhao JP, Hu Y, Cheng ZS, Liu LL, Qian ZH, Qin C, Jin Q, Cao B, Wang JW. Identification of a novel coronavirus causing severe pneumonia in human: a descriptive study. Chin Med J (Engl) 2020; 133(9): 1015–1024

    Article  CAS  PubMed  Google Scholar 

  13. Peiris JS, Guan Y, Yuen KY. Severe acute respiratory syndrome. Nat Med 2004; 10(12 Suppl): S88–S97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Pike J, Bogich T, Elwood S, Finnoff DC, Daszak P. Economic optimization of a global strategy to address the pandemic threat. Proc Natl Acad Sci USA 2014; 111(52): 18519–18523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, Cheung CL, Luo SW, Li PH, Zhang LJ, Guan YJ, Butt KM, Wong KL, Chan KW, Lim W, Shortridge KF, Yuen KY, Peiris JS, Poon LL. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 2003; 302(5643): 276–278

    Article  CAS  PubMed  Google Scholar 

  16. Song HD, Tu CC, Zhang GW, Wang SY, Zheng K, Lei LC, Chen QX, Gao YW, Zhou HQ, Xiang H, Zheng HJ, Chern SW, Cheng F, Pan CM, Xuan H, Chen SJ, Luo HM, Zhou DH, Liu YF, He JF, Qin PZ, Li LH, Ren YQ, Liang WJ, Yu YD, Anderson L, Wang M, Xu RH, Wu XW, Zheng HY, Chen JD, Liang G, Gao Y, Liao M, Fang L, Jiang LY, Li H, Chen F, Di B, He LJ, Lin JY, Tong S, Kong X, Du L, Hao P, Tang H, Bernini A, Yu XJ, Spiga O, Guo ZM, Pan HY, He WZ, Manuguerra JC, Fontanet A, Danchin A, Niccolai N, Li YX, Wu CI, Zhao GP. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci USA 2005; 102(7): 2430–2435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chinese SARS Molecular Epidemiology Consortium. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 2004; 303(5664): 1666–1669

    Article  Google Scholar 

  18. Ge XY, Li JL, Yang XL, Chmura AA, Zhu G, Epstein JH, Mazet JK, Hu B, Zhang W, Peng C, Zhang YJ, Luo CM, Tan B, Wang N, Zhu Y, Crameri G, Zhang SY, Wang LF, Daszak P, Shi ZL. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 2013; 503(7477): 535–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hu B, Zeng LP, Yang XL, Ge XY, Zhang W, Li B, Xie JZ, Shen XR, Zhang YZ, Wang N, Luo DS, Zheng XS, Wang MN, Daszak P, Wang LF, Cui J, Shi ZL. Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathog 2017; 13(11): e1006698

    Article  PubMed  PubMed Central  Google Scholar 

  20. Drexler JF, Gloza-Rausch F, Glende J, Corman VM, Muth D, Goettsche M, Seebens A, Niedrig M, Pfefferle S, Yordanov S, Zhelyazkov L, Hermanns U, Vallo P, Lukashev A, Müller MA, Deng H, Herrler G, Drosten C. Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. J Virol 2010; 84(21): 11336–11349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Tao Y, Tong S. Complete genome sequence of a severe acute respiratory syndrome-related coronavirus from Kenyan bats. Microbiol Resour Announc 2019; 8(28): e00548–e19

    Article  PubMed  PubMed Central  Google Scholar 

  22. Cui J, Li F, Shi ZL. Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol 2019; 17(3): 181–192

    Article  CAS  PubMed  Google Scholar 

  23. Wang N, Li SY, Yang XL, Huang HM, Zhang YJ, Guo H, Luo CM, Miller M, Zhu G, Chmura AA, Hagan E, Zhou JH, Zhang YZ, Wang LF, Daszak P, Shi ZL. Serological evidence of bat SARS-related coronavirus infection in humans, China. Virol Sin 2018; 33(1): 104–107

    Article  PubMed  PubMed Central  Google Scholar 

  24. Guo H, Hu BJ, Yang XL, Zeng LP, Li B, Ouyang S, Shi ZL. Evolutionary arms race between virus and host drives genetic diversity in bat severe acute respiratory syndrome-related coronavirus spike genes. J Virol 2020; 94(20): e00902–e00920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, Cheng Z, Yu T, Xia J, Wei Y, Wu W, Xie X, Yin W, Li H, Liu M, Xiao Y, Gao H, Guo L, Xie J, Wang G, Jiang R, Gao Z, Jin Q, Wang J, Cao B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395(10223): 497–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Wu F, Zhao S, Yu B, Chen YM, Wang W, Song ZG, Hu Y, Tao ZW, Tian JH, Pei YY, Yuan ML, Zhang YL, Dai FH, Liu Y, Wang QM, Zheng JJ, Xu L, Holmes EC, Zhang YZ. A new coronavirus associated with human respiratory disease in China. Nature 2020; 579(7798): 265–269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Coronaviridae Study Group of the International Committee on Taxonomy of Viruses. The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol 2020; 5(4): 536–544

    Article  Google Scholar 

  28. Holmes EC, Goldstein SA, Rasmussen AL, Robertson DL, Crits-Christoph A, Wertheim JO, Anthony SJ, Barclay WS, Boni MF, Doherty PC, Farrar J, Geoghegan JL, Jiang X, Leibowitz JL, Neil SJD, Skern T, Weiss SR, Worobey M, Andersen KG, Garry RF, Rambaut A. The origins of SARS-CoV-2: a critical review. Cell 2021; 184(19): 4848–4856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. World Health Organization. WHO-Convened Global Study of Origins of SARS-CoV-2: China Part, Joint Report. 2021. Available at the website of WHO

  30. Zhang X, Tan Y, Ling Y, Lu G, Liu F, Yi Z, Jia X, Wu M, Shi B, Xu S, Chen J, Wang W, Chen B, Jiang L, Yu S, Lu J, Wang J, Xu M, Yuan Z, Zhang Q, Zhang X, Zhao G, Wang S, Chen S, Lu H. Viral and host factors related to the clinical outcome of COVID-19. Nature 2020; 583(7816): 437–440

    Article  CAS  PubMed  Google Scholar 

  31. Temmam S, Vongphayloth K, Baquero E, Munier S, Bonomi M, Regnault B, Douangboubpha B, Karami Y, Chrétien D, Sanamxay D, Xayaphet V, Paphaphanh P, Lacoste V, Somlor S, Lakeomany K, Phommavanh N, Pérot P, Dehan O, Amara F, Donati F, Bigot T, Nilges M, Rey FA, van der Werf S, Brey PT, Eloit M. Bat coronaviruses related to SARS-CoV-2 and infectious for human cells. Nature 2022; 604(7905): 330–336

    Article  CAS  PubMed  Google Scholar 

  32. Lam TT, Jia N, Zhang YW, Shum MH, Jiang JF, Zhu HC, Tong YG, Shi YX, Ni XB, Liao YS, Li WJ, Jiang BG, Wei W, Yuan TT, Zheng K, Cui XM, Li J, Pei GQ, Qiang X, Cheung WY, Li LF, Sun FF, Qin S, Huang JC, Leung GM, Holmes EC, Hu YL, Guan Y, Cao WC. Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins. Nature 2020; 583(7815): 282–285

    Article  CAS  PubMed  Google Scholar 

  33. Liu WJ, Liu P, Lei W, Jia Z, He X, Shi W, Tan Y, Zou S, Wong G, Wang J, Wang F, Wang G, Qin K, Gao R, Zhang J, Li M, Xiao W, Guo Y, Xu Z, Zhao Y, Song J, Zhang J, Zhen W, Zhou W, Ye B, Song J, Yang M, Zhou W, Dai Y, Lu G, Bi Y, Tan W, Han J, Gao GF, Wu G. Surveillance of SARS-CoV-2 at the Huanan Seafood Market. Nature 2023; [Epub ahead of print] doi:https://doi.org/10.1038/s41586-023-06043-2

  34. Rambaut A, Holmes EC, O’Toole Á, Hill V, McCrone JT, Ruis C, du Plessis L, Pybus OG. A dynamic nomenclature proposal for SARS-CoV-2 lineages to assist genomic epidemiology. Nat Microbiol 2020; 5(11): 1403–1407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Chi Y, Wang Q, Chen G, Zheng S. The long-term presence of SARS-CoV-2 on cold-chain food packaging surfaces indicates a new COVID-19 winter outbreak: a mini review. Front Public Health 2021; 9: 650493

    Article  PubMed  PubMed Central  Google Scholar 

  36. Feng XL, Li B, Lin HF, Zheng HY, Tian RR, Luo RH, Liu MQ, Jiang RD, Zheng YT, Shi ZL, Bi YH, Yang XL. Stability of SARS-CoV-2 on the surfaces of three meats in the setting that simulates the cold chain transportation. Virol Sin 2021; 36(5): 1069–1072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Pang X, Ren L, Wu S, Ma W, Yang J, Di L, Li J, Xiao Y, Kang L, Du S, Du J, Wang J, Li G, Zhai S, Chen L, Zhou W, Lai S, Gao L, Pan Y, Wang Q, Li M, Wang J, Huang Y, Wang J; COVID-19 Field Response Group; COVID-19 Laboratory Testing Group. Cold-chain food contamination as the possible origin of COVID-19 resurgence in Beijing. Natl Sci Rev 2020; 7(12): 1861–1864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Zhao X, Mao L, Zhang J, Zhang Y, Song Y, Bo Z, Wang H, Wang J, Chen C, Xiao J, Ji T, Yang Q, Xu W, Wang D, Yao W. Reemergent cases of COVID-19—Dalian City, Liaoning Province, China, July 22, 2020. China CDC Wkly 2020; 2(34): 658–660

    Article  PubMed  PubMed Central  Google Scholar 

  39. Yuan Q, Kou Z, Jiang F, Li Z, Zhang L, Liu H, Zhao X, Kang D, Gao R, Lei J. A nosocomial COVID-19 outbreak initiated by an infected dockworker at Qingdao City Port—Shandong Province, China, October, 2020. China CDC Wkly 2020; 2(43): 838–840

    Article  PubMed  PubMed Central  Google Scholar 

  40. Liu P, Yang M, Zhao X, Guo Y, Wang L, Zhang J, Lei W, Han W, Jiang F, Liu WJ, Gao GF, Wu G. Cold-chain transportation in the frozen food industry may have caused a recurrence of COVID-19 cases in destination: successful isolation of SARS-CoV-2 virus from the imported frozen cod package surface. Biosafety Health 2020; 2(4): 199–201

    Article  PubMed  Google Scholar 

  41. Bai L, Wang Y, Wang Y, Wu Y, Li N, Liu Z. Controlling COVID-19 transmission due to contaminated imported frozen food and food packaging. China CDC Wkly 2021; 3(2): 30–33

    Article  PubMed  PubMed Central  Google Scholar 

  42. Chavarria-Miró G, Anfruns-Estrada E, Guix S, Paraira M, Galofré B, Sánchez G, Pintó RM, Bosch A. Sentinel surveillance of SARS-CoV-2 in wastewater anticipates the occurrence of COVID-19 cases. medRxiv 2020: 2020.06.13.20129627

  43. Fongaro G, Hermes Stoco P, Marques Souza DS, Grisard EC, Magri ME, Rogovski P, André Schörner M, Barazzetti FH, Christoff AP, de Oliveira LFV, Bazzo ML, Wagner G, Hernández M, Rodriguez-Lázaro D. SARS-CoV-2 in human sewage in Santa Catalina, Brazil, November 2019. medRxiv 2020: 2020.06.26.20140731

  44. Giovanetti M, Benvenuto D, Angeletti S, Ciccozzi M. The first two cases of 2019-nCoV in Italy: where they come from? J Med Virol 2020; 92(5): 518–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Apolone G, Montomoli E, Manenti A, Boeri M, Sabia F, Hyseni I, Mazzini L, Martinuzzi D, Cantone L, Milanese G, Sestini S, Suatoni P, Marchianò A, Bollati V, Sozzi G, Pastorino U. Unexpected detection of SARS-CoV-2 antibodies in the prepandemic period in Italy. Tumori 2021; 107(5): 446–451

    Article  CAS  PubMed  Google Scholar 

  46. Carrat F, Figoni J, Henny J, Desenclos JC, Kab S, de Lamballerie X, Zins M. Evidence of early circulation of SARS-CoV-2 in France: findings from the population-based “CONSTANCES” cohort. Eur J Epidemiol 2021; 36(2): 219–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ruan Y, Wen H, Hou M, He Z, Lu X, Xue Y, He X, Zhang YP, Wu CI. The twin-beginnings of COVID-19 in Asia and Europeone prevails quickly. Natl Sci Rev 2022; 9(4): nwab223

    Article  PubMed  Google Scholar 

  48. Bai Y, Jiang D, Lon JR, Chen X, Hu M, Lin S, Chen Z, Wang X, Meng Y, Du H. Comprehensive evolution and molecular characteristics of a large number of SARS-CoV-2 genomes reveal its epidemic trends. Int J Infect Dis 2020; 100: 164–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lu J, du Plessis L, Liu Z, Hill V, Kang M, Lin H, Sun J, François S, Kraemer MUG, Faria NR, McCrone JT, Peng J, Xiong Q, Yuan R, Zeng L, Zhou P, Liang C, Yi L, Liu J, Xiao J, Hu J, Liu T, Ma W, Li W, Su J, Zheng H, Peng B, Fang S, Su W, Li K, Sun R, Bai R, Tang X, Liang M, Quick J, Song T, Rambaut A, Loman N, Raghwani J, Pybus OG, Ke C. Genomic epidemiology of SARS-CoV-2 in Guangdong Province, China. Cell 2020; 181(5): 997–1003.e9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Duchene S, Featherstone L, Haritopoulou-Sinanidou M, Rambaut A, Lemey P, Baele G. Temporal signal and the phylodynamic threshold of SARS-CoV-2. Virus Evol 2020; 6(2): veaa061

    Article  PubMed  PubMed Central  Google Scholar 

  51. Wu CI, Wen H, Lu J, Su XD, Hughes AC, Zhai W, Chen C, Chen H, Li M, Song S, Qian Z, Wang Q, Chen B, Guo Z, Ruan Y, Lu X, Wei F, Jin L, Kang L, Xue Y, Zhao G, Zhang YP. On the origin of SARS-CoV-2—the blind watchmaker argument. Sci China Life Sci 2021; 64(9): 1560–1563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ruan Y, Wen H, He X, Wu CI. A theoretical exploration of the origin and early evolution of a pandemic. Sci Bull (Beijing) 2021; 66(10): 1022–1029

    Article  PubMed  Google Scholar 

  53. Sit THC, Brackman CJ, Ip SM, Tam KWS, Law PYT, To EMW, Yu VYT, Sims LD, Tsang DNC, Chu DKW, Perera RAPM, Poon LLM, Peiris M. Infection of dogs with SARS-CoV-2. Nature 2020; 586(7831): 776–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Goumenou M, Spandidos DA, Tsatsakis A. Possibility of transmission through dogs being a contributing factor to the extreme COVID-19 outbreak in North Italy. Mol Med Rep 2020; 21(6): 2293–2295

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Patterson EI, Elia G, Grassi A, Giordano A, Desario C, Medardo M, Smith SL, Anderson ER, Prince T, Patterson GT, Lorusso E, Lucente MS, Lanave G, Lauzi S, Bonfanti U, Stranieri A, Martella V, Solari Basano F, Barrs VR, Radford AD, Agrimi U, Hughes GL, Paltrinieri S, Decaro N. Evidence of exposure to SARS-CoV-2 in cats and dogs from households in Italy. Nat Commun 2020; 11(1): 6231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hamer SA, Pauvolid-Corrêa A, Zecca IB, Davila E, Auckland LD, Roundy CM, Tang W, Torchetti MK, Killian ML, Jenkins-Moore M, Mozingo K, Akpalu Y, Ghai RR, Spengler JR, Barton Behravesh C, Fischer RSB, Hamer GL. SARS-CoV-2 infections and viral isolations among serially tested cats and dogs in households with infected owners in Texas, USA. Viruses 2021; 13(5): 938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Sailleau C, Dumarest M, Vanhomwegen J, Delaplace M, Caro V, Kwasiborski A, Hourdel V, Chevaillier P, Barbarino A, Comtet L, Pourquier P, Klonjkowski B, Manuguerra JC, Zientara S, Le Poder S. First detection and genome sequencing of SARS-CoV-2 in an infected cat in France. Transbound Emerg Dis 2020; 67(6): 2324–2328

    Article  CAS  PubMed  Google Scholar 

  58. Garigliany M, Van Laere AS, 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(12): 3069–3071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Barrs VR, Peiris M, Tam KWS, Law PYT, Brackman CJ, To EMW, Yu VYT, Chu DKW, Perera RAPM, Sit THC. SARS-CoV-2 in quarantined domestic cats from COVID-19 households or close contacts, Hong Kong, China. Emerg Infect Dis 2020; 26(12): 3071–3074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Newman A, Smith D, Ghai RR, Wallace RM, Torchetti MK, Loiacono C, Murrell LS, Carpenter A, Moroff S, Rooney JA, Barton Behravesh C. First reported cases of SARS-CoV-2 infection in companion animals—New York, March–April 2020. MMWR Morb Mortal Wkly Rep 2020; 69(23): 710–713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Ruiz-Arrondo I, Portillo A, Palomar AM, Santibáñez S, Santibáñez P, Cervera C, Oteo JA. 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. Transbound Emerg Dis 2021; 68(2): 973–976

    Article  CAS  PubMed  Google Scholar 

  62. Segalés J, Puig M, Rodon J, Avila-Nieto C, Carrillo J, Cantero G, Terrón MT, 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. Detection of SARS-CoV-2 in a cat owned by a COVID-19-affected patient in Spain. Proc Natl Acad Sci USA 2020; 117(40): 24790–24793

    Article  PubMed  PubMed Central  Google Scholar 

  63. Hosie MJ, Epifano I, Herder V, Orton RJ, Stevenson A, Johnson N, MacDonald E, Dunbar D, McDonald M, Howie F, Tennant B, Herrity D, Da Silva Filipe A, Streicker DG; COVID-19 Genomics UK (COG-UK) consortium; Willett BJ, Murcia PR, Jarrett RF, Robertson DL, Weir W. Detection of SARS-CoV-2 in respiratory samples from cats in the UK associated with human-to-cat transmission. Vet Rec 2021; 188(8): e247

    Article  PubMed  PubMed Central  Google Scholar 

  64. 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 ZL, Jin M. A serological survey of SARS-CoV-2 in cat in Wuhan. Emerg Microbes Infect 2020; 9(1): 2013–2019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Bartlett SL, Diel DG, Wang L, Zec S, Laverack M, Martins M, Caserta LC, Killian ML, Terio K, Olmstead C, Delaney MA, Stokol T, Ivančić M, Jenkins-Moore M, Ingerman K, Teegan T, McCann C, Thomas P, McAloose D, Sykes JM, Calle PP. 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. J Zoo Wildl Med 2021; 51(4): 733–744

    Article  PubMed  Google Scholar 

  66. McAloose D, Laverack M, Wang L, Killian ML, Caserta LC, Yuan F, Mitchell PK, Queen K, Mauldin MR, Cronk BD, Bartlett SL, Sykes JM, Zec S, Stokol T, Ingerman K, Delaney MA, Fredrickson R, Ivančić M, Jenkins-Moore M, Mozingo K, Franzen K, Bergeson NH, Goodman L, Wang H, Fang Y, Olmstead C, McCann C, Thomas P, Goodrich E, Elvinger F, Smith DC, Tong S, Slavinski S, Calle PP, Terio K, Torchetti MK, Diel DG. From people to Panthera: natural SARS-CoV-2 infection in tigers and lions at the Bronx Zoo. MBio 2020; 11(5): e02220–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Gibbons A. Captive gorillas test positive for coronavirus. 2021. Available at the website of Science

  68. de Morais HA, Dos Santos AP, do Nascimento NC, Kmetiuk LB, Barbosa DS, Brandão PE, Guimarães AMS, Pettan-Brewer C, Biondo AW. Natural infection by SARS-CoV-2 in companion animals: a review of case reports and current evidence of their role in the epidemiology of COVID-19. Front Vet Sci 2020; 7(823): 591216

    Article  PubMed  PubMed Central  Google Scholar 

  69. European Food Safety Authority and European Centre for Disease Prevention and Control; Boklund A, Gortázar C, Pasquali P, Roberts H, Nielsen SS, Stahl K, Stegeman A, Baldinelli F, Broglia A, Van Der Stede Y, Adlhoch C, Alm E, Melidou A, Mirinaviciute G. Monitoring of SARS-CoV-2 infection in mustelids. EFSA J 2021; 19(3): e06459

    Article  PubMed Central  Google Scholar 

  70. Oude Munnink BB, Sikkema RS, Nieuwenhuijse DF, Molenaar RJ, 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 MCA, Bouwstra RJ, GeurtsvanKessel C, van der Eijk AA, Velkers FC, Smit LAM, Stegeman A, van der Poel WHM, Koopmans MPG. Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans. Science 2021; 371(6525): 172–177

    Article  CAS  PubMed  Google Scholar 

  71. Oreshkova N, Molenaar RJ, Vreman S, Harders F, Oude Munnink BB, Hakze-van der Honing RW, Gerhards N, Tolsma P, Bouwstra R, Sikkema RS, Tacken MG, de Rooij MM, Weesendorp E, Engelsma MY, Bruschke CJ, Smit LA, Koopmans M, van der Poel WH, Stegeman A. SARS-CoV-2 infection in farmed minks, the Netherlands, April and May 2020. Euro Surveill 2020; 25(23): 2001005

    Article  PubMed  PubMed Central  Google Scholar 

  72. Shriner SA, Ellis JW, Root JJ, Roug A, Stopak SR, Wiscomb GW, Zierenberg JR, Ip HS, Torchetti MK, DeLiberto TJ. SARS-CoV-2 exposure in escaped mink, Utah, USA. Emerg Infect Dis 2021; 27(3): 988–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Aguiló-Gisbert J, Padilla-Blanco M, Lizana V, Maiques E, Muñoz-Baquero M, Chillida-Martínez E, Cardells J, Rubio-Guerri C. First description of SARS-CoV-2 infection in two feral American mink (Neovison vison) caught in the wild. Animals (Basel) 2021; 11(5): 1422

    Article  PubMed  Google Scholar 

  74. 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, Bu Z. Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2. Science 2020; 368(6494): 1016–1020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Rockx B, Kuiken T, Herfst S, Bestebroer T, Lamers MM, Oude Munnink BB, de Meulder D, van Amerongen G, van den Brand J, Okba NMA, Schipper D, van Run P, Leijten L, Sikkema R, Verschoor E, Verstrepen B, Bogers W, Langermans J, Drosten C, Fentener van Vlissingen M, Fouchier R, de Swart R, Koopmans M, Haagmans BL. Comparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model. Science 2020; 368(6494): 1012–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lu S, Zhao Y, Yu W, Yang Y, Gao J, Wang J, Kuang D, Yang M, Yang J, Ma C, Xu J, Qian X, Li H, Zhao S, Li J, Wang H, Long H, Zhou J, Luo F, Ding K, Wu D, Zhang Y, Dong Y, Liu Y, Zheng Y, Lin X, Jiao L, Zheng H, Dai Q, Sun Q, Hu Y, Ke C, Liu H, Peng X. Comparison of nonhuman primates identified the suitable model for COVID-19. Signal Transduct Target Ther 2020; 5(1): 157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Kim YI, Kim SG, Kim SM, Kim EH, Park SJ, Yu KM, Chang JH, Kim EJ, Lee S, Casel MAB, Um J, Song MS, Jeong HW, Lai VD, Kim Y, Chin BS, Park JS, Chung KH, Foo SS, Poo H, Mo IP, Lee OJ, Webby RJ, Jung JU, Choi YK. Infection and rapid transmission of SARS-CoV-2 in ferrets. Cell Host Microbe 2020; 27(5): 704–709.e2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Sun SH, Chen Q, Gu HJ, Yang G, Wang YX, Huang XY, Liu SS, Zhang NN, Li XF, Xiong R, Guo Y, Deng YQ, Huang WJ, Liu Q, Liu QM, Shen YL, Zhou Y, Yang X, Zhao TY, Fan CF, Zhou YS, Qin CF, Wang YC. A mouse model of SARS-CoV-2 infection and pathogenesis. Cell Host Microbe 2020; 28(1): 124–133.e4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Jiang RD, Liu MQ, Chen Y, Shan C, Zhou YW, Shen XR, Li Q, Zhang L, Zhu Y, Si HR, Wang Q, Min J, Wang X, Zhang W, Li B, Zhang HJ, Baric RS, Zhou P, Yang XL, Shi ZL. Pathogenesis of SARS-CoV-2 in transgenic mice expressing human angiotensin-converting enzyme 2. Cell 2020; 182(1): 50–58.e8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Bao L, Deng W, Huang B, Gao H, Liu J, Ren L, Wei Q, Yu P, Xu Y, Qi F, Qu Y, Li F, Lv Q, Wang W, Xue J, Gong S, Liu M, Wang G, Wang S, Song Z, Zhao L, Liu P, Zhao L, Ye F, Wang H, Zhou W, Zhu N, Zhen W, Yu H, Zhang X, Guo L, Chen L, Wang C, Wang Y, Wang X, Xiao Y, Sun Q, Liu H, Zhu F, Ma C, Yan L, Yang M, Han J, Xu W, Tan W, Peng X, Jin Q, Wu G, Qin C. The pathogenicity of SARS-CoV-2 in hACE2 transgenic mice. Nature 2020; 583(7818): 830–833

    Article  CAS  PubMed  Google Scholar 

  81. Speranza E, Williamson BN, Feldmann F, Sturdevant GL, Pérez-Pérez L, Meade-White K, Smith BJ, Lovaglio J, Martens C, Munster VJ, Okumura A, Shaia C, Feldmann H, Best SM, de Wit E. Single-cell RNA sequencing reveals SARS-CoV-2 infection dynamics in lungs of African green monkeys. Sci Transl Med 2021; 13(578): eabe8146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Chandrashekar A, Liu J, Martinot AJ, McMahan K, Mercado NB, Peter L, Tostanoski LH, Yu J, Maliga Z, Nekorchuk M, Busman-Sahay K, Terry M, Wrijil LM, Ducat S, Martinez DR, Atyeo C, Fischinger S, Burke JS, Slein MD, Pessaint L, Van Ry A, Greenhouse J, Taylor T, Blade K, Cook A, Finneyfrock B, Brown R, Teow E, Velasco J, Zahn R, Wegmann F, Abbink P, Bondzie EA, Dagotto G, Gebre MS, He X, Jacob-Dolan C, Kordana N, Li Z, Lifton MA, Mahrokhian SH, Maxfield LF, Nityanandam R, Nkolola JP, Schmidt AG, Miller AD, Baric RS, Alter G, Sorger PK, Estes JD, Andersen H, Lewis MG, Barouch DH. SARS-CoV-2 infection protects against rechallenge in rhesus macaques. Science 2020; 369(6505): 812–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Richard M, Kok A, de Meulder D, Bestebroer TM, Lamers MM, Okba NMA, Fentener van Vlissingen M, Rockx B, Haagmans BL, Koopmans MPG, Fouchier RAM, Herfst S. SARS-CoV-2 is transmitted via contact and via the air between ferrets. Nat Commun 2020; 11(1): 3496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Munster VJ, Feldmann F, Williamson BN, van Doremalen N, Pérez-Pérez L, Schulz J, Meade-White K, Okumura A, Callison J, Brumbaugh B, Avanzato VA, Rosenke R, Hanley PW, Saturday G, Scott D, Fischer ER, de Wit E. Respiratory disease in rhesus macaques inoculated with SARS-CoV-2. Nature 2020; 585(7824): 268–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Gu H, Chen Q, Yang G, He L, Fan H, Deng YQ, Wang Y, Teng Y, Zhao Z, Cui Y, Li Y, Li XF, Li J, Zhang NN, Yang X, Chen S, Guo Y, Zhao G, Wang X, Luo DY, Wang H, Yang X, Li Y, Han G, He Y, Zhou X, Geng S, Sheng X, Jiang S, Sun S, Qin CF, Zhou Y. Adaptation of SARS-CoV-2 in BALB/c mice for testing vaccine efficacy. Science 2020; 369(6511): 1603–1607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Montagutelli X, Prot M, Levillayer L, Salazar EB, Jouvion G, Conquet L, Beretta M, Donati F, Albert M, Gambaro F, Behillil S, Enouf V, Rousset D, Mouquet H, Jaubert J, Rey F, van der Werf S, Simon-Loriere E. Variants with the N501Y mutation extend SARS-CoV-2 host range to mice, with contact transmission. BioRxiv 2021; 2021.03.18.436013

  87. Shuai H, Chan JF, Yuen TT, Yoon C, Hu JC, Wen L, Hu B, Yang D, Wang Y, Hou Y, Huang X, Chai Y, Chan CC, Poon VK, Lu L, Zhang RQ, Chan WM, Ip JD, Chu AW, Hu YF, Cai JP, Chan KH, Zhou J, Sridhar S, Zhang BZ, Yuan S, Zhang AJ, Huang JD, To KK, Yuen KY, Chu H. Emerging SARS-CoV-2 variants expand species tropism to murines. EBioMedicine 2021; 73: 103643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Sia SF, Yan LM, Chin AWH, Fung K, Choy KT, Wong AYL, Kaewpreedee P, Perera RAPM, Poon LLM, Nicholls JM, Peiris M, Yen HL. Pathogenesis and transmission of SARS-CoV-2 in golden hamsters. Nature 2020; 583(7818): 834–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Hou YJ, Chiba S, Halfmann P, Ehre C, Kuroda M, Dinnon KH3rd, Leist SR, Schäfer A, Nakajima N, Takahashi K, Lee RE, Mascenik TM, Graham R, Edwards CE, Tse LV, Okuda K, Markmann AJ, Bartelt L, de Silva A, Margolis DM, Boucher RC, Randell SH, Suzuki T, Gralinski LE, Kawaoka Y, Baric RS. SARS-CoV-2 D614G variant exhibits efficient replication ex vivo and transmission in vivo. Science 2020; 370(6523): 1464–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Tostanoski LH, Wegmann F, Martinot AJ, Loos C, McMahan K, Mercado NB, Yu J, Chan CN, Bondoc S, Starke CE, Nekorchuk M, Busman-Sahay K, Piedra-Mora C, Wrijil LM, Ducat S, Custers J, Atyeo C, Fischinger S, Burke JS, Feldman J, Hauser BM, Caradonna TM, Bondzie EA, Dagotto G, Gebre MS, Jacob-Dolan C, Lin Z, Mahrokhian SH, Nampanya F, Nityanandam R, Pessaint L, Porto M, Ali V, Benetiene D, Tevi K, Andersen H, Lewis MG, Schmidt AG, Lauffenburger DA, Alter G, Estes JD, Schuitemaker H, Zahn R, Barouch DH. Ad26 vaccine protects against SARS-CoV-2 severe clinical disease in hamsters. Nat Med 2020; 26(11): 1694–1700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Baum A, Ajithdoss D, Copin R, Zhou A, Lanza K, Negron N, Ni M, Wei Y, Mohammadi K, Musser B, Atwal GS, Oyejide A, Goez-Gazi Y, Dutton J, Clemmons E, Staples HM, Bartley C, Klaffke B, Alfson K, Gazi M, Gonzalez O, Dick E Jr, Carrion R Jr, Pessaint L, Porto M, Cook A, Brown R, Ali V, Greenhouse J, Taylor T, Andersen H, Lewis MG, Stahl N, Murphy AJ, Yancopoulos GD, Kyratsous CA. REGN-COV2 antibodies prevent and treat SARS-CoV-2 infection in rhesus macaques and hamsters. Science 2020; 370(6520): 1110–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Halfmann PJ, Hatta M, Chiba S, Maemura T, Fan S, Takeda M, Kinoshita N, Hattori SI, Sakai-Tagawa Y, Iwatsuki-Horimoto K, Imai M, Kawaoka Y. Transmission of SARS-CoV-2 in domestic cats. N Engl J Med 2020; 383(6): 592–594

    Article  PubMed  PubMed Central  Google Scholar 

  93. Wu L, Chen Q, Liu K, Wang J, Han P, Zhang Y, Hu Y, Meng Y, Pan X, Qiao C, Tian S, Du P, Song H, Shi W, Qi J, Wang HW, Yan J, Gao GF, Wang Q. Broad host range of SARS-CoV-2 and the molecular basis for SARS-CoV-2 binding to cat ACE2. Cell Discov 2020; 6(1): 68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Conceicao C, Thakur N, Human S, Kelly JT, Logan L, Bialy D, Bhat S, Stevenson-Leggett P, Zagrajek AK, Hollinghurst P, Varga M, Tsirigoti C, Tully M, Chiu C, Moffat K, Silesian AP, Hammond JA, Maier HJ, Bickerton E, Shelton H, Dietrich I, Graham SC, Bailey D. The SARS-CoV-2 Spike protein has a broad tropism for mammalian ACE2 proteins. PLoS Biol 2020; 18(12): e3001016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Suarez DL, Pantin-Jackwood MJ, Swayne DE, Lee SA, DeBlois SM, Spackman E. Lack of susceptibility to SARS-CoV-2 and MERS-CoV in poultry. Emerg Infect Dis 2020; 26(12): 3074–3076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Zhao X, Chen D, Szabla R, Zheng M, Li G, Du P, Zheng S, Li X, Song C, Li R, Guo JT, Junop M, Zeng H, Lin H. Broad and differential animal angiotensin-converting enzyme 2 receptor usage by SARS-CoV-2. J Virol 2020; 94(18): e00940–20

    Article  PubMed  PubMed Central  Google Scholar 

  97. Xu L, Yu DD, Ma YH, Yao YL, Luo RH, Feng XL, Cai HR, Han JB, Wang XH, Li MH, Ke CW, Zheng YT, Yao YG. COVID-19-like symptoms observed in Chinese tree shrews infected with SARS-CoV-2. Zool Res 2020; 41(5): 517–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Zhao Y, Wang J, Kuang D, Xu J, Yang M, Ma C, Zhao S, Li J, Long H, Ding K, Gao J, Liu J, Wang H, Li H, Yang Y, Yu W, Yang J, Zheng Y, Wu D, Lu S, Liu H, Peng X. Susceptibility of tree shrew to SARS-CoV-2 infection. Sci Rep 2020; 10(1): 16007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Starr TN, Zepeda SK, Walls AC, Greaney AJ, Alkhovsky S, Veesler D, Bloom JD. ACE2 binding is an ancestral and evolvable trait of sarbecoviruses. Nature 2022; 603(7903): 913–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Zhou H, Chen X, Hu T, Li J, Song H, Liu Y, Wang P, Liu D, Yang J, Holmes EC, Hughes AC, Bi Y, Shi W. A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1/S2 cleavage site of the spike protein. Curr Biol 2020; 30(11): 2196–2203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Zhou H, Ji J, Chen X, Bi Y, Li J, Wang Q, Hu T, Song H, Zhao R, Chen Y, Cui M, Zhang Y, Hughes AC, Holmes EC, Shi W. Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses. Cell 2021; 184(17): 4380–4391.e14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Wacharapluesadee S, Tan CW, Maneeorn P, Duengkae P, Zhu F, Joyjinda Y, Kaewpom T, Chia WN, Ampoot W, Lim BL, Worachotsueptrakun K, Chen VC, Sirichan N, Ruchisrisarod C, Rodpan A, Noradechanon K, Phaichana T, Jantarat N, Thongnumchaima B, Tu C, Crameri G, Stokes MM, Hemachudha T, Wang LF. Evidence for SARS-CoV-2 related coronaviruses circulating in bats and pangolins in Southeast Asia. Nat Commun 2021; 12(1): 972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Guo H, Hu B, Si HR, Zhu Y, Zhang W, Li B, Li A, Geng R, Lin HF, Yang XL, Zhou P, Shi ZL. Identification of a novel lineage bat SARS-related coronaviruses that use bat ACE2 receptor. Emerg Microbes Infect 2021; 10(1): 1507–1514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Delaune D, Hul V, Karlsson EA, Hassanin A, Ou TP, Baidaliuk A, Gámbaro F, Prot M, Tu VT, Chea S, Keatts L, Mazet J, Johnson CK, Buchy P, Dussart P, Goldstein T, Simon-Lorière E, Duong V. A novel SARS-CoV-2 related coronavirus in bats from Cambodia. Nat Commun 2021; 12(1): 6563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Ou X, Xu G, Li P, Liu Y, Zan F, Liu P, Hu J, Lu X, Dong S, Zhou Y, Mu Z, Wu Z, Wang J, Jin Q, Liu P, Lu J, Wang X, Qian Z. Host susceptibility and structural and immunological insight of S proteins of two SARS-CoV-2 closely related bat coronaviruses. Cell Discov 2023; 9(1): 78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Deng S, Xing K, He X. Mutation signatures inform the natural host of SARS-CoV-2. Natl Sci Rev 2022; 9(2): nwab220

    Article  CAS  PubMed  Google Scholar 

  107. Xiao K, Zhai J, Feng Y, Zhou N, Zhang X, Zou JJ, Li N, Guo Y, Li X, Shen X, Zhang Z, Shu F, Huang W, Li Y, Zhang Z, Chen RA, Wu YJ, Peng SM, Huang M, Xie WJ, Cai QH, Hou FH, Chen W, Xiao L, Shen Y. Isolation of SARS-CoV-2-related coronavirus from Malayan pangolins. Nature 2020; 583(7815): 286–289

    Article  CAS  PubMed  Google Scholar 

  108. Liu P, Jiang JZ, Wan XF, Hua Y, Li L, Zhou J, Wang X, Hou F, Chen J, Zou J, Chen J. Are pangolins the intermediate host of the 2019 novel coronavirus (SARS-CoV-2)? PLoS Pathog 2020; 16(5): e1008421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. He WT, Hou X, Zhao J, Sun J, He H, Si W, Wang J, Jiang Z, Yan Z, Xing G, Lu M, Suchard MA, Ji X, Gong W, He B, Li J, Lemey P, Guo D, Tu C, Holmes EC, Shi M, Su S. Total virome characterizations of game animals in China reveals a spectrum of emerging viral pathogens. Cell 2022; 185(7): 1117–1129.e8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Letko M, Marzi A, Munster V. Functional assessment of cell entry and receptor usage for SARS-CoV-2 and other lineage B betacoronaviruses. Nat Microbiol 2020; 5(4): 562–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Starr TN, Greaney AJ, Hilton SK, Ellis D, Crawford KHD, Dingens AS, Navarro MJ, Bowen JE, Tortorici MA, Walls AC, King NP, Veesler D, Bloom JD. Deep mutational scanning of SARS-CoV-2 receptor binding domain reveals constraints on folding and ACE2 binding. Cell 2020; 182(5): 1295–1310.e20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Niu S, Wang J, Bai B, Wu L, Zheng A, Chen Q, Du P, Han P, Zhang Y, Jia Y, Qiao C, Qi J, Tian WX, Wang HW, Wang Q, Gao GF. Molecular basis of cross-species ACE2 interactions with SARS-CoV-2-like viruses of pangolin origin. EMBO J 2021; 40(16): e107786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Liu K, Pan X, Li L, Yu F, Zheng A, Du P, Han P, Meng Y, Zhang Y, Wu L, Chen Q, Song C, Jia Y, Niu S, Lu D, Qiao C, Chen Z, Ma D, Ma X, Tan S, Zhao X, Qi J, Gao GF, Wang Q. Binding and molecular basis of the bat coronavirus RaTG13 virus to ACE2 in humans and other species. Cell 2021; 184(13): 3438–3451.e10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Mou H, Quinlan BD, Peng H, Liu G, Guo Y, Peng S, Zhang L, Davis-Gardner ME, Gardner MR, Crynen G, DeVaux LB, Voo ZX, Bailey CC, Alpert MD, Rader C, Gack MU, Choe H, Farzan M. Mutations derived from horseshoe bat ACE2 orthologs enhance ACE2-Fc neutralization of SARS-CoV-2. PLoS Pathog 2021; 17(4): e1009501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Liu MQ, Lin HF, Li J, Chen Y, Luo Y, Zhang W, Hu B, Tian FJ, Hu YJ, Liu YJ, Jiang RD, Gong QC, Li A, Guo ZS, Li B, Yang XL, Tong YG, Shi ZLA. A SARS-CoV-2-related virus from Malayan pangolin causes lung infection without severe disease in human ACE2-transgenic mice. J Virol 2023; 97(2): e0171922

    Article  PubMed  Google Scholar 

  116. Luo CM, Wang N, Yang XL, Liu HZ, Zhang W, Li B, Hu B, Peng C, Geng QB, Zhu GJ, Li F, Shi ZL. Discovery of novel bat coronaviruses in South China that use the same receptor as middle east respiratory syndrome coronavirus. J Virol 2018; 92(13): e00116–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Chen J, Yang X, Si H, Gong Q, Que T, Li J, Li Y, Wu C, Zhang W, Chen Y, Luo Y, Zhu Y, Li B, Luo D, Hu B, Lin H, Jiang R, Jiang T, Li Q, Liu M, Xie S, Su J, Zheng X, Li A, Yao Y, Yang Y, Chen P, Wu A, He M, Lin X, Tong Y, Hu Y, Shi ZL, Zhou P. A bat MERS-like coronavirus circulates in pangolins and utilizes human DPP4 and host proteases for cell entry. Cell 2023; 186(4): 850–863.e16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Jeworowski LM, Mühlemann B, Walper F, Schmidt ML, Jansen J, Krumbholz A, Simon-Lorière E, Jones TC, Corman VM, Drosten C. Humoral immune escape by current SARS-CoV-2 variants BA.2.86 and JN.1, December 2023. Euro Surveill 2024; 29(2): 2300740

    Article  PubMed  PubMed Central  Google Scholar 

  119. Rubin R. As COVID-19 cases surge, here’s what to know about JN.1, the latest SARS-CoV-2 “Variant of Interest”. JAMA 2024; 331(5): 382–383

    Article  PubMed  Google Scholar 

  120. Markov PV, Ghafari M, Beer M, Lythgoe K, Simmonds P, Stilianakis NI, Katzourakis A. The evolution of SARS-CoV-2. Nat Rev Microbiol 2023; 21(6): 361–379

    Article  CAS  PubMed  Google Scholar 

  121. Carabelli AM, Peacock TP, Thorne LG, Harvey WT, Hughes J; COVID-19 Genomics UK Consortium; Peacock SJ, Barclay WS, de Silva TI, Towers GJ, Robertson DL. SARS-CoV-2 variant biology: immune escape, transmission and fitness. Nat Rev Microbiol 2023; 21(3): 162–177

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Wang MN, Zhang W, Gao YT, Hu B, Ge XY, Yang XL, Zhang YZ, Shi ZL. Longitudinal surveillance of SARS-like coronaviruses in bats by quantitative real-time PCR. Virol Sin 2016; 31(1): 78–80

    Article  PubMed  PubMed Central  Google Scholar 

  123. Zhang W, Du RH, Li B, Zheng XS, Yang XL, Hu B, Wang YY, Xiao GF, Yan B, Shi ZL, Zhou P. Molecular and serological investigation of 2019-nCoV infected patients: implication of multiple shedding routes. Emerg Microbes Infect 2020; 9(1): 386–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Nathan A, Rossin EJ, Kaseke C, Park RJ, Khatri A, Koundakjian D, Urbach JM, Singh NK, Bashirova A, Tano-Menka R, Senjobe F, Waring MT, Piechocka-Trocha A, Garcia-Beltran WF, Iafrate AJ, Naranbhai V, Carrington M, Walker BD, Gaiha GD. Structure-guided T cell vaccine design for SARS-CoV-2 variants and sarbecoviruses. Cell 2021; 184(17): 4401–4413.e10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Martinez DR, Schäfer A, Leist SR, De la Cruz G, West A, Atochina-Vasserman EN, Lindesmith LC, Pardi N, Parks R, Barr M, Li D, Yount B, Saunders KO, Weissman D, Haynes BF, Montgomery SA, Baric RS. Chimeric spike mRNA vaccines protect against Sarbecovirus challenge in mice. Science 2021; 373(6558): 991–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Ma C, Su S, Wang J, Wei L, Du L, Jiang S. From SARS-CoV to SARS-CoV-2: safety and broad-spectrum are important for coronavirus vaccine development. Microbes Infect 2020; 22(6–7): 245–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Liu Z, Xu W, Chen Z, Fu W, Zhan W, Gao Y, Zhou J, Zhou Y, Wu J, Wang Q, Zhang X, Hao A, Wu W, Zhang Q, Li Y, Fan K, Chen R, Jiang Q, Mayer CT, Schoofs T, Xie Y, Jiang S, Wen Y, Yuan Z, Wang K, Lu L, Sun L, Wang Q. An ultrapotent pan-β-coronavirus lineage B (β-CoV-B) neutralizing antibody locks the receptor-binding domain in closed conformation by targeting its conserved epitope. Protein Cell 2022; 13(9): 655–675

    Article  CAS  PubMed  Google Scholar 

  128. Wec AZ, Wrapp D, Herbert AS, Maurer DP, Haslwanter D, Sakharkar M, Jangra RK, Dieterle ME, Lilov A, Huang D, Tse LV, Johnson NV, Hsieh CL, Wang N, Nett JH, Champney E, Burnina I, Brown M, Lin S, Sinclair M, Johnson C, Pudi S, Bortz R 3rd, Wirchnianski AS, Laudermilch E, Florez C, Fels JM, O’Brien CM, Graham BS, Nemazee D, Burton DR, Baric RS, Voss JE, Chandran K, Dye JM, McLellan JS, Walker LM. Broad neutralization of SARS-related viruses by human monoclonal antibodies. Science 2020; 369(6504): 731–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Rappazzo CG, Tse LV, Kaku CI, Wrapp D, Sakharkar M, Huang D, Deveau LM, Yockachonis TJ, Herbert AS, Battles MB, O’Brien CM, Brown ME, Geoghegan JC, Belk J, Peng L, Yang L, Hou Y, Scobey TD, Burton DR, Nemazee D, Dye JM, Voss JE, Gunn BM, McLellan JS, Baric RS, Gralinski LE, Walker LM. Broad and potent activity against SARS-like viruses by an engineered human monoclonal antibody. Science 2021; 371(6531): 823–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Tortorici MA, Czudnochowski N, Starr TN, Marzi R, Walls AC, Zatta F, Bowen JE, Jaconi S, Di Iulio J, Wang Z, De Marco A, Zepeda SK, Pinto D, Liu Z, Beltramello M, Bartha I, Housley MP, Lempp FA, Rosen LE, Dellota E Jr, Kaiser H, Montiel-Ruiz M, Zhou J, Addetia A, Guarino B, Culap K, Sprugasci N, Saliba C, Vetti E, Giacchetto-Sasselli I, Fregni CS, Abdelnabi R, Foo SC, Havenar-Daughton C, Schmid MA, Benigni F, Cameroni E, Neyts J, Telenti A, Virgin HW, Whelan SPJ, Snell G, Bloom JD, Corti D, Veesler D, Pizzuto MS. Broad sarbecovirus neutralization by a human monoclonal antibody. Nature 2021; 597(7874): 103–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Walls AC, Miranda MC, Schäfer A, Pham MN, Greaney A, Arunachalam PS, Navarro MJ, Tortorici MA, Rogers K, O’Connor MA, Shirreff L, Ferrell DE, Bowen J, Brunette N, Kepl E, Zepeda SK, Starr T, Hsieh CL, Fiala B, Wrenn S, Pettie D, Sydeman C, Sprouse KR, Johnson M, Blackstone A, Ravichandran R, Ogohara C, Carter L, Tilles SW, Rappuoli R, Leist SR, Martinez DR, Clark M, Tisch R, O’Hagan DT, Van Der Most R, Van Voorhis WC, Corti D, McLellan JS, Kleanthous H, Sheahan TP, Smith KD, Fuller DH, Villinger F, Bloom J, Pulendran B, Baric RS, King NP, Veesler D. Elicitation of broadly protective sarbecovirus immunity by receptor-binding domain nanoparticle vaccines. Cell 2021; 184(21): 5432–5447.e16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Tan CW, Chia WN, Young BE, Zhu F, Lim BL, Sia WR, Thein TL, Chen MI, Leo YS, Lye DC, Wang LF. Pan-sarbecovirus neutralizing antibodies in BNT162b2-immunized SARS-CoV-1 survivors. N Engl J Med 2021; 385(15): 1401–1406

    Article  CAS  PubMed  Google Scholar 

  133. Lu L, Su S, Yang H, Jiang S. Antivirals with common targets against highly pathogenic viruses. Cell 2021; 184(6): 1604–1620

    Article  CAS  PubMed  Google Scholar 

  134. Li X, Zhang L, Chen S, Ouyang H, Ren L. Possible targets of pan-coronavirus antiviral strategies for emerging or re-emerging coronaviruses. Microorganisms 2021; 9(7): 1479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Couzin-Frankel J. Antiviral pills could change pandemic’s course. Science 2021; 374(6569): 799–800

    Article  CAS  PubMed  Google Scholar 

  136. Malone B, Campbell EA. Molnupiravir: coding for catastrophe. Nat Struct Mol Biol 2021; 28(9): 706–708

    Article  CAS  PubMed  Google Scholar 

  137. Mahase E. Covid-19: Pfizer’s paxlovid is 89% effective in patients at risk of serious illness, company reports. BMJ 2021; 375(2713): n2713

    Article  PubMed  Google Scholar 

  138. Cao B, Wang Y, Lu H, Huang C, Yang Y, Shang L, Chen Z, Jiang R, Liu Y, Lin L, Peng P, Wang F, Gong F, Hu H, Cheng C, Yao X, Ye X, Zhou H, Shen Y, Liu C, Wang C, Yi Z, Hu B, Xu J, Gu X, Shen J, Xu Y, Zhang L, Fan J, Tang R, Wang C. Oral simnotrelvir for adult patients with mild-to-moderate Covid-19. N Engl J Med 2024; 390(3): 230–241

    Article  CAS  PubMed  Google Scholar 

  139. Wang X, Xia S, Zhu Y, Lu L, Jiang S. Pan-coronavirus fusion inhibitors as the hope for today and tomorrow. Protein Cell 2021; 12(2): 84–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Xia S, Liu M, Wang C, Xu W, Lan Q, Feng S, Qi F, Bao L, Du L, Liu S, Qin C, Sun F, Shi Z, Zhu Y, Jiang S, Lu L. Inhibition of SARS-CoV-2 (previously 2019-nCoV) infection by a highly potent pan-coronavirus fusion inhibitor targeting its spike protein that harbors a high capacity to mediate membrane fusion. Cell Res 2020; 30(4): 343–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Lu J. One Health: an effective strategy to tackle new challenges in human health. One Health Bull 2021; 1(1): 2

    Article  Google Scholar 

Download references

Acknowledgements

This work is jointly supported by the National Key Research and Development Program of China (Nos. 2022YFC2305101 and 2021YFC0863400), and the Strategic Research and Consulting Program of Chinese Academy of Engineering (No. 2022-JB-06-04).

Author information

Author notes

  1. These authors contributed equally.

Authors and Affiliations

  1. CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, 430071, China

    Ben Hu, Hua Guo, Haorui Si & Zhengli Shi

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Haorui Si

Authors
  1. Ben Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hua Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haorui Si
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhengli Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhengli Shi.

Ethics declarations

Conflicts of interest Ben Hu, Hua Guo, Haorui Si, and Zhengli Shi declare that they have no conflict of interest.

This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, B., Guo, H., Si, H. et al. Emergence of SARS and COVID-19 and preparedness for the next emerging disease X. Front. Med. 18, 1–18 (2024). https://doi.org/10.1007/s11684-024-1066-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11684-024-1066-6

Keywords

Search

Navigation