1932

Abstract

Severe acute respiratory syndrome (SARS) emerged from China as an untreatable and rapidly spreading respiratory illness of unknown etiology. Following point source exposure in February 2003, more than a dozen guests infected at a Hong Kong hotel seeded multi-country outbreaks that persisted through the spring of 2003. The World Health Organization responded by invoking traditional public health measures and advanced technologies to control the illness and contain the cause. A novel coronavirus was implicated and its entire genome was sequenced by mid-April 2003. The urgency of responding to this threat focused scientific endeavor and stimulated global collaboration. Through real-time application of accumulating knowledge, the world proved capable of arresting the first pandemic threat of the twenty-first century, despite early respiratory-borne spread and global susceptibility. This review synthesizes lessons learned from this remarkable achievement. These lessons can be applied to re-emergence of SARS or to the next pandemic threat to arise.

Loading

Article metrics loading...

/content/journals/10.1146/annurev.med.56.091103.134135
2005-02-18
2024-10-05
Loading full text...

Full text loading...

/deliver/fulltext/me/56/1/annurev.med.56.091103.134135.html?itemId=/content/journals/10.1146/annurev.med.56.091103.134135&mimeType=html&fmt=ahah

Literature Cited

  1. World Health Organization 2003. Consensus document on the epidemiology of severe acute respiratory syndrome (SARS). Rep. WHO/CDS/CSR/GAR/2003.11
  2. World Health Organization 2003. Severe acute respiratory syndrome (SARS): report by the Secretariat. Rep. EB113/33
  3. World Health Organization 2004. Situation updates—SARS http://www.who.int/csr/sars/archive/ [Google Scholar]
  4. Drosten C, Gunther S, Preiser W. et al. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967–76 [Google Scholar]
  5. Ksiazek TG, Erdman D, Goldsmith CS. et al. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med 348:1953–66 [Google Scholar]
  6. Fouchier RA, Kuiken T, Schutten M. et al. 2003. Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423:240 [Google Scholar]
  7. Kuiken T, Fouchier RA, Schutten M. et al. 2003. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263–70 [Google Scholar]
  8. World Health Organization 2004. Summary of probable SARS cases with onset of illness from 1 November 2002 to 31 July 2003 Communicable Disease Surveillance & Response (CSR) http://www.who.int/csr/sars/country/table2004_04_21/en [Google Scholar]
  9. Lai MM, Holmes KV. 2001. Coronaviridae: the viruses and their replication. In Virology ed. BN Fields, DM Knipe, PM Howley, et al. pp. 1163–85 Philadelphia: Lippincott Williams & Wilkins [Google Scholar]
  10. Holmes KV. 2001. Coronaviruses. In Virology ed. BN Fields, DM Knipe, PM Howley, et al. pp. 1187–1203 Philadelphia: Lippincott Williams & Wilkins [Google Scholar]
  11. Sizun J, Soupre D, Legrand MC. et al. 1995. Neonatal nosocomial respiratory infection with coronavirus: a prospective study in a neonatal intensive care unit. Acta Paediatr. 84:617–20 [Google Scholar]
  12. Sizun J, Yu MW, Talbot PJ. 2000. Survival of human coronaviruses 229E and OC43 in suspension and after drying on surfaces: a possible source of hospital-acquired infections. J. Hosp. Infect. 46:55–60 [Google Scholar]
  13. Van Der Hoek L, Pyrc K, Jebbink MF. et al. 2004. Identification of a new human coronavirus. Nat. Med. 10:368–73 [Google Scholar]
  14. Fouchier RA, Hartwig NG, Bestebroer TM. et al. 2004. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. USA 101:6212–16 [Google Scholar]
  15. Zhong NS, Zheng BJ, Li YM. et al. 2003. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. Lancet 362:1353–58 [Google Scholar]
  16. He JF, Xu RH, Yu DW. et al. 2003. Severe acute respiratory syndrome in Guangdong Province of China: epidemiology and control measures. Chin. J. Prev. Med. 37:227–32 [Google Scholar]
  17. Yu D, Li H, Xu R. et al. 2003. Prevalence of IgG antibody to SARS-associated coronavirus in animal traders—Guangdong Province, China, 2003. Morb. Mortal. Wkly. Rep. 52:986–87 [Google Scholar]
  18. Guan Y, Zheng BJ, He YQ. et al. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:276–78 [Google Scholar]
  19. Martina BE, Haagmans BL, Kuiken T. et al. 2003. Virology: SARS virus infection of cats and ferrets. Nature 425:915 [Google Scholar]
  20. Peiris JS, Yuen KY, Osterhaus AD. et al. 2003. The severe acute respiratory syndrome. N. Engl. J. Med. 349:2431–41 [Google Scholar]
  21. Zheng BJ, Guan Y, Wong KH. et al. 2004. SARS-related virus predating SARS outbreak, Hong Kong. Emerg. Infect. Dis. 10:176–78 [Google Scholar]
  22. St-Jean JR, Jacomy H, Desforges M. et al. 2004. Human respiratory coronavirus OC4s: genetic stability and neuroinvasion. J. Virol. 78:8824–34 [Google Scholar]
  23. Marra MA, Jones SJ, Astell CR. et al. 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399–404 [Google Scholar]
  24. Rota PA, Oberste MS, Monroe SS. et al. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394–99 [Google Scholar]
  25. Guo JP, Petric M, Campbell W. et al. 2004. SARS corona virus peptides recognized by antibodies in the sera of convalescent cases. Virology 324:251 [Google Scholar]
  26. Chinese SARS Molecular Epidemiology Consortium 2004. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303:1666–69 [Google Scholar]
  27. Rest JS, Mindell DP. 2003. SARS associated coronavirus has a recombinant polymerase and coronaviruses have a history of host-shifting. Infect. Genet. Evol. 3:219–25 [Google Scholar]
  28. Snijder EJ, Bredenbeek PJ, Dobbe JC. et al. 2003. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331:991–1004 [Google Scholar]
  29. Poutanen SM, Low DE, Henry B. et al. 2003. Identification of severe acute respiratory syndrome in Canada. N. Engl. J. Med. 348:1995–2005 [Google Scholar]
  30. Lipsitch M, Cohen T, Cooper B. et al. 2003. Transmission dynamics and control of severe acute respiratory syndrome. Science 300:1966–70 [Google Scholar]
  31. Riley S, Fraser C, Donnelly CA. et al. 2003. Transmission dynamics of the etiological agent of SARS in Hong Kong: impact of public health interventions. Science 300:1961–66 [Google Scholar]
  32. Shen Z, Ning F, Zhou W. et al. 2004. Superspreading SARS events, Beijing, 2003. Emerg. Infect. Dis. 10:256–60 [Google Scholar]
  33. Dye C, Gay N. 2003. Modeling the SARS epidemic. Science 300:1884–85 [Google Scholar]
  34. Christian MD, Loutfy M, McDonald LC. et al. 2004. Possible SARS coronavirus transmission during cardiopulmonary resuscitation. Emerg. Infect. Dis. 10:287–93 [Google Scholar]
  35. Wong TW, Lee CK, Tam W. et al. 2004. Cluster of SARS among medical students exposed to single patient, Hong Kong. Emerg. Infect. Dis. 10:269–76 [Google Scholar]
  36. Peiris JS, Chu CM, Cheng VC. et al. 2003. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 361:1767–72 [Google Scholar]
  37. Ng SKC. 2003. Possible role of an animal vector in the SARS outbreak at Amoy Gardens. Lancet 362:570–72 [Google Scholar]
  38. Yu IT, Li Y, Wong TW. et al. 2004. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N. Engl. J Med. 350:1731–39 [Google Scholar]
  39. Seto WH, Tsang D, Yung RW. et al. 2003. Effectiveness of precautions against droplets and contact in prevention of nosocomial transmission of severe acute respiratory syndrome (SARS). Lancet 361:1519–20 [Google Scholar]
  40. Varia M, Wilson S, Sarwal S. et al. 2003. Investigation of a nosocomial outbreak of severe acute respiratory syndrome (SARS) in Toronto, Canada. Can. Med. Assoc. J. 169:285–92 [Google Scholar]
  41. Fisher DA, Lim TK, Lim YT. et al. 2003. Atypical presentations of SARS. Lancet 361:1740 [Google Scholar]
  42. Goh DL, Lee BW, Chia KS. et al. 2004. Secondary household transmission of SARS, Singapore. Emerg. Infect. Dis. 10:232–34 [Google Scholar]
  43. Health Canada, Population and Public Health Branch (PPHB) 2003. Health Canada summary of severe acute respiratory syndrome (SARS) cases: Canada and international, April 16, 2003 http://www.hc-sc.gc.ca/pphb-dgspsp/sars-sras/eu-ae/sars20030416_e.html [Google Scholar]
  44. Monto AS. 1997. Coronaviruses. In Viral Infections of Humans: Epidemiology and Control ed. AS Vans, RA Kaslow pp. 211–27 New York: Plenum Medical Book Co. [Google Scholar]
  45. Cheng VC, Hung IF, Tang BS. et al. 2004. Viral replication in the nasopharynx is associated with diarrhea in patients with severe acute respiratory syndrome. Clin. Infect. Dis. 38:467–75 [Google Scholar]
  46. Leung WK, To KF, Chan PK. et al. 2003. Enteric involvement of severe acute respiratory syndrome-associated coronavirus infection. Gastroenterology 125:1011–17 [Google Scholar]
  47. Lau KK, Yu WC, Chu CM. et al. 2004. Possible central nervous system infection by SARS coronavirus. Emerg. Infect. Dis. 10:342–44 [Google Scholar]
  48. Ding Y, He L, Zhang Q. et al. 2004. Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J. Pathol. 203:622–30 [Google Scholar]
  49. Tsui PT, Kwok ML, Yuen H. et al. 2003. Severe acute respiratory syndrome: clinical outcome and prognostic correlates. Emerg. Infect. Dis. 9:1064–69 [Google Scholar]
  50. Nicolaou S, Al Nakshabandi NA, Muller NL. 2003. Images in clinical medicine. Radiologic manifestations of severe acute respiratory syndrome. N. Engl. J. Med. 348:2006 [Google Scholar]
  51. World Health Organization 2003. Alert, verification and public health management of SARS in the post-outbreak period. Communicable Disease Surveillance & Response (CSR) http://www.who.int/csr/sars/postoutbreak/en/ [Google Scholar]
  52. World Health Organization 2003. Case definitions for surveillance of severe acute respiratory syndrome (SARS). Communicable Disease Surveillance & Response (CSR) http://www.who.int/csr/sars/casedefinition/en/ [Google Scholar]
  53. Choi KW, Chau TN, Tsang O. et al. 2003. Outcomes and prognostic factors in 267 patients with severe acute respiratory syndrome in Hong Kong. Ann. Intern. Med. 139:715–23 [Google Scholar]
  54. Booth CM, Matukas LM, Tomlinson GA. et al. 2003. Clinical features and short-term outcomes of 144 patients with SARS in the Greater Toronto Area. JAMA 289:2801–9 [Google Scholar]
  55. Christian MD, Poutanen SM, Loutfy MR. et al. 2004. Severe acute respiratory syndrome. Clin. Infect. Dis. 38:1420–27 [Google Scholar]
  56. Wong KT, Antonio GE, Hui DS. et al. 2003. Thin-section CT of severe acute respiratory syndrome: evaluation of 74 patients exposed to or with the disease. Radiology 228:395–400 [Google Scholar]
  57. Li G, Zhao Z, Chen L. et al. 2003. Mild severe acute respiratory syndrome. Emerg. Infect. Dis. 9:1182–83 [Google Scholar]
  58. Hon K, Leung CW, Cheng W. et al. 2003. Clinical presentations and outcome of severe acute respiratory syndrome in children. Lancet 361:1701–3 [Google Scholar]
  59. Gold WL, Mederski B, Rose D. et al.2003 Prevalence of asymptomatic (AS) infection by severe acute respiratory syndrome coronavirus (SARS-CoV) in exposed healthcare workers (HCW)43rd Intersci. Conf. Antimicrobial Agents and ChemotherapyChicago, IL Sep. 14–17. Program/Abstracts Addendum p. 18 (Abstr. K-1315c) [Google Scholar]
  60. Fowler RA, Lapinsky SE, Hallett D. et al. 2003. Critically ill patients with severe acute respiratory syndrome. JAMA 290:367–73 [Google Scholar]
  61. Lew TW, Kwek TK, Tai D. et al. 2003. Acute respiratory distress syndrome in critically ill patients with severe acute respiratory syndrome. JAMA 290:374–80 [Google Scholar]
  62. Chan KS, Zheng JP, Mok YW. et al. 2003. SARS: prognosis, outcome and sequelae. Respirology 8:(Suppl.)S36–S40 [Google Scholar]
  63. Bitnun A, Allen U, Heurter H. et al. 2003. Children hospitalized with severe acute respiratory syndrome-related illness in Toronto. Pediatrics 112:e261 [Google Scholar]
  64. Wong RS, Wu A, To KF. et al. 2003. Haematological manifestations in patients with severe acute respiratory syndrome: retrospective analysis. BMJ 326:1358–62 [Google Scholar]
  65. Wang C. National Research Project for SARS Beijing Group 2003. Dynamic changes in blood cytokine levels as clinical indicators in severe acute respiratory syndrome. Chin. Med. J. (Engl.) 116:1283–87 [Google Scholar]
  66. Lin M, Tseng HK, Trejaut JA. et al. 2003. Association of HLA class I with severe acute respiratory syndrome coronavirus infection. BMC Med. Genet. 4:9 [Google Scholar]
  67. Franks TJ, Chong PY, Chui P. et al. 2003. Lung pathology of severe acute respiratory syndrome (SARS): a study of 8 autopsy cases from Singapore. Hum. Pathol. 34:743–48 [Google Scholar]
  68. Li G, Chen X, Xu A. 2003. Profile of specific antibodies to the SARS-associated coronavirus. N. Engl. J. Med. 349:508–9 [Google Scholar]
  69. Shi Y, Yi Y, Li P. et al. 2003. Diagnosis of severe acute respiratory syndrome (SARS) by detection of SARS coronavirus nucleocapsid antibodies in an antigen-capturing enzyme-linked immunosorbent assay. J. Clin. Microbiol. 41:5781–82 [Google Scholar]
  70. Cui W, Fan Y, Wu W. et al. 2003. Expression of lymphocytes and lymphocyte subsets in patients with severe acute respiratory syndrome. Clin. Infect. Dis. 37:857–59 [Google Scholar]
  71. Li L, Wo J, Shao J. et al. 2003. SARS-coronavirus replicates in mononuclear cells of peripheral blood (PBMCs) from SARS patients. J. Clin. Virol. 28:239–44 [Google Scholar]
  72. Li W, Moore MJ, Vasilieva N. et al. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450–54 [Google Scholar]
  73. Hamming I, Timens W, Bulthuis M. et al. 2004. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 203:631–37 [Google Scholar]
  74. Koren G, King S, Knowles S. et al. 2003. Ribavirin in the treatment of SARS: a new trick for an old drug. Can. Med. Assoc. J. 168:1289–92 [Google Scholar]
  75. Nicholls JM, Poon LL, Lee KC. et al. 2003. Lung pathology of fatal severe acute respiratory syndrome. Lancet 361:1773–78 [Google Scholar]
  76. World Health Organization 2004. Sampling for severe acute respiratory syndrome (SARS) diagnostic tests. Communicable Disease Surveillance & Response (CSR) http://www.who.int/csr/sars/sampling/en/ [Google Scholar]
  77. World Health Organization 2003. WHO post-outbreak biosafety guidelines for handling of SARS-CoV specimens and cultures. Communicable Disease Surveillance & Response (CSR) http://www.who.int/csr/sars/biosafety2003_12_18/en/ [Google Scholar]
  78. Lim PL, Kurup A, Gopalakrishna G. et al. 2004. Laboratory-acquired severe acute respiratory syndrome. N. Engl. J. Med. 350:1740–45 [Google Scholar]
  79. Ng EKO, Ng PC, Hon KL. et al. 2003. Serial analysis of the plasma concentration of SARS coronavirus RNA in pediatric patients with severe acute respiratory syndrome. Clin. Chem. 49:2085–88 [Google Scholar]
  80. Poon LL, Chan KH, Wong OK. et al. 2004. Detection of SARS coronavirus in patients with severe acute respiratory syndrome by conventional and real-time quantitative reverse transcription-PCR assays. Clin. Chem. 50:67–72 [Google Scholar]
  81. Ng EK, Hui DS, Chan KC. et al. 2003. Quantitative analysis and prognostic implication of SARS coronavirus RNA in the plasma and serum of patients with severe acute respiratory syndrome. Clin. Chem. 49:1976–80 [Google Scholar]
  82. Chan KH, Poon LL, Cheng VC. et al. 2004. Detection of SARS coronavirus in patients with suspected SARS. Emerg. Infect. Dis. 10:294–99 [Google Scholar]
  83. Yam WC, Chan KH, Poon LL. et al. 2003. Evaluation of reverse transcription-PCR assays for rapid diagnosis of severe acute respiratory syndrome associated with a novel coronavirus. J. Clin. Microbiol. 41:4521–24 [Google Scholar]
  84. Ng ML, Tan SH, See EE. et al. 2003. Proliferative growth of SARS coronavirus in Vero E6 cells. J. Gen. Virol. 84:3291–303 [Google Scholar]
  85. Wu HS, Chiu SC, Tseng TC. et al. 2004. Serologic and molecular biologic methods for SARS-associated coronavirus infection, Taiwan. Emerg. Infect. Dis. 10:304–10 [Google Scholar]
  86. Tang P, Louie M, Richardson SE. et al. 2004. Interpretation of diagnostic laboratory tests for severe acute respiratory syndrome: the Toronto experience. Can. Med. Assoc. J. 170:47–54 [Google Scholar]
  87. Cinatl J, Morgenstern B, Bauer G. et al. 2003. Treatment of SARS with human interferons. Lancet 362:293–94 [Google Scholar]
  88. Loutfy MR, Blatt LM, Siminovitch KA. et al. 2003. Interferon alfacon-1 plus corticosteroids in severe acute respiratory syndrome: a preliminary study. JAMA 290:3222–28 [Google Scholar]
  89. Zhao Z, Zhang F, Xu M. et al. 2003. Description and clinical treatment of an early outbreak of severe acute respiratory syndrome (SARS) in Guangzhou, PR China. J. Med. Microbiol. 52:715–20 [Google Scholar]
  90. Hsu LY, Lee CC, Green JA. et al. 2003. Severe acute respiratory syndrome (SARS) in Singapore: clinical features of index patient and initial contacts. Emerg. Infect. Dis. 9:713–17 [Google Scholar]
  91. Knowles SR, Phillips EJ, Dresser L. et al. 2003. Common adverse events associated with the use of ribavirin for severe acute respiratory syndrome in Canada. Clin. Infect. Dis. 37:1139–42 [Google Scholar]
  92. Charles M. CDC SARS Investigative Team 2003. Severe acute respiratory syndrome (SARS) and coronavirus testing—United States, 2003. Morb. Mortal. Wkly. Rep. 52:297–302 [Google Scholar]
  93. Mazzulli T. 2004. Severe acute respiratory syndrome-associated coronavirus in lung tissue. Emerg. Infect. Dis. 10:20–24 [Google Scholar]
  94. Sung J. 2003 Clinical diagnosis and management of severe acute respiratory syndrome (SARS) Presented at WHO Global Conf. Severe Acute Respiratory Syndrome (SARS)Kuala Lumpur, Malaysia June 17 http://www.who.int/csr/sars/conference/june_2003/materials/presentations/en/clinical_diagnosis[1].pdf [Google Scholar]
  95. Ho JC, Ooi GC, Mok TY. et al. 2003. High-dose pulse versus nonpulse corticosteroid regimens in severe acute respiratory syndrome. Am. J. Respir. Crit. Care Med. 168:1449–56 [Google Scholar]
  96. Oba Y. 2003. The use of corticosteroids in SARS. N. Engl. J. Med. 348:2034–35 [Google Scholar]
  97. Wang H, Ding Y, Li X. et al. 2003. Fatal aspergillosis in a patient with SARS who was treated with corticosteroids. N. Engl. J. Med. 349:507–8 [Google Scholar]
  98. Johnson MA, Pooley C, Ignjatovic J. et al. 2003. A recombinant fowl adenovirus expressing the S1 gene of infectious bronchitis virus protects against challenge with infectious bronchitis virus. Vaccine 21:2730–36 [Google Scholar]
  99. Weiss RC, Scott FW. 1981. Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp. Immunol. Microbiol. Infect. Dis. 4:175–89 [Google Scholar]
  100. Corapi WV, Olsen CW, Scott FW. 1992. Monoclonal antibody analysis of neutralization and antibody-dependent enhancement of feline infectious peritonitis virus. J. Virol. 66:6695–705 [Google Scholar]
  101. Olsen CW, Corapi WV, Ngichabe CK. et al. 1992. Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J. Virol. 66:956–65 [Google Scholar]
  102. Yang Z-Y, Kong W-P, Huang Y. et al. 2004. A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice. Nature 428:561–64 [Google Scholar]
  103. ter Meulen J, Bakker ABH, van den Brink E. et al. 2004. Human monoclonal antibody as prophylaxis for SARS coronavirus infection in ferrets. Lancet 363:2139–41 [Google Scholar]
/content/journals/10.1146/annurev.med.56.091103.134135
Loading
/content/journals/10.1146/annurev.med.56.091103.134135
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error