Skip to main content
Thorax logoLink to Thorax
. 2005 May;60(5):401–409. doi: 10.1136/thx.2004.030205

Impact of severe acute respiratory syndrome (SARS) on pulmonary function, functional capacity and quality of life in a cohort of survivors

D Hui 1, G Joynt 1, K Wong 1, C Gomersall 1, T Li 1, G Antonio 1, F Ko 1, M Chan 1, D Chan 1, M Tong 1, T Rainer 1, A Ahuja 1, C Cockram 1, J Sung 1
PMCID: PMC1758905  PMID: 15860716

Abstract

Objective: To examine the impact of severe acute respiratory syndrome (SARS) on pulmonary function, exercise capacity, and health-related quality of life (HRQoL) among survivors.

Methods: 110 survivors with confirmed SARS were evaluated at the Prince of Wales Hospital, HK at the end of 3 and 6 months after symptom onset. The assessment included lung volumes (TLC, VC, RV, FRC), spirometry (FVC, FEV1), carbon monoxide transfer factor (TLCO adjusted for haemoglobin), inspiratory and expiratory respiratory muscle strength (Pimax and Pemax), 6 minute walk distance (6MWD), chest radiographs, and HRQoL by SF-36 questionnaire.

Results: There were 44 men and 66 women with a mean (SD) age of 35.6 (9.8) years and body mass index of 23.1 (4.8) kg/m2. Seventy (64%) were healthcare workers. At 6 months 33 subjects (30%) had abnormal chest radiographs; four (3.6%), eight (7.4%), and 17 (15.5%) patients had FVC, TLC, and TLCO below 80% of predicted values; and 15 (13.9%) and 24 (22.2%) had Pimax and Pemax values below 80 cm H2O, respectively. The 6MWD increased from a mean (SD) of 464 (83) m at 3 months to 502 (95) m (95% CI 22 to 54 m, p<0.001), but the results were lower than normal controls in the same age groups. There was impairment of HRQoL at 6 months. Patients who required ICU admission (n = 31) had significantly lower FVC, TLC, and TLCO than those who did not.

Conclusion: The exercise capacity and health status of SARS survivors was considerably lower than that of a normal population at 6 months. Significant impairment in surface area for gas exchange was noted in 15.5% of survivors. The functional disability appears out of proportion to the degree of lung function impairment and may be related to additional factors such as muscle deconditioning and steroid myopathy.

Full Text

The Full Text of this article is available as a PDF (205.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Antonio Gregory E., Wong K. T., Hui David S. C., Wu Alan, Lee Nelson, Yuen Edmund H. Y., Leung C. B., Rainer T. H., Cameron Peter, Chung Sydney S. C. Thin-section CT in patients with severe acute respiratory syndrome following hospital discharge: preliminary experience. Radiology. 2003 Jun 12;228(3):810–815. doi: 10.1148/radiol.2283030726. [DOI] [PubMed] [Google Scholar]
  2. Black L. F., Hyatt R. E. Maximal respiratory pressures: normal values and relationship to age and sex. Am Rev Respir Dis. 1969 May;99(5):696–702. doi: 10.1164/arrd.1969.99.5.696. [DOI] [PubMed] [Google Scholar]
  3. Booth Christopher M., Matukas Larissa M., Tomlinson George A., Rachlis Anita R., Rose David B., Dwosh Hy A., Walmsley Sharon L., Mazzulli Tony, Avendano Monica, Derkach Peter. Clinical features and short-term outcomes of 144 patients with SARS in the greater Toronto area. JAMA. 2003 May 6;289(21):2801–2809. doi: 10.1001/jama.289.21.JOC30885. [DOI] [PubMed] [Google Scholar]
  4. Chan C. C., Cheong T. H., Wang Y. T., Poh S. C. Transdiaphragmatic pressure in young adult Singaporean subjects--normal values and a comparison between different respiratory manoeuvres. Aust N Z J Med. 1996 Feb;26(1):75–81. doi: 10.1111/j.1445-5994.1996.tb02910.x. [DOI] [PubMed] [Google Scholar]
  5. Chan J. W. M., Ng C. K., Chan Y. H., Mok T. Y. W., Lee S., Chu S. Y. Y., Law W. L., Lee M. P., Li P. C. K. Short term outcome and risk factors for adverse clinical outcomes in adults with severe acute respiratory syndrome (SARS). Thorax. 2003 Aug;58(8):686–689. doi: 10.1136/thorax.58.8.686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cooper A. B., Ferguson N. D., Hanly P. J., Meade M. O., Kachura J. R., Granton J. T., Slutsky A. S., Stewart T. E. Long-term follow-up of survivors of acute lung injury: lack of effect of a ventilation strategy to prevent barotrauma. Crit Care Med. 1999 Dec;27(12):2616–2621. doi: 10.1097/00003246-199912000-00002. [DOI] [PubMed] [Google Scholar]
  7. Dekhuijzen P. N., Decramer M. Steroid-induced myopathy and its significance to respiratory disease: a known disease rediscovered. Eur Respir J. 1992 Sep;5(8):997–1003. [PubMed] [Google Scholar]
  8. Ding Yanqing, Wang Huijun, Shen Hong, Li Zhuguo, Geng Jian, Han Huixia, Cai Junjie, Li Xin, Kang Wei, Weng Desheng. The clinical pathology of severe acute respiratory syndrome (SARS): a report from China. J Pathol. 2003 Jul;200(3):282–289. doi: 10.1002/path.1440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Drosten Christian, Günther Stephan, Preiser Wolfgang, van der Werf Sylvie, Brodt Hans-Reinhard, Becker Stephan, Rabenau Holger, Panning Marcus, Kolesnikova Larissa, Fouchier Ron A. M. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med. 2003 Apr 10;348(20):1967–1976. doi: 10.1056/NEJMoa030747. [DOI] [PubMed] [Google Scholar]
  10. Enright P. L., Sherrill D. L. Reference equations for the six-minute walk in healthy adults. Am J Respir Crit Care Med. 1998 Nov;158(5 Pt 1):1384–1387. doi: 10.1164/ajrccm.158.5.9710086. [DOI] [PubMed] [Google Scholar]
  11. Fraenkel D. J., Bardin P. G., Sanderson G., Lampe F., Johnston S. L., Holgate S. T. Lower airways inflammation during rhinovirus colds in normal and in asthmatic subjects. Am J Respir Crit Care Med. 1995 Mar;151(3 Pt 1):879–886. doi: 10.1164/ajrccm/151.3_Pt_1.879. [DOI] [PubMed] [Google Scholar]
  12. Franks Teri J., Chong Pek Y., Chui Paul, Galvin Jeffrey R., Lourens Raina M., Reid Ann H., Selbs Elena, McEvoy Col Peter L., Hayden Col Dennis L., Fukuoka Junya. Lung pathology of severe acute respiratory syndrome (SARS): a study of 8 autopsy cases from Singapore. Hum Pathol. 2003 Aug;34(8):743–748. doi: 10.1016/S0046-8177(03)00367-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Herridge Margaret S., Cheung Angela M., Tansey Catherine M., Matte-Martyn Andrea, Diaz-Granados Natalia, Al-Saidi Fatma, Cooper Andrew B., Guest Cameron B., Mazer C. David, Mehta Sangeeta. One-year outcomes in survivors of the acute respiratory distress syndrome. N Engl J Med. 2003 Feb 20;348(8):683–693. doi: 10.1056/NEJMoa022450. [DOI] [PubMed] [Google Scholar]
  14. Hsu Li-Yang, Lee Cheng-Chuan, Green Justin A., Ang Brenda, Paton Nicholas I., Lee Lawrence, Villacian Jorge S., Lim Poh-Lian, Earnest Arul, Leo Yee-Sin. Severe acute respiratory syndrome (SARS) in Singapore: clinical features of index patient and initial contacts. Emerg Infect Dis. 2003 Jun;9(6):713–717. doi: 10.3201/eid0906.030264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hui David S. C., Sung Joseph J. Y. Severe acute respiratory syndrome. Chest. 2003 Jul;124(1):12–15. doi: 10.1378/chest.124.1.12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hund E. Myopathy in critically ill patients. Crit Care Med. 1999 Nov;27(11):2544–2547. doi: 10.1097/00003246-199911000-00036. [DOI] [PubMed] [Google Scholar]
  17. Joynt Gavin M., Antonio Gregory E., Lam Philip, Wong Ka Tak, Li Thomas, Gomersall Charles D., Ahuja Anil T. Late-stage adult respiratory distress syndrome caused by severe acute respiratory syndrome: abnormal findings at thin-section CT. Radiology. 2004 Feb;230(2):339–346. doi: 10.1148/radiol.2303030894. [DOI] [PubMed] [Google Scholar]
  18. Kaplan P. W., Rocha W., Sanders D. B., D'Souza B., Spock A. Acute steroid-induced tetraplegia following status asthmaticus. Pediatrics. 1986 Jul;78(1):121–123. [PubMed] [Google Scholar]
  19. Koulouris N., Mulvey D. A., Laroche C. M., Green M., Moxham J. Comparison of two different mouthpieces for the measurement of Pimax and Pemax in normal and weak subjects. Eur Respir J. 1988 Oct;1(9):863–867. [PubMed] [Google Scholar]
  20. Ksiazek Thomas G., Erdman Dean, Goldsmith Cynthia S., Zaki Sherif R., Peret Teresa, Emery Shannon, Tong Suxiang, Urbani Carlo, Comer James A., Lim Wilina. A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med. 2003 Apr 10;348(20):1953–1966. doi: 10.1056/NEJMoa030781. [DOI] [PubMed] [Google Scholar]
  21. Kuiken Thijs, Fouchier Ron A. M., Schutten Martin, Rimmelzwaan Guus F., van Amerongen Geert, van Riel Debby, Laman Jon D., de Jong Ton, van Doornum Gerard, Lim Wilina. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet. 2003 Jul 26;362(9380):263–270. doi: 10.1016/S0140-6736(03)13967-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Laitinen L. A., Elkin R. B., Empey D. W., Jacobs L., Mills J., Nadel J. A. Bronchial hyperresponsiveness in normal subjects during attenuated influenza virus infection. Am Rev Respir Dis. 1991 Feb;143(2):358–361. doi: 10.1164/ajrccm/143.2.358. [DOI] [PubMed] [Google Scholar]
  23. Lakshminarayan S., Hudson L. D. Pulmonary function following the adult respiratory distress syndrome. Chest. 1978 Nov;74(5):489–490. doi: 10.1378/chest.74.5.489. [DOI] [PubMed] [Google Scholar]
  24. Lam C. L., Gandek B., Ren X. S., Chan M. S. Tests of scaling assumptions and construct validity of the Chinese (HK) version of the SF-36 Health Survey. J Clin Epidemiol. 1998 Nov;51(11):1139–1147. doi: 10.1016/s0895-4356(98)00105-x. [DOI] [PubMed] [Google Scholar]
  25. Larsson L., Li X., Edström L., Eriksson L. I., Zackrisson H., Argentini C., Schiaffino S. Acute quadriplegia and loss of muscle myosin in patients treated with nondepolarizing neuromuscular blocking agents and corticosteroids: mechanisms at the cellular and molecular levels. Crit Care Med. 2000 Jan;28(1):34–45. doi: 10.1097/00003246-200001000-00006. [DOI] [PubMed] [Google Scholar]
  26. Lee Nelson, Hui David, Wu Alan, Chan Paul, Cameron Peter, Joynt Gavin M., Ahuja Anil, Yung Man Yee, Leung C. B., To K. F. A major outbreak of severe acute respiratory syndrome in Hong Kong. N Engl J Med. 2003 Apr 7;348(20):1986–1994. doi: 10.1056/NEJMoa030685. [DOI] [PubMed] [Google Scholar]
  27. Man William D-C, Kyroussis Dimitris, Fleming Tracey A., Chetta Alfredo, Harraf Farzaneh, Mustfa Naveed, Rafferty Gerrard F., Polkey Michael I., Moxham John. Cough gastric pressure and maximum expiratory mouth pressure in humans. Am J Respir Crit Care Med. 2003 Jul 11;168(6):714–717. doi: 10.1164/rccm.200303-334BC. [DOI] [PubMed] [Google Scholar]
  28. McHorney C. A., Ware J. E., Jr, Lu J. F., Sherbourne C. D. The MOS 36-item Short-Form Health Survey (SF-36): III. Tests of data quality, scaling assumptions, and reliability across diverse patient groups. Med Care. 1994 Jan;32(1):40–66. doi: 10.1097/00005650-199401000-00004. [DOI] [PubMed] [Google Scholar]
  29. Mitch W. E., Goldberg A. L. Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med. 1996 Dec 19;335(25):1897–1905. doi: 10.1056/NEJM199612193352507. [DOI] [PubMed] [Google Scholar]
  30. Nava S., Fracchia C., Callegari G., Ambrosino N., Barbarito N., Felicetti G. Weakness of respiratory and skeletal muscles after a short course of steroids in patients with acute lung rejection. Eur Respir J. 2002 Aug;20(2):497–499. doi: 10.1183/09031936.02.01732002. [DOI] [PubMed] [Google Scholar]
  31. Neff Thomas A., Stocker Reto, Frey Hans-Rudolf, Stein Sonja, Russi Erich W. Long-term assessment of lung function in survivors of severe ARDS. Chest. 2003 Mar;123(3):845–853. doi: 10.1378/chest.123.3.845. [DOI] [PubMed] [Google Scholar]
  32. Ng C. K., Chan J. W. M., Kwan T. L., To T. S., Chan Y. H., Ng F. Y. Y., Mok T. Y. W. Six month radiological and physiological outcomes in severe acute respiratory syndrome (SARS) survivors. Thorax. 2004 Oct;59(10):889–891. doi: 10.1136/thx.2004.023762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nicholls John M., Poon Leo L. M., Lee Kam C., Ng Wai F., Lai Sik T., Leung Chung Y., Chu Chung M., Hui Pak K., Mak Kong L., Lim Wilina. Lung pathology of fatal severe acute respiratory syndrome. Lancet. 2003 May 24;361(9371):1773–1778. doi: 10.1016/S0140-6736(03)13413-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ong K-C, Ng A. W-K, Lee L. S-U, Kaw G., Kwek S-K, Leow M. K-S, Earnest A. Pulmonary function and exercise capacity in survivors of severe acute respiratory syndrome. Eur Respir J. 2004 Sep;24(3):436–442. doi: 10.1183/09031936.04.00007104. [DOI] [PubMed] [Google Scholar]
  35. Orme James, Jr, Romney Joshua S., Hopkins Ramona O., Pope Donna, Chan Karen J., Thomsen George, Crapo Robert O., Weaver Lindell K. Pulmonary function and health-related quality of life in survivors of acute respiratory distress syndrome. Am J Respir Crit Care Med. 2002 Dec 18;167(5):690–694. doi: 10.1164/rccm.200206-542OC. [DOI] [PubMed] [Google Scholar]
  36. Peiris J. S. M., Chu C. M., Cheng V. C. C., Chan K. S., Hung I. F. N., Poon L. L. M., Law K. I., Tang B. S. F., Hon T. Y. W., Chan C. S. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet. 2003 May 24;361(9371):1767–1772. doi: 10.1016/S0140-6736(03)13412-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Peters J. I., Bell R. C., Prihoda T. J., Harris G., Andrews C., Johanson W. G. Clinical determinants of abnormalities in pulmonary functions in survivors of the adult respiratory distress syndrome. Am Rev Respir Dis. 1989 May;139(5):1163–1168. doi: 10.1164/ajrccm/139.5.1163. [DOI] [PubMed] [Google Scholar]
  38. Polsonetti Bryan W., Joy Saju D., Laos Luis F. Steroid-induced myopathy in the ICU. Ann Pharmacother. 2002 Nov;36(11):1741–1744. doi: 10.1345/aph.1C095. [DOI] [PubMed] [Google Scholar]
  39. Schelling G., Stoll C., Vogelmeier C., Hummel T., Behr J., Kapfhammer H. P., Rothenhäusler H. B., Haller M., Durst K., Krauseneck T. Pulmonary function and health-related quality of life in a sample of long-term survivors of the acute respiratory distress syndrome. Intensive Care Med. 2000 Sep;26(9):1304–1311. doi: 10.1007/s001340051342. [DOI] [PubMed] [Google Scholar]
  40. Simpson D. L., Goodman M., Spector S. L., Petty T. L. Long-term follow-up and bronchial reactivity testing in survivors of the adult respiratory distress syndrome. Am Rev Respir Dis. 1978 Mar;117(3):449–454. doi: 10.1164/arrd.1978.117.3.449. [DOI] [PubMed] [Google Scholar]
  41. Sterk P. J. Virus-induced airway hyperresponsiveness in man. Eur Respir J. 1993 Jun;6(6):894–902. [PubMed] [Google Scholar]
  42. Sung J. J. Y., Wu A., Joynt G. M., Yuen K. Y., Lee N., Chan P. K. S., Cockram C. S., Ahuja A. T., Yu L. M., Wong V. W. Severe acute respiratory syndrome: report of treatment and outcome after a major outbreak. Thorax. 2004 May;59(5):414–420. doi: 10.1136/thx.2003.014076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Trigg C. J., Nicholson K. G., Wang J. H., Ireland D. C., Jordan S., Duddle J. M., Hamilton S., Davies R. J. Bronchial inflammation and the common cold: a comparison of atopic and non-atopic individuals. Clin Exp Allergy. 1996 Jun;26(6):665–676. doi: 10.1111/j.1365-2222.1996.tb00593.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tse G. M-K, To K-F, Chan P. K-S, Lo A. W. I., Ng K-C, Wu A., Lee N., Wong H-C, Mak S-M, Chan K-F. Pulmonary pathological features in coronavirus associated severe acute respiratory syndrome (SARS). J Clin Pathol. 2004 Mar;57(3):260–265. doi: 10.1136/jcp.2003.013276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tsui Ping Tim, Kwok Man Leung, Yuen Hon, Lai Sik To. Severe acute respiratory syndrome: clinical outcome and prognostic correlates. Emerg Infect Dis. 2003 Sep;9(9):1064–1069. doi: 10.3201/eid0909.030362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Weinert C. R., Gross C. R., Kangas J. R., Bury C. L., Marinelli W. A. Health-related quality of life after acute lung injury. Am J Respir Crit Care Med. 1997 Oct;156(4 Pt 1):1120–1128. doi: 10.1164/ajrccm.156.4.9611047. [DOI] [PubMed] [Google Scholar]
  47. Weisman I. M., Zeballos R. J. Clinical exercise testing. Clin Chest Med. 2001 Dec;22(4):679-701, viii. doi: 10.1016/s0272-5231(05)70060-5. [DOI] [PubMed] [Google Scholar]
  48. Wong G. W. K., Hui D. S. C. Severe acute respiratory syndrome (SARS): epidemiology, diagnosis and management. Thorax. 2003 Jul;58(7):558–560. doi: 10.1136/thorax.58.7.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wong K. T., Antonio Gregory E., Hui David S. C., Lee Nelson, Yuen Edmund H. Y., Wu Alan, Leung C. B., Rainer T. H., Cameron Peter, Chung Sydney S. C. Severe acute respiratory syndrome: radiographic appearances and pattern of progression in 138 patients. Radiology. 2003 May 20;228(2):401–406. doi: 10.1148/radiol.2282030593. [DOI] [PubMed] [Google Scholar]
  50. Wong Raymond S. M., Hui David S. Index patient and SARS outbreak in Hong Kong. Emerg Infect Dis. 2004 Feb;10(2):339–341. doi: 10.3201/eid1002.030645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. da Costa J. L. Pulmonary function studies in healthy Chinese adults in Singapore. Am Rev Respir Dis. 1971 Jul;104(1):128–131. doi: 10.1164/arrd.1971.104.1.128. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

[Web-only tables]
thorax_60_5_401__1.pdf (22.8KB, pdf)
thorax_60_5_401__2.pdf (87.8KB, pdf)

Articles from Thorax are provided here courtesy of BMJ Publishing Group

RESOURCES