Skip to main content

Advertisement

Log in

The risk of tuberculosis in SLE patients from an Asian tertiary hospital

  • Observational Research
  • Published:
Rheumatology International Aims and scope Submit manuscript

Abstract

Systemic lupus erythematosus (SLE) has been associated with increased risk of tuberculosis (TB). However, little is known about the extent and risk factors for TB among Asian patient with SLE. We aimed to assess the rate of TB in patients with SLE, and investigate the risk of SLE on TB development using hospital administrative database. This is an historical cohort study of hospital discharge database from 2004 to 2011 to identify cases with SLE and TB using International Statistical Classification of Diseases and Related Health Problems, 9th Revision, Australian Modification (ICD-9-AM) codes. Of 301568 hospitalized patients, 841 (0.3%) patients had SLE, 1843 (0.6%) patients had TB, including 17 SLE patients (2.0%). SLE patients had a significantly higher rate of TB (2.0 vs. 0.6%, p < 0.001) compared to that of patients without SLE. The differences in the higher rate after breaking down was in the pulmonary TB group (1.7 vs. 0.5%, p < 0.00) but not in extrapulmonary TB group (0.4 vs. 0.1%, p = 0.060). Logistic regression analyses showed that SLE was a significant and independent predictor of TB (odds ratio 4.6, 95% CI 2.8–7.5, p < 0.001) after adjustment for factors such as age group, gender, ethnicity, admission class, nutritional deficiency, organ transplantation, and Charlson comorbidity index. SLE patients were found to experience higher rates of tuberculosis in this group of Asian patient population. Patients with SLE should be considered as a high-risk group for TB, active screening for latent patients and treatment for positive TB patients is needed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Chakravarty EF, Bush TM, Manzi S, Clarke AE, Ward MM (2007) Prevalence of adult systemic lupus erythematosus in California and Pennsylvania in 2000: estimates obtained using hospitalization data. Rheum 56(6):2092–2094. doi:10.1002/art.22641

    Google Scholar 

  2. Chiu YM, Lai CH (2010) Nationwide population-based epidemiologic study of systemic lupus erythematosus in Taiwan. Lupus 19(10):1250–1255. doi:10.1177/0961203310373780

    Article  PubMed  Google Scholar 

  3. Fessler BJ (2002) Infectious diseases in systemic lupus erythematosus: risk factors, management and prophylaxis. Best Pract Res Clin Rheumatol 16 (2):281–291. doi:10.1053/berh.2001.0226

    Article  PubMed  Google Scholar 

  4. Danza A, Ruiz-Irastorza G (2013) Infection risk in systemic lupus erythematosus patients: susceptibility factors and preventive strategies. Lupus 22(12):1286–1294. doi:10.1177/0961203313493032

    Article  CAS  PubMed  Google Scholar 

  5. Tam LS, Li EK, Wong SM, Szeto CC (2002) Risk factors and clinical features for tuberculosis among patients with systemic lupus erythematosus in Hong Kong. Scand J Rheumatol 31(5):296–300

    Article  PubMed  Google Scholar 

  6. Prabu V, Agrawal S (2010) Systemic lupus erythematosus and tuberculosis: a review of complex interactions of complicated diseases. J Postgrad Med 56(3):244–250. doi:10.4103/0022-3859.68653

    Article  PubMed  Google Scholar 

  7. Hou CL, Tsai YC, Chen LC, Huang JL (2008) Tuberculosis infection in patients with systemic lupus erythematosus: pulmonary and extra-pulmonary infection compared. Clin Rheumatol 27(5):557–563. doi:10.1007/s10067-007-0741-8

    Article  PubMed  Google Scholar 

  8. Ramagopalan SV, Goldacre R, Skingsley A, Conlon C, Goldacre MJ (2013) Associations between selected immune-mediated diseases and tuberculosis: record-linkage studies. BMC Med 11:97. doi:10.1186/1741-7015-11-97

    Article  PubMed  PubMed Central  Google Scholar 

  9. Victorio-Navarra ST, Dy EE, Arroyo CG, Torralba TP (1996) Tuberculosis among Filipino patients with systemic lupus erythematosus. Semin Arthritis Rheum 26(3):628–634

    Article  CAS  PubMed  Google Scholar 

  10. Yun JE, Lee SW, Kim TH, Jun JB, Jung S, Bae SC, Kim TY, Yoo DH (2002) The incidence and clinical characteristics of Mycobacterium tuberculosis infection among systemic lupus erythematosus and rheumatoid arthritis patients in Korea. Clin Exp Rheumatol 20(2):127–132

    CAS  PubMed  Google Scholar 

  11. Balakrishnan C, Mangat G, Mittal G, Joshi VR (1998) Tuberculosis in patients with systemic lupus erythematosus. J Assoc Physicians India 46(8):682–683

    CAS  PubMed  Google Scholar 

  12. Navarra SV, Leynes MS (2010) Infections in systemic lupus erythematosus. Lupus 19(12):1419–1424. doi:10.1177/0961203310374486

    Article  CAS  PubMed  Google Scholar 

  13. Feng PH, Tan TH (1982) Tuberculosis in patients with systemic lupus erythematosus. Ann Rheum Dis 41(1):11–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ministry of Health Singapore (2016) Tuberculosis. https://www.moh.gov.sg/content/moh_web/home/diseases_and_conditions/t/tuberculosis.html. Accessed 26 Jan 2017

  15. Statistics Singapore (2016) Time Series on Population (Mid-Year Estimates). Singapore Department of Statistics, 2016: http://www.singstat.gov.sg/statistics/latest-data#16. Accessed 26 Jan 2017

  16. Singapore General Hospital (2017) Types of wards in SGH. Singapore General Hospital: http://www.sgh.com.sg/Patient-Services/Charges-Payment/Pages/types-wards.aspx. Accessed 26 Jan 2017

  17. Chen C, Naidoo N, Er B, Cheong A, Fong NP, Tay CY, Chan KM, Tan BY, Menon E, Ee CH, Lee KK, Ng YS, Teo YY, Koh GC (2013) Factors associated with nursing home placement of all patients admitted for inpatient rehabilitation in Singapore community hospitals from 1996 to 2005: a disease stratified analysis. PloS one 8(12):e82697. doi:10.1371/journal.pone.0082697

    Article  PubMed  PubMed Central  Google Scholar 

  18. Bernatsky S, Linehan T, Hanly JG (2011) The accuracy of administrative data diagnoses of systemic autoimmune rheumatic diseases. J Rheumatol 38(8):1612–1616. doi:10.3899/jrheum.101149

    Article  PubMed  Google Scholar 

  19. Yang Y, Thumboo J, Earnest A, Yong S, Fong K (2014) The effect of comorbidity on hospital mortality in patients with SLE from an Asian tertiary hospital. Lupus. doi:10.1177/0961203314522340

    Google Scholar 

  20. Dentan C, Epaulard O, Seynaeve D, Genty C, Bosson JL (2014) Active tuberculosis and venous thromboembolism: association according to international classification of diseases, ninth revision hospital discharge diagnosis codes. Clin Infect Dis 58(4):495–501. doi:10.1093/cid/cit780

    Article  PubMed  Google Scholar 

  21. Chee CB, James L (2003) The Singapore tuberculosis elimination programme: the first five years. Bull World Health Organ 81(3):217–221

    PubMed  PubMed Central  Google Scholar 

  22. Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40(5):373–383

    Article  CAS  PubMed  Google Scholar 

  23. Cegielski JP, McMurray DN (2004) The relationship between malnutrition and tuberculosis: evidence from studies in humans and experimental animals. Int J Tuberc Lung Dis 8(3):286–298

    CAS  PubMed  Google Scholar 

  24. Herring AA, Woolhandler S, Himmelstein DU (2008) Insurance status of U.S. organ donors and transplant recipients: the uninsured give, but rarely receive. Int J Health Serv 38(4):641–652

    Article  PubMed  Google Scholar 

  25. Erdozain JG, Ruiz-Irastorza G, Egurbide MV, Martinez-Berriotxoa A, Aguirre C (2006) High risk of tuberculosis in systemic lupus erythematosus? Lupus 15(4):232–235

    Article  CAS  PubMed  Google Scholar 

  26. González León R, Garrido Rasco R, Chinchilla Palomares E, García Hernández FJ, Castillo Palma MJ, Sánchez Román J (2010) Tuberculosis in a cohort of patients with systemic lupus erythematosus. Reumatol Clin 6 (5):256–261

    Article  PubMed  Google Scholar 

  27. WHO (2016) Global tuberculosis report 2016. http://apps.who.int/iris/bitstream/10665/250441/250441/9789241565394-eng.pdf?ua=9789241565391. Accessed 26 Jan 2017

  28. Sayarlioglu M, Inanc M, Kamali S, Cefle A, Karaman O, Gul A, Ocal L, Aral O, Konice M (2004) Tuberculosis in Turkish patients with systemic lupus erythematosus: increased frequency of extrapulmonary localization. Lupus 13(4):274–278

    Article  CAS  PubMed  Google Scholar 

  29. Pasoto SG, Borba EF, Bonfa E, Shinjo SK (2010) Lupus pleuritis: a relevant risk factor for pulmonary tuberculosis. Lupus 19(14):1585–1590. doi:10.1177/0961203310375269

    Article  CAS  PubMed  Google Scholar 

  30. Ghosh K, Patwardhan M, Pradhan V (2009) Mycobacterium tuberculosis infection precipitates SLE in patients from endemic areas. Rheumatol Int 29(9):1047–1050. doi:10.1007/s00296-009-0903-x

    Article  PubMed  Google Scholar 

  31. Agrawal PN, Gupta D, Aggarwal AN, Behera D (2000) Incidence of tuberculosis among patients receiving treatment with oral corticosteroids. J Assoc Physicians India 48(9):881–884

    CAS  PubMed  Google Scholar 

  32. Jick SS, Lieberman ES, Rahman MU, Choi HK (2006) Glucocorticoid use, other associated factors, and the risk of tuberculosis. Arthritis Rheum 55(1):19–26. doi:10.1002/art.21705

    Article  PubMed  Google Scholar 

  33. Alarcon GS (2006) Infections in systemic connective tissue diseases: systemic lupus erythematosus, scleroderma, and polymyositis/dermatomyositis. Infect Dis Clin North Am 20 (4):849–875. doi:10.1016/j.idc.2006.09.007

    Article  PubMed  Google Scholar 

  34. Lawn SD, Zumla AI (2011) Tuberculosis. Lancet 378(9785):57–72. doi:10.1016/S0140-6736(10)62173-3

    Article  PubMed  Google Scholar 

  35. Ribeiro FM, Szyper-Kravitz M, Klumb EM, Lannes G, Ribeiro FR, Albuquerque EM, Shoenfeld Y (2010) Can lupus flares be associated with tuberculosis infection? Clin Rev Allergy Immunol 38 (2–3):163–168. doi:10.1007/s12016-009-8149-7

    Article  CAS  PubMed  Google Scholar 

  36. Isenberg DA, Maddison P, Swana G, Skinner RP, Swana M, Jones M, Addison I, Dudeney C, Shall S, el Roiey A et al (1987) Profile of autoantibodies in the serum of patients with tuberculosis, klebsiella and other gram-negative infections. Clin Exp Immunol 67(3):516–523

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Alard JE, Dueymes M, Youinou P, Jamin C (2007) Modulation of endothelial cell damages by anti-Hsp60 autoantibodies in systemic autoimmune diseases. Autoimmun Rev 6(7):438–443. doi:10.1016/j.autrev.2007.01.012

    Article  CAS  PubMed  Google Scholar 

  38. Orbach H, Zandman-Goddard G, Amital H, Barak V, Szekanecz Z, Szucs G, Danko K, Nagy E, Csepany T, Carvalho JF, Doria A, Shoenfeld Y (2007) Novel biomarkers in autoimmune diseases: prolactin, ferritin, vitamin D, and TPA levels in autoimmune diseases. Ann N Y Acad Sci 1109:385–400. doi:10.1196/annals.1398.044

    Article  CAS  PubMed  Google Scholar 

  39. Carvalho JF, Blank M, Kiss E, Tarr T, Amital H, Shoenfeld Y (2007) Anti-vitamin D, vitamin D in SLE: preliminary results. Ann N Y Acad Sci 1109:550–557. doi:10.1196/annals.1398.061

    Article  CAS  PubMed  Google Scholar 

  40. Jhung MA, Banerjee SN (2009) Administrative coding data and health care-associated infections. Clin Infect Dis 49(6):949–955. doi:10.1086/605086

    Article  PubMed  Google Scholar 

  41. Arenas Miras Mdel M, Hidalgo Tenorio C, Jimenez Alonso J (2013) Tuberculosis in patients with systemic lupus erythematosus: Spain’s situation. Reumatol Clin 9(6):369–372

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge Mr Benedict Tan and Mrs Bessie Ang for their contribution with the database preparation. We also thank all other staff of the Department of Epidemiology at for logistical support and the patients, who all made the study possible.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong Yang.

Ethics declarations

Conflict of interest

The authors declare that no financial or other relationships exist that might lead to a conflict of interest.

Financial support

None reported.

Ethical approval

The protocol for this study was approved by the Institutional Review Board of our hospital with waive of informed consent, as only database review was used in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Thumboo, J., Tan, B.H. et al. The risk of tuberculosis in SLE patients from an Asian tertiary hospital. Rheumatol Int 37, 1027–1033 (2017). https://doi.org/10.1007/s00296-017-3696-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00296-017-3696-3

Keywords

Navigation