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Safety of tumor necrosis factor inhibitors use for rheumatoid arthritis and ankylosing spondylitis in Africa, the Middle East, and Asia: focus on severe infections and tuberculosis

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Abstract

Multiple studies of patients in Western countries with rheumatoid arthritis (RA) and ankylosing spondylitis (AS) have indicated increased risk for active tuberculosis (TB) and other infections among these individuals. It has also been consistently reported that patients receiving tumor necrosis factor (TNF) inhibitors for these conditions have higher rates of active TB and other infections than RA or AS patients not receiving these medications. These issues have been studied less extensively in the Asia and Africa–Middle East regions, and information from these regions is important because of higher rates of TB in the general population. This paper reviews studies of RA and AS patients from Asia, Africa, and the Middle East who received TNF inhibitors. A literature search was conducted using http://www.ncbi.nlm.nih.gov/pubmed to collect and report these data. The years included in the PubMed literature search ranged from January 2000 to October 2011. Additionally, information from the China Hospital Knowledge Database was used to report data from Chinese patients with RA and AS treated with TNF inhibitors. Results from these studies indicate that the risk for active TB and other infections in AS and RA patients from Asia, Africa, and the Middle East are increased in patients receiving TNF inhibitors and that the risk is higher among those treated with monoclonal antibodies versus soluble TNF receptor.

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References

  1. Lawrence RC, Felson DT, Helmick CG et al (2008) Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum 58:26–35

    Article  Google Scholar 

  2. Zeng QY, Chen R, Daramawan J et al (2008) Rheumatic diseases in China. Arthritis Res Ther 10:R17

    Article  PubMed  Google Scholar 

  3. Symmons D, Mathers C, Pfleger B (2006) The global burden of rheumatoid arthritis in the year 2000. Working Paper, World Health Organization, Geneva www.who.int/healthinfo/statistics/bod_rheumatoidarthritis.pdf. Accessed 26 Apr 2012

  4. Al-Rawi ZS, Alazzawi AJ, Alajili FM, Alwakil R (1978) Rheumatoid arthritis in population samples in Iraq. Ann Rheum Dis 37:73–75

    Article  PubMed  CAS  Google Scholar 

  5. Pountain G (1991) The prevalence of rheumatoid arthritis in the Sultanate of Oman. Br J Rheumatol 30:24–28

    Article  PubMed  CAS  Google Scholar 

  6. Gabriel SE, Michaud K (2009) Epidemiological studies in incidence, prevalence, mortality, and comorbidity of the rheumatic diseases. Arthritis Res Ther 11:229

    Article  PubMed  Google Scholar 

  7. Hukuda S, Minami M, Saito T et al (2001) Spondyloarthropathies in Japan: nationwide questionnaire survey performed by the Japan Ankylosing Spondylitis Society. J Rheumatol 28:554–559

    PubMed  CAS  Google Scholar 

  8. Mijiyawa M, Oniankitan O, Khan MA (2000) Spondyloarthropathies in sub-Saharan Africa. Curr Opin Rheumatol 12:281–286

    Article  PubMed  CAS  Google Scholar 

  9. Brown MA, Jepson A, Young A, Whittle HC, Greenwood BM, Wordsworth BP (1997) Ankylosing spondylitis in West Africans—evidence for a non-HLA-B27 protective effect. Ann Rheum Dis 56:68–70

    Article  PubMed  CAS  Google Scholar 

  10. Amroun H, Djoudi H, Busson M et al (2005) Early-onset ankylosing spondylitis is associated with a functional MICA polymorphism. Hum Immunol 66:1057–1061

    Article  PubMed  CAS  Google Scholar 

  11. Younsi R, Azrib S, Aitouazar M, Hari WG, El Hassani S (2007) Evaluation de ’incidence du gène HLA-B27 chez le patient attaint de spondlyarthrite ankylosante au Maroc. Revue de Rhumatisme 74:1013

    Google Scholar 

  12. Alonso-Ruiz A, Pijoan JI, Ansuategui E, Urkaregi A, Calabozo M, Quintana A (2008) Tumor necrosis factor alpha drugs in rheumatoid arthritis: systematic review and metaanalysis of efficacy and safety. BMC Musculoskelet Disord 9:52

    Article  PubMed  Google Scholar 

  13. Braun J, van den Berg R, Baraliakos X et al (2011) 2010 update of the ASAS/EULAR recommendations for the management of ankylosing spondylitis. Ann Rheum Dis 70:896–904

    Article  PubMed  CAS  Google Scholar 

  14. Raychaudhuri SP, Nguyen CT, Raychaudhuri SK, Gershwin ME (2009) Incidence and nature of infectious disease in patients treated with anti-TNF agents. Autoimmun Rev 9:67–81

    Article  PubMed  CAS  Google Scholar 

  15. Bernatsky S, Habel Y, Rahme E (2010) Observational studies of infections in rheumatoid arthritis: a metaanalysis of tumor necrosis factor antagonists. J Rheumatol 37:928–931

    Article  PubMed  CAS  Google Scholar 

  16. Gliklich RE, Dreyer NA et al (2010) Registries for evaluating patient outcomes: a user’s guide. Agency for Healthcare Research and Quality (US), Rockville

    Google Scholar 

  17. Singh JA, Wells GA, Christensen R et al (2011) Adverse effects of biologics: a network meta-analysis and Cochrane overview. Cochrane Database Syst Rev: CD008794

  18. Dixon WG, Symmons DPM, Lunt M et al (2007) Serious infection following anti-tumor necrosis factor α therapy in patients with rheumatoid arthritis: lessons from interpreting data from observational studies. Arthritis Rheum 56:2896–2904

    Article  PubMed  CAS  Google Scholar 

  19. United Nations (2009) Tuberculosis prevalence rate per 100,000 population (mid-point) http://data.un.org/Data.aspx?d=MDG&f=seriesRowID%3A617. Accessed 26 Apr 2012

  20. Dabbous O, Gilmer K, Tatsuki Y et al (2007) Tuberculosis in Japanese patients with rheumatoid arthritis treated with infliximab: findings from the post marketing surveillance trial. 2007 Annual ACR Meeting

  21. Komano Y, Tanaka M, Nanki T et al (2011) Incidence and risk factors for serious infection in patients with rheumatoid arthritis treated with tumor necrosis factor inhibitors: a report from the Registry of Japanese Rheumatoid Arthritis Patients for Longterm Safety. J Rheumatol 38:1258–1264

    Article  PubMed  CAS  Google Scholar 

  22. National Technic Steering Group of the Epidemiological Sampling Survey for Tuberculosis, Duanmu H (2002) [Report on fourth national epidemiological sampling survey of tuberculosis]. Zhonghua Jie He He Hu Xi Za Zhi 25:3–7

    PubMed  Google Scholar 

  23. Hu DW, Bao CD, Chen SL et al (2005) Treatment of rheumatoid arthritis with a recombinant human tumor necrosis factor-Fc fusion protein: a multicenter, randomized, double blind, controlled trial. Chin J Rheumatol 9:664–668

    Google Scholar 

  24. Hou Y, Zhang FC, Huang F et al (2005) Infliximab versus placebo in rheumatoid arthritis receiving concomitant methotrexate: a randomized double blind phase III trial in China. Chin J Rheumatol 10:658–663

    Google Scholar 

  25. Huang F, Wang L, Zhang J, Deng X, Guo J, Zhang Y (2006) Risk of tuberculosis in a Chinese registry of rheumatoid arthritis and ankylosing spondylitis for tumour necrosis factor-α antagonists. APLAR J Rheumatol 9:170–174

    Article  Google Scholar 

  26. Huang F, Zhang FC, Bao CD et al (2009) Adalimumab plus methotrexate for the treatment of rheumatoid arthritis: a multi-center randomized, double-blind, placebo-controlled clinical study. Zhonghua Nei Ke Za Zhi 48:916–921

    PubMed  Google Scholar 

  27. Tam LS, Leung CC, Ying SK et al (2010) Risk of tuberculosis in patients with rheumatoid arthritis in Hong Kong—the role of TNF blockers in an area of high tuberculosis burden. Clin Exp Rheumatol 28:679–685

    PubMed  Google Scholar 

  28. Wang LS, Huang F, Zhang JL et al (2007) A cohort analysis of safety tumor necrosis factor- antagonists in the treatment of Chinese patients with ankylosing spondylitis. Chin J New Drugs 16:556–561

    Google Scholar 

  29. Chen DY, Chou SJ, Hsieh TY et al (2009) Randomized, double-blind, placebo-controlled, comparative study of human anti-TNF antibody adalimumab in combination with methotrexate and methotrexate alone in Taiwanese patients with active rheumatoid arthritis. J Formos Med Assoc 108:310–319

    Article  PubMed  CAS  Google Scholar 

  30. Chen DY, Shen GH, Hsieh TY, Hsieh CW, Lan JL (2008) Effectiveness of the combination of a whole-blood interferon-gamma assay and the tuberculin skin test in detecting latent tuberculosis infection in rheumatoid arthritis patients receiving adalimumab therapy. Arthritis Rheum 59:800–806

    Article  PubMed  CAS  Google Scholar 

  31. Chen DY, Shen GH, Hsieh TY, Hsieh CW, Lan JL (2012) Biphasic emergence of active tuberculosis in rheumatoid arthritis patients receiving TNF{alpha} inhibitors: the utility of IFNγ assay. Ann Rheum Dis 71:231–237

    Article  PubMed  CAS  Google Scholar 

  32. Navarra S, Raso AA, Linchauco JJ, Tan P (2006) Clinical experience with infliximab among Filipino patients with rheumatic diseases. Int J Rheumatic Dis 9:150–156

    Google Scholar 

  33. Seong SS, Choi CB, Woo JH et al (2007) Incidence of tuberculosis in Korean patients with rheumatoid arthritis (RA): effects of RA itself and of tumor necrosis factor blockers. J Rheumatol 34:706–711

    PubMed  CAS  Google Scholar 

  34. Kim EM, Uhm WS, Bae SC, Yoo DH, Kim TH (2011) Incidence of tuberculosis among Korean patients with ankylosing spondylitis who are taking tumor necrosis factor blockers. J Rheumatol 38:2218–2223

    Article  PubMed  Google Scholar 

  35. Suwannalai P, Auethavekiat P, Udomsubpayakul U, Janvitayanujit S (2009) The infectious profiles of anti-tumor necrosis factor agents in a Thai population: a retrospective study a the university-based hospital. Int J Rheum Dis 12:118–124

    Article  PubMed  Google Scholar 

  36. Kumar A (2006) Experience with anti-tumor necrosis factor-α therapy in India. APLAR J Rheumatol 9:141

    Article  Google Scholar 

  37. Allali F, Rkain H, Faik A, El Hassani S, Hajjaj-Hassouni N (2005) Prevalence and clinical characteristics of tuberculosis in rheumatoid arthritis patients. Clin Rheumatol 24:656–657

    Google Scholar 

  38. El Mansouri L, Bahiri R, Abourazzak FE, Abouqal R, Hajjaj-Hassouni N (2009) Two distinct patterns of ankylosing spondylitis in Moroccan patients. Rheumatol Int 29:1423–1429

    Article  PubMed  Google Scholar 

  39. Public Health Agency of Canada (2011) International tuberculosis incidence rates. http://www.phac-aspc.gc.ca/tbpc-latb/itir-eng.php. Accessed 17 Jul 2012

  40. Salmon-Ceron D, Tubach F, Lortholary O et al (2011) Drug-specific risk of non-tuberculosis opportunistic infections in patients receiving anti-TNF therapy reported to the 3-year prospective French RATIO registry. Ann Rheum Dis 70:616–623

    Article  PubMed  CAS  Google Scholar 

  41. Galloway JB, Hyrich KL, Mercer LK et al (2011) Anti-TNF therapy is associated with an increased risk of serious infections in patients with rheumatoid arthritis especially in the first 6 months of treatment: updated results from the British Society for Rheumatology Biologics Register with special emphasis on risks in the elderly. Rheumatol (Oxford) 50:124–131

    Article  CAS  Google Scholar 

  42. Dixon WG, Hyrich KL, Watson KD et al (2010) Drug-specific risk of tuberculosis in patients with rheumatoid arthritis treated with anti-TNF therapy: results from the British Society for Rheumatology Biologics Register (BSRBR). Ann Rheum Dis 69:522–528

    Article  PubMed  CAS  Google Scholar 

  43. Greenberg JD, Reed G, Kremer JM et al (2010) Association of methotrexate and tumour necrosis factor antagonists with risk of infectious outcomes including opportunistic infections in the CORRONA registry. Ann Rheum Dis 69:380–386

    Article  PubMed  CAS  Google Scholar 

  44. Carmona L, Gómez-Reino JJ, BIOBADASER Group (2006) Survival of TNF antagonists in spondylarthritis is better than in rheumatoid arthritis. Data from the Spanish registry BIOBADASER. Arthritis Res Ther 8:R72

    Article  PubMed  Google Scholar 

  45. Al-Ghamdi A, Attar SM (2009) Extra-articular manifestations of rheumatoid arthritis: a hospital-based study. Ann Saudi Med 29:189–193

    PubMed  Google Scholar 

  46. Attar SM, Al-Ghamdi A (2010) Radiological changes in rheumatoid arthritis patients at a teaching hospital in Saudi Arabia. East Mediterr Health J 16:953–957

    PubMed  CAS  Google Scholar 

  47. Kazkaz L, Marotte H, Hamwi M et al (2007) Rheumatoid arthritis and genetic markers in Syrian and French populations: different effect of the shared epitope. Ann Rheum Dis 66:195–201

    Article  PubMed  CAS  Google Scholar 

  48. Winthrop KL (2010) The risk and prevention of tuberculosis: screening strategies to detect latent tuberculosis among rheumatoid arthritis patients who use biologic therapy. Int J Adv Rheumatol 8:43–52

    Google Scholar 

  49. Wallis RS, Ehlers S (2005) Tumor necrosis factor and granuloma biology: explaining the differential infection risk of etanercept and infliximab. Semin Arthritis Rheum 34:34–38

    Article  PubMed  CAS  Google Scholar 

  50. Tubach F, Salmon D, Ravaud P et al (2009) Risk of tuberculosis is higher with anti-tumor necrosis factor monoclonal antibody therapy than with soluble tumor necrosis factor receptor therapy: the three-year prospective French Research Axed on Tolerance of Biotherapies Registry. Arthritis Rheum 60:1884–1894

    Google Scholar 

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Acknowledgments

Editorial/medical writing support was provided by WC Hatch at ACUMED and was funded by Pfizer Inc. No financial support was provided to the authors for this work.

Disclosures

Abdurhman Alarfaj has consulted and received honorarium from Pfizer Inc. Mohammed Hammoudeh has consulted for Schering-Plough Corp and consulted and received honoraria from Abbott Laboratories, Pfizer Inc, Roche Pharmaceuticals, and Wyeth Pharmaceuticals. He has received grant/research support from Pfizer Inc, Roche Pharmaceuticals, Schering-Plough Corp, and Wyeth Pharmaceuticals. Ehab Youseif is a Senior Regional Director, Medical Affairs for Pfizer Latin America. Der-Yuan Chen, Hachemi Djoudi, and Jian Zhu declare no conflicts of interest.

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Authors and Affiliations

  1. Hamad Medical Corporation, PO Box 3050, Doha, Qatar

    Mohammed Hammoudeh

  2. Department of Medicine, College of Medicine, King Saud University, Riyadh, P.O. Box. 7805 (38), 11472, Saudi Arabia

    Abdurhman Alarfaj

  3. Faculty of Medicine, National Yang Ming University, Taipei, Taiwan

    Der-Yuan Chen

  4. Division of Allergy, Immunology and Rheumatology, Taichung Veterans General Hospital, No. 160, Sec 3, Chung-Kang Rd, Taichung City, 00407, Taiwan

    Der-Yuan Chen

  5. Rheumatology Department, EHS Douéra, Algiers, Algeria

    Hachemi Djoudi

  6. Pfizer Inc, Collegeville, PA, 19426, USA

    Ehab Youseif

  7. Chinese PLA General Hospital, 28 FuXing Road, Beijing, 100853, China

    Jian Zhu

  8. Division of Rheumatology, Department of Medicine, Hamad Medical Corporation, PO Box 3050, Doha, Qatar

    Mohammed Hammoudeh

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  1. Mohammed Hammoudeh
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  2. Abdurhman Alarfaj
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Correspondence to Mohammed Hammoudeh.

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Hammoudeh, M., Alarfaj, A., Chen, DY. et al. Safety of tumor necrosis factor inhibitors use for rheumatoid arthritis and ankylosing spondylitis in Africa, the Middle East, and Asia: focus on severe infections and tuberculosis. Clin Rheumatol 32, 293–300 (2013). https://doi.org/10.1007/s10067-012-2137-7

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  • DOI: https://doi.org/10.1007/s10067-012-2137-7

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