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Opportunistic Infections Associated with TNF-Α Treatment

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Opportunistic Infections Associated with TNF-Α Treatment REVIEW Opportunistic infections associated with TNF-α treatment Robert Orenstein & The therapeutic agents known as TNF-α inhibitors have been widely adopted as effective Eric L Matteson† and standard therapy for many rheumatic diseases. Since their introduction into clinical †Author for correspondence practice, there has been concern that these agents that blunt host immunity to intracellular Mayo Clinic College of pathogens would lead to the development of opportunistic infections. Early reports of Medicine, Division of Rheumatology, Department of extrapulmonary tuberculosis, listeriosis, Pneumocystis jiroveci pneumonia and invasive Internal Medicine, fungal diseases seemed to confirm this association. Prospective and retrospective studies, 200 First Street SW registries, adverse reporting databases and experience from clinical practices indicate at Rochester, MN 55905, USA least a twofold risk of serious bacterial infections with TNFs versus standard DMARDs but data Tel.: +1 507 284 8450; are limited on opportunistic infections (OIs). This article will review the available data on OIs Fax: +1 507 284 0564; [email protected] describing these risks and studies that have been done to reduce that risk. Opportunistic infections (OIs) are infections innate immune system [2]. It is critical in the for- caused by organisms that ordinarily do not lead to mation and maintenance of granulomas and disease unless the host is immunodeficient, when production of IFN-γ. The complete inhibition they may cause significant morbidity and mortal- of TNF may allow for the dissolution of granu- ity [1]. The predisposition to OIs often relates to lomas and inability to maintain latency. On the an inherited, acquired or medication-induced other hand, less potent inhibition may affect defect in immune function. Often, multiple granuloma formation but not maintenance, thus defects are present due to the underlying illness of allowing for acute infection but not reactivation. the host and its treatment. The host defects TNF is required for defense against intracellu- induced by various immunosuppressive agents lar pathogens, is involved in the Th1-mediated differ and their effects may be multiplicative. One immune response and affects apoptosis. In mice, of the challenges in defining opportunistic TNF induces apoptosis of macrophages, which infections in this group of patients is their under- may provide sanctuary sites to intracellular lying risk for granulomatous and intracellular organisms. infections, even in the absence of therapy. In these mice, the absence of TNF-α may Many OIs are due to intracellular pathogens, lead to dissolution of granulomas that previously whereby the principal host defect lies in the initi- contained mycobacteria [3,4]. Infliximab may ation of the cellular immune response. These induce apoptosis in monocytes potentially inhib- include tuberculosis (TB), atypical mycobacte- iting the memory T-cell immune response for rial infection, salmonellosis, listeriosis, invasive maintenance of granulomas [5,6]. Studies in mice and endemic fungal disease, legionellosis, para- in whom the ability to produce TNF-α was sitic diseases (Strongyloides, Leishmania, Toxo- genetically blocked demonstrated enhanced sus- plasma) and opportunistic viruses such as ceptibility to intracellular pathogens and dissem- cytomegalovirus (CMV) varicella zoster virus ination of previously contained granulomatous (VZV), herpes simplex virus (HSV) and infections [7]. Epstein–Barr virus (EBV). TNF is important in chemokine regulation; TNF-α inhibitor therapy has become widely increasing adhesion molecule expression; mediat- used in the management of autoimmune disor- ing macrophage apoptosis and limiting excessive ders, including rheumatoid arthritis, Crohn’s dis- type 1 immune activation during intracellular ease, ankylosing spondylitis and psoriatic infection [8,9]. It has a direct impact on the innate arthritis. The currently available anti-TNF immune system by affecting specific Toll-like Keywords: adalimumab, agents infliximab, etanercept and adalimumab receptors (TLRs) and decreasing the presentation etanercept, infliximab, opportunistic infections, vary in structure, pharmacology, effect duration, of antigens to T-cells [10]. Although we tend to TNF-α inhibitors specific targets, effectiveness and side effects. generalize about the role of TNF-α, the specific TNF plays several critical roles in the host actions upon inflammatory and immune func- part of immune response: affecting cytokine regulation, tion may vary depending upon the component neutrophil recruitment, T-cell activation and the which is blocked. Blockade of the soluble portion 10.2217/17460816.2.6.567 © 2007 Future Medicine Ltd ISSN 1746-0816 Future Rheumatol. (2007) 2(6), 567–576 567 REVIEW – Orenstein & Matteson of TNF activity may inhibit the inflammatory Despite this apparent low risk, there are response without adversely impacting the innate numerous case reports and series of serious and immune response to infection [11,12]. Conversely, opportunistic infections in recipients of TNF blockade of both transmembrane and soluble blocking agents. In an attempt to clarify the con- TNF may blunt both. fusion between serious infection rates reported The risk of infections associated with TNF from clinical trials and that of clinical practice, blockade may also be related to genomic and Salliot and colleagues looked at a large-clinic pharmacodynamic factors. Specific poly- practice of patients with rheumatic diseases morphisms in the TNF-α gene may predispose treated before and after the use of TNF inhibi- to more serious or frequent infections in tors, using the patients themselves as controls. In certain individuals, which may also be dose this study of 709 patients, they found the inci- dependent [13]. dence of serious infections in the TNF inhibitor- Because of TNF-α’s central role in host treated group was increased threefold. They cal- defenses, several clinically important questions culated a number needed to harm (NNH) of impact those receiving TNF-blocking agents: only 14 for the first year of treatment [22]. The • Are there more infections in patients receiving serious infections were evenly distributed these agents? amongst the three agents. Serious skin and soft- tissue infections and pulmonary infections pre- • Which specific infections are most frequently dominated. Bacterial infections accounted for seen? 74.5%, viral for 10.6%, mycobacterial for 4.2%, • Are these infections serious or opportunistic? parasitic for 2.1% and fungal for 2.1% of serious infections. In a multivariate model, the risk fac- Serious infections & TNF inhibitors tors most often associated with serious infections The precise degree to which TNF inhibitors are were previous joint surgery and high previous associated with increased infection risks is diffi- cumulative steroid dose. cult to ascertain due to a host of study design In a meta-analysis of randomized controlled limitations. From experience in clinical practice, trials of infliximab and adalimumab in RA, the it is apparent that patients receiving these agents overall risk of serious infections in TNF inhibi- develop serious and disseminated infections tor-treated patients was twice that of those often early in their use. treated with standard therapies, even excluding While this review focuses on OIs, any infec- the granulomatous infections, although the rela- tion that requires hospitalization, intravenous tive risk of OIs could not be assessed [23]. In a anti-infectives or causes significant morbidity or stratified analysis according to dose, higher doses death is defined as a serious infection. The fre- of adalimumab and infliximab appeared to be quency and types of infection may vary with the associated with an increased risk. These authors host’s underlying disease. Patients with RA have calculated the NNH was 59 within a treatment an increased baseline risk of serious infection period of 3–12 months [23]. 1.8-times that of non-RA patients [14]. In a large Case reports and passive surveillance provide primary care cohort of patients with polyarthri- another window to the infectious morbidity asso- tis, the overall infection incidence was greater ciated with these agents. In a review of the US than 2.5-times that of the general population. FDA’s MedWatch Adverse Event Reporting Sys- Smoking, corticosteroid use and a positive rheu- tem for reports of granulomatous infections asso- matoid factor were independent predictors of ciated with infliximab or etanercept use, from infection-related hospitalization. Those with all 1998 to 2002, a total of 639 granulomatous three risk factors were seven-times more likely to infections were reported among 197,000 patients be hospitalized [15]. who had received infliximab and 113,000 etaner- In clinical trials of the three TNF inhibitors, cept respectively [24,25]. Of these patients, 40% the observed serious infection event (SIE) rate is received concomitant immunosuppression with two to six serious infections/100 patient-years either methotrexate or corticosteroids. The over- [16–21]. The incidence of serious infections was all rate of granulomatous infection was 4.1 per 100 patient-years (1%) with etanercept 129/100,000 treated patients for infliximab and [16], four per 100 patient-years with adalimumab 60/100,000 for etanercept. The most frequently and both similar to placebo [17]. The overall seri- reported granulomatous infections were tubercu- ous infection risk from most clinical trials
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