Abstract
The evolution of inflammatory diseases has radically changed since the introduction of biologic therapies, such as tumour necrosis factor alpha inhibitors (anti-TNFα). They, therefore, represent a widely used therapeutic modality. Nevertheless, post-marketing studies reveal an increased risk of infection in patients taking these drugs, especially granulomatous infections such as listeriosis. We aimed to evaluate the reported cases of listeriosis in patients treated with biologic treatments. We used the United States Food and Drug Administration (FDA) Adverse Event Reporting System (AERS) from 2004 to 2011. We also perform a literature review of previously reported cases of listeriosis in patients taking biologic therapies. We identified 266 cases of Listeria monocytogenes infection associated with biologic therapies. The majority of patients were receiving infliximab (77.1 %), followed by etanercept (11.7 %), adalimumab (9.8 %), rituximab (4.1 %), abatacept (0.4 %) and golimumab (0.4 %). Indications for the use of biologics were as follows: 47.7 % for rheumatologic diseases, 38 % for inflammatory bowel diseases, 3.4 % for haematological diseases and 10.5 % for other indications. Seventy-three percent of the patients were receiving concomitant immunosuppressant drugs, especially steroids (56 %) and methotrexate (31.6 %). The median time to the onset of infection was 184 days. Mortality rates range from 11.1 % in adalimumab-treated patients to 27.3 % in rituximab-treated patients (p = 0.7). Listeriosis is common in biologics-treated patients, especially related to infliximab use given concomitantly with other immunosuppressive therapies. Infections after treatment with biologics mostly occurred in the first year after initiating treatment.
This is a preview of subscription content, access via your institution.
References
Netea MG, Radstake T, Joosten LA, van der Meer JW, Barrera P, Kullberg BJ (2003) Salmonella septicemia in rheumatoid arthritis patients receiving anti-tumor necrosis factor therapy: association with decreased interferon-gamma production and toll-like receptor 4 expression. Arthritis Rheum 48(7):1853–1857
Popa C, Netea MG, Barrera P, Radstake TR, van Riel PL, Kullberg BJ, Van der Meer JW (2005) Cytokine production of stimulated whole blood cultures in rheumatoid arthritis patients receiving short-term infliximab therapy. Cytokine 30(2):72–77
Camussi G, Albano E, Tetta C, Bussolino F (1991) The molecular action of tumor necrosis factor-alpha. Eur J Biochem 202(1):3–14
Mohan VP, Scanga CA, Yu K, Scott HM, Tanaka KE, Tsang E, Tsai MM, Flynn JL, Chan J (2001) Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect Immun 69(3):1847–1855
Saunders BM, Tran S, Ruuls S, Sedgwick JD, Briscoe H, Britton WJ (2005) Transmembrane TNF is sufficient to initiate cell migration and granuloma formation and provide acute, but not long-term, control of Mycobacterium tuberculosis infection. J Immunol 174(8):4852–4859
Janeway CA, Travers P, Walport M, Capra JD (1999) Immunobiology: the immune system in health and disease. Elsevier Science, London
Wallis RS, Broder MS, Wong JY, Hanson ME, Beenhouwer DO (2004) Granulomatous infectious diseases associated with tumor necrosis factor antagonists. Clin Infect Dis 38(9):1261–1265
Dixon WG, Watson K, Lunt M, Hyrich KL, Silman AJ, Symmons DP; British Society for Rheumatology Biologics Register (2006) Rates of serious infection, including site-specific and bacterial intracellular infection, in rheumatoid arthritis patients receiving anti-tumor necrosis factor therapy: results from the British Society for Rheumatology Biologics Register. Arthritis Rheum 54(8):2368–2376
Slifman NR, Gershon SK, Lee JH, Edwards ET, Braun MM (2003) Listeria monocytogenes infection as a complication of treatment with tumor necrosis factor alpha-neutralizing agents. Arthritis Rheum 48(2):319–324
Ramos JM, García-Sepulcre MF, Masiá M, Brotons A, Grau MC, Gutiérrez F (2010) Listeria monocytogenes infection in patients with inflammatory bowel diseases receiving anti-tumor necrosis factor therapy. Rev Esp Enferm Dig 102(10):614–616
Salmon-Ceron D, Tubach F, Lortholary O, Chosidow O, Bretagne S, Nicolas N, Cuillerier E, Fautrel B, Michelet C, Morel J, Puéchal X, Wendling D, Lemann M, Ravaud P, Mariette X; RATIO group (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(4):616–623
Hansen RA, Gartlehner G, Powell GE, Sandler RS (2007) Serious adverse events with infliximab: analysis of spontaneously reported adverse events. Clin Gastroenterol Hepatol 5(6):729–735
Rothe J, Lesslauer W, Lötscher H, Lang Y, Koebel P, Köntgen F, Althage A, Zinkernagel R, Steinmetz M, Bluethmann H (1993) Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364(6440):798–802
Nakane A, Minagawa T, Kato K (1988) Endogenous tumor necrosis factor (cachectin) is essential to host resistance against Listeria monocytogenes infection. Infect Immun 56(10):2563–2569
United States Food and Drug Administration (FDA) Adverse Event Reporting System (AERS) reports. Available online at: http://www.fda.gov/Drugs/GuidanceComplianceRegulatoryInformation/Surveillance/AdverseDrugEffects/ucm083765.htm
Kelesidis T, Salhotra A, Fleisher J, Uslan DZ (2010) Listeria endocarditis in a patient with psoriatic arthritis on infliximab: are biologic agents as treatment for inflammatory arthritis increasing the incidence of Listeria infections? J Infect 60(5):386–396
Williams G, Khan AA, Schweiger F (2005) Listeria meningitis complicating infliximab treatment for Crohn’s disease. Can J Infect Dis Med Microbiol 16(5):289–292
Tweezer-Zaks N, Shiloach E, Spivak A, Rapoport M, Novis B, Langevitz P (2003) Listeria monocytogenes sepsis in patients treated with anti-tumor necrosis factor-alpha. Isr Med Assoc J 5(11):829–830
Morelli J, Wilson FA (2000) Does administration of infliximab increase susceptibility to listeriosis? Am J Gastroenterol 95(3):841–842
Kesteman T, Yombi JC, Gigi J, Durez P (2007) Listeria infections associated with infliximab: case reports. Clin Rheumatol 26(12):2173–2175
Kamath BM, Mamula P, Baldassano RN, Markowitz JE (2002) Listeria meningitis after treatment with infliximab. J Pediatr Gastroenterol Nutr 34(4):410–412
Izbéki F, Nagy F, Szepes Z, Kiss I, Lonovics J, Molnár T (2008) Severe Listeria meningoencephalitis in an infliximab-treated patient with Crohn’s disease. Inflamm Bowel Dis 14(3):429–431
Bowie VL, Snella KA, Gopalachar AS, Bharadwaj P (2004) Listeria meningitis associated with infliximab. Ann Pharmacother 38(1):58–61
Ljung T, Karlén P, Schmidt D, Hellström PM, Lapidus A, Janczewska I, Sjöqvist U, Löfberg R (2004) Infliximab in inflammatory bowel disease: clinical outcome in a population based cohort from Stockholm County. Gut 53(6):849–853
Glück T, Linde HJ, Schölmerich J, Müller-Ladner U, Fiehn C, Bohland P (2002) Anti-tumor necrosis factor therapy and Listeria monocytogenes infection: report of two cases. Arthritis Rheum 46(8):2255–2257, author reply 2257
Aparicio AG, Muñoz-Fernández S, Bonilla G, Miralles A, Cerdeño V, Martín-Mola E (2003) Report of an additional case of anti-tumor necrosis factor therapy and Listeria monocytogenes infection: comment on the letter by Glück et al. Arthritis Rheum 48(6):1764–1765, author reply 1765–1766
Peña-Sagredo JL, Hernández MV, Fernandez-Llanio N, Giménez-Ubeda E, Muñoz-Fernández S, Ortiz A, Gonzalez-Gay MA, Fariñas MC; Biobadaser group (2008) Listeria monocytogenes infection in patients with rheumatic diseases on TNF-alpha antagonist therapy: the Spanish Study Group experience. Clin Exp Rheumatol 26(5):854–859
Fernàndez-Sabé N, Cervera C, López-Medrano F, Llano M, Sáez E, Len O, Fortún J, Blanes M, Laporta R, Torre-Cisneros J, Gavaldà J, Muñoz P, Fariñas MC, María Aguado J, Moreno A, Carratalà J (2009) Risk factors, clinical features, and outcomes of listeriosis in solid-organ transplant recipients: a matched case–control study. Clin Infect Dis 49(8):1153–1159
Chiba M, Fukushima T, Koganei K, Nakamura N, Masamune O (1998) Listeria monocytogenes in the colon in a case of fulminant ulcerative colitis. Scand J Gastroenterol 33(7):778–782
Goulet V, Hebert M, Hedberg C, Laurent E, Vaillant V, De Valk H, Desenclos JC (2012) Incidence of listeriosis and related mortality among groups at risk of acquiring listeriosis. Clin Infect Dis 54(5):652–660
Ehlers S (2005) Tumor necrosis factor and its blockade in granulomatous infections: differential modes of action of infliximab and etanercept? Clin Infect Dis 41(Suppl 3):S199–S203
Wallis RS, Ehlers S (2005) Tumor necrosis factor and granuloma biology: explaining the differential infection risk of etanercept and infliximab. Semin Arthritis Rheum 34(5 Suppl1):34–38
Scallon B, Cai A, Solowski N, Rosenberg A, Song XY, Shealy D, Wagner C (2002) Binding and functional comparisons of two types of tumor necrosis factor antagonists. J Pharmacol Exp Ther 301(2):418–426
Bortolussi R (2008) Listeriosis: a primer. CMAJ 179(8):795–797
Skogberg K, Syrjänen J, Jahkola M, Renkonen OV, Paavonen J, Ahonen J, Kontiainen S, Ruutu P, Valtonen V (1992) Clinical presentation and outcome of listeriosis in patients with and without immunosuppressive therapy. Clin Infect Dis 14(4):815–821
Centers for Disease Control and Prevention (CDC) disease information. Listeria (Listeriosis). Available online at: http://www.cdc.gov/listeria/. Accessed 28 Nov 2012
Acknowledgments
Dr. Bodro is the recipient of a research grant from the Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona, Spain, and a mobility grant from the Sociedad Española de Enfermedades Infecciosas y Microbiología Clínica (SEIMC).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bodro, M., Paterson, D.L. Listeriosis in patients receiving biologic therapies. Eur J Clin Microbiol Infect Dis 32, 1225–1230 (2013). https://doi.org/10.1007/s10096-013-1873-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10096-013-1873-1
Keywords
- Infliximab
- Etanercept
- Adalimumab
- Biologic Therapy
- Abatacept