Pai M, Denkinger CM, Kik SV, Rangaka MX, Zwerling A, Oxlade O, Metcalfe JZ, Cattamanchi A, Dowdy DW, Dheda K, Banaei N, 2014. Gamma interferon release assays for detection of Mycobacterium tuberculosis infection. Clin Microbiol Rev 27: 3–20.
Santin M, Muñoz L, Rigau D, 2012. Interferon-γ release assays for the diagnosis of tuberculosis and tuberculosis infection in HIV-infected adults: a systematic review and meta-analysis. PLoS One 7: e32482.
Sester M, van Leth F, Bruchfeld J, Bumbacea D, Cirillo DM, Dilektasli AG, Domínguez J, Duarte R, Ernst M, Eyuboglu FO, Gerogianni I, Girardi E, Goletti D, Janssens J-P, Julander I, Lange B, Latorre I, Losi M, Markova R, Matteelli A, Milburn H, Ravn P, Scholman T, Soccal PM, Straub M, Wagner D, Wolf T, Yalcin A, Lange C; TBNET, 2014. Risk assessment of tuberculosis in immunocompromised patients. A TBNET study. Am J Respir Crit Care Med 190: 1168–1176.
Goletti D, Raja A, Syed Ahamed Kabeer B, Rodrigues C, Sodha A, Carrara S, Vernet G, Longuet C, Ippolito G, Thangaraj S, Leportier M, Girardi E, Lagrange PH, 2010. Is IP-10 an accurate marker for detecting M. tuberculosis-specific response in HIV-infected persons? PLoS One 5: e12577.
Vanini V, Petruccioli E, Gioia C, Cuzzi G, Orchi N, Rianda A, Alba L, Giancola ML, Conte A, Schininà V, Busi Rizzi E, Girardi E, Goletti D, 2012. IP-10 is an additional marker for tuberculosis (TB) detection in HIV-infected persons in a low-TB endemic country. J Infect 65: 49–59.
Belard E, Semb S, Ruhwald M, Werlinrud AM, Soborg B, Jensen FK, Thomsen H, Brylov A, Hetland ML, Nordgaard-Lassen I, Ravn P, 2011. Prednisolone treatment affects the performance of the QuantiFERON gold in-tube test and the tuberculin skin test in patients with autoimmune disorders screened for latent tuberculosis infection. Inflamm Bowel Dis 17: 2340–2349.
Aabye MG, Hermansen TS, Ruhwald M, Praygod G, Faurholt-Jepsen D, Jeremiah K, Faurholt-Jepsen M, Range N, Friis H, Changalucha J, Andersen AB, Ravn P, 2012. Negative effect of smoking on the performance of the QuantiFERON TB gold in tube test. BMC Infect Dis 12: 379.
Rose MV, Kimaro G, Nissen TN, Kroidl I, Hoelscher M, Bygbjerg IC, Mfinanga SG, Ravn P, 2012. QuantiFERON®-TB Gold in-tube performance for diagnosing active tuberculosis in children and adults in a high burden setting. PLoS One 7: e37851.
Lucas M, Nicol P, McKinnon E, Whidborne R, Lucas A, Thambiran A, Burgner D, Waring J, French M, 2010. A prospective large-scale study of methods for the detection of latent Mycobacterium tuberculosis infection in refugee children. Thorax 65: 442–448.
Banfield S, Pascoe E, Thambiran A, Siafarikas A, Burgner D, 2012. Factors associated with the performance of a blood-based interferon-gamma release assay in diagnosing tuberculosis. PLoS One 7: e38556.
Ruhwald M, Aabye MG, Ravn P, 2012. IP-10 release assays in the diagnosis of tuberculosis infection: current status and future directions. Expert Rev Mol Diagn 12: 175–187.
Chegou NN, Heyckendorf J, Walzl G, Lange C, Ruhwald M, 2014. Beyond the IFN-γ horizon: biomarkers for immunodiagnosis of infection with Mycobacterium tuberculosis. Eur Respir J 43: 1472–1486.
Kabeer BSA, Sikhamani R, Raja A, 2010. Comparison of interferon gamma and interferon gamma-inducible protein-10 secretion in HIV-tuberculosis patients. AIDS 24: 323–325.
Aabye MG, Ruhwald M, Praygod G, Jeremiah K, Faurholt-Jepsen M, Faurholt-Jepsen D, Range N, Friis H, Changalucha J, Andersen AB, Ravn P, 2010. Potential of interferon-γ-inducible protein 10 in improving tuberculosis diagnosis in HIV-infected patients. Eur Respir J 36: 1488–1490.
Schofield L, Grau GE, 2005. Immunological processes in malaria pathogenesis. Nat Rev Immunol 5: 722–735.
Enwere GC, Ota MO, Obaro SK, 1999. The host response in malaria and depression of defence against tuberculosis. Ann Trop Med Parasitol 93: 669–678.
Chougnet C, Tallet S, Ringwald P, Deloron P, 1992. Kinetics of lymphocyte subsets from peripheral blood during a Plasmodium falciparum malaria attack. Clin Exp Immunol 90: 405–408.
Hviid L, Kurtzhals JA, Goka BQ, Oliver-Commey JO, Nkrumah FK, Theander TG, 1997. Rapid reemergence of T cells into peripheral circulation following treatment of severe and uncomplicated Plasmodium falciparum malaria. Infect Immun 65: 4090–4093.
Van Geertruyden J-P, Mulenga M, Kasongo W, Polman K, Colebunders R, Kestens L, D'Alessandro U, 2006. CD4 T-cell count and HIV-1 infection in adults with uncomplicated malaria. J Acquir Immune Defic Syndr 43: 363–367.
Elhassan IM, Hviid L, Satti G, Akerstrom B, Jakobsen PH, Jensen JB, Theander TG, 1994. Evidence of endothelial inflammation, T cell activation, and T cell reallocation in uncomplicated Plasmodium falciparum malaria. Am J Trop Med Hyg 51: 372–379.
Cellestis XXX. Manufacturer of QuantiFERON® Diagnostics and Research Products: Homepage. Available at: http://www.quantiferon.com/irm/content/PI/QFT/2PK/US.pdf. Accessed June 11, 2013.
Aabye MG, Eugen-Olsen J, Werlinrud AM, Holm LL, Tuuminen T, Ravn P, Ruhwald M, 2012. A simple method to quantitate IP-10 in dried blood and plasma spots. PLoS One 7: e39228.
Ruhwald M, Latorre I, Diaz J, Maldonado J, Mialdea I, Ravn P, Dominguez J, Aabye M, 2011. Specific diagnosis of tuberculosis infection sent via mail—IGRAs on paper. Eur Respir J 38 (Suppl 55): 1897.
Lucchi NW, Jain V, Wilson NO, Singh N, Udhayakumar V, Stiles JK, 2011. Potential serological biomarkers of cerebral malaria. Markers 31: 327–335.
Armah HB, Wilson NO, Sarfo BY, Powell MD, Bond VC, Anderson W, Adjei AA, Gyasi RK, Tettey Y, Wiredu EK, Tongren JE, Udhayakumar V, Stiles JK, 2007. Cerebrospinal fluid and serum biomarkers of cerebral malaria mortality in Ghanaian children. Malar J 6: 147.
Wilson NO, Jain V, Roberts CE, Lucchi N, Joel PK, Singh MP, Nagpal AC, Dash AP, Udhayakumar V, Singh N, Stiles JK, 2011. CXCL4 and CXCL10 predict risk of fatal cerebral malaria. Markers 30: 39–49.
McCall MBB, Sauerwein RW, 2010. Interferon—central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. J Leukoc Biol 88: 1131–1143.
Petrone L, Cannas A, Aloi F, Nsubuga M, Sserumkuma J, Nazziwa RA, Jugheli L, Lukindo T, Girardi E, Reither K, Goletti D, 2015. Blood or urine IP-10 cannot discriminate between active tuberculosis and respiratory diseases different from tuberculosis in children. BioMed Res Int 2015: 1–11.
Hviid L, Theander TG, Abu-Zeid YA, Abdulhadi NH, Jakobsen PH, Saeed BO, Jepsen S, Bayoumi RA, Jensen JB, 1991. Loss of cellular immune reactivity during acute Plasmodium falciparum malaria. FEMS Microbiol Immunol 3: 219–227.
Tagmouti S, Slater M, Benedetti A, Kik SV, Banaei N, Cattamanchi A, Metcalfe J, Dowdy D, van Zyl Smit R, Dendukuri N, Pai M, Denkinger C, 2014. Reproducibility of interferon gamma (IFN-γ) release assays. A systematic review. Ann Am Thorac Soc 11: 1267–1276.
Falade CO, Adesina-Adewole B, Dada-Adegbola HO, Ajayi IO, Akinyemi JO, Ademowo OG, Adewole IF, Kanki P, 2013. Evaluation of Paracheck-Pf™ rapid malaria diagnostic test for the diagnosis of malaria among HIV-positive patients in Ibadan, south-western Nigeria. Pathog Glob Health 107: 69–77.
Djallé D, Gody JC, Moyen JM, Tekpa G, Ipero J, Madji N, Breurec S, Manirakiza A, 2014. Performance of ParacheckTM-Pf, SD Bioline malaria Ag-Pf and SD Bioline malaria Ag-Pf/pan for diagnosis of falciparum malaria in the Central African Republic. BMC Infect Dis 14: 109.
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Interferon-gamma (IFN-γ) release assays (IGRAs) are used to detect cellular immune recognition of Mycobacterium tuberculosis. The chemokine IFN-γ-inducible protein 10 (IP-10) is an alternative diagnostic biomarker to IFN-γ. Several conditions interfere with IGRA test performance. We aimed to assess the possible influence of Plasmodium falciparum infection on the IGRA test QuantiFERON-TB GOLD® In-Tube (QFT) test and an in-house IP-10 release assay. In total, 241 Tanzanian adults were included; 184 patients with uncomplicated malaria (88 human immunodeficiency virus [HIV] coinfected) and 57 HIV-infected patients without malaria infection. Malaria was treated with artemether–lumefantrine (Coartem®). QFT testing was performed before initiation of malaria treatment and at days 7 and 42. In total, 172 patients completed follow-up. IFN-γ and IP-10 was measured in QFT supernatants. We found that during malaria infection IFN-γ and IP-10 levels in the unstimulated samples were elevated, mitogen responsiveness was impaired, and CD4 cell counts were decreased. These alterations reverted after malaria treatment. Concurrent malaria infection did not affect QFT test results, whereas there were more indeterminate IP-10 results during acute malaria infection. We suggest that IGRA and IP-10 release assay results of malaria patients should be interpreted with caution and that testing preferably should be postponed until after malaria treatment.
Financial support: The ACT Consortium was funded through a grant from the Bill & Melinda Gates Foundation to the London School of Hygiene and Tropical Medicine. This sub-study was partly funded by Danida. Camilla H. Drabe is a recipient of a research grant from Copenhagen University Hospital Nordsjaelland Hospital, Hillerød.
Disclosure: PR and MR hold a pending patent on the IP-10 release assay. MR is employed at Statens Serum Institut who holds and licenses IP on immunodiagnostic antigens included in QuantiFERON®. No other conflicts of interests declared.
Authors' addresses: Camilla H. Drabe, Department of Infectious Diseases, Copenhagen University Hospital, Hvidovre, Kettegaard Alle 30, 2650 Hvidovre, Denmark, E-mail: camilla.h.drabe@gmail.com. Lasse S. Vestergaard, InterACT Project, Muheza District Hospital, Muheza, Tanzania, Department of Immunology and Microbiology, Centre for Medical Parasitology, University of Copenhagen, Copenhagen, Denmark, Department of Public Health, University of Copenhagen, Copenhagen, Denmark, Department of Infectious Diseases, Copenhagen University Hospital Rigshospitalet, Copenhagen, Denmark, and Department of Clinical Microbiology, Copenhagen University Hospital Rigshospitalet, Copenhagen, Denmark, E-mail: lasse.vestergaard@dadlnet.dk. Marie Helleberg, Department of Infectious Diseases, Copenhagen University Hospital Rigshospitalet, University of Copenhagen, CHIP, Copenhagen, Denmark, E-mail: marie.helleberg@regionh.dk. Nyagonde Nyagonde, Tanzania National Institute for Medical Research, Tanga Center, Tanga, Tanzania, E-mail: drnyagonde@yahoo.com. Michala V. Rose, Department of Infectious Diseases, Copenhagen University Hospital, Hvidovre, Denmark, E-mail: michala.rose@gmail.com. Filbert Francis, National Institute for Medical Research, Tanga, Tanzania, E-mail: ffrancis8@gmail.com. Ola P. Theilgaard, Lægehuset i Hedehusene, Hedehusene, Denmark, E-mail: olaptheilgaard@gmail.com. Jens Asbjørn, Danish Health and Medicines Authority, Public Health Medical Officers of Southern Denmark, Kolding, Denmark, E-mail: asbjorn_1@hotmail.com. Ben Amos, InterACT Project, Muheza District Hospital, Muheza, Tanzania, E-mail: ben@teule.org.uk. Ib Christian Bygbjerg, Department of Public Health, University of Copenhagen, Copenhagen, Denmark, E-mail: iby@sund.ku.dk. Morten Ruhwald, Department of Infectious Disease Immunology, Statens Serum Institut, Copenhagen, Denmark, E-mail: moru@ssi.dk. Pernille Ravn, Department of Pulmonary and Infectious Diseases, Nordsjaelland Hospital, Hillerød, Denmark, E-mail: peravn@gmail.dk.
Pai M, Denkinger CM, Kik SV, Rangaka MX, Zwerling A, Oxlade O, Metcalfe JZ, Cattamanchi A, Dowdy DW, Dheda K, Banaei N, 2014. Gamma interferon release assays for detection of Mycobacterium tuberculosis infection. Clin Microbiol Rev 27: 3–20.
Santin M, Muñoz L, Rigau D, 2012. Interferon-γ release assays for the diagnosis of tuberculosis and tuberculosis infection in HIV-infected adults: a systematic review and meta-analysis. PLoS One 7: e32482.
Sester M, van Leth F, Bruchfeld J, Bumbacea D, Cirillo DM, Dilektasli AG, Domínguez J, Duarte R, Ernst M, Eyuboglu FO, Gerogianni I, Girardi E, Goletti D, Janssens J-P, Julander I, Lange B, Latorre I, Losi M, Markova R, Matteelli A, Milburn H, Ravn P, Scholman T, Soccal PM, Straub M, Wagner D, Wolf T, Yalcin A, Lange C; TBNET, 2014. Risk assessment of tuberculosis in immunocompromised patients. A TBNET study. Am J Respir Crit Care Med 190: 1168–1176.
Goletti D, Raja A, Syed Ahamed Kabeer B, Rodrigues C, Sodha A, Carrara S, Vernet G, Longuet C, Ippolito G, Thangaraj S, Leportier M, Girardi E, Lagrange PH, 2010. Is IP-10 an accurate marker for detecting M. tuberculosis-specific response in HIV-infected persons? PLoS One 5: e12577.
Vanini V, Petruccioli E, Gioia C, Cuzzi G, Orchi N, Rianda A, Alba L, Giancola ML, Conte A, Schininà V, Busi Rizzi E, Girardi E, Goletti D, 2012. IP-10 is an additional marker for tuberculosis (TB) detection in HIV-infected persons in a low-TB endemic country. J Infect 65: 49–59.
Belard E, Semb S, Ruhwald M, Werlinrud AM, Soborg B, Jensen FK, Thomsen H, Brylov A, Hetland ML, Nordgaard-Lassen I, Ravn P, 2011. Prednisolone treatment affects the performance of the QuantiFERON gold in-tube test and the tuberculin skin test in patients with autoimmune disorders screened for latent tuberculosis infection. Inflamm Bowel Dis 17: 2340–2349.
Aabye MG, Hermansen TS, Ruhwald M, Praygod G, Faurholt-Jepsen D, Jeremiah K, Faurholt-Jepsen M, Range N, Friis H, Changalucha J, Andersen AB, Ravn P, 2012. Negative effect of smoking on the performance of the QuantiFERON TB gold in tube test. BMC Infect Dis 12: 379.
Rose MV, Kimaro G, Nissen TN, Kroidl I, Hoelscher M, Bygbjerg IC, Mfinanga SG, Ravn P, 2012. QuantiFERON®-TB Gold in-tube performance for diagnosing active tuberculosis in children and adults in a high burden setting. PLoS One 7: e37851.
Lucas M, Nicol P, McKinnon E, Whidborne R, Lucas A, Thambiran A, Burgner D, Waring J, French M, 2010. A prospective large-scale study of methods for the detection of latent Mycobacterium tuberculosis infection in refugee children. Thorax 65: 442–448.
Banfield S, Pascoe E, Thambiran A, Siafarikas A, Burgner D, 2012. Factors associated with the performance of a blood-based interferon-gamma release assay in diagnosing tuberculosis. PLoS One 7: e38556.
Ruhwald M, Aabye MG, Ravn P, 2012. IP-10 release assays in the diagnosis of tuberculosis infection: current status and future directions. Expert Rev Mol Diagn 12: 175–187.
Chegou NN, Heyckendorf J, Walzl G, Lange C, Ruhwald M, 2014. Beyond the IFN-γ horizon: biomarkers for immunodiagnosis of infection with Mycobacterium tuberculosis. Eur Respir J 43: 1472–1486.
Kabeer BSA, Sikhamani R, Raja A, 2010. Comparison of interferon gamma and interferon gamma-inducible protein-10 secretion in HIV-tuberculosis patients. AIDS 24: 323–325.
Aabye MG, Ruhwald M, Praygod G, Jeremiah K, Faurholt-Jepsen M, Faurholt-Jepsen D, Range N, Friis H, Changalucha J, Andersen AB, Ravn P, 2010. Potential of interferon-γ-inducible protein 10 in improving tuberculosis diagnosis in HIV-infected patients. Eur Respir J 36: 1488–1490.
Schofield L, Grau GE, 2005. Immunological processes in malaria pathogenesis. Nat Rev Immunol 5: 722–735.
Enwere GC, Ota MO, Obaro SK, 1999. The host response in malaria and depression of defence against tuberculosis. Ann Trop Med Parasitol 93: 669–678.
Chougnet C, Tallet S, Ringwald P, Deloron P, 1992. Kinetics of lymphocyte subsets from peripheral blood during a Plasmodium falciparum malaria attack. Clin Exp Immunol 90: 405–408.
Hviid L, Kurtzhals JA, Goka BQ, Oliver-Commey JO, Nkrumah FK, Theander TG, 1997. Rapid reemergence of T cells into peripheral circulation following treatment of severe and uncomplicated Plasmodium falciparum malaria. Infect Immun 65: 4090–4093.
Van Geertruyden J-P, Mulenga M, Kasongo W, Polman K, Colebunders R, Kestens L, D'Alessandro U, 2006. CD4 T-cell count and HIV-1 infection in adults with uncomplicated malaria. J Acquir Immune Defic Syndr 43: 363–367.
Elhassan IM, Hviid L, Satti G, Akerstrom B, Jakobsen PH, Jensen JB, Theander TG, 1994. Evidence of endothelial inflammation, T cell activation, and T cell reallocation in uncomplicated Plasmodium falciparum malaria. Am J Trop Med Hyg 51: 372–379.
Cellestis XXX. Manufacturer of QuantiFERON® Diagnostics and Research Products: Homepage. Available at: http://www.quantiferon.com/irm/content/PI/QFT/2PK/US.pdf. Accessed June 11, 2013.
Aabye MG, Eugen-Olsen J, Werlinrud AM, Holm LL, Tuuminen T, Ravn P, Ruhwald M, 2012. A simple method to quantitate IP-10 in dried blood and plasma spots. PLoS One 7: e39228.
Ruhwald M, Latorre I, Diaz J, Maldonado J, Mialdea I, Ravn P, Dominguez J, Aabye M, 2011. Specific diagnosis of tuberculosis infection sent via mail—IGRAs on paper. Eur Respir J 38 (Suppl 55): 1897.
Lucchi NW, Jain V, Wilson NO, Singh N, Udhayakumar V, Stiles JK, 2011. Potential serological biomarkers of cerebral malaria. Markers 31: 327–335.
Armah HB, Wilson NO, Sarfo BY, Powell MD, Bond VC, Anderson W, Adjei AA, Gyasi RK, Tettey Y, Wiredu EK, Tongren JE, Udhayakumar V, Stiles JK, 2007. Cerebrospinal fluid and serum biomarkers of cerebral malaria mortality in Ghanaian children. Malar J 6: 147.
Wilson NO, Jain V, Roberts CE, Lucchi N, Joel PK, Singh MP, Nagpal AC, Dash AP, Udhayakumar V, Singh N, Stiles JK, 2011. CXCL4 and CXCL10 predict risk of fatal cerebral malaria. Markers 30: 39–49.
McCall MBB, Sauerwein RW, 2010. Interferon—central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. J Leukoc Biol 88: 1131–1143.
Petrone L, Cannas A, Aloi F, Nsubuga M, Sserumkuma J, Nazziwa RA, Jugheli L, Lukindo T, Girardi E, Reither K, Goletti D, 2015. Blood or urine IP-10 cannot discriminate between active tuberculosis and respiratory diseases different from tuberculosis in children. BioMed Res Int 2015: 1–11.
Hviid L, Theander TG, Abu-Zeid YA, Abdulhadi NH, Jakobsen PH, Saeed BO, Jepsen S, Bayoumi RA, Jensen JB, 1991. Loss of cellular immune reactivity during acute Plasmodium falciparum malaria. FEMS Microbiol Immunol 3: 219–227.
Tagmouti S, Slater M, Benedetti A, Kik SV, Banaei N, Cattamanchi A, Metcalfe J, Dowdy D, van Zyl Smit R, Dendukuri N, Pai M, Denkinger C, 2014. Reproducibility of interferon gamma (IFN-γ) release assays. A systematic review. Ann Am Thorac Soc 11: 1267–1276.
Falade CO, Adesina-Adewole B, Dada-Adegbola HO, Ajayi IO, Akinyemi JO, Ademowo OG, Adewole IF, Kanki P, 2013. Evaluation of Paracheck-Pf™ rapid malaria diagnostic test for the diagnosis of malaria among HIV-positive patients in Ibadan, south-western Nigeria. Pathog Glob Health 107: 69–77.
Djallé D, Gody JC, Moyen JM, Tekpa G, Ipero J, Madji N, Breurec S, Manirakiza A, 2014. Performance of ParacheckTM-Pf, SD Bioline malaria Ag-Pf and SD Bioline malaria Ag-Pf/pan for diagnosis of falciparum malaria in the Central African Republic. BMC Infect Dis 14: 109.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 340 | 295 | 9 |
Full Text Views | 310 | 11 | 0 |
PDF Downloads | 117 | 8 | 0 |