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Incidence of tuberculosis among HIV-infected patients receiving highly active antiretroviral therapy in Europe and North America

  • Enrico Girardi*
  • , Dominique Costagliola
  • , François Dabis
  • , Antonella D.Arminio Monforte
  • , Frank de Wolf
  • , Matthias Egger
  • , Gerd Fatkenheuer
  • , John Gill
  • , Robert Hogg
  • , Amy Justice
  • , Bruno Ledergerber
  • , Jens Lundgren
  • , Margaret May
  • , Andrew Phillips
  • , Peter Reiss
  • , Caroline Sabin
  • , Schlomo Staszewski
  • , Jonathan Sterne
  • , Ian Weller
  • , Brenda Beckthold
  • Benita Yip, Brenda Dauer, Jenifer Fusco, Sophie Grabar, Emilie Lanoy, Cornelia Junghans, Valerie Lavignolle, Frank van Leth, Edwige Pereira, Patrizio Pezzotti, Nobert Schmeisser, E. Billaud, F. Boué, X. Duval, C. Duvivier, P. Enel, S. Fournier, J. Gasnault, C. Gaud, J. Gilquin, M. A. Khuong, J. M. Lang, M. Mary-Krause, S. Matheron, M. C. Meyohas, G. Pialoux, I. Poizot-Martin, C. Pradier, E. Rouveix, D. Salmon-Ceron, A. Sobel, P. Tattevin, H. Tissot-Dupont, Y. Yasdanpanah, E. Aronica, V. Tirard-Fleury, I. Tortay, S. Abgrall, M. Guiguet, H. Leneman, L. Lièvre, V. Potard, S. Saidi, J. L. Vildé, C. Leport, P. Yeni, E. Bouvet, C. Gaudebout, B. Crickx, C. Picard-Dahan, L. Weiss, D. Tisne-Dessus, D. Sicard, D. Salmon, I. Auperin, J. P. Viard, L. Roudière, R. Fior, J. F. Delfraissy, C. Goujard, P. Lesprit, C. Jung, J. L. Meynard, O. Picard, N. Desplanque, J. Cadranel, C. Mayaud, W. Rozenbaum, F. Bricaire, C. Katlama, S. Herson, A. Simon, J. M. Decazes, J. M. Molina, J. P. Clauvel, L. Gerard, P. Sellier, M. Diemer, C. Dupont, H. Berthé, P. Saïag, E. Mortier, C. Chandemerle, P. de Truchis, M. Bentata, P. Honoré, S. Tassi, V. Jeantils, D. Mechali, B. Taverne, H. Laurichesse, F. Gourdon, F. Lucht, A. Fresard, J. P. Faller, P. Eglinger, C. Bazin, R. Verdon, D. Peyramond, A. Boibieux, J. L. Touraine, J. M. Livrozet, C. Trepo, L. Cotte, I. Ravaux, J. P. Delmont, J. Moreau, J. A. Gastaut, J. Soubeyrand, F. Retornaz, P. A. Blanc, T. Allegre, A. Galinier, J. M. Ruiz, G. Lepeu, P. Granet-Brunello, L. Pelissier, J. P. Esterni, M. Nezri, R. Cohen-Valensi, A. Laffeuillade, S. Chadapaud, J. Reynes, T. May, C. Rabaud, F. Raffi, P. Pugliese, C. Michelet, C. Arvieux, F. Caron, F. Borsa-Lebas, D. Rey, P. Fraisse, P. Massip, L. Cuzin, E. Arlet-Suau, M. F. Thiercelin Legrand, M. Sobesky, R. Pradinaud, M. Contant, M. Montroni, G. Scalise, M. C. Braschi, A. Riva, U. Tirelli, R. Cinelli, G. Pastore, N. Ladisa, G. Minafra, F. Suter, C. Arici, F. Chiodo, V. Colangeli, C. Fiorini, O. Coronado, G. Carosi, G. P. Cadeo, C. Torti, C. Minardi, D. Bertelli, G. Rizzardini, S. Melzi, P. E. Manconi, P. Piano, L. Cosco, A. Scerbo, J. Vecchiet, M. D'Alessandro, D. Santoro, L. Pusterla, G. Carnevale, P. Citterio, P. Viganò, M. Mena, F. Ghinelli, L. Sighinolfi, F. Leoncini, F. Mazzotta, M. Pozzi, S. Lo Caputo, G. Angarano, B. Grisorio, A. Saracino, S. Ferrara, P. Grima, P. Tundo, G. Pagano, G. Cassola, A. Alessandrini, R. Piscopo, M. Toti, S. Chigiotti, F. Soscia, L. Tacconi, A. Orani, P. Perini, A. Scasso, A. Vincenti, F. Chiodera, P. Castelli, A. Scalzini, L. Palvarini, M. Moroni, A. Lazzarin, A. Cargnel, G. M. Vigevani, L. Caggese, D. Repetto, A. Galli, S. Merli, C. Pastecchia, M. C. Moioli, R. Esposito, C. Mussini, N. Abrescia, A. Chirianni, C. M. Izzo, M. Piazza, M. De Marco, R. Viglietti, E. Manzillo, S. Nappa, A. Colomba, V. Abbadessa, T. Prestileo, S. Mancuso, C. Ferrari, P. Pizzaferri, G. Filice, L. Minoli, R. Bruno, S. Novati, F. Baldelli, M. Tinca, E. Petrelli, A. Cioppi, F. Alberici, A. Ruggieri, F. Menichetti, C. Martinelli, C. De Stefano, A. La Gala, G. Ballardini, E. Rizzo, G. Magnani, M. A. Ursitti, M. Arlotti, P. Ortolani, R. Cauda, F. Dianzani, G. Ippolito, A. Antinori, G. Antonucci, S. D'Elia, P. Narciso, N. Petrosillo, V. Vullo, A. De Luca, A. Bacarelli, M. Zaccarelli, R. Acinapura, P. De Longis, A. Brandi, M. P. Trotta, P. Noto, M. Lichtner, M. R. Capobianchi, F. Carletti, G. Rezza, M. S. Mura, M. Mannazzu, P. Caramello, G. Di Perri, M. L. Soranzo, G. C. Orofino, I. Arnaudo, M. Bonasso, P. A. Grossi, C. Basilico, A. Poggio, G. Bottari, E. Raise, F. Ebo, F. De Lalla, G. Tositti, F. Resta, K. Loso, A. Cozzi Lepri, M. Battegay, E. Bernasconi, J. Böni, H. Bucher, P. Bürgisser, S. Cattacin, M. Cavassini, R. Dubs, L. Elzi, P. Erb, K. Fantelli, M. Fischer, M. Flepp, A. Fontana, P. Francioli, H. Furrer, M. Gorgievski, H. Günthard, B. Hirschel, L. Kaiser, C. Kind, T. Klimkait, U. Lauper, M. Opravil, F. Paccaud, G. Pantaleo, L. Perrin, J. C. Piffaretti, M. Rickenbach, C. Rudin, P. Schmid, J. Schüpbach, R. Speck, A. Telenti, A. Trkola, P. Vernazza, R. Weber, S. Yerly, W. Bronsveld, M. E. Hillebrand-Haverkort, J. M. Prins, J. C. Bos, J. K.M. Eeftinck Schattenkerk, S. E. Geerlings, M. H. Godfried, J. M.A. Lange, F. C. van Leth, S. H. Lowe, J. T.M. van der Meer, F. J.B. Nellen, K. Pogány, T. van der Poll, T. A. Ruys, S. Sankatsing, R. Steingrover, G. van Twillert, M. van der Valk, M. G.A. van Vonderen, S. M.E. Vrouenraets, M. van Vugt, F. W.M.N. Wit, T. W. Kuijpers, D. Pajkrt, H. J. Scherpbier, A. van Eeden, J. H. ten Veen, P. S. van Dam, J. C. Roos, K. Brinkman, P. H.J. Frissen, H. M. Weigel, J. W. Mulder, E. C.M. van Gorp, P. L. Meenhorst, A. T.A. Mairuhu, J. Veenstra, S. A. Danner, M. A. van Agtmael, F. A.P. Claessen, R. M. Perenboom, A. Rijkeboer, M. van Vonderen, C. Richter, J. van der Berg, R. van Leusen, R. Vriesendorp, F. J.F. Jeurissen, R. H. Kauffmann, E. L.W. Koger, B. Bravenboer, C. H.H. ten Napel, G. J. Kootstra, H. G. Sprenger, W. M.A.J. Miesen, R. Doedens, E. H. Scholvinck, R. W. ten Kate, D. P.F. van Houte, M. Polee, F. P. Kroon, den Broek van den Broek, J. T. van Dissel, E. F. Schippers, G. Schreij, S. van de Geest, A. Verbon, P. P. Koopmans, M. Keuter, F. Post, A. J.A.M. van der Ven, M. E. van der Ende, I. C. Gyssens, M. van der Feltz, J. G. den Hollander, S. de Marie, J. L. Nouwen, B. J.A. Rijnders, T. E.M.S. de Vries, G. Driessen, R. de Groot, N. Hartwig, J. R. Juttmann, C. van de Heul, M. E.E. van Kasteren, M. M.E. Schneider, M. J.M. Bonten, J. C.C. Borleffs, P. M. Ellerbroek, I. M. Hoepelman, C. A.J.J. Jaspers, I. Schouten, C. A.M. Schurink, S. P.M. Geelen, T. F.W. Wolfs, W. L. Blok, A. A. Tanis, P. H.P. Groeneveld, N. K.T. Back, M. E.G. Bakker, B. Berkhout, S. Jurriaans, Th Cuijpers, P. J.G.M. Rietra, K. J. Roozendaal, W. Pauw, A. P. van Zanten, B. M.E. von Blomberg, P. Savelkoul, C. M.A. Swanink, P. F.H. Franck, A. S. Lampe, R. Hendriks, J. Schirm, Dhr Benne, D. Veenendaal, H. Storm, J. Weel, J. H. van Zeijl, A. C.M. Kroes, H. C.J. Claas, C. A.M.V.A. Bruggeman, V. J. Goossens, J. M.D. Galama, W. J.G. Melchers, Y. A.G. Poort, G. J.J. Doornum, M. G. Niesters, A. D.M.E. Osterhaus, M. Schutten, A. G.M. Buiting, C. A.M. Swaans, C. A.B. Boucher, R. Schuurman, E. Boel, A. F. Jansz, M. Losso, A. Duran, N. Vetter, I. Karpov, A. Vassilenko, N. Clumeck, S. de Wit, B. Poll, R. Colebunders, L. Machala, H. Rozsypal, D. Sedlacek, J. Nielsen, T. Benfield, O. Kirk, J. Gerstoft, T. Katzenstein, A. B.E. Hansen, P. Skinhoj, C. Pedersen, K. Zilmer, P. M. Girard, T. Saint-Marc, P. Vanhems, M. Dietrich, C. Manegold, J. van Lunzen, H. J. Stellbrink, M. Bickel, F. D. Goebel, G. Fätkenheuer, J. Rockstroh, R. Schmidt, J. Kosmidis, P. Gargalianos, H. Sambatakou, J. Perdios, G. Panos, A. Filandras, E. Karabatsaki, D. Banhegyi, F. Mulcahy, I. Yust, D. Turner, M. Burke, S. Pollack, G. Hassoun, Z. Sthoeger, S. Maayan, A. Chiesi, R. Borghi, R. Pristera, A. Gabbuti, E. Montesarchio, F. Iacomi, R. Finazzi, L. Viksna, S. Chaplinskas, R. Hemmer, T. Staub, J. Bruun, A. Maeland, V. Ormaasen, B. Knysz, J. Gasiorowski, A. Horban, D. Prokopowicz, A. Wiercinska-Drapalo, A. Boron-Kaczmarska, M. Pynka, M. Beniowski, E. Mularska, H. Trocha, F. Antunes, E. Valadas, K. Mansinho, F. Matez, D. Duiculescu, Victor Babes, A. Streinu-Cercel, E. Vinogradova, A. Rakhmanova, D. Jevtovic, M. Mokráš, D. Staneková, J. González-Lahoz, M. Sánchez-Conde, T. García-Benayas, L. Martin-Carbonero, V. Soriano, B. Clotet, A. Jou, J. Conejero, C. Tural, J. M. Gatell, J. M. Miró, A. Blaxhult, A. Karlsson, P. Pehrson, V. Soravia-Dunand, E. Kravchenko, N. Chentsova, S. Barton, A. M. Johnson, D. Mercey, M. A. Johnson, A. Mocroft, M. Murphy, J. Weber, G. Scullard, M. Fisher, R. Brettle, C. Loveday, J. Gatell, S. Vella, I. Gjørup, N. Friis-Moeller, A. Cozzi-Lepri, W. Bannister, D. Mollerup, D. Podlevkareva, C. Holkmann Olsen, J. Kjær, S. Raffanti, D. Dieterch, S. Becker, A. Scarsella, G. Fusco, B. Most, R. Balu, R. Rana, R. Beckerman, T. Ising, R. Irek, B. Johnson, A. Hirani, E. Dejesus, G. Pierone, P. Lackey, C. Irek, J. Burdick, S. Leon, J. Arch, E. B. Helm, A. Carlebach, A. Müller, A. Haberl, G. Nisius, T. Lennemann, C. Rottmann, T. Wolf, C. Stephan, M. Mösch, P. Gute, L. Locher, T. Lutz, S. Klauke, G. Knecht, H. W. Doerr, M. Stürmer, N. von Hentig, B. Jennings, J. Beylot, G. Chêne, M. Dupon, M. Longy-Boursier, J. L. Pellegrin, J. M. Ragnaud, R. Salamon, G. Chêne, R. Thiébaut, C. Lewden, S. Lawson-Ayayi, P. Mercié, J. F. Moreau, P. Morlat, N. Bernard, D. Lacoste, D. Malvy, D. Neau, M. J. Blaizeau, M. Decoin, S. Delveaux, C. Hannapier, S. Labarrère, V. Lavignolle-Aurillac, B. Uwamaliya-Nziyumvira, G. Palmer, D. Touchard, E. Balestre, A. Alioum, H. Jacqmin-Gadda, M. Bonarek, F. Bonnet, B. Coadou, P. Gellie, C. Nouts, F. Bocquentin, H. Dutronc, S. Lafarie, A. Aslan, T. Pistonne, P. Thibaut, R. Vatan, D. Chambon, C. De La Taille, C. Cazorla, A. Ocho, J. F. Viallard, O. Caubet, C. Cipriano, E. Lazaro, P. Couzigou, L. Castera, H. Fleury, M. E. Lafon, B. Masquelier, I. Pellegrin, D. Breilh, P. Blanco, P. Loste, L. Caunègre, F. Bonnal, S. Farbos, M. Ferrand, J. Ceccaldi, S. Tchamgoué, S. De Witte, E. Buy, C. Alexander, R. Barrios, P. Braitstein, Z. Brumme, K. Chan, H. Cote, N. Gataric, J. Geller, S. Guillemi, Harrigan, M. Harris, R. Joy, A. Levy, J. Montaner, V. Montessori, A. Palepu, E. Phillips, P. Phillips, N. Press, M. Tyndall, E. Wood, J. Ballinger, S. Bhagani, R. Breen, P. Byrne, A. Carroll, I. Cropley, Z. Cuthbertson, T. Drinkwater, T. Fernandez, A. M. Geretti, Gary Murphy, D. Ivens, M. Johnson, S. Kinloch-De Loes, M. Lipman, S. Madge, B. Prinz, D. Robertson Bell, S. Shah, L. Swaden, M. Tyrer, M. Youle, C. Chaloner, H. Gumley, J. Holloway, D. Puradiredja, J. Sweeney, R. Tsintas, L. Bansi, Z. Fox, F. Lampe, C. Smith, E. Amoah, G. Clewley, L. Dann, B. Gregory, I. Jani, G. Janossy, M. Kahan, M. Thomas, M. J. Gill, R. Read, V. Schmeisser, K. Voigt, J. C. Wasmuth, A. Wohrmann
*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

197 Citations (Scopus)

Abstract

Background. We obtained estimates of the incidence of tuberculosis (TB) among patients receiving HAART and identified determinants of the incidence. Methods. We analyzed the incidence of TB during the first 3 years after initiation of HAART among 17,142 treatment-naive, AIDS-free persons starting HAART who were enrolled in 12 cohorts from Europe and North America. We used univariable and multivariable Poisson regression models to identify factors associated with the incidence. Results. During the first 3 years (36,906 person-years), 173 patients developed TB (incidence, 4.69 cases per 1000 person-years). In multivariable analysis, the incidence rate was lower for men who have sex with men, compared with injection drug users (relative rate, 2.46; 95% confidence interval [CI], 1.51-4.01), heterosexuals (relative rate, 2.42; 95% CI, 1.64-3.59), those with other suspected modes of transmission (relative rate, 1.66; 95% CI, 0.91-3.06), and those with a higher CD4+ count at the time of HAART initiation (relative rate per log2 cells/ μL, 0.87; 95% CI, 0.84-0.91). During 28,846 person-years of follow-up after the first 6 months of HAART, 88 patients developed TB (incidence, 3.1 cases per 1000 person-years of follow-up). In multivariable analyses, a low baseline CD4+ count (relative rate per log2 cells/μL, 0.89; 95% CI, 0.83-0.96), 6-month CD4+ count (relative rate per log2 cells/μL, 0.90; 95% CI, 0.81-0.99), and a 6-month HIV RNA level 1400 copies/μL (relative rate, 2.21; 95% CI, 1.33-3.67) were significantly associated with the risk of acquiring TB after 6 months of HAART. Conclusion. The level of immunodeficiency at which HAART is initiated and the response to HAART are important determinants of the risk of TB. However, this risk remains appreciable even among those with a good response to HAART, suggesting that other interventions may be needed to control the TB epidemic in the HIVinfected population.

Original languageEnglish
Pages (from-to)1772-1782
Number of pages11
JournalClinical Infectious Diseases
Volume41
Issue number12
DOIs
Publication statusPublished - 15 Dec 2005

Bibliographical note

Publisher Copyright:
© 2005 by the Infectious Diseases Society of America. All rights reserved.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

  1. SDG 3 - Good Health and Well-being
    SDG 3 Good Health and Well-being

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