Late Antiretroviral Therapy (ART) Initiation Is Associated with Long-Term Persistence of Systemic Inflammation and Metabolic Abnormalities

Mathilde Ghislain, Jean-Philippe Bastard, Laurence Meyer, Jacqueline Capeau, Soraya Fellahi, Laurence Gérard, Thierry May, Anne Simon, Corinne Vigouroux, Cécile Goujard, ANRS-COPANA Cohort Study Group, Claudine Duvivier, Fatima Touam, Gilles Pialoux, Sophie Le Nagat, Laurence Slama, Julie Chas, Thomas L'Yavanc, Jacqueline Capeau, Corinne Vigouroux, Soraya Fellahi, Jean-Philippe Bastard, Jean-Paul Viard, Aline Maignan, Agnès Cros, Alain Sobel, Laurence Gérard, Daniel Séréni, Le Van Dien, Jean-Michel Molina, Caroline Lascoux-Combe, Alexandre Aslan, Suna Balkan, Nathalie Colin de Verdière, Nathalie De Castro, Jeanine Delgado, Sylvie Parlier, Claire Pintado, Diane Ponscarme, Willy Rozenbaum, Olivier Taulera, Sébastien Gallien, Valérie Garrait, Caroline Gatey, Sandrine Gazaignes, Jérôme Goguel, Matthieu Lafaurie, Anne-Lise Munier, Jean-François Bergmann, Agathe Rami, Maguy Parrinello, Pierre-Marie Girard, Julie Bottero, Zineb Ouazene, Bénédicte Lefebvre, Nadia Vacin, Pauline Campa, Diane Boccens, Serge Herson, Hassiba Remidi, Malik Iguertsira, Smaïl Nafissa, Catherine Lupin, Anne Simon, Nadia Edeb, Dominique Salmon-Céron, Loïc Guillevin, Tassadit Tahi, Marie Pierre Pietri, Laurence Weiss, Juliette Pavie, Marina Karmochkine, Dominique Batisse, Martin Buisson, Jean Derouineau, Maria Manea, Marie-Laure Lucas, Matheron Sophie, Golriz Pahlavan, Emmanuelle Paput, Françoise Louni, Stanislas Harent, Sylvie Legal, Guylaine Castor, Phung Bao, Isabelle Fournier, Ralaimazava Pascal Julia Zelie, Cindy Godard, François Boué, Valérie Martinez, Elsa Miekoutima, Marion Favier, Carole Pignon, Véronique Chambrin, Imad kansau, Fior Renato, Mariem Raho-Moussa, Bruno Fantin, Agnès Uludag, Ali Tadlaoui, Caroline Poder, Valentin Iwaka Bamae, Sihasi Makloufi, Patricia Honoré, Olivier Bouchaud, Sophie Aberall, Cécile Goujard, Yann Quertainmont, Raluca Sterpu, Frédéric Fourreau, Delphine Peretti, Taylor Pindi Sala, Katia Bourdic, Yves Levy, Jean-Daniel Lelièvre, Stéphanie Dominguez, Giovanna Melica, Carine Belzunce, Maryline Saidani, Anne-Sophie Lascaux, Jose Luis Lopez Zaragoza, Cécile Dumont, André Cabié, Sylvie Abel, Patrick Hochedez, François Ronin, Anne-Sophie Batalla, Christophe Cerland, Sandrine Pierre-François, Benoit Roze, Isabelle Poizot-Martin, Anne-Suzel Ritleng, Meriem Guignard, Nicolas Croarec, Carle Blanco Bétancourt, Olivia Zaegel-Faucher, Alena Ivanova, Jacques Moreau, Marie-Josèphe Carmantrand, Saadia Mokhtari, Marie-Christine Thiebaut-Drobacheff, Adeline Foltzer Cécile Haffner-Mauvais, François Parcelier, Quentin Gardiennet, Catherine Chireuze, Jean-François Faucher, Laurent Hustache-Mathieu, Gabriella Illes, Didier Neau, Charles Cazanave, Thierry Pistone, Michel Dupon, Frédéric Dauchy, Hervé Dutronc, Isabelle Raymond, Laetitia Lacaze-Buzy, Séverine Le Puil, Philippe Morlat, François Paccalin, Sabrina Caldato, Julien Roger-Schmeltz, Marie-Carmen Pertusa, Marie-Catherine Receveur, Cédric Martell, Denis Lacoste, Pierre Duffau, Mojgan Hessamfar, Jacques Reynes, Claude Crisol, Vincent Baillat, Vincent Le Moing, Jean-Marc Jacquet, Marie-Laure Casanova, Alain Makinson, Antoine Villadoro, Carine Favier, Pascal André, Cristina Psomas, Corinne Merle De Boever, Christine Tramoni, Louis Bernard, Pascale Nau, Gaëlle Sajole, Carine Sèvre, Antoine Soufflet, Patrick Guadagnin, Frédéric Bastides, Patrick Choutet, François Raffi, Clothilde Anavena, Martine Colas, Laurence Larmet, Pascale Morineau Le Houssinc, Cécile Brunet-Cartier, Véronique Reliquet, Patrick Point, Olivier Aubry, Hervé Hue, Thierry May, Marie-Pierre Bouillon, Mickaël Delestan, Marie André, Antoine Chéret, Faiza Ajana, Isabelle Alcaraz, Véronique Baclet, Raphaël Biekre, Hugues Melliez, Michel Valette, Nathalie Viget, Thomas Huleux, Emmanuelle Aïssi, David Rey, Marialuisa Partisani, Christine Cheneau, Michèle Priester, Marie-Laure Batard, Mahsa Mohseni Zadeh, Aurélie Richard, Gilles Blaison, Martin Martinot, Anne Pachard, Djamila Makhloufi, Jean-Michel Livrozet, Pierre Chiarello, Florence Brunel-Dalmas, Florence Garnier, Dominique Peyramond, Christian Chidiac, Claude Augustin-Normand, Joseph Koffi, Patrick Miailhes, Sophie Pailhes, Isabelle Schlienger, Thomas Perpoint, André Boibieux, Corinne Brochier, Philippe Perré, Olivia Bolengia Stragia, Thomas Guimant, Sophie Leautez Nainville, Jean Luc-Esnault, Laetitia Laine, Nadine Rabille, Catherine Albrecht, Hélène Durand, Isabelle Suaud, Mathilde Ghislain, Jean-Philippe Bastard, Laurence Meyer, Jacqueline Capeau, Soraya Fellahi, Laurence Gérard, Thierry May, Anne Simon, Corinne Vigouroux, Cécile Goujard, ANRS-COPANA Cohort Study Group, Claudine Duvivier, Fatima Touam, Gilles Pialoux, Sophie Le Nagat, Laurence Slama, Julie Chas, Thomas L'Yavanc, Jacqueline Capeau, Corinne Vigouroux, Soraya Fellahi, Jean-Philippe Bastard, Jean-Paul Viard, Aline Maignan, Agnès Cros, Alain Sobel, Laurence Gérard, Daniel Séréni, Le Van Dien, Jean-Michel Molina, Caroline Lascoux-Combe, Alexandre Aslan, Suna Balkan, Nathalie Colin de Verdière, Nathalie De Castro, Jeanine Delgado, Sylvie Parlier, Claire Pintado, Diane Ponscarme, Willy Rozenbaum, Olivier Taulera, Sébastien Gallien, Valérie Garrait, Caroline Gatey, Sandrine Gazaignes, Jérôme Goguel, Matthieu Lafaurie, Anne-Lise Munier, Jean-François Bergmann, Agathe Rami, Maguy Parrinello, Pierre-Marie Girard, Julie Bottero, Zineb Ouazene, Bénédicte Lefebvre, Nadia Vacin, Pauline Campa, Diane Boccens, Serge Herson, Hassiba Remidi, Malik Iguertsira, Smaïl Nafissa, Catherine Lupin, Anne Simon, Nadia Edeb, Dominique Salmon-Céron, Loïc Guillevin, Tassadit Tahi, Marie Pierre Pietri, Laurence Weiss, Juliette Pavie, Marina Karmochkine, Dominique Batisse, Martin Buisson, Jean Derouineau, Maria Manea, Marie-Laure Lucas, Matheron Sophie, Golriz Pahlavan, Emmanuelle Paput, Françoise Louni, Stanislas Harent, Sylvie Legal, Guylaine Castor, Phung Bao, Isabelle Fournier, Ralaimazava Pascal Julia Zelie, Cindy Godard, François Boué, Valérie Martinez, Elsa Miekoutima, Marion Favier, Carole Pignon, Véronique Chambrin, Imad kansau, Fior Renato, Mariem Raho-Moussa, Bruno Fantin, Agnès Uludag, Ali Tadlaoui, Caroline Poder, Valentin Iwaka Bamae, Sihasi Makloufi, Patricia Honoré, Olivier Bouchaud, Sophie Aberall, Cécile Goujard, Yann Quertainmont, Raluca Sterpu, Frédéric Fourreau, Delphine Peretti, Taylor Pindi Sala, Katia Bourdic, Yves Levy, Jean-Daniel Lelièvre, Stéphanie Dominguez, Giovanna Melica, Carine Belzunce, Maryline Saidani, Anne-Sophie Lascaux, Jose Luis Lopez Zaragoza, Cécile Dumont, André Cabié, Sylvie Abel, Patrick Hochedez, François Ronin, Anne-Sophie Batalla, Christophe Cerland, Sandrine Pierre-François, Benoit Roze, Isabelle Poizot-Martin, Anne-Suzel Ritleng, Meriem Guignard, Nicolas Croarec, Carle Blanco Bétancourt, Olivia Zaegel-Faucher, Alena Ivanova, Jacques Moreau, Marie-Josèphe Carmantrand, Saadia Mokhtari, Marie-Christine Thiebaut-Drobacheff, Adeline Foltzer Cécile Haffner-Mauvais, François Parcelier, Quentin Gardiennet, Catherine Chireuze, Jean-François Faucher, Laurent Hustache-Mathieu, Gabriella Illes, Didier Neau, Charles Cazanave, Thierry Pistone, Michel Dupon, Frédéric Dauchy, Hervé Dutronc, Isabelle Raymond, Laetitia Lacaze-Buzy, Séverine Le Puil, Philippe Morlat, François Paccalin, Sabrina Caldato, Julien Roger-Schmeltz, Marie-Carmen Pertusa, Marie-Catherine Receveur, Cédric Martell, Denis Lacoste, Pierre Duffau, Mojgan Hessamfar, Jacques Reynes, Claude Crisol, Vincent Baillat, Vincent Le Moing, Jean-Marc Jacquet, Marie-Laure Casanova, Alain Makinson, Antoine Villadoro, Carine Favier, Pascal André, Cristina Psomas, Corinne Merle De Boever, Christine Tramoni, Louis Bernard, Pascale Nau, Gaëlle Sajole, Carine Sèvre, Antoine Soufflet, Patrick Guadagnin, Frédéric Bastides, Patrick Choutet, François Raffi, Clothilde Anavena, Martine Colas, Laurence Larmet, Pascale Morineau Le Houssinc, Cécile Brunet-Cartier, Véronique Reliquet, Patrick Point, Olivier Aubry, Hervé Hue, Thierry May, Marie-Pierre Bouillon, Mickaël Delestan, Marie André, Antoine Chéret, Faiza Ajana, Isabelle Alcaraz, Véronique Baclet, Raphaël Biekre, Hugues Melliez, Michel Valette, Nathalie Viget, Thomas Huleux, Emmanuelle Aïssi, David Rey, Marialuisa Partisani, Christine Cheneau, Michèle Priester, Marie-Laure Batard, Mahsa Mohseni Zadeh, Aurélie Richard, Gilles Blaison, Martin Martinot, Anne Pachard, Djamila Makhloufi, Jean-Michel Livrozet, Pierre Chiarello, Florence Brunel-Dalmas, Florence Garnier, Dominique Peyramond, Christian Chidiac, Claude Augustin-Normand, Joseph Koffi, Patrick Miailhes, Sophie Pailhes, Isabelle Schlienger, Thomas Perpoint, André Boibieux, Corinne Brochier, Philippe Perré, Olivia Bolengia Stragia, Thomas Guimant, Sophie Leautez Nainville, Jean Luc-Esnault, Laetitia Laine, Nadine Rabille, Catherine Albrecht, Hélène Durand, Isabelle Suaud

Abstract

Objectives: HIV-induced immunodeficiency is associated with metabolic abnormalities and systemic inflammation. We investigated the effect of antiretroviral therapy (ART) on restoration of insulin sensitivity, markers of immune activation and inflammation.

Methods: Immunological, metabolic and inflammatory status was assessed at antiretroviral therapy initiation and three years later in 208 patients from the ANRS-COPANA cohort. Patients were compared according to their pre-ART CD4+ cell count (group 1: ≤ 200/mm3, n = 66 vs. group 2: > 200/mm3, n = 142).

Results: Median CD4+ cell count increased in both groups after 3 years of successful ART but remained significantly lower in group 1 than in group 2 (404 vs 572 cells/mm3). Triglyceride and insulin levels were higher or tended to be higher in group 1 than in group 2 at ART initiation (median: 1.32 vs 0.97 mmol/l, p = 0.04 and 7.6 vs 6.8 IU, p = 0.09, respectively) and remained higher after three years of ART (1.42 vs 1.16 mmol/L, p = 0.0009 and 8.9 vs 7.2 IU, p = 0.01). After adjustment for individual characteristics and antiretroviral therapy regimens (protease inhibitor (PI), zidovudine), insulin levels remained significantly higher in patients with low baseline CD4+ cell count. Baseline IL-6, sCD14 and sTNFR2 levels were higher in group 1 than in group 2. Most biomarkers of immune activation/inflammation declined during ART, but IL-6 and hsCRP levels remained higher in patients with low baseline CD4+ cell count than in the other patients (median are respectively 1.4 vs 1.1 pg/ml, p = 0.03 and 2.1 vs 1.3 mg/ml, p = 0.07).

Conclusion: After three years of successful ART, low pretreatment CD4+ T cell count remained associated with elevated insulin, triglyceride, IL-6 and hsCRP levels. These persistent metabolic and inflammatory abnormalities could contribute to an increased risk of cardiovascular and metabolic disease.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Distribution of inflammatory markers according…
Fig 1. Distribution of inflammatory markers according to CD4 T cell count at ART initiation.

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