Immunovirological status in people with perinatal and adult-acquired HIV-1 infection: a multi-cohort analysis from France

Rémonie Seng; Pierre Frange; Albert Faye; Catherine Dollfus; Jérôme le Chenadec; Faroudy Boufassa; Asma Essat; Tessa Goetghebuer; Elisa Arezes; Véronique Avettand-Fènoël; Jean-Joël Bigna; Stéphane Blanche; Cécile Goujard; Laurence Meyer; Josiane Warszawski; Jean-Paul Viard; ANRS EPF; COVERTE; PRIMO; SEROPRI; COPANA study groups

doi:10.1016/j.lanepe.2024.100885

Immunovirological status in people with perinatal and adult-acquired HIV-1 infection: a multi-cohort analysis from France

Lancet Reg Health Eur. 2024 Apr 1:40:100885. doi: 10.1016/j.lanepe.2024.100885. eCollection 2024 May.

Authors

Rémonie Seng^{1

2}, Pierre Frange^{3

4}, Albert Faye^{5

6}, Catherine Dollfus⁷, Jérôme le Chenadec¹, Faroudy Boufassa¹, Asma Essat¹, Tessa Goetghebuer^{8

9}, Elisa Arezes¹, Véronique Avettand-Fènoël^{10

11}, Jean-Joël Bigna¹², Stéphane Blanche¹³, Cécile Goujard^{1

14}, Laurence Meyer^{1

2}, Josiane Warszawski^{1

2}, Jean-Paul Viard¹⁵; ANRS EPF; COVERTE; PRIMO; SEROPRI; COPANA study groups

Collaborators

H Aumaitre, E Froguel, F Caby, S Dellion, L Gerard, F Lucht, C Chirouze, M Dupon, Jl Schmit, C Goujard, T Allegre, B Cazenave, G Hittinger, P De Truchis, J Cailhol, C Duvivier, A Canestri, O Bouchaud, M Karmochkine, D Salmon-Ceron, D Zucman, E Mortier, R Tubiana, P M Girard, C Pintado, A Cabie, V Rabier, P Morlat, D Neau, C Genet, D Makhloufi, S Bregigeon Ronot, J Ghosn, V Reliquet, P Perré, Jl Pellegrin, C Arvieux, C Cheneau, L Bernard, P Delobel, R Verdon, C Jacomet, L Piroth, F Ajana, S Bevilacqua, Y Debab, A L Lecapitaine, L Cotte, S Mokhtari, P Mercie, P Poubeau, V Garrait, Ma Khuong, G Beck-Wirth, L Blum, S Blanche, F Boccara, T Prazuck, C Barbuat, J P Viard, S Stegmann-Planchard, B Martha, J M Treluyer, E Dore, C Gaud, M Niault, E Fernandes, H Hitoto, A Compagnucci, N Elenga, A Faye, C Dollfus, A Chace, M Levine, S A Martha, C Floch-Tudal, K Kebaïli, N Entz-Werle, J Tricoire, F Mazingue, P Bolot, P Brazille, T Goetghebuer, A F Gennotte, D Van Der Linden, V Schmitz, M Moutschen, C Crenn-Hebert, F Habibi, A Coursol, E Guesdon, P F Ceccaldi, M Dehlinger-Paul, E Pannier, V Marcou, J Ghosn, V Garrait, C Elleau, M Achkar, P Delobel, M O Vareil, A Chace, S Couderc, C Routier, M A Bouldouyre, F Caby, L Selleret, P Bolot, A Chabrol, C Bellahcene, C Pluchart, R Tubiana, A Yangui, D Vignes, A Alissa, A Johnson, E Lachassinne, A Benbara, L Karaoui, A Bongain, B Yakeu, J L Schmit, L Cravello, C Hubert, C Dollfus, P Faucher, D Pinquier, C Borie, D Rocchi, C Chirouze, C Brunet-Cartier, C Briandet, J Brouard, A Chalvon-Demersay, M Rajguru, L Bernard, K Billiemaz, A Fresard, A Moulin, P Fialaire, L Mesnard, E Werner, E Vintejoux, J Marian, S Ranaivojaona, F Bissuel, M Abdelhadi, Y Hammou, C Genet-Villeger, Y Hatchuel, N Elenga, G Hittinger, G Bachelard, M Medus, J Dendale-Nguyen, T S Guimard, A Martha, M Rouha, P Perfezou, L De Saint Martin, S Jaffuel, R Buzele, C Arvieux, M Gousseff, C Cudeville, M Niault, V Vitrat, C Michau, G Palenzuela, M Driessen, B Heller-Roussin, J M Labaune, B Muanza, G Hittinger, D Makhloufi, J Massardier, M Partisani, C Floch-Tudal, V Marcou, I Hau, C Runel-Belliard, C Brehin, A Chace, K Kebaili, M Lalande, M Lagree, N Entz-Werle, K Lacombe, J-M Molina, J Ghosn, J Reynes, O Robineau, F Raffi, P Morlat, P Delobel, A Becker, C Goujard, L Weiss, T Allègre, G Pialoux, F Souala, A Rami, C Katlama, A Cabié, D Makhloufi, J-P Viard, C Cheneau, F Bastides, D Neau, H Aumaitre, C Duvivier, O Bouchaud, P Fialaire, L Piroth, C Michel, D Salmon, J-D Le Lièvre, G Hittinger, P De Truchis, A Sotto, C Jacomet, E Rouveix, A Naqvi, D Zucman, S Brégigeon, R Rodet, C Chirouze, A Simon-Coutelier, V Garrait, J-L Esnault, E Mortier, R Buzelé, S Bevilacqua, R Verdon, A Stein, C Godin-Colet, G Pichancourt, A Chabrol, P Caraux-Paz, M Mohseni Zadeh, L Gérard, C Lascaux-Cametz, L Bodard, J-L Pellegrin, C Genet, N Ettahar, A Uludag, F Caby, E Rosenthal, F Prevoteau du Clary, A Fresard, S Jaureguiberry, L Blum, P Philibert, A-L Lecapitaine, Y Debab, E Chakvetadze, H Champagne, M Gousseff, E Froguel, V Daneluzzi, J Goupil de Bouillé, A Leprêtre, I Lamaury, I Darasteanu, B Abraham, D Garipuy, T Prazuck, J-L Berger, J-L Schmit, K Diallo, F Gourdon, O Vaillant, V Gaborieau, B Martha, J Doll, D Quinsat, L Geffray, J-J Girard, D Houlbert, C Michau, B Cazenave, V Perronne, E Klement, O Antioniotti, C Rouzioux, V Avettand-Fenoel, O Lortholary, J P Viard, S Boucly, A Maignan, C Duvivier, R Thiebaut, L Meyer, F Boufassa, M A Charles, R Dray-Spira, C Legeai, V Amon, N Benammar, R Seng, G Pialoux, L Slama, P Bonnard, C Chakvetadze, T L'Yavanc, J Capeau, C Vigouroux, S Fellahi, J P Bastard, E Oksenhendler, L Gerard, J F Bourge, V Bajzik, D Sereni, C Lascoux-Combe, C Pintado, O Taulera, L V Dien, J Delgado, J M Molina, T Saint-Marc, S Ferret, J Pavie, J F Bergmann, A Rami, M Parrinello, P M Girard, BLefebvre, C Boudraa, B Diallo, C Lupin, S Herson, A Simon, N Edeb, D Salmon-Ceron, L Guillevin, T Tahi, M P Pietri, L Weiss, D Tisne-Dessus, C Jalbert, P Yeni, S Matheron, G Pahlavan, B Phung, N El-Alami Talbi, Z Ramani, G Catalano, C Godard, F Boue, V Chambrin, D Bornarel, H Schoen, R Carlier, B Fantin, A Uludag, C Poder, R Dhote, M Bentata, P Honore, O Bouchaud, Xuan Tuyet, J F Delfraissy, C Goujard, F Chaix, M T Rannou, Y Levy, A Sobel, C Dumont, A Cabie, S Abel, S Pierre-François, V Beaujolais, I Poizot-Martin, O Zaegel-Faucher, C Debreux, J Moreau, S Mokhtari, E Van Der Gheynst, M C Thiebaut-Drobacheff, A Foltzer, B Hoen, J F Faucher, H Gil, M Dupon, J M Ragnaud, I Raymond, P Morlat, I Louis, M Hessamfar, J Reynes, V Baillat, C Merle De Boever, C Tramoni, A Soufflet, P Guadagnin, F Bastides, P Choutet, L Bernard, F Raffi, O Mounoury, V Reliquet, D Brosseau, H Hue, T May, S Wassoumbou, M Stenzel, M P Bouillon, Y Yazdanpanah, T Huleux, E Aissi, S Pavel, D Rey, C Cheneau, P Fischer, M Partisani, G Blaison, M Mohseni Zadeh, M Martinot, A Pachart, F Jeanblanc, J L Touraine, C Trepo, P Miailhes, K Kouadjo, V Thoirain, C Brochier, P Perre, S Leautez, J L Esnault, I Suaud

Affiliations

¹ INSERM CESP U1018, Université Paris-Saclay, Le Kremlin-Bicêtre, France.
² Assistance Publique-Hôpitaux de Paris (AP-HP), Epidemiology and Public Health Department, Hôpitaux Universitaires Paris-Saclay, Le Kremlin-Bicêtre, France.
³ Assistance Publique-Hôpitaux de Paris (AP-HP), Department of Clinical Microbiology, Necker-Enfants Malades Hospital, Paris, France.
⁴ URP 7328 FETUS, Université Paris Cité, Paris, France.
⁵ Assistance Publique-Hôpitaux de Paris (AP-HP), General Pediatrics and Infectious Diseases, Robert Debré Hospital, Paris, France.
⁶ Université Paris Cité, Paris, France.
⁷ Assistance Publique-Hôpitaux de Paris (AP-HP), Pediatric Hematology and Oncology Department, Trousseau Hospital, Paris, France.
⁸ Pediatric Department, Saint-Pierre Hospital, Brussels, Belgium.
⁹ Université Libre de Bruxelles, Belgium.
¹⁰ Université d'Orléans, CHU Orléans, Laboratoire de Virologie, Orléans, France.
¹¹ Université Paris Cité, INSERM U1016, CNRS UMR8104, Institut Cochin, Paris, France.
¹² Department of Public Health, Faculty of Medicine and Biomedical Sciences, University of Yaoundé 1, Yaoundé, Cameroon.
¹³ Assistance Publique-Hôpitaux de Paris (AP-HP), Paediatric Immunology and Hematology Unit, Necker Enfants Malades Hospital, Paris, France.
¹⁴ Assistance Publique-Hôpitaux de Paris (AP-HP), Internal Medicine and Clinical Immunology Department, Hôpitaux Universitaires Paris-Saclay, Le Kremlin-Bicêtre, France.
¹⁵ Assistance Publique-Hôpitaux de Paris (AP-HP), Immunology-Infectious Diseases Unit, Hôtel-Dieu Hospital, Université Paris Cité, Paris, France.

Abstract

Background: No study has compared the virological and immunological status of young people with perinatally-acquired HIV infection (P-HIV) with that of people with HIV adulthood (A-HIV) having a similar duration of infection.

Methods: 5 French cohorts of P-HIV and A-HIV patients with a known date of HIV-infection and receiving antiretroviral treatment (ART), were used to compare the following proportions of: virological failure (VF) defined as plasma HIV RNA ≥ 50 copies/mL, CD4 cell percentages and CD4:CD8 ratios, at the time of the most recent visit since 2012. The analysis was stratified on time since infection, and multivariate models were adjusted for demographics and treatment history.

Findings: 310 P-HIV were compared to 1515 A-HIV (median current ages 20.9 [IQR:14.4-25.5] and 45.9 [IQR:37.9-53.5] respectively). VF at the time of the most recent evaluation was significantly higher among P-HIV (22.6%, 69/306) than A-HIV (3.3%, 50/1514); p ≤ 0.0001. The risk of VF was particularly high among the youngest children (2-5 years), adolescents (13-17 years) and young adults (18-24 years), compared to A-HIV with a similar duration of infection: adjusted Odds-Ratio (aOR) 7.0 [95% CI: 1.7; 30.0], 11.4 [4.2; 31.2] and 3.3 [1.0; 10.8] respectively. The level of CD4 cell percentages did not differ between P-HIV and A-HIV. P-HIV aged 6-12 and 13-17 were more likely than A-HIV to have a CD4:CD8 ratio ≥ 1: 84.1% vs. 58.8% (aOR = 3.5 [1.5; 8.3]), and 60.9% vs. 54.7% (aOR = 1.9 [0.9; 4.2]) respectively.

Interpretation: P-HIV were at a higher risk of VF than A-HIV with a similar duration of infection, even after adjusting for treatment history, whereas they were not at a higher risk of immunological impairment. Exposure to viral replication among young patients living with HIV since birth or a very early age, probably because of lower adherence, could have an impact on health, raising major concerns about the selection of resistance mutations and the risk of HIV transmission.

Funding: Inserm - ANRS MIE.

Keywords: Cohort; Epidemiology; Immunological outcome; Perinatal HIV infection; Viral failure.