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Published in: Journal of Translational Medicine 1/2018

Open Access 01-12-2018 | Research

Improved CD4 T cell profile in HIV-infected subjects on maraviroc-containing therapy is associated with better responsiveness to HBV vaccination

Authors: Inés Herrero-Fernández, Isaac Rosado-Sánchez, Miguel Genebat, Laura Tarancón-Díez, María Mar Rodríguez-Méndez, María Mar Pozo-Balado, Carmen Lozano, Ezequiel Ruiz-Mateos, Manuel Leal, Yolanda M. Pacheco

Published in: Journal of Translational Medicine | Issue 1/2018

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Abstract

Background

Maraviroc-containing combined antiretroviral therapy (MVC-cART) improved the response to the hepatitis B virus (HBV) vaccine in HIV-infected subjects younger than 50 years old. We aimed here to explore the effect of this antiretroviral therapy on different immunological parameters that could account for this effect.

Methods

We analysed baseline samples of vaccinated subjects under 50 years old (n = 41). We characterized the maturational subsets and the expression of activation, senescence and prone-to-apoptosis markers on CD4 T-cells; we also quantified T-regulatory cells (Treg) and dendritic cell (DC) subsets. We used binary logistic regression to evaluate the immunological impact of MVC-cART, correlation with MVC exposure and linear regression for association with the magnitude of the HBV vaccine response.

Results

HIV-infected subjects on MVC-cART prior to vaccination showed increased recent thymic emigrants levels and reduced myeloid-DC levels. A longer exposure to MVC-cART was associated with lower frequencies of Tregs and activated and proliferating CD4 T-cells. Furthermore, the frequencies of activated and proliferating CD4 T-cells were inversely associated with the magnitude of the HBV vaccine response.

Conclusion

The beneficial effect of MVC-cART in the HBV vaccine response in subjects below 50 years old could be partially mediated by its reducing effect on the frequencies of activated and proliferating CD4 T-cells prior to vaccination.
Appendix
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Literature
1.
go back to reference Thio CL. Hepatitis B and human immunodeficiency virus coinfection. Hepatology. 2009;49(5 suppl):S138–45.CrossRefPubMed Thio CL. Hepatitis B and human immunodeficiency virus coinfection. Hepatology. 2009;49(5 suppl):S138–45.CrossRefPubMed
2.
go back to reference Clifford GM, Rickenbach M, Polesel J, Dal Maso L, Steffen I, Ledergerber B, et al. Influence of HIV-related immunodeficiency on the risk of hepatocellular carcinoma. AIDS. 2008;22(16):2135–41.CrossRefPubMed Clifford GM, Rickenbach M, Polesel J, Dal Maso L, Steffen I, Ledergerber B, et al. Influence of HIV-related immunodeficiency on the risk of hepatocellular carcinoma. AIDS. 2008;22(16):2135–41.CrossRefPubMed
3.
go back to reference Whitaker JA, Rouphael NG, Edupuganti S, Lai L, Mulligan MJ. Strategies to increase responsiveness to hepatitis B vaccination in adults with HIV-1. Lancet Infect Dis. 2012;12:966–76.CrossRefPubMedPubMedCentral Whitaker JA, Rouphael NG, Edupuganti S, Lai L, Mulligan MJ. Strategies to increase responsiveness to hepatitis B vaccination in adults with HIV-1. Lancet Infect Dis. 2012;12:966–76.CrossRefPubMedPubMedCentral
4.
go back to reference Westrop SJ, Moyle G, Jackson A, Nelson M, Mandalia S, Imami N. CCR5 antagonism impacts vaccination response and immune profile in HIV-1 infection. Mol Med. 2012;18:1240–8.CrossRefPubMedPubMedCentral Westrop SJ, Moyle G, Jackson A, Nelson M, Mandalia S, Imami N. CCR5 antagonism impacts vaccination response and immune profile in HIV-1 infection. Mol Med. 2012;18:1240–8.CrossRefPubMedPubMedCentral
5.
go back to reference Herrero-Fernández I, Pacheco YM, Genebat M, Rodriguez-Méndez MDM, Lozano MDC, Polaino MJ, et al. Association between a suppressive combined antiretroviral therapy containing maraviroc and the hepatitis B virus vaccine response. Antimicrob Agents Chemother. 2017;62(1):e02050–117.CrossRefPubMedPubMedCentral Herrero-Fernández I, Pacheco YM, Genebat M, Rodriguez-Méndez MDM, Lozano MDC, Polaino MJ, et al. Association between a suppressive combined antiretroviral therapy containing maraviroc and the hepatitis B virus vaccine response. Antimicrob Agents Chemother. 2017;62(1):e02050–117.CrossRefPubMedPubMedCentral
6.
go back to reference Romero-Sánchez MC, Alvarez-Ríos AI, Bernal-Morell E, Genebat M, Vera F, Benhnia MR, et al. Maintenance of virologic efficacy and decrease in levels of β2-microglobulin, soluble CD40L and soluble CD14 after switching previously treated HIV-infected patients to an NRTI-sparing dual therapy. Antiviral Res. 2014;111:26–32.CrossRefPubMed Romero-Sánchez MC, Alvarez-Ríos AI, Bernal-Morell E, Genebat M, Vera F, Benhnia MR, et al. Maintenance of virologic efficacy and decrease in levels of β2-microglobulin, soluble CD40L and soluble CD14 after switching previously treated HIV-infected patients to an NRTI-sparing dual therapy. Antiviral Res. 2014;111:26–32.CrossRefPubMed
7.
go back to reference Funderburg N, Kalinowska M, Eason J, Goodrich J, Heera J, Mayer H, et al. Effects of maraviroc and efavirenz on markers of immune activation and inflammation and associations with CD4+ cell rises in HIV-infected patients. PLoS ONE. 2010;5(10):e13188.CrossRefPubMedPubMedCentral Funderburg N, Kalinowska M, Eason J, Goodrich J, Heera J, Mayer H, et al. Effects of maraviroc and efavirenz on markers of immune activation and inflammation and associations with CD4+ cell rises in HIV-infected patients. PLoS ONE. 2010;5(10):e13188.CrossRefPubMedPubMedCentral
8.
go back to reference Romero-Sánchez MC, Machmach K, Gonzalez-Serna A, Genebat M, Pulido I, García-García M, et al. Effect of maraviroc on HIV disease progression-related biomarkers. Antimicrob Agents Chemother. 2012;56:5858–64.CrossRefPubMedPubMedCentral Romero-Sánchez MC, Machmach K, Gonzalez-Serna A, Genebat M, Pulido I, García-García M, et al. Effect of maraviroc on HIV disease progression-related biomarkers. Antimicrob Agents Chemother. 2012;56:5858–64.CrossRefPubMedPubMedCentral
9.
go back to reference Serrano-Villar S, Sainz T, Ma ZM, Utay NS, Wook-Chun T, Mann S, et al. Effects of combined CCR5/integrase inhibitors-based regimen on mucosal immunity in HIV-infected patients naïve to antiretroviral therapy: a pilot randomized trial. PLoS Pathog. 2016;12:e1005540.CrossRefPubMedPubMedCentral Serrano-Villar S, Sainz T, Ma ZM, Utay NS, Wook-Chun T, Mann S, et al. Effects of combined CCR5/integrase inhibitors-based regimen on mucosal immunity in HIV-infected patients naïve to antiretroviral therapy: a pilot randomized trial. PLoS Pathog. 2016;12:e1005540.CrossRefPubMedPubMedCentral
10.
go back to reference Taiwo BO, Chan ES, Fichtenbaum CJ, Ribaudo H, Tsibris A, Klingman KL, et al. Less bone loss with maraviroc-versus tenofovir-containing antiretroviral therapy in the AIDS Clinical Trials Group A5303 Study. Clin Infect Dis. 2015;61:1179–88.CrossRefPubMedPubMedCentral Taiwo BO, Chan ES, Fichtenbaum CJ, Ribaudo H, Tsibris A, Klingman KL, et al. Less bone loss with maraviroc-versus tenofovir-containing antiretroviral therapy in the AIDS Clinical Trials Group A5303 Study. Clin Infect Dis. 2015;61:1179–88.CrossRefPubMedPubMedCentral
11.
go back to reference Pozo-Balado MM, Martínez-Bonet M, Rosado I, Ruiz-Mateos E, Méndez- Lagares G, Rodríguez-Méndez MM, et al. Maraviroc reduces the regulatory T-cell frequency in antiretroviral-naive HIV-infected subjects. J Infect Dis. 2014;210:890–8.CrossRefPubMed Pozo-Balado MM, Martínez-Bonet M, Rosado I, Ruiz-Mateos E, Méndez- Lagares G, Rodríguez-Méndez MM, et al. Maraviroc reduces the regulatory T-cell frequency in antiretroviral-naive HIV-infected subjects. J Infect Dis. 2014;210:890–8.CrossRefPubMed
12.
go back to reference Pozo-Balado MM, Rosado-Sánchez I, Méndez-Lagares G, Rodríguez-Méndez MM, Ruiz-Mateos E, Benhnia MR, et al. Maraviroc contributes to the restoration of the homeostasis of regulatory T-cell subsets in antiretroviral-naive HIV-infected subjects. Clin Microbiol Infect. 2016;22:461.CrossRefPubMed Pozo-Balado MM, Rosado-Sánchez I, Méndez-Lagares G, Rodríguez-Méndez MM, Ruiz-Mateos E, Benhnia MR, et al. Maraviroc contributes to the restoration of the homeostasis of regulatory T-cell subsets in antiretroviral-naive HIV-infected subjects. Clin Microbiol Infect. 2016;22:461.CrossRefPubMed
13.
go back to reference Pozo-Balado MM, Leal M, Méndez Lagares G, Mata RC, López-Cortés LF, Viciana P, et al. Increased regulatory T cell counts in HIV-infected nonresponders to hepatitis B virus vaccine. J Infect Dis. 2010;202:362–9.CrossRef Pozo-Balado MM, Leal M, Méndez Lagares G, Mata RC, López-Cortés LF, Viciana P, et al. Increased regulatory T cell counts in HIV-infected nonresponders to hepatitis B virus vaccine. J Infect Dis. 2010;202:362–9.CrossRef
14.
go back to reference Egea E, Iglesias A, Salazar M, Morimoto C, Kruskall MS, Awdeh Z, et al. The cellular basis for lack of antibody response to hepatitis B vaccine in humans. J Exp Med. 1991;173:531–8.CrossRefPubMed Egea E, Iglesias A, Salazar M, Morimoto C, Kruskall MS, Awdeh Z, et al. The cellular basis for lack of antibody response to hepatitis B vaccine in humans. J Exp Med. 1991;173:531–8.CrossRefPubMed
15.
go back to reference Filion LG, Saginur R, Szczerbak N. Humoral and cellular immune responses by normal individuals to hepatitis B surface antigen vaccination. J Exp Immunol. 1988;71:405–9. Filion LG, Saginur R, Szczerbak N. Humoral and cellular immune responses by normal individuals to hepatitis B surface antigen vaccination. J Exp Immunol. 1988;71:405–9.
16.
go back to reference Yao ZQ, Moorman JP. Immune exhaustion and immune senescence: two distinct pathways for HBV vaccine failure during HCV and/or HIV infection. Arch Immunol Ther Exp. 2013;61:193–201.CrossRef Yao ZQ, Moorman JP. Immune exhaustion and immune senescence: two distinct pathways for HBV vaccine failure during HCV and/or HIV infection. Arch Immunol Ther Exp. 2013;61:193–201.CrossRef
17.
go back to reference Vrisekoop N, van Gent R, de Boer AB, Otto SA, Borleffs JC, Steingrover R, et al. Restoration of the CD4 T cell compartment after long-term highly active antiretroviral therapy without phenotypical signs of accelerated immunological aging. J Immunol. 2008;181:1573–81.CrossRefPubMed Vrisekoop N, van Gent R, de Boer AB, Otto SA, Borleffs JC, Steingrover R, et al. Restoration of the CD4 T cell compartment after long-term highly active antiretroviral therapy without phenotypical signs of accelerated immunological aging. J Immunol. 2008;181:1573–81.CrossRefPubMed
18.
go back to reference Overton ET, Sungkanuparph S, Powderly WG, Seyfried W, Groger RK, Aberg JA. Undetectable plasma HIV RNA load predicts success after hepatitis B vaccination in HIV-infected persons. Clin Infect Dis. 2005;41:1045–8.CrossRefPubMed Overton ET, Sungkanuparph S, Powderly WG, Seyfried W, Groger RK, Aberg JA. Undetectable plasma HIV RNA load predicts success after hepatitis B vaccination in HIV-infected persons. Clin Infect Dis. 2005;41:1045–8.CrossRefPubMed
19.
go back to reference Leeansyah E, Cameron PU, Solomon A, Tennakoon S, Velayudham P, Gouillou M, et al. Inhibition of telomerase activity by human immunodeficiency virus (HIV) nucleos(t)ide reverse transcriptase inhibitors: a potential factor contributing to HIV-associated accelerated aging. J Infect Dis. 2013;207:1157–65.CrossRefPubMed Leeansyah E, Cameron PU, Solomon A, Tennakoon S, Velayudham P, Gouillou M, et al. Inhibition of telomerase activity by human immunodeficiency virus (HIV) nucleos(t)ide reverse transcriptase inhibitors: a potential factor contributing to HIV-associated accelerated aging. J Infect Dis. 2013;207:1157–65.CrossRefPubMed
20.
go back to reference Najarro K, Nguyen H, Chen G, Xu M, Alcorta S, Yao X, et al. Telomere length as an indicator of the robustness of B- and T-cell response to influenza in older adults. J Infect Dis. 2015;212(8):1261–9.CrossRefPubMedPubMedCentral Najarro K, Nguyen H, Chen G, Xu M, Alcorta S, Yao X, et al. Telomere length as an indicator of the robustness of B- and T-cell response to influenza in older adults. J Infect Dis. 2015;212(8):1261–9.CrossRefPubMedPubMedCentral
21.
go back to reference Gonzalez-Serna A, Ferrando-Martinez S, Tarancon-Diez L, De Pablo-Bernal RS, Dominguez-Molina B, Jiménez JL, et al. Increased CD127+ and decreased CD57+ T cell expression levels in HIV-infected patients on NRTI-sparing regimens. J Transl Med. 2017;15(1):259.CrossRefPubMedPubMedCentral Gonzalez-Serna A, Ferrando-Martinez S, Tarancon-Diez L, De Pablo-Bernal RS, Dominguez-Molina B, Jiménez JL, et al. Increased CD127+ and decreased CD57+ T cell expression levels in HIV-infected patients on NRTI-sparing regimens. J Transl Med. 2017;15(1):259.CrossRefPubMedPubMedCentral
22.
go back to reference Pulido I, Genebat M, Alvarez-Rios AI, De Pablo-Bernal RS, Rafii-El-Idrissi Benhnia M, Pacheco YM, et al. Immunovirological efficacy of once-daily maraviroc plus ritonavir-boosted atazanavir After 48 weeks in naive HIV-infected patients. Viral Immunol. 2016;29(8):471–7.CrossRefPubMed Pulido I, Genebat M, Alvarez-Rios AI, De Pablo-Bernal RS, Rafii-El-Idrissi Benhnia M, Pacheco YM, et al. Immunovirological efficacy of once-daily maraviroc plus ritonavir-boosted atazanavir After 48 weeks in naive HIV-infected patients. Viral Immunol. 2016;29(8):471–7.CrossRefPubMed
23.
go back to reference Wilson CM, Ellenberg JH, Sawyer MK, Belzer M, Crowley-Nowick PA, Puga A, et al. Adolescent Medicine HIV/AIDS Research Network. Serologic response to hepatitis B vaccine in HIV infected and high-risk HIV uninfected adolescents in the REACH cohort. Reaching for excellence in adolescent care and health. J Adolesc Health. 2001;29:123–9.CrossRefPubMed Wilson CM, Ellenberg JH, Sawyer MK, Belzer M, Crowley-Nowick PA, Puga A, et al. Adolescent Medicine HIV/AIDS Research Network. Serologic response to hepatitis B vaccine in HIV infected and high-risk HIV uninfected adolescents in the REACH cohort. Reaching for excellence in adolescent care and health. J Adolesc Health. 2001;29:123–9.CrossRefPubMed
24.
go back to reference Anthony DD, Umbleja T, Aberg JA, Kang M, Medvik K, Lederman MM, et al. Lower peripheral blood CD14+ monocyte frequency and higher CD34+ progenitor cell frequency are associated with HBV vaccine induced response in HIV infected individuals. Vaccine. 2011;29:3558–63.CrossRefPubMedPubMedCentral Anthony DD, Umbleja T, Aberg JA, Kang M, Medvik K, Lederman MM, et al. Lower peripheral blood CD14+ monocyte frequency and higher CD34+ progenitor cell frequency are associated with HBV vaccine induced response in HIV infected individuals. Vaccine. 2011;29:3558–63.CrossRefPubMedPubMedCentral
25.
go back to reference Veiga AP, Casseb J, Duarte AJ. Humoral response to hepatitis B vaccination and its relationship with T CD45RA+ (naive) and CD45RO+ (memory) subsets in HIV-1-infected subjects. Vaccine. 2006;4:7124–8.CrossRef Veiga AP, Casseb J, Duarte AJ. Humoral response to hepatitis B vaccination and its relationship with T CD45RA+ (naive) and CD45RO+ (memory) subsets in HIV-1-infected subjects. Vaccine. 2006;4:7124–8.CrossRef
26.
go back to reference Jing M, Wang J, Zhu S, Ao F, Wang L, Han T, et al. Development of a more efficient hepatitis B virus vaccine by targeting hepatitis B virus preS to dendritic cells. Vaccine. 2016;34(4):516–22.CrossRefPubMed Jing M, Wang J, Zhu S, Ao F, Wang L, Han T, et al. Development of a more efficient hepatitis B virus vaccine by targeting hepatitis B virus preS to dendritic cells. Vaccine. 2016;34(4):516–22.CrossRefPubMed
27.
go back to reference Jiang W, Younes SA, Funderburg NT, Mudd JC, Espinosa E, Davenport MP, et al. Cycling memory CD4+ T cells in HIV disease have a diverse T cell receptor repertoire and a phenotype consistent with bystander activation. J Virol. 2014;88(10):5369–80.CrossRefPubMedPubMedCentral Jiang W, Younes SA, Funderburg NT, Mudd JC, Espinosa E, Davenport MP, et al. Cycling memory CD4+ T cells in HIV disease have a diverse T cell receptor repertoire and a phenotype consistent with bystander activation. J Virol. 2014;88(10):5369–80.CrossRefPubMedPubMedCentral
28.
go back to reference Sauce D, Larsen M, Fastenackels S, Roux A, Gorochov G, Katlama C, et al. Lymphopenia-driven homeostatic regulation of naive T cells in elderly and thymectomized young adults. J Immunol. 2012;189(12):5541–8.CrossRefPubMed Sauce D, Larsen M, Fastenackels S, Roux A, Gorochov G, Katlama C, et al. Lymphopenia-driven homeostatic regulation of naive T cells in elderly and thymectomized young adults. J Immunol. 2012;189(12):5541–8.CrossRefPubMed
29.
go back to reference Kohler S, Thiel A. Life after the thymus: CD31+ and CD31− human naïve CD4+ T-cell subsets. Blood. 2009;113:769–74.CrossRefPubMed Kohler S, Thiel A. Life after the thymus: CD31+ and CD31− human naïve CD4+ T-cell subsets. Blood. 2009;113:769–74.CrossRefPubMed
30.
go back to reference Toka FN, Suvas S, Rouse BT. CD4+ CD25+ T cells regulate vaccine-generated primary and memory CD8+ T-cell responses against herpes simplex virus type 1. J Virol. 2004;78(23):13082–9.CrossRefPubMedPubMedCentral Toka FN, Suvas S, Rouse BT. CD4+ CD25+ T cells regulate vaccine-generated primary and memory CD8+ T-cell responses against herpes simplex virus type 1. J Virol. 2004;78(23):13082–9.CrossRefPubMedPubMedCentral
31.
go back to reference Espinoza-Mora MR, Steeg C, Tartz S, Heussler V, Sparwasser T, Link A, et al. Depletion of regulatory T cells augments a vaccine-induced T effector cell response against the liver-stage of malaria but fails to increase memory. PLoS ONE. 2014;9(8):e104627.CrossRefPubMedPubMedCentral Espinoza-Mora MR, Steeg C, Tartz S, Heussler V, Sparwasser T, Link A, et al. Depletion of regulatory T cells augments a vaccine-induced T effector cell response against the liver-stage of malaria but fails to increase memory. PLoS ONE. 2014;9(8):e104627.CrossRefPubMedPubMedCentral
33.
go back to reference Miyara M, Sakaguchi S. Natural regulatory T cells: mechanisms of suppression. Trends Mol Med. 2007;13:108–16.CrossRefPubMed Miyara M, Sakaguchi S. Natural regulatory T cells: mechanisms of suppression. Trends Mol Med. 2007;13:108–16.CrossRefPubMed
34.
go back to reference Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJ, John S, Taams LS. CD4+CD25+Foxp3+regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci USA. 2007;104:19446–51.CrossRefPubMed Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJ, John S, Taams LS. CD4+CD25+Foxp3+regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci USA. 2007;104:19446–51.CrossRefPubMed
35.
go back to reference Lim HW, Hillsamer P, Banham AH. KimCH. Cutting edge: direct suppression of B cells by CD4+CD25+ regulatory T cells. J Immunol. 2005;175:4180–3.CrossRefPubMed Lim HW, Hillsamer P, Banham AH. KimCH. Cutting edge: direct suppression of B cells by CD4+CD25+ regulatory T cells. J Immunol. 2005;175:4180–3.CrossRefPubMed
36.
go back to reference Shive CL, Judge CJ, Clagett B, Kalayjian RC, Osborn M, Sherman KE, et al. Pre-vaccine plasma levels of soluble inflammatory indices negatively predict responses to HAV, HBV, and tetanus vaccines in HCV and HIV infection. Vaccine. 2018;36(4):453–60.CrossRefPubMed Shive CL, Judge CJ, Clagett B, Kalayjian RC, Osborn M, Sherman KE, et al. Pre-vaccine plasma levels of soluble inflammatory indices negatively predict responses to HAV, HBV, and tetanus vaccines in HCV and HIV infection. Vaccine. 2018;36(4):453–60.CrossRefPubMed
37.
go back to reference Verschoor CP, Lelic A, Parsons R, Evelegh C, Bramson JL, Johnstone J, et al. Serum C-reactive protein and congestive heart failure as significant predictors of herpes zoster vaccine response in elderly nursing home residents. J Infect Dis. 2017;216(2):191–7.CrossRefPubMedPubMedCentral Verschoor CP, Lelic A, Parsons R, Evelegh C, Bramson JL, Johnstone J, et al. Serum C-reactive protein and congestive heart failure as significant predictors of herpes zoster vaccine response in elderly nursing home residents. J Infect Dis. 2017;216(2):191–7.CrossRefPubMedPubMedCentral
38.
go back to reference Fisman DN, Agrawal D, Leder K. The effect of age on immunologic response to recombinant hepatitis B vaccine: a meta-analysis. Clin Infect Dis. 2002;35:1368–75.CrossRefPubMed Fisman DN, Agrawal D, Leder K. The effect of age on immunologic response to recombinant hepatitis B vaccine: a meta-analysis. Clin Infect Dis. 2002;35:1368–75.CrossRefPubMed
39.
go back to reference Fuster F, Vargas JI, Jensen D, Sarmiento V, Acuña P, Peirano F, et al. CD4/CD8 ratio as a predictor of the response to HBV vaccination in HIV-positive patients: a prospective cohort study. Vaccine. 2016;34:1889–95.CrossRefPubMed Fuster F, Vargas JI, Jensen D, Sarmiento V, Acuña P, Peirano F, et al. CD4/CD8 ratio as a predictor of the response to HBV vaccination in HIV-positive patients: a prospective cohort study. Vaccine. 2016;34:1889–95.CrossRefPubMed
40.
go back to reference Caby F, Guihot A, Lambert-Niclot S, Guiguet M, Boutolleau D, Agher R, et al. Determinants of a low CD4/CD ratio in HIV-1 infected individuals despite long term viral suppression. Clin Infect Dis. 2016;62:1297–303.CrossRefPubMed Caby F, Guihot A, Lambert-Niclot S, Guiguet M, Boutolleau D, Agher R, et al. Determinants of a low CD4/CD ratio in HIV-1 infected individuals despite long term viral suppression. Clin Infect Dis. 2016;62:1297–303.CrossRefPubMed
41.
go back to reference Nozza S, Svicher V, Saracino A, d’Ettorre G, De Luca A, Maggiolo F, et al. State of the art of dual therapy in 2015. AIDS Rev. 2015;17:127–34.PubMed Nozza S, Svicher V, Saracino A, d’Ettorre G, De Luca A, Maggiolo F, et al. State of the art of dual therapy in 2015. AIDS Rev. 2015;17:127–34.PubMed
Metadata
Title
Improved CD4 T cell profile in HIV-infected subjects on maraviroc-containing therapy is associated with better responsiveness to HBV vaccination
Authors
Inés Herrero-Fernández
Isaac Rosado-Sánchez
Miguel Genebat
Laura Tarancón-Díez
María Mar Rodríguez-Méndez
María Mar Pozo-Balado
Carmen Lozano
Ezequiel Ruiz-Mateos
Manuel Leal
Yolanda M. Pacheco
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2018
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-018-1617-1

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