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Original Articles

Can Probiotics Reduce Inflammation and Enhance Gut Immune Health in People Living with HIV: Study Designs for the Probiotic Visbiome for Inflammation and Translocation (PROOV IT) Pilot Trials

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References

  • van Sighem AI, Gras LA, Reiss P, Brinkman K, de Wolf F, study Anoc. Life expectancy of recently diagnosed asymptomatic HIV-infected patients approaches that of uninfected individuals. AIDS. 2010;24:1527–1535.10.1097/QAD.0b013e32833a3946
  • Capeau J. Premature aging and premature age-related comorbidities in HIV-infected patients: Facts and hypotheses. Clin Infect Dis. 2011;53:1127–1129.10.1093/cid/cir628
  • Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods. 2010;7:335–336.
  • Deeks SG. Immune dysfunction, inflammation, and accelerated aging in patients on antiretroviral therapy. Top HIV Med. 2009;17:118–123.
  • Rajasuriar R, Khoury G, Kamarulzaman A, French MA, Cameron PU, Lewin SR. Persistent immune activation in chronic HIV infection AIDS. 2013;27:1199–1208.10.1097/QAD.0b013e32835ecb8b
  • Klatt NR, Canary LA, Sun X, et al. Probiotic/prebiotic supplementation of antiretrovirals improves gastrointestinal immunity in SIV-infected macaques. J Clin Invest. 2013;123:903–907.
  • Estes JD, Harris LD, Klatt NR, et al. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. 2010;6:e1001052.10.1371/journal.ppat.1001052
  • Kim CJ, Nazli A, Rojas OL, et al. A role for mucosal IL-22 production and Th22 cells in HIV-associated mucosal immunopathogenesis. Mucosal Immunol. 2012;5:670–680.10.1038/mi.2012.72
  • Nazli A, Chan O, Dobson-Belaire WN, et al. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog. 2010;6:e1000852.10.1371/journal.ppat.1000852
  • Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12:1365–1371.
  • Brenchley JM, Schacker TW, Ruff LE, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med. 2004;200:749–759.10.1084/jem.20040874
  • Veazey RS, DeMaria M, Chalifoux LV, et al. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science. 1998;280:427–431.10.1126/science.280.5362.427
  • Kim CJ, McKinnon LR, Kovacs C, et al. Mucosal Th17 cell function is altered during HIV infection and is an independent predictor of systemic immune activation. J Immunol. 2013;191:2164–2173.10.4049/jimmunol.1300829
  • Chege D, Sheth PM, Kain T, et al. Sigmoid Th17 populations, the HIV latent reservoir, and microbial translocation in men on long-term antiretroviral therapy. AIDS. 2011;25:741–749.10.1097/QAD.0b013e328344cefb
  • Glocker EO, Hennigs A, Nabavi M, et al. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med. 2009;361:1727–1735.10.1056/NEJMoa0810719
  • Symons A, Budelsky AL, Towne JE. Are Th17 cells in the gut pathogenic or protective? Mucosal Immunol. 2012;5:4–6.10.1038/mi.2011.51
  • Kisand K, Bøe Wolff AS, Podkrajšek KT, et al. Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J Exp Med. 2010;207:299–308.10.1084/jem.20091669
  • Cavani A, Pennino D, Eyerich K. Th17 and Th22 in skin allergy. Chem Immunol Allergy. 2012;96:39–44.10.1159/000331870
  • Vujkovic-Cvijin I, Dunham RM, Iwai S, et al. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci Transl Med. 2013;5:193–191.
  • Dillon SM, Lee EJ, Kotter CV, et al. An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia. Mucosal Immunol. 2014;7:983–994.
  • Klase Z, Ortiz A, Deleage C, et al. Dysbiotic bacteria translocate in progressive SIV infection. Mucosal Immunol. 2015;8:1009–1020.10.1038/mi.2014.128
  • Sandler NG, Wand H, Roque A, et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis. 2011;203:780–790.10.1093/infdis/jiq118
  • Mehandru S, Poles MA, Tenner-Racz K, et al. Lack of mucosal immune reconstitution during prolonged treatment of acute and early HIV-1 infection. PLoS Med. 2006;3:e484.10.1371/journal.pmed.0030484
  • Guadalupe M, Sankaran S, George MD, et al. Viral suppression and immune restoration in the gastrointestinal mucosa of human immunodeficiency virus type 1-infected patients initiating therapy during primary or chronic infection. J Virol. 2006;80:8236–8247.10.1128/JVI.00120-06
  • Fernandes SM, Pires AR, Ferreira C, et al. Enteric mucosa integrity in the presence of a preserved innate interleukin 22 compartment in HIV type 1-treated individuals. J Infect Dis. 2014;210:630–640.10.1093/infdis/jiu126
  • Marchetti G, Gori A, Casabianca A, et al. Comparative analysis of T-cell turnover and homeostatic parameters in HIV-infected patients with discordant immune-virological responses to HAART. AIDS. 2006;20:1727–1736.10.1097/01.aids.0000242819.72839.db
  • Hunt PW, Deeks SG, Rodriguez B, et al. Continued CD4 cell count increases in HIV-infected adults experiencing 4 years of viral suppression on antiretroviral therapy. AIDS. 2003;17:1907–1915.10.1097/00002030-200309050-00009
  • Lederman MM, Calabrese L., Funderburg NT, et al. Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J Infect Dis. 2011;204:1217–1226.10.1093/infdis/jir507
  • Lichtenstein KA, Armon C, Buchacz K, et al. Low CD4+ T cell count is a risk factor for cardiovascular disease events in the HIV outpatient study. Clin Infect Dis. 2010;51:435–447.10.1086/652978
  • Zoufaly A, Cozzi-Lepri A, Reekie J, et al. Immuno-virological discordance and the risk of non-AIDS and AIDS events in a large observational cohort of HIV-patients in Europe. PLoS One. 2014;9:e87160.10.1371/journal.pone.0087160
  • Engsig FN, Zangerle R, Katsarou O, et al. Long-term mortality in HIV-positive individuals virally suppressed for >3 years with incomplete CD4 recovery. Clin Infect Dis. 2014;58:1312–1321.10.1093/cid/ciu038
  • Tincati C, Merlini E, Braidotti P, et al. Impaired gut junctional complexes feature late-treated individuals with suboptimal CD4+ T-cell recovery upon virologically-suppressive cART. AIDS. 2016;30:991–1003.
  • Klatt NR, Funderburg NT, Brenchley JM, et al. Microbial translocation, immune activation, and HIV disease. Trends Microbiol. 2013;21:6–13.10.1016/j.tim.2012.09.001
  • Bica I, Tang AM, Skinner S, et al. Use of complementary and alternative therapies by patients with human immunodeficiency virus disease in the era of highly active antiretroviral therapy. J Altern Complement Med. 2003;9:65–76.10.1089/107555303321222955
  • Josephs JS, Fleishman JA, Gaist P, Gebo KA, Network HIVR. Use of complementary and alternative medicines among a multistate, multisite cohort of people living with HIV/AIDS. HIV Med. 2007;8:300–305.10.1111/hiv.2007.8.issue-5
  • Ontario HIV Treatment Network (OHTN). Priority populations. 2014; Accessed June, 2015. http://www.ohtn.on.ca/otw-portfolio/priority-populations/
  • Morelli L, Capurso L. FAO/WHO guidelines on probiotics. J Clin Gastroenterol. 2012;46:S1–S2.10.1097/MCG.0b013e318269fdd5
  • Zielinski CE, Mele F, Aschenbrenner D, et al. Pathogen-induced human TH17 cells produce IFN-γ or IL-10 and are regulated by IL-1β. Nature. 2012;484:514–518.10.1038/nature10957
  • Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–498.10.1016/j.cell.2009.09.033
  • Mutlu EA, Keshavarzian A, Losurdo J, et al. A compositional look at the human gastrointestinal microbiome and immune activation parameters in HIV infected subjects. PLoS Pathog. 2014;10:e1003829.10.1371/journal.ppat.1003829
  • Chapman TM, Plosker GL, Figgitt DP. VSL#3 probiotic mixture: A review of its use in chronic inflammatory bowel diseases. Drugs. 2006;66:1371–1387.10.2165/00003495-200666100-00006
  • Ortiz AM, Klase ZA, DiNapoli SR, et al. IL-21 and probiotic therapy improve Th17 frequencies, microbial translocation, and microbiome in ARV-treated, SIV-infected macaques. Mucosal Immunology. 2016;9:458–467.
  • Miller H, Ferris R, Phelps BR. The effect of probiotics on CD4 counts among people living with HIV: A systematic review. Benef Microbes. 2016;1–8.10.3920/BM2015.0163
  • Villar-García J, Hernández JJ, Güerri-Fernández R, et al. Effect of probiotics (Saccharomyces boulardii) on microbial translocation and inflammation in HIV-treated patients. J Acquir Immune Defic Syndr. 2015;68:256–263.10.1097/QAI.0000000000000468
  • Stiksrud B, Nowak P, Nwosu FC, et al. Reduced levels of D-dimer and changes in gut microbiota composition after probiotic intervention in HIV-infected individuals on stable ART. J Acquir Immune Defic Syndr. 2015;70:329–337.10.1097/QAI.0000000000000784
  • Yang OO, Kelesidis T, Cordova R, Khanlou H. Immunomodulation of antiretroviral drug-suppressed chronic HIV-1 infection in an oral probiotic double-blind placebo-controlled trial. AIDS Res Hum Retroviruses. 2014;30:988–995.10.1089/aid.2014.0181
  • d’Ettorre G, Ceccarelli G, Giustini N, et al. Probiotics reduce inflammation in antiretroviral treated, HIV-infected individuals: Results of the “Probio-HIV” clinical trial. PLoS One. 2015;10:137200.
  • Services DoHaH. Panel on antiretroviral guidelines for adults and adolescents. Guidelines for the use of antiretroviral agents in HIV-1-infected adults and adolescents. Department of Health and Human Services. . Available at http://www.aidsinfo.nih.gov/ContentFiles/AdultandAdolescentGL.pdf. 2015; Accessed June 18, 2015.
  • Eyerich S, Eyerich K, Pennino D, et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest. 2009;119:3573–3585.
  • Ciccone EJ, Read SW, Mannon PJ, et al. Cycling of gut mucosal CD4+ T cells decreases after prolonged anti-retroviral therapy and is associated with plasma LPS levels. Mucosal Immunol. 2010;3:172–181.10.1038/mi.2009.129
  • Kuller LH, Tracy R, Belloso W, et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med. 2008;5:e203.10.1371/journal.pmed.0050203
  • Teshima CW, Meddings JB. The measurement and clinical significance of intestinal permeability. Curr Gastroenterol Rep. 2008;10:443–449.10.1007/s11894-008-0083-y
  • Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474:327–336.10.1038/nature10213
  • Liu CM, Osborne BJ, Hungate BA, et al. The semen microbiome and its relationship with local immunology and viral load in HIV infection. PLoS Pathog. 2014;10:e1004262.10.1371/journal.ppat.1004262
  • Sheth PM, Chege D, Shin LY, et al. Immune reconstitution in the sigmoid colon after long-term HIV therapy. Mucosal Immunol. 2008;1:382–388.10.1038/mi.2008.23
  • Adams MR. Safety of industrial lactic acid bacteria. J Biotechnol. 1999;68:171–178.10.1016/S0168-1656(98)00198-9
  • Borriello SP, Hammes WP, Holzapfel W, et al. Safety of probiotics that contain lactobacilli or bifidobacteria. Clin Infect Dis. 2003;36:775–780.10.1086/cid.2003.36.issue-6
  • Boyle RJ, Tang ML. The role of probiotics in the management of allergic disease. Clin Exp Allergy. 2006;36:568–576.10.1111/cea.2006.36.issue-5
  • Sankaran-Walters S, Macal M, Grishina I, et al. Sex differences matter in the gut: Effect on mucosal immune activation and inflammation. Biol Sex Differ. 2013;4:10.10.1186/2042-6410-4-10
  • Remis RS, Liu J. HIV/AIDS in Ontario: Preliminary Report, 2011. Toronto: University of Toronto; 2013.
  • Hunt PW, Martin JN, Sinclair E, et al. T cell activation is associated with lower CD4+ T cell gains in human immunodeficiency virus–infected patients with sustained viral suppression during antiretroviral therapy. J Infect Dis. 2003;187:1534–1543.10.1086/jid.2003.187.issue-10
  • Schacker TW, Reilly C, Beilman GJ, et al. Amount of lymphatic tissue fibrosis in HIV infection predicts magnitude of HAART-associated change in peripheral CD4 cell count. AIDS. 2005;19:2169–2171.10.1097/01.aids.0000194801.51422.03
  • Liu Z, Cumberland WG, Hultin LE, Prince HE, Detels R, Giorgi JV. Elevated CD38 antigen expression on CD8+ T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and Death in the multicenter AIDS cohort study than CD4+ cell count, soluble immune activation markers, or combinations of HLA-DR and CD38 expression. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;16:83–92.10.1097/00042560-199710010-00003
  • Paiardini M, Müller-Trutwin M. HIV-associated chronic immune activation. Immunol Rev. 2013;254:78–101.10.1111/imr.12079

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