Effects of supplementation with probiotics on patients with the human immunodeficiency virus: a systematic review.
Article Sidebar
Main Article Content
Abstract
Objective: It is known that certain microorganisms improve the function of the intestinal barrier, which in turn is affected by infection by the Human Immunodeficiency Virus (HIV). This review aimed to identify the possible effects of supplementation with probiotics on patients affected by HIV. Methods: MEDLINE/PubMed and Lilacs databases published in English, from 2008 to 2018, with the descriptors “probiotics” AND “HIV” were used. Randomized clinical trials carried out on adult individuals with HIV who used probiotics were included. Non-original articles and works in a language other than English, animal and in vitro studies, studies on pregnant women, infants and people under the age of 18 years were excluded. Results: Of the 149 articles found, 10 met the inclusion criteria. The main strains used were of the genus Lactobacillus and Bifidobacterium. The main findings of the studies were related to the reduction of bacterial translocation and inflammation, increase in the number of CD4 + T cells and reduction of D-dimer, as well as improvement of gastrointestinal symptoms. Conclusions: There is evidence that supplementation with probiotics can be recommended in clinical practice as an adjunct to antiretroviral therapy. Due to the complexity of the subject, the scarcity and heterogeneity of the studies, further works are needed in order to determine strains, intervention time, dosages, and the effectiveness of probiotics in HIV-infected patients.
Article Details
Authors maintain copyright and grant the HSJ the right to first publication. From 2024, the publications wiil be licensed under Attribution 4.0 International 
, allowing their sharing, recognizing the authorship and initial publication in this journal.
Authors are authorized to assume additional contracts separately for the non-exclusive distribution of the version of the work published in this journal (e.g., publishing in an institutional repository or as a book chapter), with acknowledgment of authorship and initial publication in this journal.
Authors are encouraged to publish and distribute their work online (e.g., in institutional repositories or on their personal page) at any point after the editorial process.
Also, the AUTHOR is informed and consents that the HSJ can incorporate his article into existing or future scientific databases and indexers, under the conditions defined by the latter at all times, which will involve, at least, the possibility that the holders of these databases can perform the following actions on the article.
References
World Health Organization [Internet]. HIV/AIDS; Data and statistics 2019 [cited 2020 Apr 28]. Avaiable from: www.who.int/hiv/data/en/
Programa Conjunto das Nações Unidas sobre HIV e AIDS (UNAIDS) [Internet]. 2018 Global HIV Statistics [cited 2020 Mar 13]. Avaiable from: www.unaids.org/en/resources/fact-sheet
Villar-García J, Hernández JJ, Fernández RG, González A, Lerma E, Guelar A, et al. Effect of probiotics (Saccharomyces boulardii) on microbial translocation and inflammation in HIV-treated patients: a double-blind, randomized, placebo-controlled trial. J Acquir Immune Defic Syndr. 2015;68(3):256-63. doi: 10.1097/QAI.0000000000000468
Villar-García J, Fernández RG, Moya A, González A, Hernández JJ, Lerma E, et al. Impact of probiotic Saccharomyces boulardii on the gut microbiome composition in HIV treated patients: A double-blind, randomized, placebo-controlled trial. PLoS One. 2017;12(4):1-15. doi: 10.1371/journal.pone.0173802
FAO/WHO [Internet]. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Córdoba: 2001 [cited 2020 Apr 28]. Avaiable from: www.fao.org/3/a-a0512e.pdf
Anukam KC, Osazuwa EO, Osadolor HB, Bruce AW, Reid G. Yoghurt containing probiotic Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 helps resolve moderate diarrhoea and increases CD4 count in HIV/AIDS patients. J Clin Gastroenterol. 2008;42(3):239-43. doi: 10.1097/MCG.0b013e31802c7465
Souza, MLR. Probióticos e a permeabilidade intestinal. Pós em Revista. 2012;(6):299-306.
Hummelen R, Hemsworth J, Changalucha J, Butamanya NL, Hekmat S, Habbema JD, et al. Effect of micronutrient and probiotic fortified yogurt on immune-function of antiretroviral therapy naive HIV patients. Nutrients. 2011;3(10):897–909. doi: 10.3390/nu3100897
Feria MG, Taborda NA, Hernandez JC, Rugeles MT. Efecto de la terapia con probióticos/prebióticos sobre la reconstitución del tejido linfoide asociado a la mucosa gastrointestinal durante la infección por el virus de la inmunodeficiencia humana-1. Rev Med Chile. 2017;145(2):219-29. doi: 10.4067/s0034-9887201700020001
Moher D, Liberati A, Tetzlaff J, Altman DG, Prisma Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7): e1000097. doi: 10.1371/journal.pmed.1000097
Hummelen R, Changalucha J, Butamanya NL, Koyama TE, Cook A, Habbema DF, et al. Effect of 25 weeks probiotic supplementation on immune function of HIV patients. Gut Microbes. 2011;2(2):80-5. doi: 10.4161/gmic.2.2.15787
Hemsworth JC, Hekmat S, Reid G. Micronutrient supplemented probiotic yogurt for HIV-infected adults taking HAART in London, Canada. Gut Microbes. 2012;3(5):414–9. doi: 10.4161/gmic.21248
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(10):988–95. doi: 10.1089/AID.2014.0181
Stiksrud B, Nowak P, Nwosu FC, Kvale D, Thalme A, Sonnerborg A, 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(4):329–37. doi: 10.1097/QAI.0000000000000784
d‘Ettorre G, Ceccarelli G, Giustini N, Serafino S, Calantone N, De Girolamo G, et al. Probiotics reduce inflammation in antiretroviral treated, HIV-infected individuals: Results of the “Probio-HIV” Clinical trial. PLoS One. 2015;10(9):e0137200. doi: 10.1371/journal.pone.0137200
d‘Ettorre G, Rossi G, Scagnolari C, Andreotti M, Giustini N, Serafino S, et al. Probiotic supplementation promotes a reduction in T-cell activation, an increase in Th17 frequencies, and a recovery of intestinal epithelium integrity and mitochondrial morphology in ART-treated HIV-1-positive patients. Immun Inflamm Dis. 2017;5(3):244-60. doi: 10.1002/iid3.160
Arnbjerg CJ, Vestad B, Hov JR, Pedersen KK, Jespersen S, Johannesen HH, et al. Effect of Lactobacillus rhamnosus GG Supplementation on intestinal inflammation assessed by PET/MRI scans and gut microbiota composition in HIV-infected Individuals. J Acquir Immune Defic Syndr. 2018;78(4):450–7. doi: 10.1097/QAI.0000000000001693
Kaiser JD, Campa AM, Ondercin JP, Leoung GS, Pless RF, Baum MK. Micronutrient supplementation increases CD4 count in HIV-infected individuals on highly active antiretroviral therapy: A prospective, double-blinded, placebo-controlled trial. J Acquir Immune Defic Syndr. 2006;42(5):523-8. doi: 10.1097/01.qai.0000230529.25083.42
Kelly P, Shawa T, Mwanamakondo S, Soko R, Smith G, Barclay GR, et al. Gastric and intestinal barrier impairment in tropical enteropathy and HIV: limited impact of micronutrient supplementation during a randomised controlled trial. BMC Gastroenterol. 2010;10:72. doi: 10.1186/1471-230X-10-72
Fuller R, Gibson GR. Modification of the intestinal microflora using probiotics and prebiotics. Scand J Gastroenterol Suppl. 1997;222:28-31. doi: 10.1080/00365521.1997.11720714
Sandler NG, Douek DC. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol. 2012;10(9):655–66. doi: 10.1038/nrmicro2848
Zevin AS, McKinnon L, Burgener A, Klatt NR. Microbial translocation and microbiome dysbiosis in HIV-associated immune activation. Curr Opin HIV AIDS. 2016;11(2):182–90. doi: 10.1097/COH.0000000000000234
González-Hernández LA, Jave-Suarez LF, Fafutis-Morris M, Montes-Salcedo KE, Valle-Gutierrez LG, Campos-Loza AE, et al. Synbiotic therapy decreases microbial translocation and inflammation and improves immunological status in HIV-infected patients: a double blind randomized controlled pilot trial. Nutr J. 2012;11:90. doi: 10.1186/1475-2891-11-90
Trois, L. Uso de Probióticos em Crianças HIV Positivas: Um ensaio clínico randomizado duplo cego [Dissertação de Mestrado]. Porto Alegre (RS): Universidade Federal Rio Grande do Sul; 2005. Avaiable from: hdl.handle.net/10183/5984
Petersen ER, Claesson MH, Schmidt EG, Jensen SS, Ravn P, Olsen J, et al. Consumption of probiotics increases the effect of regulatory T cells in transfer colitis. Inflamm Bowel Dis. 2012;18(1):131–42. doi :10.1002/ibd.21709
Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol. 2009;27:485–517. doi: 10.1146/annurev.immunol.021908.132710
Lozupone CA, Li M, Campbell TB, Flores SC, Linderman D, Gebert MJ, et al. Alterations in the gut microbiota associated with HIV-1 infection. Cell Host Microbe. 2013;14(3):329–39. doi: 10.1016/j.chom.2013.08.006
Mutlu EA, Keshavarzian A, Losurdo J, Swanson G, Siewe B, Forsyth C, et al. A compositional look at the human gastrointestinal microbiome and immune activation parameters in HIV infected subjects. PLoS Pathog. 2014;10(2): e1003829. doi: 10.1371/journal.ppat.1003829
Vázquez-Castellanos JF, Serrano-Villar S, Latorre A, Artacho A, Ferrús ML, Madrid N, et al. Altered metabolism of gut microbiota contributes to chronic immune activation in HIV-infected individuals. Mucosal Immunol. 2015;8(4):760-72. doi: 10.1038/mi.2014.107
Ling Z, Jin C, Xie T, Cheng Y, Li L, Wu N. Alterations in the fecal microbiota of patients with HIV-1 infection: An observational study in a Chinese population. Sci Rep. 2016;6:30673. doi: 10.1038/srep30673
Dillon SM, Kibbie J, Lee EJ, Guo K, Santiago ML, Austin GL, et al. Low abundance of colonic butyrate-producing bacteria in HIV infection is associated with microbial translocation and immune activation. AIDS. 2017;31(4):511–21. doi: 10.1097/QAD.0000000000001366
Freiberg M, Bebu I, Tracy R, So-Armah K, Okulicz J, Ganesan A, et al. D-Dimer levels before HIV seroconversion remain elevated even after viral suppression and are associated with an increased risk of non-AIDS events. PLoS One. 2016;11(4): e0152588. doi: 10.1371/journal.pone.0152588
D’Angelo C, Reale M, Costantini E. Microbiota and probiotics in health and HIV infection. Nutrients. 2017;9(6). pii: E615. doi: 10.3390/nu9060615
Falasca K, Vecchiet J, Ucciferri C, Di Nicola M, D’Angelo C, Reali M. Effect of probiotic supplement on cytokine levels in HIV-infected individuals: a preliminary study. Nutrients. 2015;7(10):8335–47. doi: 10.3390/nu7105396
López P, González-Rodríguez I, Gueimonde M, Margolles A, Suárez A. Immune response to Bifidobacterium bifidum strains support Treg/Th17 plasticity. PLoS ONE. 2011;6(9):e24776. doi: 10.1371/journal.pone.0024776
Hardy H, Harris J, Lyon E, Beal J, Foey AD. Probiotics, prebiotics and immunomodulation of gut mucosal defences: Homeostasis and immunopathology. Nutrients. 2013;5(6):1869–912. doi: 10.3390/nu5061869
Hummelen R, Vos AP, van’t Land B, van Norren K, Reid G. Altered host-microbe interaction in HIV: A target for intervention with pro- and prebiotics. Int Rev Immunol. 2010;29(5):485–513. doi: 10.3109/08830185.2010.505310
Fernandes A, Sanches R, Mill J, Lucy D, Palha PF, Dalri MCB. Síndrome da lipodistrofia associada com a terapia anti-retroviral em portadores do HIV: considerações para os aspectos psicossociais. Rev Latino-Am Enfermagem. 2007;15(5):1041-5. doi: 10.1590/S0104-11692007000500024
Modanêsi PVG, Mercer NS, Bernardi JFB. Efeitos do uso de probióticos na hipercolesterolemia. Rev Pesq Saúde [Internet]. 2016 [cited 2020 Apr 28];17(1):47-50. Avaiable from: www.periodicoseletronicos.ufma.br/index.php/revistahuufma/article/view/5507
Ramasamy K, Abdullah N, Wong MC, Karuthan C, Ho YW. Bile salt deconjugation and cholesterol removal from media by Lactobacillus strains used as probiotics in chickens. J Sci Food Agric. 2010;90(1):65-9. doi: 10.1002/jsfa.3780
Higgins JPT, Green S, editors. Cochrane handbook for systematic reviews of interventions. Version 5.1.0 [updated March 2011]. The Cochrane Collaboration; 2011 [cited 2020 Apr 28]. Avaiable from: handbook-5-1.cochrane.org/