Generic placeholder image

Current HIV Research

Editor-in-Chief

ISSN (Print): 1570-162X
ISSN (Online): 1873-4251

Research Article

Antiviral Activity of Fecal Water Samples from HIV-1 Infected Subjects Treated with a Specific Probiotic Formulation

Author(s): Francesca Falasca, Eugenio Nelson Cavallari, Giuseppe Pietro Innocenti, Carolina Scagnolari, Ivano Mezzaroma, Letizia Santinelli, Giancarlo Ceccarelli, Vincenzo Vullo, Ombretta Turriziani and Gabriella d'Ettorre*

Volume 17, Issue 3, 2019

Page: [183 - 189] Pages: 7

DOI: 10.2174/1570162X17666190903230622

Price: $65

Abstract

Objectives: The aim of the study was to investigate if the supplementation with multistrain probiotics may be able to modulate T cell response in HIV-1 infected patients and to evaluate the anti-HIV activity of probiotic by studying fecal water (FW) samples.

Methods: Three HIV-1-positive patients (Pt1, Pt2 and Pt3) on long-term suppressive combined antiretroviral therapy (cART) received a specific multi-strain probiotic supplementation (Vivomixx ®), for six months (T6). Levels of T cell subsets were evaluated by flow cytometry. Anti- HIV activity of FW samples was evaluated in vitro.

Results: CD4+ T cells levels increased in all HIV-1 infected patients whereas activation markers (CD38 and HLA-DR) were decreased both on CD4+ and CD8+ T cells. FW samples presented an increased inhibitory activity against HIV-1 compared to T0 (FW-Pt1: T0 =40%, T6 = 65% of reduction; FW Pt2: T0 = 26%, T6 = 46% of reduction; FW Pt3: T0 = 47%, T6 = 94% of reduction).

Discussion: Our data suggest that the administration of the specific probiotic formulation improves the antiviral status of people living with HIV-1 under cART, also modulating T cell response.

Conclusion: Anti-HIV activity of FW may have several public health and social implications for sexually transmitted diseases that need to be further explored.

Keywords: HIV-1, probiotics, fecal water, viral replication, immune activation, cART.

Graphical Abstract

[1]
Lu W, Feng Y, Jing F, et al. Association between Gut microbiota and CD4 recovery in HIV-1 infected patients. Front Microbiol 2018; 9: 1451.
[http://dx.doi.org/10.3389/fmicb.2018.01451] [PMID: 30034377]
[2]
van Marle G, Church DL, van der Meer F, Gill MJ. Combating the HIV reservoirs. Biotechnol Genet Eng Rev 2018; 34(1): 76-89.
[http://dx.doi.org/10.1080/02648725.2018.1471641] [PMID: 29781356]
[3]
Morón-López S, Puertas MC, Gálvez C, et al. Sensitive quantification of the HIV-1 reservoir in gut-associated lymphoid tissue. PLoS One 2017; 12(4)e0175899
[http://dx.doi.org/10.1371/journal.pone.0175899] [PMID: 28414780]
[4]
Vergnon-Miszczycha D, Lucht F, Roblin X, Pozzetto B, Paul S, Bourlet T. [Key role played by the gut associated lymphoid tissue during human immunodeficiency virus infection] Med Sci (Paris) 2015; 31(12): 1092-101.
[http://dx.doi.org/10.1051/medsci/20153112012] [PMID: 26672662]
[5]
Carter GM, Esmaeili A, Shah H, et al. Probiotics in Human Immunodeficiency virus infection: A systematic review and evidence synthesis of benefits and risks. Open Forum Infect Dis 2016; 3(4)ofw164
[http://dx.doi.org/10.1093/ofid/ofw164] [PMID: 27747250]
[6]
Hunt PW. Th17, gut, and HIV: therapeutic implications. Curr Opin HIV AIDS 2010; 5(2): 189-93.
[http://dx.doi.org/10.1097/COH.0b013e32833647d9] [PMID: 20543599]
[7]
d’Ettorre G, Ceccarelli G, Andreotti M, et al. Analysis of Th17 and Tc17 Frequencies and Antiviral Defenses in Gut-Associated Lymphoid Tissue of Chronic HIV-1 Positive Patients. Mediators Inflamm 2015; 2015395484
[http://dx.doi.org/10.1155/2015/395484] [PMID: 26221062]
[8]
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(6): 670-80.
[http://dx.doi.org/10.1038/mi.2012.72] [PMID: 22854709]
[9]
Shacklett BL. Mucosal Immunity in HIV/SIV Infection: T Cells, B Cells and Beyond. Curr Immunol Rev 2019; 15(1): 63-75.
[http://dx.doi.org/10.2174/1573395514666180528081204] [PMID: 31327960]
[10]
Klatt NR, Funderburg NT, Brenchley JM. Microbial translocation, immune activation, and HIV disease. Trends Microbiol 2013; 21(1): 6-13.
[http://dx.doi.org/10.1016/j.tim.2012.09.001] [PMID: 23062765]
[11]
Assimakopoulos SF, Dimitropoulou D, Marangos M, Gogos CA. Intestinal barrier dysfunction in HIV infection: pathophysiology, clinical implications and potential therapies. Infection 2014; 42(6): 951-9.
[http://dx.doi.org/10.1007/s15010-014-0666-5] [PMID: 25070877]
[12]
Somsouk M, Estes JD, Deleage C, et al. Gut epithelial barrier and systemic inflammation during chronic HIV infection. AIDS 2015; 29(1): 43-51.
[http://dx.doi.org/10.1097/QAD.0000000000000511] [PMID: 25387317]
[13]
Luján JA, Rugeles MT, Taborda NA. Contribution of the Microbiota to Intestinal Homeostasis and its Role in the Pathogenesis of HIV-1 Infection. Curr HIV Res 2019; 17(1): 13-25.
[http://dx.doi.org/10.2174/1570162X17666190311114808] [PMID: 30854974]
[14]
Bandera A, De Benedetto I, Bozzi G, Gori A. Altered gut microbiome composition in HIV infection: Causes, effects and potential intervention. Curr Opin HIV AIDS 2018; 13(1): 73-80.
[http://dx.doi.org/10.1097/COH.0000000000000429] [PMID: 29045252]
[15]
Mudd JC, Brenchley JM. Gut mucosal barrier dysfunction, microbial dysbiosis, and their role in HIV-1 disease progression. J Infect Dis 2016; 214(Suppl. 2): S58-66.
[http://dx.doi.org/10.1093/infdis/jiw258] [PMID: 27625432]
[16]
Younas M, Psomas C, Reynes J, Corbeau P. Immune activation in the course of HIV-1 infection: Causes, phenotypes and persistence under therapy. HIV Med 2016; 17(2): 89-105.
[http://dx.doi.org/10.1111/hiv.12310] [PMID: 26452565]
[17]
d’Ettorre G, Paiardini M, Zaffiri L, et al. HIV persistence in the gut mucosa of HIV-infected subjects undergoing antiretroviral therapy correlates with immune activation and increased levels of LPS. Curr HIV Res 2011; 9(3): 148-53.
[http://dx.doi.org/10.2174/157016211795945296] [PMID: 21457131]
[18]
d’Ettorre G, Paiardini M, Ceccarelli G, Silvestri G, Vullo V. HIV-associated immune activation: From bench to bedside. AIDS Res Hum Retroviruses 2011; 27(4): 355-64.
[http://dx.doi.org/10.1089/aid.2010.0342] [PMID: 21309730]
[19]
D’Ettorre G, Douek D, Paiardini M, Ceccarelli G, Vullo V. Microbial translocation and infectious diseases: What is the link? Int J Microbiol 2012; 2012356981
[http://dx.doi.org/10.1155/2012/356981] [PMID: 23091494]
[20]
Gori A, Tincati C, Rizzardini G, et al. Early impairment of gut function and gut flora supporting a role for alteration of gastrointestinal mucosa in human immunodeficiency virus pathogenesis. J Clin Microbiol 2008; 46(2): 757-8.
[http://dx.doi.org/10.1128/JCM.01729-07] [PMID: 18094140]
[21]
Wang Z, Qi Q. Gut microbial metabolites associated with HIV infection. Future Virol 2019; 14(5): 335-47.
[http://dx.doi.org/10.2217/fvl-2019-0002] [PMID: 31263508]
[22]
Ceccarelli G, Statzu M, Santinelli L, et al. Challenges in the management of HIV infection: Update on the role of probiotic supplementation as a possible complementary therapeutic strategy for cART treated people living with HIV/AIDS. Expert Opin Biol Ther 2019; 19(9): 949-65.
[http://dx.doi.org/10.1080/14712598.2019.1638907] [PMID: 31260331]
[23]
Crakes KR, Jiang G. Gut Microbiome Alterations During HIV/SIV Infection: Implications for HIV Cure. Front Microbiol 2019; 10: 1104.
[http://dx.doi.org/10.3389/fmicb.2019.01104] [PMID: 31191468]
[24]
Rocafort M, Noguera-Julian M, Rivera J, et al. Evolution of the gut microbiome following acute HIV-1 infection. Microbiome 2019; 7(1): 73.
[http://dx.doi.org/10.1186/s40168-019-0687-5] [PMID: 31078141]
[25]
Vujkovic-Cvijin I, Somsouk M. HIV and the Gut Microbiota: Composition, Consequences, and Avenues for Amelioration. Curr HIV/AIDS Rep 2019; 16(3): 204-13.
[http://dx.doi.org/10.1007/s11904-019-00441-w] [PMID: 31037552]
[26]
Villanueva-Millán MJ, Pérez-Matute P, Recio-Fernández E, Lezana Rosales JM, Oteo JA. Characterization of gut microbiota composition in HIV-infected patients with metabolic syndrome. J Physiol Biochem 2019. [Epub Ahead of Print]
[http://dx.doi.org/10.1007/s13105-019-00673-9] [PMID: 30924020]
[27]
Rhoades N, Mendoza N, Jankeel A, et al. Altered Immunity and Microbial Dysbiosis in Aged Individuals With Long-Term Controlled HIV Infection. Front Immunol 2019; 10: 463.
[http://dx.doi.org/10.3389/fimmu.2019.00463] [PMID: 30915086]
[28]
Luján JA, Rugeles MT, Taborda NA. Contribution of the Microbiota to Intestinal Homeostasis and its Role in the Pathogenesis of HIV-1 Infection. Curr HIV Res 2019; 17(1): 13-25.
[http://dx.doi.org/10.2174/1570162X17666190311114808] [PMID: 30854974]
[29]
Williams B. Gut Microbiome in HIV Infection: Overcoming Barriers? Dig Dis Sci 2019; 64(7): 1725-7.
[http://dx.doi.org/10.1007/s10620-019-05500-1] [PMID: 30725298]
[30]
Tincati C, Ancona G, Marchetti G. The fecal microbiome directly drives immune activation in HIV infection. Ann Transl Med 2018; 6(Suppl. 1): S45.
[http://dx.doi.org/10.21037/atm.2018.09.66] [PMID: 30613620]
[31]
Storm-Larsen C, Stiksrud B, Eriksen C, et al. Microbial translocation revisited: targeting the endotoxic potential of gut microbes in HIV-infected individuals. AIDS 2019; 33(4): 645-53.
[http://dx.doi.org/10.1097/QAD.0000000000002087] [PMID: 30531315]
[32]
Schooley RT. The human microbiome: implications for health and disease, including HIV infection. Top Antivir Med 2018; 26(3): 75-8.
[PMID: 30384329]
[33]
Nazir Y, Hussain SA, Abdul Hamid A, Song Y. Probiotics and Their Potential Preventive and Therapeutic Role for Cancer, High Serum Cholesterol, and Allergic and HIV Diseases. BioMed Res Int 2018; 20183428437
[http://dx.doi.org/10.1155/2018/3428437] [PMID: 30246019]
[34]
Pinacchio C, Scheri GC, Statzu M, et al. Type I/II Interferon in HIV-1-Infected Patients: Expression in Gut Mucosa and in Peripheral Blood Mononuclear Cells and Its Modification upon Probiotic Supplementation. J Immunol Res 2018; 20181738676
[http://dx.doi.org/10.1155/2018/1738676] [PMID: 30186879]
[35]
Happel AU, Barnabas SL, Froissart R, Passmore JS. Weighing in on the risks and benefits of probiotic use in HIV-infected and immunocompromised populations. Benef Microbes 2018; 9(2): 239-46.
[http://dx.doi.org/10.3920/BM2017.0106] [PMID: 29345159]
[36]
Kazemi A, Djafarian K, Speakman JR, Sabour P, Soltani S, Shab-Bidar S. Effect of Probiotic Supplementation on CD4 Cell Count in HIV-Infected Patients: A Systematic Review and Meta-analysis. J Diet Suppl 2018; 15(5): 776-88.
[http://dx.doi.org/10.1080/19390211.2017.1380103] [PMID: 29185825]
[37]
D’Angelo C, Reale M, Costantini E. Microbiota and Probiotics in Health and HIV Infection. Nutrients 2017; 9(6)E615
[http://dx.doi.org/10.3390/nu9060615] [PMID: 28621726]
[38]
Scheri GC, Fard SN, Schietroma I, et al. Modulation of Tryptophan/Serotonin Pathway by Probiotic Supplementation in Human Immunodeficiency Virus-Positive Patients: Preliminary Results of a New Study Approach. Int J Tryptophan Res 2017; 10: 1177.
[PMID: 28607543]
[39]
d’Ettorre G, Rossi G, Scagnolari C, 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.
[http://dx.doi.org/10.1002/iid3.160] [PMID: 28474815]
[40]
Scagnolari C, Corano Scheri G, Selvaggi C, et al. Probiotics Differently Affect Gut-Associated Lymphoid Tissue Indolamine-2,3-Dioxygenase mRNA and Cerebrospinal Fluid Neopterin Levels in Antiretroviral-Treated HIV-1 Infected Patients: A Pilot Study. Int J Mol Sci 2016; 17(10)E1639
[http://dx.doi.org/10.3390/ijms17101639] [PMID: 27689995]
[41]
Miller H, Ferris R, Phelps BR. The effect of probiotics on CD4 counts among people living with HIV: a systematic review. Benef Microbes 2016; 7(3): 345-51.
[http://dx.doi.org/10.3920/BM2015.0163] [PMID: 27013461]
[42]
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(9)e0137200
[http://dx.doi.org/10.1371/journal.pone.0137200] [PMID: 26376436]
[43]
Falasca K, Vecchiet J, Ucciferri C, Di Nicola M, D’Angelo C, Reale M. Effect of Probiotic Supplement on Cytokine Levels in HIV-Infected Individuals: A Preliminary Study. Nutrients 2015; 7(10): 8335-47.
[http://dx.doi.org/10.3390/nu7105396] [PMID: 26426044]
[44]
Effects of the Probiotic Visbiome Extra Strength on Gut Microbiome & Immune Activation Markers ClinicalTrials.gov Identifier: NCT02706717ACTG 5350 Available at:. https://clinicaltrials.gov/ct2/show/ NCT02706717: (Accessed on 6/6/2019).
[45]
Conrad JA, Lindsley CW. Is the Microbiome the Fifth Horseman of the Apocalypse in Drug Discovery? Implications for the Gut-Brain Axis. ACS Chem Neurosci 2017; 8(7): 1430.
[http://dx.doi.org/10.1021/acschemneuro.7b00234] [PMID: 28719971]
[46]
Ceccarelli G, Brenchley JM, Cavallari EN, et al. Impact of High-Dose Multi-Strain Probiotic Supplementation on Neurocognitive Performance and Central Nervous System Immune Activation of HIV-1 Infected Individuals. Nutrients 2017; 9(11)E1269
[http://dx.doi.org/10.3390/nu9111269] [PMID: 29160817]
[47]
Ceccarelli G, Fratino M, Selvaggi C, et al. A pilot study on the effects of probiotic supplementation on neuropsychological performance and microRNA-29a-c levels in antiretroviral-treated HIV-1-infected patients. Brain Behav 2017; 7(8)e00756
[http://dx.doi.org/10.1002/brb3.756] [PMID: 28828217]
[48]
Vasquez EC, Pereira TMC, Peotta VA, Baldo MP, Campos-Toimil M. Probiotics as Beneficial Dietary Supplements to Prevent and Treat Cardiovascular Diseases: Uncovering Their Impact on Oxidative Stress. Oxid Med Cell Longev 2019; 20193086270
[http://dx.doi.org/10.1155/2019/3086270] [PMID: 31205584]
[49]
Silva-Cutini MA, Almeida SA, Nascimento AM, et al. Long-term treatment with kefir probiotics ameliorates cardiac function in spontaneously hypertensive rats. J Nutr Biochem 2019; 66: 79-85.
[http://dx.doi.org/10.1016/j.jnutbio.2019.01.006] [PMID: 30776608]
[50]
Liu YW, Liong MT, Tsai YC. New perspectives of Lactobacillus plantarum as a probiotic: The gut-heart-brain axis. J Microbiol 2018; 56(9): 601-13.
[http://dx.doi.org/10.1007/s12275-018-8079-2] [PMID: 30141154]
[51]
Schiattarella GG, Sannino A, Esposito G, Perrino C. Diagnostics and therapeutic implications of gut microbiota alterations in cardiometabolic diseases. Trends Cardiovasc Med 2019; 29(3): 141-7.
[http://dx.doi.org/10.1016/j.tcm.2018.08.003] [PMID: 30126689]
[52]
Rao S, Hu S, McHugh L, et al. Toward a live microbial microbicide for HIV: Commensal bacteria secreting an HIV fusion inhibitor peptide. Proc Natl Acad Sci USA 2005; 102(34): 11993-8.
[http://dx.doi.org/10.1073/pnas.0504881102] [PMID: 16040799]
[53]
Botić T, Klingberg TD, Weingartl H, Cencic A. A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria. Int J Food Microbiol 2007; 115(2): 227-34.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2006.10.044] [PMID: 17261339]
[54]
Liu F, Li G, Wen K, et al. Porcine small intestinal epithelial cell line (IPEC-J2) of rotavirus infection as a new model for the study of innate immune responses to rotaviruses and probiotics. Viral Immunol 2010; 23(2): 135-49.
[http://dx.doi.org/10.1089/vim.2009.0088] [PMID: 20373994]
[55]
Khani S, Motamedifar M, Golmoghaddam H, Hosseini HM, Hashemizadeh Z. In vitro study of the effect of a probiotic bacterium Lactobacillus rhamnosus against herpes simplex virus type 1. Braz J Infect Dis 2012; 16(2): 129-35.
[http://dx.doi.org/10.1590/S1413-86702012000200004] [PMID: 22552453]
[56]
Cha MK, Lee DK, An HM, et al. Antiviral activity of Bifidobacterium adolescentis SPM1005-A on human papillomavirus type 16. BMC Med 2012; 10: 72.
[http://dx.doi.org/10.1186/1741-7015-10-72] [PMID: 22788922]
[57]
Ceccarelli G, Cavallari EN, Savinelli S, et al. Clearance of human papillomavirus related anal condylomas after oral and endorectal multistrain probiotic supplementation in an HIV positive male: A case report. Medicine (Baltimore) 2018; 97(16)e0329
[http://dx.doi.org/10.1097/MD.0000000000010329] [PMID: 29668581]
[58]
Arena MP, Capozzi V, Russo P, Drider D, Spano G, Fiocco D. Immunobiosis and probiosis: Antimicrobial activity of lactic acid bacteria with a focus on their antiviral and antifungal properties. Appl Microbiol Biotechnol 2018; 102(23): 9949-58.
[http://dx.doi.org/10.1007/s00253-018-9403-9] [PMID: 30280241]
[59]
Shojadoost B, Kulkarni RR, Brisbin JT, Quinteiro-Filho W, Alkie TN, Sharif S. Interactions between lactobacilli and chicken macrophages induce antiviral responses against avian influenza virus. Res Vet Sci 2017; Oct 31.. 5288(17): 30043-7.
[60]
Kanmani P, Albarracin L, Kobayashi H, et al. Exopolysaccharides from Lactobacillus delbrueckii OLL1073R-1 modulate innate antiviral immune response in porcine intestinal epithelial cells. Mol Immunol 2018; 93: 253-65.
[http://dx.doi.org/10.1016/j.molimm.2017.07.009] [PMID: 28800975]
[61]
Ermolenko EI, Desheva YA, Kolobov AA, Kotyleva MP, Sychev IA, Suvorov AN. Anti-Influenza Activity of Enterocin B In vitro and Protective Effect of Bacteriocinogenic Enterococcal Probiotic Strain on Influenza Infection in Mouse Model. Probiotics Antimicrob Proteins 2019; 11(2): 705-12.
[http://dx.doi.org/10.1007/s12602-018-9457-0] [PMID: 30143997]
[62]
Starosila D, Rybalko S, Varbanetz L, Ivanskaya N, Sorokulova I. Anti-influenza Activity of a Bacillus subtilis Probiotic Strain. Antimicrob Agents Chemother 2017; 61(7): e00539-17.
[http://dx.doi.org/10.1128/AAC.00539-17] [PMID: 28416546]
[63]
Ankel H, Turriziani O, Antonelli G. Prostaglandin A inhibits replication of human immunodeficiency virus during acute infection. J Gen Virol 1991; 72(Pt 11): 2797-800.
[http://dx.doi.org/10.1099/0022-1317-72-11-2797] [PMID: 1940869]
[64]
Wachsman MB, Castilla V, de Ruiz Holgado AP, de Torres RA, Sesma F, Coto CE. Enterocin CRL35 inhibits late stages of HSV-1 and HSV-2 replication in vitro. Antiviral Res 2003; 58(1): 17-24.
[http://dx.doi.org/10.1016/S0166-3542(02)00099-2] [PMID: 12719003]
[65]
Cavicchioli VQ, Carvalho OV, Paiva JC, Todorov SD, Silva Júnior A, Nero LA. Inhibition of herpes simplex virus 1 (HSV-1) and poliovirus (PV-1) by bacteriocins from Lactococcus lactis subsp. lactis and enterococcus durans strains isolated from goat milk. Int J Antimicrob Agents 2018; 51(1): 33-7.
[http://dx.doi.org/10.1016/j.ijantimicag.2017.04.020] [PMID: 28668682]
[66]
Férir G, Petrova MI, Andrei G, et al. The lantibiotic peptide labyrinthopeptin A1 demonstrates broad anti-HIV and anti-HSV activity with potential for microbicidal applications. PLoS One 2013; 8(5)e64010
[http://dx.doi.org/10.1371/journal.pone.0064010] [PMID: 23724015]
[67]
Alvarez-Sieiro P, Montalbán-López M, Mu D, Kuipers OP. Bacteriocins of lactic acid bacteria: extending the family. Appl Microbiol Biotechnol 2016; 100(7): 2939-51.
[http://dx.doi.org/10.1007/s00253-016-7343-9] [PMID: 26860942]
[68]
Cotter PD, Hill C, Ross RP. Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 2005; 3(10): 777-88.
[http://dx.doi.org/10.1038/nrmicro1273] [PMID: 16205711]
[69]
Dobson A, Cotter PD, Ross RP, Hill C. Bacteriocin production: A probiotic trait? Appl Environ Microbiol 2012; 78(1): 1-6.
[http://dx.doi.org/10.1128/AEM.05576-11] [PMID: 22038602]
[70]
Balciunas EM, Martinez FAC, Todorov SD, Franco BDGM, Converti A, Oliveira RPS. Novel biotechnological applications of bacteriocins: a review. Food Control 2013; 32: 134-42.
[http://dx.doi.org/10.1016/j.foodcont.2012.11.025]
[71]
Al Kassaa I, Hober D, Hamze M, Chihib NE, Drider D. Antiviral potential of lactic acid bacteria and their bacteriocins. Probiotics Antimicrob Proteins 2014; 6(3-4): 177-85.
[http://dx.doi.org/10.1007/s12602-014-9162-6] [PMID: 24880436]
[72]
Todorov SD, Wachsman MB, Knoetze H, Meincken M, Dicks LM. An antibacterial and antiviral peptide produced by Enterococcus mundtii ST4V isolated from soya beans. Int J Antimicrob Agents 2005; 25(6): 508-13.
[http://dx.doi.org/10.1016/j.ijantimicag.2005.02.005] [PMID: 15869868]
[73]
Fahey JV, Bodwell JE, Hickey DK, Ghosh M, Muia MN, Wira CR. New approaches to making the microenvironment of the female reproductive tract hostile to HIV. Am J Reprod Immunol 2011; 65(3): 334-43.
[http://dx.doi.org/10.1111/j.1600-0897.2010.00949.x] [PMID: 21223421]
[74]
Farcasanu M, Kwon DS. The Influence of Cervicovaginal Microbiota on Mucosal Immunity and Prophylaxis in the Battle against HIV. Curr HIV/AIDS Rep 2018; 15(1): 30-8.
[http://dx.doi.org/10.1007/s11904-018-0380-5] [PMID: 29516267]
[75]
Gosmann C, Anahtar MN, Handley SA, et al. Lactobacillus-Deficient Cervicovaginal Bacterial Communities Are Associated with Increased HIV Acquisition in Young South African Women. Immunity 2017; 46(1): 29-37.
[http://dx.doi.org/10.1016/j.immuni.2016.12.013] [PMID: 28087240]
[76]
Hearps AC, Tyssen D, Srbinovski D, et al. Vaginal lactic acid elicits an anti-inflammatory response from human cervicovaginal epithelial cells and inhibits production of pro-inflammatory mediators associated with HIV acquisition. Mucosal Immunol 2017; 10(6): 1480-90.
[http://dx.doi.org/10.1038/mi.2017.27] [PMID: 28401934]
[77]
Aldunate M, Tyssen D, Johnson A, et al. Vaginal concentrations of lactic acid potently inactivate HIV. J Antimicrob Chemother 2013; 68(9): 2015-25.
[http://dx.doi.org/10.1093/jac/dkt156] [PMID: 23657804]
[78]
Hearps AC, Tyssen D, Srbinovski D, et al. Vaginal lactic acid elicits an anti-inflammatory response from human cervicovaginal epithelial cells and inhibits production of pro-inflammatory mediators associated with HIV acquisition. Mucosal Immunol 2017; 10(6): 1480-90.
[http://dx.doi.org/10.1038/mi.2017.27] [PMID: 28401934]
[79]
Dabee S, Barnabas SL, Lennard KS, et al. Defining characteristics of genital health in South African adolescent girls and young women at high risk for HIV infection. PLoS One 2019; 14(4)e0213975
[http://dx.doi.org/10.1371/journal.pone.0213975] [PMID: 30947260]
[80]
Chetwin E, Manhanzva MT, Abrahams AG, et al. Antimicrobial and inflammatory properties of South African clinical Lactobacillus isolates and vaginal probiotics. Sci Rep 2019; 9(1): 1917.
[http://dx.doi.org/10.1038/s41598-018-38253-4] [PMID: 30760770]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy