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Erschienen in: AIDS and Behavior 7/2021

04.01.2021 | Original Paper

Evaluation of the Microbiome in Men Taking Pre-exposure Prophylaxis for HIV Prevention

verfasst von: Bryce K. Perler, Elizabeth M. Reinhart, Madeline Montgomery, Michaela Maynard, Jason M. Shapiro, Peter Belenky, Philip A. Chan

Erschienen in: AIDS and Behavior | Ausgabe 7/2021

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Abstract

Tenofovir-based regimens as pre-exposure prophylaxis (PrEP) are highly effective at preventing HIV infection. The most common side-effect is gastrointestinal (GI) distress which may be associated with changes in the microbiome. Dysbiosis of the microbiome can have numerous health-related consequences. To understand the effect of PrEP on dysbiosis, we evaluated 27 individuals; 14 were taking PrEP for an average of 171 weeks. Sequencing of 16S rRNA was performed using self-collected rectal swabs. Mixed beta diversity testing demonstrated significant differences between PrEP and non-PrEP users with Bray–Curtis and unweighted UniFrac analyses (p = 0.05 and 0.049, respectively). At the genus level, there was a significant reduction in Finegoldia, along with a significant increase in Catenibacterium and Prevotella in PrEP users. Prevotella has been associated with inflammatory pathways, insulin resistance and cardiovascular disease, while Catenibacterium has been associated with morbid obesity and metabolic syndrome. Overall, these results suggest that PrEP may be associated with some degree of microbiome dysbiosis, which may contribute to GI symptoms. Long-term impact of these changes is unknown.
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Literatur
1.
Zurück zum Zitat Maartens G, Celum C, Lewin S. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet. 2014;384(9939):19–25.CrossRef Maartens G, Celum C, Lewin S. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet. 2014;384(9939):19–25.CrossRef
2.
Zurück zum Zitat Grant RM, Lama JR, Anderson PL, et al. Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med. 2010;363:2587–99.CrossRef Grant RM, Lama JR, Anderson PL, et al. Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med. 2010;363:2587–99.CrossRef
3.
Zurück zum Zitat Solomon MM, Lama JR, Glidden DV. Changes in renal function associated with oral emtricitabine/tenofovir disoproxil fumarate use for HIV pre-exposure prophylaxis. AIDS. 2014;28(6):851–9.CrossRef Solomon MM, Lama JR, Glidden DV. Changes in renal function associated with oral emtricitabine/tenofovir disoproxil fumarate use for HIV pre-exposure prophylaxis. AIDS. 2014;28(6):851–9.CrossRef
4.
Zurück zum Zitat Gandhi M, Glidden DV, Mayer K, et al. Association of age, baseline kidney function, and medication exposure with declines in creatinine clearance on pre-exposure prophylaxis: an observational cohort study. Lancet HIV. 2016;3(11):e521–8.CrossRef Gandhi M, Glidden DV, Mayer K, et al. Association of age, baseline kidney function, and medication exposure with declines in creatinine clearance on pre-exposure prophylaxis: an observational cohort study. Lancet HIV. 2016;3(11):e521–8.CrossRef
5.
Zurück zum Zitat Mulligan K, Glidden DV, Anderson PL, et al. Effects of emtricitabine/tenofovir on bone mineral density in HIV-negative persons in a randomized, double-blind, Placebo-Controlled Trial. Clin Infect Dis. 2015;61(4):572–80.CrossRef Mulligan K, Glidden DV, Anderson PL, et al. Effects of emtricitabine/tenofovir on bone mineral density in HIV-negative persons in a randomized, double-blind, Placebo-Controlled Trial. Clin Infect Dis. 2015;61(4):572–80.CrossRef
6.
Zurück zum Zitat Villanueva- MJ, Perez-Matute P, Recio-Fernandez E, Lezana Rosales JM, Oteo JA. Differential effects of antiretrovirals on microbial translocation and gut microbiota composition of HIV-infected patients. J Int AIDS Soc. 2017;20(1):21526.CrossRef Villanueva- MJ, Perez-Matute P, Recio-Fernandez E, Lezana Rosales JM, Oteo JA. Differential effects of antiretrovirals on microbial translocation and gut microbiota composition of HIV-infected patients. J Int AIDS Soc. 2017;20(1):21526.CrossRef
7.
Zurück zum Zitat Klatt NR, Funderburg NT, Brenchley JM. Microbial translocation, immune activation, and HIV disease. Trends Microbiol. 2013;21:6–13.CrossRef Klatt NR, Funderburg NT, Brenchley JM. Microbial translocation, immune activation, and HIV disease. Trends Microbiol. 2013;21:6–13.CrossRef
8.
Zurück zum Zitat Zevin AS, McKinnon L, Burgener A, Klatt NR. Microbial translocation and microbiome dysbiosis in HIV-associated immune activation. Curr Opin HIV AIDS. 2016;11:182–90.CrossRef Zevin AS, McKinnon L, Burgener A, Klatt NR. Microbial translocation and microbiome dysbiosis in HIV-associated immune activation. Curr Opin HIV AIDS. 2016;11:182–90.CrossRef
9.
Zurück zum Zitat Gootenberg DB, Paer JM, Luevano JM, et al. HIV-associated changes in the enteric microbial community: potential role in loss of homeostasis and development of systemic inflammation. Curr Opin Infect Dis. 2017;30(1):31–43.CrossRef Gootenberg DB, Paer JM, Luevano JM, et al. HIV-associated changes in the enteric microbial community: potential role in loss of homeostasis and development of systemic inflammation. Curr Opin Infect Dis. 2017;30(1):31–43.CrossRef
10.
Zurück zum Zitat Dubé MP, Park SY, Ross H, et al. Daily HIV pre-exposure prophylaxis (PrEP) with tenofovir disoproxil fumarate-emtricitabine reduced Streptococcus and increased Erysipelotrichaceae in rectal microbiota. Sci Rep. 2018;8(1):15212.CrossRef Dubé MP, Park SY, Ross H, et al. Daily HIV pre-exposure prophylaxis (PrEP) with tenofovir disoproxil fumarate-emtricitabine reduced Streptococcus and increased Erysipelotrichaceae in rectal microbiota. Sci Rep. 2018;8(1):15212.CrossRef
11.
Zurück zum Zitat Fulcher JA, Li F, Cook RR, et al. Rectal microbiome alterations associated with oral human immunodeficiency virus pre-exposure prophylaxis. Open Forum Infect Dis. 2019;6(11):ofz463.CrossRef Fulcher JA, Li F, Cook RR, et al. Rectal microbiome alterations associated with oral human immunodeficiency virus pre-exposure prophylaxis. Open Forum Infect Dis. 2019;6(11):ofz463.CrossRef
12.
Zurück zum Zitat Noguera-Julian M, Rocafort M, Guillen Y, et al. Gut microbiota linked to sexual preference and HIV infection. EBioMedicine. 2016;5:135–46.CrossRef Noguera-Julian M, Rocafort M, Guillen Y, et al. Gut microbiota linked to sexual preference and HIV infection. EBioMedicine. 2016;5:135–46.CrossRef
13.
Zurück zum Zitat Kelley CF, Kraft CS, de Man TJB, et al. The rectal mucosa and condomless receptive anal intercourse in HIV negative MSM: implications for hiv transmission and prevention. Mucosal Immunol. 2017;10(4):996–1007.CrossRef Kelley CF, Kraft CS, de Man TJB, et al. The rectal mucosa and condomless receptive anal intercourse in HIV negative MSM: implications for hiv transmission and prevention. Mucosal Immunol. 2017;10(4):996–1007.CrossRef
14.
Zurück zum Zitat Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–80.CrossRef Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–80.CrossRef
15.
Zurück zum Zitat Schincaglia GP, Hong BY, Rosania A, et al. Clinical, immune, and microbiome traits of gingivitis and peri-implant mucositis. J Dent Res. 2017;96(1):47–55.CrossRef Schincaglia GP, Hong BY, Rosania A, et al. Clinical, immune, and microbiome traits of gingivitis and peri-implant mucositis. J Dent Res. 2017;96(1):47–55.CrossRef
16.
Zurück zum Zitat Scher JU, Ubeda C, Equinda M, et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum. 2012;64(10):3083–94.CrossRef Scher JU, Ubeda C, Equinda M, et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum. 2012;64(10):3083–94.CrossRef
17.
Zurück zum Zitat Moreno-Indias I, Sanchez-Alcoholado L, Garcia-Fuentes E, et al. Insulin resistance is associated with specific gut microbiota in appendix samples from morbidly obese patients. Am J Transl Res. 2016;8(12):5672–84.PubMedPubMedCentral Moreno-Indias I, Sanchez-Alcoholado L, Garcia-Fuentes E, et al. Insulin resistance is associated with specific gut microbiota in appendix samples from morbidly obese patients. Am J Transl Res. 2016;8(12):5672–84.PubMedPubMedCentral
18.
Zurück zum Zitat Mugwanya KK, Baeten JM. Safety of oral tenofovir disoproxil fumarate-based pre-exposure prophylaxis for HIV prevention. Expert Opin Drug Saf. 2017;15(2):265–73.CrossRef Mugwanya KK, Baeten JM. Safety of oral tenofovir disoproxil fumarate-based pre-exposure prophylaxis for HIV prevention. Expert Opin Drug Saf. 2017;15(2):265–73.CrossRef
19.
Zurück zum Zitat Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 2014;16(7):1024–33.CrossRef Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 2014;16(7):1024–33.CrossRef
20.
Zurück zum Zitat Binda C, Lopetuso LR, Rizzatti G, et al. Actinobacteria: a relevant minority for the maintenance of gut homeostasis. Dig Liver Dis. 2018;50(5):421–8.CrossRef Binda C, Lopetuso LR, Rizzatti G, et al. Actinobacteria: a relevant minority for the maintenance of gut homeostasis. Dig Liver Dis. 2018;50(5):421–8.CrossRef
21.
Zurück zum Zitat Budding AE, Grasman ME, Eck A, et al. Rectal swabs for analysis of the intestinal microbiota. PLoS ONE. 2014;9(7):e101344.CrossRef Budding AE, Grasman ME, Eck A, et al. Rectal swabs for analysis of the intestinal microbiota. PLoS ONE. 2014;9(7):e101344.CrossRef
22.
Zurück zum Zitat Biehl LM, Garzettia D, Farowski F, et al. Usability of rectal swabs for microbiome sampling in cohort study of hematological and oncological patients. PLoS ONE. 2019;14(4):e0215428.CrossRef Biehl LM, Garzettia D, Farowski F, et al. Usability of rectal swabs for microbiome sampling in cohort study of hematological and oncological patients. PLoS ONE. 2019;14(4):e0215428.CrossRef
23.
Zurück zum Zitat Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.CrossRef Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.CrossRef
24.
Zurück zum Zitat Caporaso JG, Lauber CL, Walters WA, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6(8):1621–4.CrossRef Caporaso JG, Lauber CL, Walters WA, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6(8):1621–4.CrossRef
25.
Zurück zum Zitat Walters W, Hyde ER, Berg-Lyons D, et al. Improved bacterial 16S rRNA gene (V4 and V4–5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems. 2016;1(1):e00009-e00015.CrossRef Walters W, Hyde ER, Berg-Lyons D, et al. Improved bacterial 16S rRNA gene (V4 and V4–5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems. 2016;1(1):e00009-e00015.CrossRef
26.
Zurück zum Zitat Thompson LR, Sanders JG, McDonald D, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551(7681):457–63.CrossRef Thompson LR, Sanders JG, McDonald D, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551(7681):457–63.CrossRef
27.
Zurück zum Zitat Callahan BJ, McMuride PJ, Rosen MJ, et al. DADA2: high resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3.CrossRef Callahan BJ, McMuride PJ, Rosen MJ, et al. DADA2: high resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3.CrossRef
28.
Zurück zum Zitat Gurevich A, Saveliev V, Vyahhi N, et al. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072–5.CrossRef Gurevich A, Saveliev V, Vyahhi N, et al. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072–5.CrossRef
29.
Zurück zum Zitat Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60.CrossRef Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60.CrossRef
30.
Zurück zum Zitat Hassan A, Blumenthal JS, Dube MP, et al. Effect of rectal douching/enema on rectal gonorrhoea and chlamydia among a cohort of men who have sex with men on HIV Pre-exposure prophylaxis. Sex Transm Infect. 2018;94(7):508–14.CrossRef Hassan A, Blumenthal JS, Dube MP, et al. Effect of rectal douching/enema on rectal gonorrhoea and chlamydia among a cohort of men who have sex with men on HIV Pre-exposure prophylaxis. Sex Transm Infect. 2018;94(7):508–14.CrossRef
31.
Zurück zum Zitat Haaland RE, Fountain J, Hu Y, et al. Repeated rectal application of a hyperosmolar lubricant is associated with microbiota shifts but does not affect PrEP drug concentrations: results from a randomized trial in men who have sex with men. J Int AIDS Soc. 2018;21(10):e25199.CrossRef Haaland RE, Fountain J, Hu Y, et al. Repeated rectal application of a hyperosmolar lubricant is associated with microbiota shifts but does not affect PrEP drug concentrations: results from a randomized trial in men who have sex with men. J Int AIDS Soc. 2018;21(10):e25199.CrossRef
32.
Zurück zum Zitat Zhernakova A, Kurilshikov A, Bonder MJ, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 2016;352(6285):565–9.CrossRef Zhernakova A, Kurilshikov A, Bonder MJ, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 2016;352(6285):565–9.CrossRef
33.
Zurück zum Zitat Armstrong AJS, Shaffer M, Nusbacher NM, et al. An exploration of Prevotella-rich microbiomes in HIV and men who have sex with men. Microbiome. 2018;6:198.CrossRef Armstrong AJS, Shaffer M, Nusbacher NM, et al. An exploration of Prevotella-rich microbiomes in HIV and men who have sex with men. Microbiome. 2018;6:198.CrossRef
34.
Zurück zum Zitat Gallardo-Becerra L, Cornejo-Granados F, Lopez-Garcia R, et al. Metatranscriptomic analysis to define the Secrebiome, and 16S rRNA profiling of the gut microbiome in obesity and metabolic syndrome of Mexican children. Microb Cell Fact. 2020;19:61.CrossRef Gallardo-Becerra L, Cornejo-Granados F, Lopez-Garcia R, et al. Metatranscriptomic analysis to define the Secrebiome, and 16S rRNA profiling of the gut microbiome in obesity and metabolic syndrome of Mexican children. Microb Cell Fact. 2020;19:61.CrossRef
35.
Zurück zum Zitat Carda-dieguez M, Cardenas N, Aparicio M, et al. Variations in vaginal, penile, and oral microbiota after sexual intercourse: a case report. Front Med (Lausanne). 2019;6:178.CrossRef Carda-dieguez M, Cardenas N, Aparicio M, et al. Variations in vaginal, penile, and oral microbiota after sexual intercourse: a case report. Front Med (Lausanne). 2019;6:178.CrossRef
36.
Zurück zum Zitat Price LB, Liu CM, Johnson KE, et al. The effects of circumcision on the penis microbiome. PLoS ONE. 2010;5(1):e8422.CrossRef Price LB, Liu CM, Johnson KE, et al. The effects of circumcision on the penis microbiome. PLoS ONE. 2010;5(1):e8422.CrossRef
37.
Zurück zum Zitat Liu CM, Prodger JL, Tobian AAR, et al. Penile anaerobic dysbiosis as a risk factor for HIV infection. mBio. 2017;4:e00996-e1017. Liu CM, Prodger JL, Tobian AAR, et al. Penile anaerobic dysbiosis as a risk factor for HIV infection. mBio. 2017;4:e00996-e1017.
38.
Zurück zum Zitat Flygel TT, Sovershaeva E, Claassen-Weitz S, et al. Composition of gut microbiota of children and adolescents with perinatal human immunodeficiency virus infection taking antiretroviral therapy in zimbabwe. J Infect Dis. 2020;221(3):483–92.PubMed Flygel TT, Sovershaeva E, Claassen-Weitz S, et al. Composition of gut microbiota of children and adolescents with perinatal human immunodeficiency virus infection taking antiretroviral therapy in zimbabwe. J Infect Dis. 2020;221(3):483–92.PubMed
39.
Zurück zum Zitat Nowak RG, Bentzen SM, Ravel J, et al. Rectal microbiota among HIV-uninfected, untreated HIV, and treated HIV-infected men who have sex with men (MSM) in Nigeria. AIDS. 2017;31(6):857–62.CrossRef Nowak RG, Bentzen SM, Ravel J, et al. Rectal microbiota among HIV-uninfected, untreated HIV, and treated HIV-infected men who have sex with men (MSM) in Nigeria. AIDS. 2017;31(6):857–62.CrossRef
Metadaten
Titel
Evaluation of the Microbiome in Men Taking Pre-exposure Prophylaxis for HIV Prevention
verfasst von
Bryce K. Perler
Elizabeth M. Reinhart
Madeline Montgomery
Michaela Maynard
Jason M. Shapiro
Peter Belenky
Philip A. Chan
Publikationsdatum
04.01.2021
Verlag
Springer US
Erschienen in
AIDS and Behavior / Ausgabe 7/2021
Print ISSN: 1090-7165
Elektronische ISSN: 1573-3254
DOI
https://doi.org/10.1007/s10461-020-03130-7

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