Maternal HIV infection and the milk microbiome.

Humans Milk, Human / microbiology HIV Infections / microbiology Female RNA, Ribosomal, 16S / genetics Pregnancy Infectious Disease Transmission, Vertical Infant Microbiota Gastrointestinal Microbiome Infant, Newborn Pregnancy Complications, Infectious / microbiology Bacteria / classification Adult Breast Feeding Lactation
Breast milk transmission CHEU Children HEU HIV HIV-1 HIV-exposed uninfected Human breast milk microbiome Infants Lactation

Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
28 Sep 2024
Historique:
received: 31 01 2024
accepted: 21 05 2024
medline: 29 9 2024
pubmed: 29 9 2024
entrez: 28 9 2024
Statut: epublish

Résumé

Children born to women with HIV but who do not become HIV infected experience increased morbidity and mortality compared with children born to women without HIV. The basis of this increased vulnerability is unknown. The microbiome, specifically the infant gut microbiome, likely plays an important role in infant immune development. The human milk microbiome is thought to have an important role in the development of the infant gut and therefore, if perturbed, may contribute to this increased vulnerability. We investigated the effects of HIV and its therapies on the milk microbiome and possible changes in the milk microbiome before or after infant HIV infection. Seven-hundred fifty-six human milk samples were selected from three separate studies conducted over a 15-year period to investigate the role of HIV and its therapies on the human milk microbiome. Our data reveal that the milk microbiome is modulated by parity (R The milk microbiome varies by stage of lactation, by parity, and by region; however, we found no evidence that the human milk microbiome is altered by maternal HIV infection, disease severity, or antiretroviral therapy. Additionally, we found no association between the milk microbiome and transmission of HIV to the infant. Investigations including higher resolution microbiome approaches or into other potential mechanisms to understand why the approximately one million children born annually to women with HIV escape infection, but do not escape harm, are urgently needed. Video Abstract.

Sections du résumé

BACKGROUND BACKGROUND
Children born to women with HIV but who do not become HIV infected experience increased morbidity and mortality compared with children born to women without HIV. The basis of this increased vulnerability is unknown. The microbiome, specifically the infant gut microbiome, likely plays an important role in infant immune development. The human milk microbiome is thought to have an important role in the development of the infant gut and therefore, if perturbed, may contribute to this increased vulnerability. We investigated the effects of HIV and its therapies on the milk microbiome and possible changes in the milk microbiome before or after infant HIV infection.
RESULTS RESULTS
Seven-hundred fifty-six human milk samples were selected from three separate studies conducted over a 15-year period to investigate the role of HIV and its therapies on the human milk microbiome. Our data reveal that the milk microbiome is modulated by parity (R
CONCLUSIONS CONCLUSIONS
The milk microbiome varies by stage of lactation, by parity, and by region; however, we found no evidence that the human milk microbiome is altered by maternal HIV infection, disease severity, or antiretroviral therapy. Additionally, we found no association between the milk microbiome and transmission of HIV to the infant. Investigations including higher resolution microbiome approaches or into other potential mechanisms to understand why the approximately one million children born annually to women with HIV escape infection, but do not escape harm, are urgently needed. Video Abstract.

Identifiants

DOI: 10.1186/s40168-024-01843-8 PMID: 39342403
pubmed: 39342403
doi: 10.1186/s40168-024-01843-8
pii: 10.1186/s40168-024-01843-8
doi:

Substances chimiques

RNA, Ribosomal, 16S 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

182

Informations de copyright

© 2024. The Author(s).

Références

Vujkovic-Cvijin I, Sortino O, Verheij E, et al. HIV-associated gut dysbiosis is independent of sexual practice and correlates with noncommunicable diseases. Nat Commun. 2020;11(1):2448. https://doi.org/10.1038/s41467-020-16222-8 .
doi: 10.1038/s41467-020-16222-8 pubmed: 32415070 pmcid: 7228978
Zhou J, Zhang Y, Cui P, et al. Gut microbiome changes associated with HIV infection and sexual orientation. Front Cell Infect Microbiol. 2020;10:434. https://doi.org/10.3389/fcimb.2020.00434 .
doi: 10.3389/fcimb.2020.00434 pubmed: 33102244 pmcid: 7546801
Noguera-Julian M, Rocafort M, Guillen Y, et al. Gut microbiota linked to sexual preference and HIV infection. EBioMedicine. 2016;5:135–46. https://doi.org/10.1016/j.ebiom.2016.01.032 .
doi: 10.1016/j.ebiom.2016.01.032 pubmed: 27077120 pmcid: 4816837
Koren O, Konnikova L, Brodin P, Mysorekar IU, Collado MC. The maternal gut microbiome in pregnancy: implications for the developing immune system. Nat Rev Gastroenterol Hepatol. 2024;21(1):35–45. https://doi.org/10.1038/s41575-023-00864-2 .
doi: 10.1038/s41575-023-00864-2 pubmed: 38097774
Gaufin T, Tobin NH, Aldrovandi GM. The importance of the microbiome in pediatrics and pediatric infectious diseases. Curr Opin Pediatr. 2018;30(1):117–24. https://doi.org/10.1097/MOP.0000000000000576 .
doi: 10.1097/MOP.0000000000000576 pubmed: 29206649 pmcid: 6588283
Prendergast AJ, Evans C. Children who are HIV-exposed and uninfected: evidence for action. AIDS. 2023;37(2):205–15. https://doi.org/10.1097/QAD.0000000000003409 .
doi: 10.1097/QAD.0000000000003409 pubmed: 36541635
Goetghebuer T, Rowland-Jones SL, Kollmann TR. Editorial: immune mechanisms underlying the increased morbidity and mortality of HIV-exposed uninfected (HEU) children. Front Immunol. 2017;8:1060. https://doi.org/10.3389/fimmu.2017.01060 .
doi: 10.3389/fimmu.2017.01060 pubmed: 28932223 pmcid: 5593069
Cohen C, Moyes J, Tempia S, et al. Epidemiology of acute lower respiratory tract infection in HIV-exposed uninfected infants. Pediatrics 2016;137(4). https://doi.org/10.1542/peds.2015-3272 .
Taron-Brocard C, Le Chenadec J, Faye A, et al. Increased risk of serious bacterial infections due to maternal immunosuppression in HIV-exposed uninfected infants in a European country. Clin Infect Dis. 2014;59(9):1332–45. https://doi.org/10.1093/cid/ciu586 .
doi: 10.1093/cid/ciu586 pubmed: 25053719
Labuda SM, Huo Y, Kacanek D, et al. Rates of hospitalization and infection-related hospitalization among human immunodeficiency virus (HIV)-exposed uninfected children compared to HIV-unexposed uninfected children in the United States, 2007–2016. Clin Infect Dis. 2020;71(2):332–9. https://doi.org/10.1093/cid/ciz820 .
doi: 10.1093/cid/ciz820 pubmed: 31504291
Brennan AT, Bonawitz R, Gill CJ, et al. A meta-analysis assessing all-cause mortality in HIV-exposed uninfected compared with HIV-unexposed uninfected infants and children. AIDS. 2016;30(15):2351–60. https://doi.org/10.1097/QAD.0000000000001211 .
doi: 10.1097/QAD.0000000000001211 pubmed: 27456985
Goetghebuer T, Smolen KK, Adler C, et al. Initiation of antiretroviral therapy before pregnancy reduces the risk of infection-related hospitalization in human immunodeficiency virus-exposed uninfected infants born in a high-income country. Clin Infect Dis. 2019;68(7):1193–203. https://doi.org/10.1093/cid/ciy673 .
doi: 10.1093/cid/ciy673 pubmed: 30215689
Amenyogbe N, Dimitriu P, Cho P, et al. Innate Immune responses and gut microbiomes distinguish hiv-exposed from HIV-unexposed children in a population-specific manner. J Immunol. 2020;205(10):2618–28. https://doi.org/10.4049/jimmunol.2000040 .
doi: 10.4049/jimmunol.2000040 pubmed: 33067377 pmcid: 7653510
Ray S, Narayanan A, Giske CG, Neogi U, Sonnerborg A, Nowak P. Altered gut microbiome under antiretroviral therapy: impact of efavirenz and zidovudine. ACS Infect Dis. 2021;7(5):1104–15. https://doi.org/10.1021/acsinfecdis.0c00536 .
doi: 10.1021/acsinfecdis.0c00536 pubmed: 33346662
Kordy K, Gaufin T, Mwangi M, et al. Contributions to human breast milk microbiome and enteromammary transfer of Bifidobacterium breve. PLoS ONE. 2020;15(1): e0219633. https://doi.org/10.1371/journal.pone.0219633 .
doi: 10.1371/journal.pone.0219633 pubmed: 31990909 pmcid: 6986747
Shilaih M, Angst DC, Marzel A, Bonhoeffer S, Gunthard HF, Kouyos RD. Antibacterial effects of antiretrovirals, potential implications for microbiome studies in HIV. Antivir Ther. 2018;23(1):91–4. https://doi.org/10.3851/IMP3173 .
doi: 10.3851/IMP3173 pubmed: 28497768
Borg-von Zepelin M, Meyer I, Thomssen R, et al. HIV-Protease inhibitors reduce cell adherence of Candida albicans strains by inhibition of yeast secreted aspartic proteases. J Invest Dermatol. 1999;113(5):747–51. https://doi.org/10.1046/j.1523-1747.1999.00747.x .
doi: 10.1046/j.1523-1747.1999.00747.x pubmed: 10571729
Perez-Matute P, Perez-Martinez L, Aguilera-Lizarraga J, Blanco JR, Oteo JA. Maraviroc modifies gut microbiota composition in a mouse model of obesity: a plausible therapeutic option to prevent metabolic disorders in HIV-infected patients. Rev Esp Quimioter. 2015;28(4):200–6 https://www.ncbi.nlm.nih.gov/pubmed/26200028 .
pubmed: 26200028
Bender JM, Li F, Martelly S, et al. Maternal HIV infection influences the microbiome of HIV-uninfected infants. Sci Transl Med 2016;8(349):349ra100. https://doi.org/10.1126/scitranslmed.aaf5103 .
Flynn PM, Taha TE, Cababasay M, et al. Prevention of HIV-1 transmission through breastfeeding: efficacy and safety of maternal antiretroviral therapy versus infant nevirapine prophylaxis for duration of breastfeeding in HIV-1-infected women with high CD4 cell count (IMPAACT PROMISE): a randomized, open-label, clinical trial. J Acquir Immune Defic Syndr. 2018;77(4):383–92. https://doi.org/10.1097/QAI.0000000000001612 .
doi: 10.1097/QAI.0000000000001612 pubmed: 29239901 pmcid: 5825265
Fowler MG, Qin M, Fiscus SA, et al. Benefits and risks of antiretroviral therapy for perinatal HIV prevention. N Engl J Med. 2016;375(18):1726–37. https://doi.org/10.1056/NEJMoa1511691 .
doi: 10.1056/NEJMoa1511691 pubmed: 27806243 pmcid: 5214343
Kuhn L, Aldrovandi GM, Sinkala M, et al. Effects of early, abrupt weaning on HIV-free survival of children in Zambia. N Engl J Med. 2008;359(2):130–41. https://doi.org/10.1056/NEJMoa073788 .
doi: 10.1056/NEJMoa073788 pubmed: 18525036 pmcid: 2577610
Bender JM, Li F, Adisetiyo H, et al. Quantification of variation and the impact of biomass in targeted 16S rRNA gene sequencing studies. Microbiome. 2018;6(1):155. https://doi.org/10.1186/s40168-018-0543-z .
doi: 10.1186/s40168-018-0543-z pubmed: 30201048 pmcid: 6131952
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3. https://doi.org/10.1038/nmeth.3869 .
doi: 10.1038/nmeth.3869 pubmed: 27214047 pmcid: 4927377
Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome. 2018;6(1):226. https://doi.org/10.1186/s40168-018-0605-2 .
doi: 10.1186/s40168-018-0605-2 pubmed: 30558668 pmcid: 6298009
McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8(4): e61217. https://doi.org/10.1371/journal.pone.0061217 .
doi: 10.1371/journal.pone.0061217 pubmed: 23630581 pmcid: 3632530
Martin BD, Witten D, Willis AD. Modeling microbial abundances and dysbiosis with beta-binomial regression. Ann Appl Stat. 2020;14(1):94–115. https://doi.org/10.1214/19-aoas1283 .
doi: 10.1214/19-aoas1283 pubmed: 32983313 pmcid: 7514055
Benjamini Y, Hochberg Y. Controlling the False discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc B 1995;57(1):289–300. (In English). https://doi.org/10.1111/j.2517-6161.1995.tb02031.x .
Maqsood R, Skidmore PT, Holland LA, et al. Dynamic changes in breast milk microbiome in the early postpartum period of Kenyan women living with HIV are influenced by antibiotics but not antiretrovirals. Microbiol Spectr. 2022;10(2): e0208021. https://doi.org/10.1128/spectrum.02080-21 .
doi: 10.1128/spectrum.02080-21 pubmed: 35384692
Grant-Beurmann S, Jumare J, Ndembi N, et al. Dynamics of the infant gut microbiota in the first 18 months of life: the impact of maternal HIV infection and breastfeeding. Microbiome. 2022;10(1):61. https://doi.org/10.1186/s40168-022-01230-1 .
doi: 10.1186/s40168-022-01230-1 pubmed: 35414043 pmcid: 9004197
Waitt CJ, Garner P, Bonnett LJ, Khoo SH, Else LJ. Is infant exposure to antiretroviral drugs during breastfeeding quantitatively important? A systematic review and meta-analysis of pharmacokinetic studies. J Antimicrob Chemother. 2015;70(7):1928–41. https://doi.org/10.1093/jac/dkv080 .
doi: 10.1093/jac/dkv080 pubmed: 25858354 pmcid: 4472329
Aebi-Popp K, Kahlert CR, Crisinel PA, et al. Transfer of antiretroviral drugs into breastmilk: a prospective study from the Swiss mother and child HIV cohort study. J Antimicrob Chemother. 2022;77(12):3436–42. https://doi.org/10.1093/jac/dkac337 .
doi: 10.1093/jac/dkac337 pubmed: 36177836 pmcid: 9704434
Kordy K, Tobin NH, Aldrovandi GM. HIV and SIV in body fluids: from breast milk to the genitourinary tract. Curr Immunol Rev. 2019;15(1):139–52. https://doi.org/10.2174/1573395514666180605085313 .
doi: 10.2174/1573395514666180605085313 pubmed: 33312088 pmcid: 7730163
Tobin NH, Aldrovandi GM. Immunology of pediatric HIV infection. Immunol Rev. 2013;254(1):143–69. https://doi.org/10.1111/imr.12074 .
doi: 10.1111/imr.12074 pubmed: 23772619 pmcid: 3737605
Kuhn L, Thea DM, Aldrovandi GM. Bystander effects: children who escape infection but not harm. J Acquir Immune Defic Syndr. 2007;46(5):517–8. https://doi.org/10.1097/QAI.0b013e31814d6600 .
doi: 10.1097/QAI.0b013e31814d6600 pubmed: 18043311 pmcid: 2803759

Auteurs

Nicole H Tobin (NH)

Division of Infectious Diseases, Department of Pediatrics, David Geffen School of Medicine at the University of California, 10833 Le Conte Ave., 22-340 MDCC, Los Angeles, CA, 90095, USA.

Fan Li (F)

Division of Infectious Diseases, Department of Pediatrics, David Geffen School of Medicine at the University of California, 10833 Le Conte Ave., 22-340 MDCC, Los Angeles, CA, 90095, USA.

Sean Brummel (S)

The Center for Biostatistics in AIDS Research, Harvard T.H. Chan School of Public Health, Boston, MA, USA.

Patricia M Flynn (PM)

Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, TN, USA.

Sufia Dababhai (S)

Johns Hopkins Bloomberg School of Public Health, Blantyre, Malawi.

Dhayendre Moodley (D)

Centre for the AIDS Programme of Research, School of Clinical Medicine, University of KwaZulu Natal, Durban, South Africa.

Lameck Chinula (L)

University of North Carolina (UNC) Project Malawi, Lilongwe, Malawi.

Avy Violari (A)

Perinatal HIV Research Unit, University of the Witwatersrand, Johannesburg, South Africa.

Mary Glenn Fowler (MG)

Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.

Vanessa Rouzier (V)

The Haitian Group for the Study of Kaposi's Sarcoma and Opportunistic Infections, GHESKIO Centers, Port-Au-Price, Ouest, 15727, Haiti.

Louise Kuhn (L)

Gertrude H. Sergievsky Center, Vagelos College of Physicians and Surgeons, New York, NY, USA.
Department of Epidemiology, Mailman School of Public Health, Columbia University Irving Medical Center, New York, NY, USA.

Grace M Aldrovandi (GM)

Division of Infectious Diseases, Department of Pediatrics, David Geffen School of Medicine at the University of California, 10833 Le Conte Ave., 22-340 MDCC, Los Angeles, CA, 90095, USA. GAldrovandi@mednet.ucla.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Aliments et boissons › Aliments › Produits laitiers › Lait › Lait humain › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Maladies du système immunitaire › Déficits immunitaires › Infections à VIH › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN ribosomique › ARN ribosomique 16S › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Phénomènes physiologiques des appareils urinaire et reproducteur › Phénomènes physiologiques de la reproduction › Reproduction › Grossesse › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Environnement et santé publique › Santé publique › Transmission de maladie infectieuse › Transmission verticale de maladie infectieuse › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Personnes › Tranches d'âge › Nourrisson › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Environnement et santé publique › Environnement › Écosystème › Biodiversité › Biote › Microbiote › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Environnement et santé publique › Environnement › Écosystème › Biodiversité › Biote › Microbiote › Microbiome gastro-intestinal › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Personnes › Tranches d'âge › Nourrisson › Nouveau-né › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Maladies urogénitales › Maladies de l'appareil urogénital féminin et complications de la grossesse › Complications de la grossesse › Complications infectieuses de la grossesse › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Bactéries › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Personnes › Tranches d'âge › Adulte › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Phénomènes physiologiques › Alimentation et nutrition › Phénomènes physiologiques nutritionnels › Comportement alimentaire › Allaitement naturel › Maternal HIV infection and the milk microbiome.
Recherchemedicale.com › Phénomènes physiologiques des appareils urinaire et reproducteur › Phénomènes physiologiques de la reproduction › Période du postpartum › Lactation › Maternal HIV infection and the milk microbiome.