Rectal mucosal inflammation, microbiome, and wound healing in men who have sex with men who engage in receptive anal intercourse
Abstract Mucosal injury is common during consensual intercourse and induces an inflammatory response that could contribute to pathogen transmission including HIV. Here, we compared mucosal immune and microbiome responses to experimentally induced mucosal injury between men who have sex with men enga...
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Nature Portfolio
2024-12-01
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| Online Access: | https://doi.org/10.1038/s41598-024-80074-1 |
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| author | Vanessa E. Van Doren Cassie G. Ackerley Robert A. Arthur Phillip M. Murray S. Abigail Smith Yi-Juan Hu Colleen F. Kelley |
| author_facet | Vanessa E. Van Doren Cassie G. Ackerley Robert A. Arthur Phillip M. Murray S. Abigail Smith Yi-Juan Hu Colleen F. Kelley |
| author_sort | Vanessa E. Van Doren |
| collection | DOAJ |
| description | Abstract Mucosal injury is common during consensual intercourse and induces an inflammatory response that could contribute to pathogen transmission including HIV. Here, we compared mucosal immune and microbiome responses to experimentally induced mucosal injury between men who have sex with men engaging in receptive anal intercourse (MSM-RAI) and men who do not engage in RAI (controls), all without HIV. Rectal mucosal secretions were collected from adult MSM-RAI (n = 19) and controls (n = 6) via anoscopy before and up to eight days after experimentally induced injury. Mucosal healing was evaluated by repeated injury surface area measurements with digital imaging. MSM-RAI demonstrated overall significantly higher concentrations of pro-inflammatory cytokines and a distinct rectal microbiome compared with controls. Wound healing was numerically faster in MSM-RAI but did not meet statistical significance (p = 0.09). Different cytokine injury response patterns were observed between MSM-RAI and controls; however, IL-6 and IP-10 were important mediators in both groups. Microbial guilds, particularly from the Lachnospiraceae and Prevotellaceae families, were associated with rectal mucosal inflammation. This work is the first experimental study of rectal mucosal injury and the immune environment in healthy humans and provides a more nuanced understanding of rectal mucosal inflammation after injury, which can inform our understanding of HIV transmission. |
| format | Article |
| id | doaj-art-cae54124618b4deb9dda9e7454bb2eac |
| institution | Kabale University |
| issn | 2045-2322 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Nature Portfolio |
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| spelling | doaj-art-cae54124618b4deb9dda9e7454bb2eac2025-01-05T12:29:47ZengNature PortfolioScientific Reports2045-23222024-12-0114111210.1038/s41598-024-80074-1Rectal mucosal inflammation, microbiome, and wound healing in men who have sex with men who engage in receptive anal intercourseVanessa E. Van Doren0Cassie G. Ackerley1Robert A. Arthur2Phillip M. Murray3S. Abigail Smith4Yi-Juan Hu5Colleen F. Kelley6The Hope Clinic of the Emory Vaccine Center, Division of Infectious Diseases, Department of Medicine, Emory University School of MedicineThe Hope Clinic of the Emory Vaccine Center, Division of Infectious Diseases, Department of Medicine, Emory University School of MedicineEmory Integrated Computational Core, Emory UniversityThe Hope Clinic of the Emory Vaccine Center, Division of Infectious Diseases, Department of Medicine, Emory University School of MedicineThe Hope Clinic of the Emory Vaccine Center, Division of Infectious Diseases, Department of Medicine, Emory University School of MedicineDepartment of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory UniversityThe Hope Clinic of the Emory Vaccine Center, Division of Infectious Diseases, Department of Medicine, Emory University School of MedicineAbstract Mucosal injury is common during consensual intercourse and induces an inflammatory response that could contribute to pathogen transmission including HIV. Here, we compared mucosal immune and microbiome responses to experimentally induced mucosal injury between men who have sex with men engaging in receptive anal intercourse (MSM-RAI) and men who do not engage in RAI (controls), all without HIV. Rectal mucosal secretions were collected from adult MSM-RAI (n = 19) and controls (n = 6) via anoscopy before and up to eight days after experimentally induced injury. Mucosal healing was evaluated by repeated injury surface area measurements with digital imaging. MSM-RAI demonstrated overall significantly higher concentrations of pro-inflammatory cytokines and a distinct rectal microbiome compared with controls. Wound healing was numerically faster in MSM-RAI but did not meet statistical significance (p = 0.09). Different cytokine injury response patterns were observed between MSM-RAI and controls; however, IL-6 and IP-10 were important mediators in both groups. Microbial guilds, particularly from the Lachnospiraceae and Prevotellaceae families, were associated with rectal mucosal inflammation. This work is the first experimental study of rectal mucosal injury and the immune environment in healthy humans and provides a more nuanced understanding of rectal mucosal inflammation after injury, which can inform our understanding of HIV transmission.https://doi.org/10.1038/s41598-024-80074-1Mucosal immunologyMicrobiomeMucosal healingBacterial guildsReceptive anal intercourse |
| spellingShingle | Vanessa E. Van Doren Cassie G. Ackerley Robert A. Arthur Phillip M. Murray S. Abigail Smith Yi-Juan Hu Colleen F. Kelley Rectal mucosal inflammation, microbiome, and wound healing in men who have sex with men who engage in receptive anal intercourse Scientific Reports Mucosal immunology Microbiome Mucosal healing Bacterial guilds Receptive anal intercourse |
| title | Rectal mucosal inflammation, microbiome, and wound healing in men who have sex with men who engage in receptive anal intercourse |
| title_full | Rectal mucosal inflammation, microbiome, and wound healing in men who have sex with men who engage in receptive anal intercourse |
| title_fullStr | Rectal mucosal inflammation, microbiome, and wound healing in men who have sex with men who engage in receptive anal intercourse |
| title_full_unstemmed | Rectal mucosal inflammation, microbiome, and wound healing in men who have sex with men who engage in receptive anal intercourse |
| title_short | Rectal mucosal inflammation, microbiome, and wound healing in men who have sex with men who engage in receptive anal intercourse |
| title_sort | rectal mucosal inflammation microbiome and wound healing in men who have sex with men who engage in receptive anal intercourse |
| topic | Mucosal immunology Microbiome Mucosal healing Bacterial guilds Receptive anal intercourse |
| url | https://doi.org/10.1038/s41598-024-80074-1 |
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