Association of key species of vaginal bacteria of recurrent bacterial vaginosis patients before and after oral metronidazole therapy with short- and long-term clinical outcomes
Bacterial vaginosis (BV) is associated with a state of vaginal dysbiosis typically involving depletion of otherwise dominant populations of Lactobacillus. The causes of this microbial succession are not known; there may be multiple causes. Standard treatment includes oral metronidazole, which typica...
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| description | Bacterial vaginosis (BV) is associated with a state of vaginal dysbiosis typically involving depletion of otherwise dominant populations of Lactobacillus. The causes of this microbial succession are not known; there may be multiple causes. Standard treatment includes oral metronidazole, which typically restores Lactobacillus species to dominance. However, recurrence rates are high; recurrent BV patients recur 3-4 times annually and are often refractory to treatment. Our previous qPCR-based study of recurrent BV patients pointed to putatively more virulent species of Gardnerella that were associated with refractory responses to oral metronidazole, and less robust recovery of Lactobacillus species associated with recurrence after an initial period of remission. However, these associations did not account for outcomes in all patients, suggesting that other bacterial species were involved. In this follow-up study, we sequenced the V4 domain of 16S rRNA sequences of 41of these same patients pre- and posttreatment. Overall compositions among pretreatment clinical outcome groups were not different, although alpha diversity significantly decreased: refractory > recurrent > remission. Combinations of key species were associated with and prognostic for outcome. Higher pretreatment abundance of Megasphaera lornae together with lower abundance of Gardnerella Gsp07 and Finegoldia magna predicted long term remission after oral metronidazole. Furthermore, a subset of refractory patients that did not have high levels of Gardnerella Gsp07, instead had elevated levels of alternative species including Atopobium vaginae, Mageeibacillus indolicus (BVAB3), and Prevotella timonensis. Patients who recurred after transient remission had elevated abundance of species including Atopobium vaginae, Gardnerella, and Aerococcus christensenii, compared to long-term remission patients. Core bacterial species among refractory patients did not change in abundance after metronidazole, suggesting resistance or tolerance, in contrast to the loss in abundance of the same species among recurrent or remission patients. These findings have potential prognostic and therapeutic implications. |
| doi_str_mv | 10.1371/journal.pone.0272012 |
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The causes of this microbial succession are not known; there may be multiple causes. Standard treatment includes oral metronidazole, which typically restores Lactobacillus species to dominance. However, recurrence rates are high; recurrent BV patients recur 3-4 times annually and are often refractory to treatment. Our previous qPCR-based study of recurrent BV patients pointed to putatively more virulent species of Gardnerella that were associated with refractory responses to oral metronidazole, and less robust recovery of Lactobacillus species associated with recurrence after an initial period of remission. However, these associations did not account for outcomes in all patients, suggesting that other bacterial species were involved. In this follow-up study, we sequenced the V4 domain of 16S rRNA sequences of 41of these same patients pre- and posttreatment. Overall compositions among pretreatment clinical outcome groups were not different, although alpha diversity significantly decreased: refractory > recurrent > remission. Combinations of key species were associated with and prognostic for outcome. Higher pretreatment abundance of Megasphaera lornae together with lower abundance of Gardnerella Gsp07 and Finegoldia magna predicted long term remission after oral metronidazole. Furthermore, a subset of refractory patients that did not have high levels of Gardnerella Gsp07, instead had elevated levels of alternative species including Atopobium vaginae, Mageeibacillus indolicus (BVAB3), and Prevotella timonensis. Patients who recurred after transient remission had elevated abundance of species including Atopobium vaginae, Gardnerella, and Aerococcus christensenii, compared to long-term remission patients. Core bacterial species among refractory patients did not change in abundance after metronidazole, suggesting resistance or tolerance, in contrast to the loss in abundance of the same species among recurrent or remission patients. These findings have potential prognostic and therapeutic implications.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0272012</identifier><identifier>PMID: 35901180</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Abundance ; Asymptomatic ; Atopobium vaginae ; Bacteria ; Biology and Life Sciences ; Care and treatment ; Clinical outcomes ; Computer and Information Sciences ; Depletion ; Diagnosis ; Dosage and administration ; Drug resistance in microorganisms ; Dysbacteriosis ; Ecological succession ; Ecology and Environmental Sciences ; Laboratories ; Lactobacillus ; Medicine and Health Sciences ; Metronidazole ; Microbiota ; Microorganisms ; Patients ; Pretreatment ; Prevention ; Remission ; Remission (Medicine) ; Risk factors ; rRNA 16S ; Sexual intercourse ; Species ; Vagina ; Vaginosis</subject><ispartof>PloS one, 2022-07, Vol.17 (7), p.e0272012-e0272012</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Mollin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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The causes of this microbial succession are not known; there may be multiple causes. Standard treatment includes oral metronidazole, which typically restores Lactobacillus species to dominance. However, recurrence rates are high; recurrent BV patients recur 3-4 times annually and are often refractory to treatment. Our previous qPCR-based study of recurrent BV patients pointed to putatively more virulent species of Gardnerella that were associated with refractory responses to oral metronidazole, and less robust recovery of Lactobacillus species associated with recurrence after an initial period of remission. However, these associations did not account for outcomes in all patients, suggesting that other bacterial species were involved. In this follow-up study, we sequenced the V4 domain of 16S rRNA sequences of 41of these same patients pre- and posttreatment. Overall compositions among pretreatment clinical outcome groups were not different, although alpha diversity significantly decreased: refractory > recurrent > remission. Combinations of key species were associated with and prognostic for outcome. Higher pretreatment abundance of Megasphaera lornae together with lower abundance of Gardnerella Gsp07 and Finegoldia magna predicted long term remission after oral metronidazole. Furthermore, a subset of refractory patients that did not have high levels of Gardnerella Gsp07, instead had elevated levels of alternative species including Atopobium vaginae, Mageeibacillus indolicus (BVAB3), and Prevotella timonensis. Patients who recurred after transient remission had elevated abundance of species including Atopobium vaginae, Gardnerella, and Aerococcus christensenii, compared to long-term remission patients. Core bacterial species among refractory patients did not change in abundance after metronidazole, suggesting resistance or tolerance, in contrast to the loss in abundance of the same species among recurrent or remission patients. These findings have potential prognostic and therapeutic implications.</description><subject>Abundance</subject><subject>Asymptomatic</subject><subject>Atopobium vaginae</subject><subject>Bacteria</subject><subject>Biology and Life Sciences</subject><subject>Care and treatment</subject><subject>Clinical outcomes</subject><subject>Computer and Information Sciences</subject><subject>Depletion</subject><subject>Diagnosis</subject><subject>Dosage and administration</subject><subject>Drug resistance in microorganisms</subject><subject>Dysbacteriosis</subject><subject>Ecological succession</subject><subject>Ecology and Environmental Sciences</subject><subject>Laboratories</subject><subject>Lactobacillus</subject><subject>Medicine and Health Sciences</subject><subject>Metronidazole</subject><subject>Microbiota</subject><subject>Microorganisms</subject><subject>Patients</subject><subject>Pretreatment</subject><subject>Prevention</subject><subject>Remission</subject><subject>Remission 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one</jtitle><date>2022-07-28</date><risdate>2022</risdate><volume>17</volume><issue>7</issue><spage>e0272012</spage><epage>e0272012</epage><pages>e0272012-e0272012</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Bacterial vaginosis (BV) is associated with a state of vaginal dysbiosis typically involving depletion of otherwise dominant populations of Lactobacillus. The causes of this microbial succession are not known; there may be multiple causes. Standard treatment includes oral metronidazole, which typically restores Lactobacillus species to dominance. However, recurrence rates are high; recurrent BV patients recur 3-4 times annually and are often refractory to treatment. Our previous qPCR-based study of recurrent BV patients pointed to putatively more virulent species of Gardnerella that were associated with refractory responses to oral metronidazole, and less robust recovery of Lactobacillus species associated with recurrence after an initial period of remission. However, these associations did not account for outcomes in all patients, suggesting that other bacterial species were involved. In this follow-up study, we sequenced the V4 domain of 16S rRNA sequences of 41of these same patients pre- and posttreatment. Overall compositions among pretreatment clinical outcome groups were not different, although alpha diversity significantly decreased: refractory > recurrent > remission. Combinations of key species were associated with and prognostic for outcome. Higher pretreatment abundance of Megasphaera lornae together with lower abundance of Gardnerella Gsp07 and Finegoldia magna predicted long term remission after oral metronidazole. Furthermore, a subset of refractory patients that did not have high levels of Gardnerella Gsp07, instead had elevated levels of alternative species including Atopobium vaginae, Mageeibacillus indolicus (BVAB3), and Prevotella timonensis. Patients who recurred after transient remission had elevated abundance of species including Atopobium vaginae, Gardnerella, and Aerococcus christensenii, compared to long-term remission patients. Core bacterial species among refractory patients did not change in abundance after metronidazole, suggesting resistance or tolerance, in contrast to the loss in abundance of the same species among recurrent or remission patients. These findings have potential prognostic and therapeutic implications.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>35901180</pmid><doi>10.1371/journal.pone.0272012</doi><tpages>e0272012</tpages><orcidid>https://orcid.org/0000-0002-2696-3740</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Abundance Asymptomatic Atopobium vaginae Bacteria Biology and Life Sciences Care and treatment Clinical outcomes Computer and Information Sciences Depletion Diagnosis Dosage and administration Drug resistance in microorganisms Dysbacteriosis Ecological succession Ecology and Environmental Sciences Laboratories Lactobacillus Medicine and Health Sciences Metronidazole Microbiota Microorganisms Patients Pretreatment Prevention Remission Remission (Medicine) Risk factors rRNA 16S Sexual intercourse Species Vagina Vaginosis |
| title | Association of key species of vaginal bacteria of recurrent bacterial vaginosis patients before and after oral metronidazole therapy with short- and long-term clinical outcomes |
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