{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T06:43:04Z","timestamp":1791268984684,"version":"4.1.0"},"reference-count":37,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2020,6,6]],"date-time":"2020-06-06T00:00:00Z","timestamp":1591401600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["UM1AI068633"],"award-info":[{"award-number":["UM1AI068633"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["UM1AI068615"],"award-info":[{"award-number":["UM1AI068615"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["UM1AI106707"],"award-info":[{"award-number":["UM1AI106707"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,8,2]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Limited evidence suggests that the nonhormonal contraceptive copper intrauterine device (Cu-IUD) may increase bacterial vaginosis (BV) risk, possibly due to increased volume and duration of menses, a common side effect of Cu-IUD use. Although increases in bleeding typically resolve within 6\u201312 months following initiation, evaluations of the association between Cu-IUD and BV have not included more than 6 months of follow-up.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>This secondary analysis of a human immunodeficiency virus type 1 prevention trial included 2585 African women ages 18\u201345 followed for up to 33 months. Women reported contraceptive use each month. BV was evaluated by Nugent score in 6-monthly intervals and, if clinically indicated, by Amsel criteria. Andersen-Gill proportional hazards models were used to (1) evaluate BV risk among Cu-IUD users relative to women using no\/another nonhormonal contraceptive and (2) test changes in BV frequency before, while using, and following Cu-IUD discontinuation.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>BV frequency was highest among Cu-IUD users at 153.6 episodes per 100 person-years (95% confidence interval [CI]: 145.2, 162.4). In adjusted models, Cu-IUD users experienced 1.28-fold (95% CI: 1.12, 1.46) higher BV risk relative to women using no\/another nonhormonal contraception. Compared to the 6 months prior to initiation, BV risk was 1.52-fold (95% CI: 1.16, 2.00) higher in the first 6 months of Cu-IUD use and remained elevated over 18 months of use (P\u2005&amp;lt;\u2005.05). Among women who discontinued Cu-IUD, BV frequency was similar to pre-initiation rates within 1 year.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Cu-IUD users experienced elevated BV risk that persisted throughout use. Women and their providers may wish to consider BV risk when discussing contraceptive options.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1093\/cid\/ciaa703","type":"journal-article","created":{"date-parts":[[2020,6,1]],"date-time":"2020-06-01T15:15:42Z","timestamp":1591024542000},"page":"513-520","source":"Crossref","is-referenced-by-count":40,"title":["Elevated Risk of Bacterial Vaginosis Among Users of the Copper Intrauterine Device: A Prospective Longitudinal Cohort Study"],"prefix":"10.1093","volume":"73","author":[{"given":"Kathryn","family":"Peebles","sequence":"first","affiliation":[{"name":"Department of Epidemiology, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Flavia M","family":"Kiweewa","sequence":"additional","affiliation":[{"name":"Makerere University - Johns Hopkins University Research Collaboration, Kampala, Uganda"},{"name":"Makerere University School of Public Health, Kampala, Uganda"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thesla","family":"Palanee-Phillips","sequence":"additional","affiliation":[{"name":"Wits Reproductive Health and HIV Institute, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Catherine","family":"Chappell","sequence":"additional","affiliation":[{"name":"Department of Obstetrics, Gynecology, and Reproductive Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Devika","family":"Singh","sequence":"additional","affiliation":[{"name":"Magee-Womens Research Institute, Pittsburgh, Pennsylvania, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katherine E","family":"Bunge","sequence":"additional","affiliation":[{"name":"Department of Obstetrics, Gynecology, and Reproductive Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Logashvari","family":"Naidoo","sequence":"additional","affiliation":[{"name":"South African Medical Research Council, Durban, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bonus","family":"Makanani","sequence":"additional","affiliation":[{"name":"Malawi College of Medicine - Johns Hopkins University Research Project, Blantyre, Malawi"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nitesha","family":"Jeenarain","sequence":"additional","affiliation":[{"name":"South African Medical Research Council, Durban, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Doerieyah","family":"Reynolds","sequence":"additional","affiliation":[{"name":"University of Cape Town Medical School, Cape Town, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sharon L","family":"Hillier","sequence":"additional","affiliation":[{"name":"Department of Obstetrics, Gynecology, and Reproductive Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth R","family":"Brown","sequence":"additional","affiliation":[{"name":"Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA"},{"name":"Department of Biostatistics, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jared M","family":"Baeten","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, University of Washington, Seattle, Washington, USA"},{"name":"Department of Global Health, University of Washington, Seattle, Washington, USA"},{"name":"Department of Medicine, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer E","family":"Balkus","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, University of Washington, Seattle, Washington, USA"},{"name":"Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA"},{"name":"Department of Global Health, University of Washington, Seattle, Washington, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"name":"MTN-020\/ASPIRE study team","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jared","family":"Baeten","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thesla","family":"Palanee-Phillips","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth","family":"Brown","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lydia","family":"Soto-Torres","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katie","family":"Schwartz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bonus","family":"Makanani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francis","family":"Martinson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linda-Gail","family":"Bekker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vaneshree","family":"Govender","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samantha","family":"Siva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zakir","family":"Gaffoor","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Logashvari","family":"Naidoo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arendevi","family":"Pather","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nitesha","family":"Jeenarain","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gonasagrie","family":"Nair","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thesla","family":"Palanee-Phillips","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Flavia","family":"Matovu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nyaradzo","family":"Mgodi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Felix","family":"Mhlanga","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,6,6]]},"reference":[{"key":"2021080205164918400_CIT0001","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1186\/s12879-015-1027-4","article-title":"Making inroads into improving treatment of bacterial vaginosis: striving for long-term cure","volume":"15","author":"Bradshaw","year":"2015","journal-title":"BMC Infect Dis"},{"key":"2021080205164918400_CIT0002","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1097\/OLQ.0b013e31827c5a5b","article-title":"Does bacterial vaginosis cause pelvic inflammatory disease?","volume":"40","author":"Taylor","year":"2013","journal-title":"Sex Transm Dis"},{"key":"2021080205164918400_CIT0003","doi-asserted-by":"crossref","first-page":"1737","DOI":"10.1056\/NEJM199512283332604","article-title":"Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group","volume":"333","author":"Hillier","year":"1995","journal-title":"N Engl J Med"},{"key":"2021080205164918400_CIT0004","doi-asserted-by":"crossref","first-page":"e1001251","DOI":"10.1371\/journal.pmed.1001251","article-title":"Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: a prospective cohort analysis among African couples","volume":"9","author":"Cohen","year":"2012","journal-title":"PLoS Med"},{"key":"2021080205164918400_CIT0005","doi-asserted-by":"crossref","first-page":"e1000416","DOI":"10.1371\/journal.pmed.1000416","article-title":"Intravaginal practices, bacterial vaginosis, and HIV infection in women: individual participant data meta-analysis","volume":"8","author":"Low","year":"2011","journal-title":"PLoS Med"},{"key":"2021080205164918400_CIT0006","first-page":"4","article-title":"Bacterial vaginosis: a synthesis of the literature on etiology, prevalence, risk factors, and relationship with chlamydia and gonorrhea infections","volume":"3","author":"Bautista","year":"2016","journal-title":"Mil Med Res"},{"key":"2021080205164918400_CIT0007","doi-asserted-by":"crossref","first-page":"17","DOI":"10.9745\/GHSP-D-17-00396","article-title":"Liftoff: the blossoming of contraceptive implant use in Africa","volume":"6","author":"Jacobstein","year":"2018","journal-title":"Glob Health Sci Pract"},{"key":"2021080205164918400_CIT0008","doi-asserted-by":"crossref","first-page":"954","DOI":"10.1097\/OLQ.0b013e31811ed0e4","article-title":"Longitudinal association between hormonal contraceptives and bacterial vaginosis in women of reproductive age","volume":"34","author":"Riggs","year":"2007","journal-title":"Sex Transm Dis"},{"key":"2021080205164918400_CIT0009","doi-asserted-by":"crossref","first-page":"e73055","DOI":"10.1371\/journal.pone.0073055","article-title":"Hormonal contraception is associated with a reduced risk of bacterial vaginosis: a systematic review and meta-analysis","volume":"8","author":"Vodstrcil","year":"2013","journal-title":"PLoS One"},{"key":"2021080205164918400_CIT0010","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/s10096-016-2768-8","article-title":"Influence of contraceptive choice on vaginal bacterial and fungal microflora","volume":"36","author":"Donders","year":"2017","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"2021080205164918400_CIT0011","first-page":"1","article-title":"Use of copper","author":"Kancheva Landolt","year":"2018","journal-title":"AIDS Care"},{"key":"2021080205164918400_CIT0012","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1097\/OLQ.0b013e31823e68fe","article-title":"Risk of bacterial vaginosis in users of the intrauterine device: a longitudinal study","volume":"39","author":"Madden","year":"2012","journal-title":"Sex Transm Dis"},{"key":"2021080205164918400_CIT0013","doi-asserted-by":"crossref","first-page":"622.e1","DOI":"10.1016\/j.ajog.2018.02.017","article-title":"Impact of contraceptive initiation on vaginal microbiota","volume":"218","author":"Achilles","year":"2018","journal-title":"Am J Obstet Gynecol"},{"key":"2021080205164918400_CIT0014","doi-asserted-by":"crossref","first-page":"e10197","DOI":"10.1371\/journal.pone.0010197","article-title":"Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis","volume":"5","author":"Srinivasan","year":"2010","journal-title":"PLoS One"},{"key":"2021080205164918400_CIT0015","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1016\/j.contraception.2008.11.012","article-title":"Side effects from the copper IUD: do they decrease over time?","volume":"79","author":"Hubacher","year":"2009","journal-title":"Contraception"},{"key":"2021080205164918400_CIT0016","doi-asserted-by":"crossref","first-page":"e0199724","DOI":"10.1371\/journal.pone.0199724","article-title":"Bleeding, cramping, and satisfaction among new copper IUD users: a prospective study","volume":"13","author":"Sanders","year":"2018","journal-title":"PLoS One"},{"key":"2021080205164918400_CIT0017","article-title":"Expanding the mix","author":"Bunge"},{"key":"2021080205164918400_CIT0018","doi-asserted-by":"crossref","first-page":"2121","DOI":"10.1056\/NEJMoa1506110","article-title":"Use of a vaginal ring containing dapivirine for HIV-1 prevention in women","volume":"375","author":"Baeten","year":"2016","journal-title":"N Engl J Med"},{"key":"2021080205164918400_CIT0019","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1128\/jcm.29.2.297-301.1991","article-title":"Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation","volume":"29","author":"Nugent","year":"1991","journal-title":"J Clin Microbiol"},{"key":"2021080205164918400_CIT0020","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/0002-9343(83)91112-9","article-title":"Nonspecific vaginitis: diagnostic criteria and microbial and epidemiologic associations","volume":"74","author":"Amsel","year":"1983","journal-title":"Am J Med"},{"key":"2021080205164918400_CIT0021","volume-title":"Guidelines for the management of sexually transmitted infections.","author":"World Health Organization","year":"2003"},{"key":"2021080205164918400_CIT0022","volume-title":"Management of sexually","author":"Ministry of Health, Malawi","year":"2007"},{"key":"2021080205164918400_CIT0023","volume-title":"Sexually transmitted infections management guidelines 2015","author":"South Africa National Department of Health.","year":"2015"},{"key":"2021080205164918400_CIT0024","volume-title":"R: a language and environment for statistical computing","author":"R Development Core Team","year":"2008"},{"key":"2021080205164918400_CIT0025","article-title":"Contraceptive-induced changes in genital tract HIV-1 cellular targets and microbiota among women enrolled in the ECHO trial.","author":"Jaspan"},{"key":"2021080205164918400_CIT0026","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.contraception.2019.06.006","article-title":"Contraceptive method switching among women living in sub-Saharan Africa participating in an HIV-1 prevention trial: a prospective cohort study","volume":"100","author":"Chappell","year":"2019","journal-title":"Contraception"},{"key":"2021080205164918400_CIT0027","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1097\/QAD.0000000000000646","article-title":"Changes in the contribution of genital tract infections to HIV acquisition among Kenyan high-risk women from 1993 to 2012","volume":"29","author":"Masese","year":"2015","journal-title":"AIDS (London, England)"},{"key":"2021080205164918400_CIT0028","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.contraception.2014.04.006","article-title":"Vaginal microbiome changes with levonorgestrel intrauterine system placement","volume":"90","author":"Jacobson","year":"2014","journal-title":"Contraception"},{"key":"2021080205164918400_CIT0029","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/j.contraception.2016.11.006","article-title":"Effects of combined oral contraceptives, depot medroxyprogesterone acetate and the levonorgestrel-releasing intrauterine system on the vaginal microbiome","volume":"95","author":"Brooks","year":"2017","journal-title":"Contraception"},{"key":"2021080205164918400_CIT0030","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1099\/jmm.0.000657","article-title":"Short- and long-term influence of the levonorgestrel-releasing intrauterine system (Mirena\u00ae) on vaginal microbiota and Candida","volume":"67","author":"Donders","year":"2018","journal-title":"J Med Microbiol"},{"key":"2021080205164918400_CIT0031","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/j.contraception.2008.01.007","article-title":"Can intrauterine contraceptive devices be a Candida albicans reservoir?","volume":"77","author":"Chassot","year":"2008","journal-title":"Contraception"},{"key":"2021080205164918400_CIT0032","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1099\/jmm.0.46197-0","article-title":"Biofilm formation on intrauterine devices in relation to duration of use","volume":"54","author":"P\u00e1l","year":"2005","journal-title":"J Med Microbiol"},{"key":"2021080205164918400_CIT0033","author":"Bayer"},{"key":"2021080205164918400_CIT0034","author":"Merck"},{"key":"2021080205164918400_CIT0035","doi-asserted-by":"crossref","first-page":"e47","DOI":"10.1097\/QAI.0000000000001455","article-title":"Brief report: dapivirine vaginal ring use does not diminish the effectiveness of hormonal contraception","volume":"76","author":"Balkus","year":"2017","journal-title":"J Acquir Immune Defic Syndr"},{"key":"2021080205164918400_CIT0036","first-page":"89","article-title":"Personalized contraceptive counseling: helping women make the right choice","volume":"7","author":"Rodriguez","year":"2016","journal-title":"Open Access J Contracept"},{"key":"2021080205164918400_CIT0037","doi-asserted-by":"crossref","article-title":"Natural History of Asymptomatic Bacterial Vaginosis among Kenyan Women at High Risk for HIV Infection.","author":"Pyra","DOI":"10.1016\/j.ajog.2019.10.035"}],"container-title":["Clinical Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/cid\/advance-article-pdf\/doi\/10.1093\/cid\/ciaa703\/33494409\/ciaa703.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/cid\/article-pdf\/73\/3\/513\/39508566\/ciaa703.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/cid\/article-pdf\/73\/3\/513\/39508566\/ciaa703.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,8,2]],"date-time":"2021-08-02T01:18:07Z","timestamp":1627867087000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cid\/article\/73\/3\/513\/5854318"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,6]]},"references-count":37,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2020,6,6]]},"published-print":{"date-parts":[[2021,8,2]]}},"URL":"https:\/\/doi.org\/10.1093\/cid\/ciaa703","relation":{},"ISSN":["1058-4838","1537-6591"],"issn-type":[{"value":"1058-4838","type":"print"},{"value":"1537-6591","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021,8,1]]},"published":{"date-parts":[[2020,6,6]]}}}