{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T12:42:36Z","timestamp":1791895356539,"version":"4.3.4"},"reference-count":35,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2025,1,24]],"date-time":"2025-01-24T00:00:00Z","timestamp":1737676800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Introduction<\/jats:title>\n<jats:p>Recently, efforts to eliminate malaria have shifted focus from symptomatic cases alone to include asymptomatic carriers, who are now recognized as significant contributors to the disease\u2019s transmission and control. This study examines the relationship between asymptomatic malaria infection and hemoglobin levels in Benin.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methods<\/jats:title>\n<jats:p>A cohort in Benin was enrolled and categorized into three age groups (under 5 years, 5\u201315 years, and over 15 years) for follow-up from August to November 2021. Participants were monitored over two months and assessed for malaria infection through microscopy and polymerase chain reaction (PCR) during their three visits. A questionnaire was employed to gather general and clinical characteristics. Multivariate models were utilized to analyze the associations between asymptomatic infection, anemia, and hemoglobin levels.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>Among 393 participants, 58.2% were diagnosed at enrolment with malaria via PCR, and 30.5% through microscopy. Anemia, defined as hemoglobin levels &lt; 11 g\/dL, was observed in 40.5% of the cohort. The risk of anemia declined with increasing age (OR for ages 5\u201315: 0.64, 95% CI [0.37; 1.09]; OR for over 15 years: 0.34, 95% CI [0.20; 0.59]) compared to children under 5. Individuals with both microscopic and submicroscopic infections exhibited higher odds of anemia (respectively OR = 4.15, 95% CI [2.41; 7.13] and OR = 2.09 [1.22; 3.57]) relative to those uninfected. Hemoglobin levels were consistently lower in participants with microscopic malaria across all age groups (\u03b2 = -2.73, 95% CI [-3.41; -2.05] for those under 5, \u03b2 = -1.35, 95% CI [-1.89; -0.82] for ages 5\u201315, and \u03b2 = -0.72, 95% CI [-1.34; -0.07]) compared to non-infected individuals.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Discussion<\/jats:title>\n<jats:p>Our findings suggest that asymptomatic malaria infections, including submicroscopic cases, are associated with anemia and decreased hemoglobin levels. This underscores the importance of employing ultrasensitive diagnostic methods for such infections and acknowledging their potential health implications.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pone.0317345","type":"journal-article","created":{"date-parts":[[2025,1,24]],"date-time":"2025-01-24T19:04:46Z","timestamp":1737745486000},"page":"e0317345","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["Association between asymptomatic submicroscopic and microscopic malaria infections and anemia: A study in southern Benin"],"prefix":"10.1371","volume":"20","author":[{"given":"Alejandro Rojas","family":"Chaves","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yannelle","family":"Dossou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Armel","family":"Dj\u00e8nontin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elis\u00e9e","family":"Adimi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Romuald","family":"Akoho","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Justine","family":"Bailly","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aziz","family":"Boura\u00efma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D\u00e9borah","family":"Matondo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yolande","family":"Sissinto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dismand","family":"Houinato","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Achille","family":"Massougbodji","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8439-9976","authenticated-orcid":true,"given":"C\u00e9lia","family":"Dechavanne","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7964-8963","authenticated-orcid":true,"given":"Gilles","family":"Cottrell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,1,24]]},"reference":[{"key":"pone.0317345.ref001","doi-asserted-by":"crossref","DOI":"10.30875\/6c551ba0-en","volume-title":"World malaria 2021 report","author":"World Health Organization","year":"2021"},{"issue":"12","key":"pone.0317345.ref002","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1080\/14787210.2019.1693259","article-title":"Asymptomatic malaria in the clinical and public health context","volume":"17","author":"J Cheaveau","year":"2019","journal-title":"Expert Rev Anti Infect Ther"},{"key":"pone.0317345.ref003","volume-title":"Global technical strategy for malaria 2016\u20132030, 2021 update","author":"World Health Organization","year":"2021"},{"issue":"9918","key":"pone.0317345.ref004","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1016\/S0140-6736(13)60024-0","article-title":"Malaria","volume":"383","author":"NJ White","year":"2014","journal-title":"The Lancet"},{"issue":"1","key":"pone.0317345.ref005","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1186\/s13071-021-04797-0","article-title":"Global trend of Plasmodium malariae and Plasmodium ovale spp. malaria infections in the last two decades (2000\u20132020): a systematic review and meta-analysis","volume":"14","author":"J Hawadak","year":"2021","journal-title":"Parasit Vectors"},{"key":"pone.0317345.ref006","unstructured":"Initiative USPsM. U.S. President\u2019s Malaria Initiative Benin Malaria Operational Plan FY 2022. 2022."},{"issue":"6","key":"pone.0317345.ref007","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1586\/eri.13.45","article-title":"The silent threat: asymptomatic parasitemia and malaria transmission","volume":"11","author":"KA Lindblade","year":"2013","journal-title":"Expert Rev Anti Infect Ther"},{"issue":"12","key":"pone.0317345.ref008","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1038\/nrmicro3364","article-title":"Asymptomatic malaria infections: detectability, transmissibility and public health relevance","volume":"12","author":"T Bousema","year":"2014","journal-title":"Nature reviews Microbiology"},{"issue":"10130","key":"pone.0317345.ref009","doi-asserted-by":"crossref","first-page":"1608","DOI":"10.1016\/S0140-6736(18)30324-6","article-title":"Malaria","volume":"391","author":"EA Ashley","year":"2018","journal-title":"The Lancet"},{"key":"pone.0317345.ref010","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1038\/ncomms2241","article-title":"Factors determining the occurrence of submicroscopic malaria infections and their relevance for control","volume":"3","author":"LC Okell","year":"2012","journal-title":"Nat Commun"},{"issue":"4","key":"pone.0317345.ref011","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.pt.2015.11.015","article-title":"Malaria Parasites in the Asymptomatic: Looking for the Hay in the Haystack","volume":"32","author":"B Galatas","year":"2016","journal-title":"Trends Parasitol"},{"issue":"1","key":"pone.0317345.ref012","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1186\/s12936-018-2509-9","article-title":"Anemia and malaria","volume":"17","author":"NJ White","year":"2018","journal-title":"Malar J"},{"issue":"1","key":"pone.0317345.ref013","doi-asserted-by":"crossref","first-page":"e1001942","DOI":"10.1371\/journal.pmed.1001942","article-title":"\"Asymptomatic\" Malaria: A Chronic and Debilitating Infection That Should Be Treated","volume":"13","author":"I Chen","year":"2016","journal-title":"PLoS Med"},{"key":"pone.0317345.ref014","doi-asserted-by":"crossref","first-page":"e10824","DOI":"10.15252\/msb.202110824","article-title":"\u201cMolecular profiling reveals features of clinical immunity and immunosuppression in asymptomatic P.falciparum malaria","volume":"18","author":"S Studniberg","year":"2022","journal-title":"Molecular Systems Biology"},{"key":"pone.0317345.ref015","doi-asserted-by":"crossref","DOI":"10.1016\/j.parint.2022.102648","article-title":"Detection of histidine-rich protein 2- and\/or 3- deleted Plasmodium falciparum using the automated hematology analyzer XN-31: A proof-of-concept study","volume":"91","author":"T Tougan","year":"2022","journal-title":"Parasitology International"},{"issue":"9","key":"pone.0317345.ref016","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1111\/tmi.13124","article-title":"Validity and reliability of methods to microscopically detect and quantify malaria parasitaemia","volume":"23","author":"J Mischlinger","year":"2018","journal-title":"Trop Med Int Health"},{"key":"pone.0317345.ref017","volume-title":"R: A Language and Environment for Statistical Computing","author":"R CorTeam","year":"2016"},{"key":"pone.0317345.ref018","unstructured":"Wickham H, Averick M, Bryan J, Chang W, McGowan L, Fran\u00e7ois R, et al. dplyr: A Grammar of Data Manipulation. R package version 1.0.7; 2021."},{"key":"pone.0317345.ref019","unstructured":"Chongsuvivatwong V. Epidemiological Data Display Package. R package version 3.5.0.1; 2018"},{"key":"pone.0317345.ref020","doi-asserted-by":"crossref","first-page":"36958","DOI":"10.1038\/srep36958","article-title":"High and Heterogeneous Prevalence of Asymptomatic and Sub-microscopic Malaria Infections on Islands in Lake Victoria, Kenya","volume":"6","author":"ZM Idris","year":"2016","journal-title":"Sci Rep"},{"issue":"1","key":"pone.0317345.ref021","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1186\/s12936-021-03952-3","article-title":"Prevalence of asymptomatic malaria, submicroscopic parasitaemia and anemia in Korogwe District, north-eastern Tanzania","volume":"20","author":"PM Hayuma","year":"2021","journal-title":"Malar J"},{"issue":"10","key":"pone.0317345.ref022","doi-asserted-by":"crossref","first-page":"e0165340","DOI":"10.1371\/journal.pone.0165340","article-title":"Submicroscopic and Asymptomatic Plasmodium Parasitaemia Associated with Significant Risk of Anemia in Papua, Indonesia","volume":"11","author":"Z Pava","year":"2016","journal-title":"PLoS One"},{"issue":"5","key":"pone.0317345.ref023","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1016\/j.jinf.2015.08.005","article-title":"Is asymptomatic malaria really asymptomatic? Hematological, vascular and inflammatory effects of asymptomatic malaria parasitemia","volume":"71","author":"Q de Mast","year":"2015","journal-title":"J Infect"},{"issue":"1","key":"pone.0317345.ref024","doi-asserted-by":"crossref","first-page":"293","DOI":"10.4269\/ajtmh.21-0316","article-title":"High Prevalence of Asymptomatic Malarial Anemia and Association with Early Conversion from Asymptomatic to Symptomatic Infection in a Plasmodium falciparum Hyperendemic Setting in Cameroon","volume":"106","author":"B Fogang","year":"2021","journal-title":"Am J Trop Med Hyg"},{"key":"pone.0317345.ref025","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1186\/s12936-016-1519-8","article-title":"Characterizing microscopic and submicroscopic malaria parasitaemia at three sites with varied transmission intensity in Uganda","volume":"15","author":"J Rek","year":"2016","journal-title":"Malar J"},{"key":"pone.0317345.ref026","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1186\/s12936-015-1009-4","article-title":"Prevalence of asymptomatic malaria infection and use of different malaria control measures among primary school children in Morogoro Municipality, Tanzania","volume":"14","author":"BJ Nzobo","year":"2015","journal-title":"Malar J"},{"key":"pone.0317345.ref027","doi-asserted-by":"crossref","first-page":"2398","DOI":"10.3389\/fimmu.2019.02398","article-title":"Understanding P. falciparum Asymptomatic Infections: A Proposition for a Transcriptomic Approach","volume":"10","author":"KM Kimenyi","year":"2019","journal-title":"Front Immunol"},{"issue":"9","key":"pone.0317345.ref028","article-title":"The Dynamics of Natural Plasmodium falciparum Infections","volume":"7","author":"RD Gosling","year":"2012","journal-title":"PLoS ONE"},{"issue":"1","key":"pone.0317345.ref029","doi-asserted-by":"crossref","DOI":"10.1186\/s12936-015-0595-5","article-title":"The relationship between Plasmodium infection, anemia and nutritional status in asymptomatic children aged under five years living in stable transmission zones in Kinshasa, Democratic Republic of Congo","volume":"14","author":"V Maketa","year":"2015","journal-title":"Malaria Journal"},{"key":"pone.0317345.ref030","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.59872","article-title":"Sex-based differences in clearance of chronic Plasmodium falciparum infection","volume":"9","author":"J Briggs","year":"2020","journal-title":"eLife"},{"issue":"1","key":"pone.0317345.ref031","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1186\/s12936-016-1548-3","article-title":"Asymptomatic malaria, growth status, and anemia among children in Lao People\u2019s Democratic Republic: a cross-sectional study","volume":"15","author":"T Akiyama","year":"2016","journal-title":"Malar J"},{"issue":"1","key":"pone.0317345.ref032","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1186\/s12936-021-03937-2","article-title":"Prevalence and associated risk factors of asymptomatic malaria and anemia among school-aged children in Dara Mallo and Uba Debretsehay districts: results from baseline cluster randomized trial","volume":"20","author":"Z Zerdo","year":"2021","journal-title":"Malar J"},{"issue":"8","key":"pone.0317345.ref033","doi-asserted-by":"crossref","first-page":"e0160917","DOI":"10.1371\/journal.pone.0160917","article-title":"Asymptomatic Vivax and Falciparum Parasitaemia with Helminth Co-Infection: Major Risk Factors for Anemia in Early Life","volume":"11","author":"FH Burdam","year":"2016","journal-title":"PLoS One"},{"issue":"9","key":"pone.0317345.ref034","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1016\/S2352-4642(22)00153-5","article-title":"Sickle cell anemia and severe Plasmodium falciparum malaria: a secondary analysis of the Transfusion and Treatment of African Children Trial (TRACT)","volume":"6","author":"S Uyoga","year":"2022","journal-title":"Lancet Child Adolesc Health"},{"key":"pone.0317345.ref035","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.puhe.2017.02.010","article-title":"Burden of asymptomatic malaria among a tribal population in a forested village of central India: a hidden challenge for malaria control in India","volume":"147","author":"MK Chourasia","year":"2017","journal-title":"Public Health"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0317345","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,24]],"date-time":"2025-01-24T19:05:05Z","timestamp":1737745505000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0317345"}},"subtitle":[],"editor":[{"given":"Jos\u00e9 Luiz Fernandes","family":"Vieira","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,1,24]]},"references-count":35,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1,24]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0317345","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,24]]}}}