{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,30]],"date-time":"2026-06-30T05:42:04Z","timestamp":1782798124108,"version":"3.54.5"},"reference-count":84,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,8,4]],"date-time":"2025-08-04T00:00:00Z","timestamp":1754265600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,8,4]],"date-time":"2025-08-04T00:00:00Z","timestamp":1754265600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"National Institute of Allergy and Infectious Diseases, National Institutes of Health, USA","award":["U19AI089672"],"award-info":[{"award-number":["U19AI089672"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Infect Dis Poverty"],"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>Understanding <jats:italic>Plasmodium<\/jats:italic> sexual differentiation is crucial for blocking transmission. This study identified risk factors for gametocyte carriage and gametocytemia in <jats:italic>P. vivax<\/jats:italic> and <jats:italic>P. falciparum<\/jats:italic> to inform malaria elimination strategies at the China-Myanmar border.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Methods<\/jats:title>\n            <jats:p>Gametocytes and asexual parasites were microscopically detected on thick smears collected from 2011 to 2020 in Laiza Township, Kachin State, Myanmar. Mono-\/polyclonality were detected by genotyping at <jats:italic>Pvmsp3\u03b1<\/jats:italic>\/<jats:italic>\u03b2<\/jats:italic> for <jats:italic>P. vivax<\/jats:italic>, and <jats:italic>Pfmsp1<\/jats:italic>\/<jats:italic>2<\/jats:italic> for <jats:italic>P. falciparum<\/jats:italic>. Kulldorff\u2019s retrospective time scan statistics tested for likely clusters of gametocyte-positive cases over time. Chi-square or Fisher\u2019s exact tests compared proportions of gametocyte-positive cases in categorical variables. Generalized linear models assessed risk factors (year, season, demographics, clinical\/parasitological features) for gametocyte carriage (logistic regression for a binomial outcome) and gametocytemia (Gaussian regression for continuous outcome), respectively.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>During 2011\u20132020, 8240 patients had <jats:italic>P. vivax<\/jats:italic> infections, with 7249 testing positive for gametocytes. Among 510 <jats:italic>P. falciparum<\/jats:italic> cases, 56 tested positive for gametocytes. A significant cluster of <jats:italic>P. vivax<\/jats:italic> gametocyte carriage occurred from May 2015 to August 2017 (<jats:italic>P<\/jats:italic>\u2009=\u20090.001). For <jats:italic>P. vivax<\/jats:italic>, dry season, previous malaria history, fever, and parasite density were associated with gametocyte carriage. Gametocyte density increased with asexual parasite density (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.001) but was lower during the rainy season and in those with a history of malaria infection (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.001). Over time, gametocytes carriage proportion increased while density decreased (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.001). For <jats:italic>P. falciparum<\/jats:italic>, younger age and previous malaria history were associated with gametocyte carriage, and density was higher in the dry season (<jats:italic>P<\/jats:italic>\u2009=\u20090.0115). Polyclonal <jats:italic>P. vivax<\/jats:italic> infections had higher gametocyte densities than monoclonal infections (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.0001) and <jats:italic>P. falciparum<\/jats:italic> gametocyte density tended to increase with multiplicity of infection.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusions<\/jats:title>\n            <jats:p>Younger age, prior malaria infection, travel, and polyclonal infections correlate with higher <jats:italic>P. vivax<\/jats:italic> gametocyte prevalence. Gametocyte carriage peakes during the dry season, highlighting the need for seasonal strategies to support malaria elimination. These findings enhance understanding of risk factors for the transmissible stage of the two main human <jats:italic>Plasmodium<\/jats:italic> species in the Greater Mekong Subregion border areas.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Graphical Abstract<\/jats:title>\n          <\/jats:sec>","DOI":"10.1186\/s40249-025-01352-2","type":"journal-article","created":{"date-parts":[[2025,8,4]],"date-time":"2025-08-04T05:00:23Z","timestamp":1754283623000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Risk factor for gametocyte carriage and gametocytemia in Plasmodium vivax and Plasmodium falciparum"],"prefix":"10.1186","volume":"14","author":[{"given":"Minxi","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Bian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shishao","family":"Ruan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zifang","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Di","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tongyu","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaming","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiao","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Duo","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia","family":"Lin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danni","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenyan","family":"Cui","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haichao","family":"Wei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuexing","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qinghui","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weilin","family":"Zeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhaoqing","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaming","family":"Cao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liwang","family":"Cui","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel M.","family":"Parker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-0472-6907","authenticated-orcid":false,"given":"Yan","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,8,4]]},"reference":[{"key":"1352_CR1","doi-asserted-by":"publisher","first-page":"844","DOI":"10.1309\/AJCP5XHDB1PNAEYT","volume":"131","author":"M Vitoria","year":"2009","unstructured":"Vitoria M, Granich R, Gilks CF, Gunneberg C, Hosseini M, Were W, et al. The global fight against HIV\/AIDS, tuberculosis, and malaria: current status and future perspectives. Am J Clin Pathol. 2009;131:844\u20138.","journal-title":"Am J Clin Pathol"},{"key":"1352_CR2","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1111\/cmi.12604","volume":"18","author":"S Bennink","year":"2016","unstructured":"Bennink S, Kiesow MJ, Pradel G. The development of malaria parasites in the mosquito midgut. Cell Microbiol. 2016;18:905\u201318.","journal-title":"Cell Microbiol"},{"key":"1352_CR3","unstructured":"WHO. World malaria report 2024. World Health Organization. https:\/\/www.who.int\/teams\/global-malaria-programme\/reports\/world-malaria-report-2024. Accessed 11 Dec 2024."},{"key":"1352_CR4","doi-asserted-by":"publisher","first-page":"388","DOI":"10.1186\/s12936-015-0921-y","volume":"14","author":"DM Parker","year":"2015","unstructured":"Parker DM, Carrara VI, Pukrittayakamee S, McGready R, Nosten FH. Malaria ecology along the Thailand-Myanmar border. Malar J. 2015;14:388.","journal-title":"Malar J"},{"key":"1352_CR5","doi-asserted-by":"publisher","DOI":"10.1016\/j.tmaid.2023.102575","volume":"53","author":"JH Yin","year":"2023","unstructured":"Yin JH, Zhang L, Yi BY, Zhou SS, Xia ZG. Imported malaria from land bordering countries in China: a challenge in preventing the reestablishment of malaria transmission. Travel Med Infect Dis. 2023;53: 102575.","journal-title":"Travel Med Infect Dis"},{"key":"1352_CR6","doi-asserted-by":"publisher","first-page":"558","DOI":"10.1038\/s41467-017-02646-2","volume":"9","author":"WJR Stone","year":"2018","unstructured":"Stone WJR, Campo JJ, Ouedraogo AL, Meerstein-Kessel L, Morlais I, Da D, et al. Unravelling the immune signature of Plasmodium falciparum transmission-reducing immunity. Nat Commun. 2018;9:558.","journal-title":"Nat Commun"},{"issue":"Suppl","key":"1352_CR7","doi-asserted-by":"publisher","first-page":"S95","DOI":"10.1017\/S0031182000084985","volume":"116","author":"KP Day","year":"1998","unstructured":"Day KP, Hayward RE, Dyer M. The biology of Plasmodium falciparum transmission stages. Parasitology. 1998;116(Suppl):S95-109.","journal-title":"Parasitology"},{"key":"1352_CR8","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1016\/S0035-9203(01)90016-1","volume":"95","author":"M Eichner","year":"2001","unstructured":"Eichner M, Diebner HH, Molineaux L, Collins WE, Jeffery GM, Dietz K. Genesis, sequestration and survival of Plasmodium falciparum gametocytes: parameter estimates from fitting a model to malariatherapy data. Trans R Soc Trop Med Hyg. 2001;95:497\u2013501.","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"1352_CR9","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1186\/1475-2875-3-24","volume":"3","author":"AM Talman","year":"2004","unstructured":"Talman AM, Domarle O, McKenzie FE, Ariey F, Robert V. Gametocytogenesis: the puberty of Plasmodium falciparum. Malar J. 2004;3:24.","journal-title":"Malar J"},{"key":"1352_CR10","doi-asserted-by":"publisher","first-page":"1837","DOI":"10.1038\/s41467-018-04221-9","volume":"9","author":"A Roth","year":"2018","unstructured":"Roth A, Maher SP, Conway AJ, Ubalee R, Chaumeau V, Andolina C, et al. A comprehensive model for assessment of liver stage therapies targeting Plasmodium vivax and Plasmodium falciparum. Nat Commun. 2018;9:1837.","journal-title":"Nat Commun"},{"key":"1352_CR11","doi-asserted-by":"publisher","first-page":"512","DOI":"10.1186\/s13071-017-2407-y","volume":"10","author":"W Nguitragool","year":"2017","unstructured":"Nguitragool W, Mueller I, Kumpitak C, Saeseu T, Bantuchai S, Yorsaeng R, et al. Very high carriage of gametocytes in asymptomatic low-density Plasmodium falciparum and P. vivax infections in western Thailand. Parasit Vectors. 2017;10:512.","journal-title":"Parasit Vectors"},{"key":"1352_CR12","doi-asserted-by":"publisher","first-page":"154","DOI":"10.4269\/ajtmh.21-1217","volume":"107","author":"M Moreno","year":"2022","unstructured":"Moreno M, Torres K, Tong C, Garcia Castillo SS, Carrasco-Escobar G, Guedez G, et al. Insights into Plasmodium vivax asymptomatic malaria infections and direct skin-feeding assays to assess onward malaria transmission in the Amazon. Am J Trop Med Hyg. 2022;107:154\u201361.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR13","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2021.790067","volume":"11","author":"M Usui","year":"2021","unstructured":"Usui M, Williamson KC. Stressed out about Plasmodium falciparum gametocytogenesis. Front Cell Infect Microbiol. 2021;11: 790067.","journal-title":"Front Cell Infect Microbiol"},{"key":"1352_CR14","doi-asserted-by":"publisher","first-page":"2140","DOI":"10.1038\/s41467-019-10172-6","volume":"10","author":"M Usui","year":"2019","unstructured":"Usui M, Prajapati SK, Ayanful-Torgby R, Acquah FK, Cudjoe E, Kakaney C, et al. Plasmodium falciparum sexual differentiation in malaria patients is associated with host factors and GDV1-dependent genes. Nat Commun. 2019;10:2140.","journal-title":"Nat Commun"},{"key":"1352_CR15","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1128\/microbiolspec.AME-0010-2019","volume":"7","author":"AA Escalante","year":"2019","unstructured":"Escalante AA, Pacheco MA. Malaria molecular epidemiology: an evolutionary genetics perspective. Microbiol Spectr. 2019;7:10.","journal-title":"Microbiol Spectr."},{"key":"1352_CR16","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-018-36493-y","volume":"9","author":"P Sondo","year":"2019","unstructured":"Sondo P, Derra K, Lefevre T, Diallo-Nakanabo S, Tarnagda Z, Zampa O, et al. Genetically diverse Plasmodium falciparum infections, within-host competition and symptomatic malaria in humans. Sci Rep. 2019;9: 127.","journal-title":"Sci Rep"},{"key":"1352_CR17","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1186\/s13071-020-04302-z","volume":"13","author":"P Sondo","year":"2020","unstructured":"Sondo P, Derra K, Rouamba T, Nakanabo Diallo S, Taconet P, Kazienga A, et al. Determinants of Plasmodium falciparum multiplicity of infection and genetic diversity in Burkina Faso. Parasit Vectors. 2020;13:427.","journal-title":"Parasit Vectors"},{"key":"1352_CR18","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/j.ijpara.2007.07.003","volume":"38","author":"D Nwakanma","year":"2008","unstructured":"Nwakanma D, Kheir A, Sowa M, Dunyo S, Jawara M, Pinder M, et al. High gametocyte complexity and mosquito infectivity of Plasmodium falciparum in the Gambia. Int J Parasitol. 2008;38:219\u201327.","journal-title":"Int J Parasitol"},{"key":"1352_CR19","doi-asserted-by":"publisher","DOI":"10.1186\/s12936-018-2479-y","volume":"17","author":"H Lamptey","year":"2018","unstructured":"Lamptey H, Ofori MF, Kusi KA, Adu B, Owusu-Yeboa E, Kyei-Baafour E, et al. The prevalence of submicroscopic Plasmodium falciparum gametocyte carriage and multiplicity of infection in children, pregnant women and adults in a low malaria transmission area in Southern Ghana. Malar J. 2018;17: 331.","journal-title":"Malar J"},{"key":"1352_CR20","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.32625","author":"WM Guelbeogo","year":"2018","unstructured":"Guelbeogo WM, Goncalves BP, Grignard L, Bradley J, Serme SS, Hellewell J, et al. Variation in natural exposure to anopheles mosquitoes and its effects on malaria transmission. Elife. 2018. https:\/\/doi.org\/10.7554\/eLife.32625.","journal-title":"Elife"},{"key":"1352_CR21","doi-asserted-by":"publisher","first-page":"722","DOI":"10.4269\/ajtmh.2001.65.722","volume":"65","author":"E Michael","year":"2001","unstructured":"Michael E, Ramaiah KD, Hoti SL, Barker G, Paul MR, Yuvaraj J, et al. Quantifying mosquito biting patterns on humans by DNA fingerprinting of bloodmeals. Am J Trop Med Hyg. 2001;65:722\u20138.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR22","doi-asserted-by":"publisher","first-page":"1133","DOI":"10.1038\/s41467-017-01270-4","volume":"8","author":"BP Goncalves","year":"2017","unstructured":"Goncalves BP, Kapulu MC, Sawa P, Guelbeogo WM, Tiono AB, Grignard L, et al. Examining the human infectious reservoir for Plasmodium falciparum malaria in areas of differing transmission intensity. Nat Commun. 2017;8:1133.","journal-title":"Nat Commun"},{"key":"1352_CR23","doi-asserted-by":"publisher","first-page":"1499","DOI":"10.1093\/infdis\/jiy686","volume":"219","author":"V Chaumeau","year":"2019","unstructured":"Chaumeau V, Kajeechiwa L, Fustec B, Landier J, Naw Nyo S, Nay Hsel S, et al. Contribution of asymptomatic Plasmodium infections to the transmission of malaria in Kayin State, Myanmar. J Infect Dis. 2019;219:1499\u2013509.","journal-title":"J Infect Dis"},{"key":"1352_CR24","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1186\/s12936-019-2924-6","volume":"18","author":"J Geng","year":"2019","unstructured":"Geng J, Malla P, Zhang J, Xu S, Li C, Zhao Y, et al. Increasing trends of malaria in a border area of the Greater Mekong Subregion. Malar J. 2019;18:309.","journal-title":"Malar J"},{"key":"1352_CR25","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1186\/1475-2875-13-145","volume":"13","author":"M Laman","year":"2014","unstructured":"Laman M, Moore BR, Benjamin J, Padapu N, Tarongka N, Siba P, et al. Comparison of an assumed versus measured leucocyte count in parasite density calculations in Papua New Guinean children with uncomplicated malaria. Malar J. 2014;13:145.","journal-title":"Malar J"},{"key":"1352_CR26","doi-asserted-by":"publisher","first-page":"613","DOI":"10.4269\/ajtmh.2003.68.613","volume":"68","author":"L Cui","year":"2003","unstructured":"Cui L, Mascorro CN, Fan Q, Rzomp KA, Khuntirat B, Zhou G, et al. Genetic diversity and multiple infections of Plasmodium vivax malaria in Western Thailand. Am J Trop Med Hyg. 2003;68:613\u20139.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR27","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0063447","volume":"8","author":"Y Liu","year":"2013","unstructured":"Liu Y, Wang X, Liu Y, Sun D, Ding S, Zhang B, et al. Detecting spatial-temporal clusters of HFMD from 2007 to 2011 in Shandong Province, China. PLoS ONE. 2013;8: e63447.","journal-title":"PLoS ONE"},{"key":"1352_CR28","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1186\/s40249-016-0175-0","volume":"5","author":"J Zhang","year":"2016","unstructured":"Zhang J, Dong JQ, Li JY, Zhang Y, Tian YH, Sun XY, et al. Effectiveness and impact of the cross-border healthcare model as implemented by non-governmental organizations: case study of the malaria control programs by Health poverty action on the China-Myanmar border. Infect Dis Poverty. 2016;5:80.","journal-title":"Infect Dis Poverty"},{"key":"1352_CR29","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/S1473-3099(20)30700-3","volume":"21","author":"DJ Weiss","year":"2021","unstructured":"Weiss DJ, Bertozzi-Villa A, Rumisha SF, Amratia P, Arambepola R, Battle KE, et al. Indirect effects of the COVID-19 pandemic on malaria intervention coverage, morbidity, and mortality in Africa: a geospatial modelling analysis. Lancet Infect Dis. 2021;21:59\u201369.","journal-title":"Lancet Infect Dis"},{"key":"1352_CR30","unstructured":"WHO. More malaria cases and deaths in 2020 linked to COVID-19 disruptions. World Health Organization. 2021. https:\/\/www.who.int\/news\/item\/06-12-2021-more-malaria-cases-and-deaths-in-2020-linked-to-covid-19-disruptions. Accessed 6 Dec 2021."},{"key":"1352_CR31","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1186\/s12916-016-0621-7","volume":"14","author":"Group WGS","year":"2016","unstructured":"Group WGS. Gametocyte carriage in uncomplicated Plasmodium falciparum malaria following treatment with artemisinin combination therapy: a systematic review and meta-analysis of individual patient data. BMC Med. 2016;14:79.","journal-title":"BMC Med"},{"key":"1352_CR32","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1186\/s12936-016-1587-9","volume":"15","author":"JE Coalson","year":"2016","unstructured":"Coalson JE, Walldorf JA, Cohee LM, Ismail MD, Mathanga D, Cordy RJ, et al. High prevalence of Plasmodium falciparum gametocyte infections in school-age children using molecular detection: patterns and predictors of risk from a cross-sectional study in southern Malawi. Malar J. 2016;15:527.","journal-title":"Malar J"},{"key":"1352_CR33","doi-asserted-by":"publisher","first-page":"1281","DOI":"10.1645\/GE-911R.1","volume":"92","author":"FE McKenzie","year":"2006","unstructured":"McKenzie FE, Wongsrichanalai C, Magill AJ, Forney JR, Permpanich B, Lucas C, et al. Gametocytemia in Plasmodium vivax and Plasmodium falciparum infections. J Parasitol. 2006;92:1281\u20135.","journal-title":"J Parasitol"},{"key":"1352_CR34","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.00625-18","author":"N Obaldia 3rd","year":"2018","unstructured":"Obaldia N 3rd, Meibalan E, Sa JM, Ma S, Clark MA, Mejia P, et al. Bone marrow is a major parasite reservoir in Plasmodium vivax infection. MBio. 2018. https:\/\/doi.org\/10.1128\/mBio.00625-18.","journal-title":"MBio"},{"key":"1352_CR35","doi-asserted-by":"publisher","DOI":"10.1016\/j.parepi.2023.e00295","volume":"21","author":"A Alemayehu","year":"2023","unstructured":"Alemayehu A. Biology and epidemiology of Plasmodium falciparum and Plasmodium vivax gametocyte carriage: implication for malaria control and elimination. Parasite Epidemiol Control. 2023;21: e00295.","journal-title":"Parasite Epidemiol Control"},{"key":"1352_CR36","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1128\/CMR.00051-10","volume":"24","author":"T Bousema","year":"2011","unstructured":"Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377\u2013410.","journal-title":"Clin Microbiol Rev"},{"key":"1352_CR37","doi-asserted-by":"publisher","first-page":"424","DOI":"10.1016\/j.pt.2006.07.001","volume":"22","author":"C Drakeley","year":"2006","unstructured":"Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006;22:424\u201330.","journal-title":"Trends Parasitol"},{"key":"1352_CR38","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a025452","author":"E Meibalan","year":"2017","unstructured":"Meibalan E, Marti M. Biology of malaria transmission. Cold Spring Harb Perspect Med. 2017. https:\/\/doi.org\/10.1101\/cshperspect.a025452.","journal-title":"Cold Spring Harb Perspect Med"},{"key":"1352_CR39","doi-asserted-by":"publisher","first-page":"328","DOI":"10.1038\/ng.554","volume":"42","author":"LC Gouagna","year":"2010","unstructured":"Gouagna LC, Bancone G, Yao F, Yameogo B, Dabire KR, Costantini C, et al. Genetic variation in human HBB is associated with Plasmodium falciparum transmission. Nat Genet. 2010;42:328\u201331.","journal-title":"Nat Genet"},{"key":"1352_CR40","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1016\/j.meegid.2016.08.025","volume":"45","author":"MM Sandeu","year":"2016","unstructured":"Sandeu MM, Abate L, Tchioffo MT, Bayibeki AN, Awono-Ambene PH, Nsango SE, et al. Impact of exposure to mosquito transmission-blocking antibodies on Plasmodium falciparum population genetic structure. Infect Genet Evol. 2016;45:138\u201344.","journal-title":"Infect Genet Evol"},{"key":"1352_CR41","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.molbiopara.2004.03.018","volume":"137","author":"P Schneider","year":"2004","unstructured":"Schneider P, Schoone G, Schallig H, Verhage D, Telgt D, Eling W, et al. Quantification of Plasmodium falciparum gametocytes in differential stages of development by quantitative nucleic acid sequence-based amplification. Mol Biochem Parasitol. 2004;137:35\u201341.","journal-title":"Mol Biochem Parasitol"},{"key":"1352_CR42","doi-asserted-by":"publisher","first-page":"378","DOI":"10.1016\/j.pt.2018.02.009","volume":"34","author":"C Koepfli","year":"2018","unstructured":"Koepfli C, Yan G. Plasmodium gametocytes in field studies: do we measure commitment to transmission or detectability? Trends Parasitol. 2018;34:378\u201387.","journal-title":"Trends Parasitol"},{"key":"1352_CR43","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1186\/s12936-017-2123-2","volume":"16","author":"Y Adomako-Ankomah","year":"2017","unstructured":"Adomako-Ankomah Y, Chenoweth MS, Tocker AM, Doumbia S, Konate D, Doumbouya M, et al. Host age and Plasmodium falciparum multiclonality are associated with gametocyte prevalence: a 1-year prospective cohort study. Malar J. 2017;16:473.","journal-title":"Malar J"},{"key":"1352_CR44","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1016\/j.trstmh.2003.10.005","volume":"98","author":"M Nacher","year":"2004","unstructured":"Nacher M, Carrara VI, Ashley E, McGready R, Hutagalung R, Nguen JV, et al. Seasonal variation in hyperparasitaemia and gametocyte carriage in patients with Plasmodium falciparum malaria on the Thai-Burmese border. Trans R Soc Trop Med Hyg. 2004;98:322\u20138.","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"1352_CR45","doi-asserted-by":"publisher","DOI":"10.1186\/s12936-023-04728-7","volume":"22","author":"P Looareesuwan","year":"2023","unstructured":"Looareesuwan P, Krudsood S, Lawpoolsri S, Tangpukdee N, Matsee W, Nguitragool W, et al. Gametocyte prevalence and risk factors of P. falciparum malaria patients admitted at the Hospital for Tropical Diseases, Thailand: a 20-year retrospective study. Malar J. 2023;22: 321.","journal-title":"Malar J"},{"key":"1352_CR46","doi-asserted-by":"publisher","first-page":"6804","DOI":"10.1038\/s41598-018-24893-z","volume":"8","author":"RW Hagan","year":"2018","unstructured":"Hagan RW, Didion EM, Rosselot AE, Holmes CJ, Siler SC, Rosendale AJ, et al. Dehydration prompts increased activity and blood feeding by mosquitoes. Sci Rep. 2018;8:6804.","journal-title":"Sci Rep"},{"key":"1352_CR47","doi-asserted-by":"publisher","DOI":"10.1016\/j.isci.2025.111760","volume":"28","author":"CJ Holmes","year":"2025","unstructured":"Holmes CJ, Chakraborty S, Ajayi OM, Uhran MR, Frigard R, Stacey CL, et al. Multiple blood feeding bouts in mosquitoes allow for prolonged survival and are predicted to increase viral transmission during dry periods. iScience. 2025;28: 111760.","journal-title":"iScience"},{"key":"1352_CR48","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1186\/s40249-023-01055-6","volume":"12","author":"Y Zhao","year":"2023","unstructured":"Zhao Y, Aung PL, Ruan S, Win KM, Wu Z, Soe TN, et al. Spatio-temporal trends of malaria incidence from 2011 to 2017 and environmental predictors of malaria transmission in Myanmar. Infect Dis Poverty. 2023;12:2.","journal-title":"Infect Dis Poverty"},{"key":"1352_CR49","doi-asserted-by":"publisher","DOI":"10.12688\/wellcomeopenres.16299.1","volume":"5","author":"AO Touray","year":"2020","unstructured":"Touray AO, Mobegi VA, Wamunyokoli F, Butungi H, Herren JK. Prevalence of asymptomatic P. falciparum gametocyte carriage among school children in Mbita, Western Kenya and assessment of the association between gametocyte density, multiplicity of infection and mosquito infection prevalence. Wellcome Open Res. 2020;5: 259.","journal-title":"Wellcome Open Res"},{"key":"1352_CR50","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1186\/s12936-025-05270-4","volume":"24","author":"C Mulamba","year":"2025","unstructured":"Mulamba C, Odufuwa OG, Kweyamba PA, Lazaro LO, Chabo MS, Kamage JJ, et al. Plasmodium falciparum gametocyte burden in a Tanzanian heterogeneous transmission setting. Malar J. 2025;24:54.","journal-title":"Malar J"},{"key":"1352_CR51","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1016\/j.pt.2008.01.004","volume":"24","author":"MW Dixon","year":"2008","unstructured":"Dixon MW, Thompson J, Gardiner DL, Trenholme KR. Sex in Plasmodium: a sign of commitment. Trends Parasitol. 2008;24:168\u201375.","journal-title":"Trends Parasitol"},{"key":"1352_CR52","doi-asserted-by":"publisher","first-page":"66","DOI":"10.12688\/wellcomeopenres.15186.1","volume":"4","author":"MK Muthui","year":"2019","unstructured":"Muthui MK, Mogeni P, Mwai K, Nyundo C, Macharia A, Williams TN, et al. Gametocyte carriage in an era of changing malaria epidemiology: a 19-year analysis of a malaria longitudinal cohort. Wellc Open Res. 2019;4:66.","journal-title":"Wellc Open Res"},{"key":"1352_CR53","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a025585","author":"JH Adams","year":"2017","unstructured":"Adams JH, Mueller I. The biology of Plasmodium vivax. Cold Spring Harb Perspect Med. 2017. https:\/\/doi.org\/10.1101\/cshperspect.a025585.","journal-title":"Cold Spring Harb Perspect Med"},{"key":"1352_CR54","doi-asserted-by":"publisher","DOI":"10.1101\/2021.11.05.467456v4","author":"DM van Hannah","year":"2024","unstructured":"van Hannah DM, Nathalia FL, Michael G, Usama D, Safiatou D, Hamidou C, et al. Number and proportion of P. falciparum gametocytes vary from acute infection to chronic parasite carriage despite unaltered sexual commitment rate. Biorxiv. 2024. https:\/\/doi.org\/10.1101\/2021.11.05.467456v4.","journal-title":"Biorxiv"},{"key":"1352_CR55","doi-asserted-by":"publisher","first-page":"1019","DOI":"10.4269\/ajtmh.1999.60.1019","volume":"60","author":"R Price","year":"1999","unstructured":"Price R, Nosten F, Simpson JA, Luxemburger C, Phaipun L, ter Kuile F, et al. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am J Trop Med Hyg. 1999;60:1019\u201323.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR56","doi-asserted-by":"publisher","first-page":"183","DOI":"10.4269\/ajtmh.1991.44.183","volume":"44","author":"JK Baird","year":"1991","unstructured":"Baird JK, Jones TR, Masbar S, Ratiwayanto S, Leksana B. Evidence for specific suppression of gametocytemia by Plasmodium falciparum in residents of hyperendemic Irian Jaya. Am J Trop Med Hyg. 1991;44:183\u201390.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR57","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0002280","volume":"3","author":"M Saeed","year":"2008","unstructured":"Saeed M, Roeffen W, Alexander N, Drakeley CJ, Targett GA, Sutherland CJ. Plasmodium falciparum antigens on the surface of the gametocyte-infected erythrocyte. PLoS ONE. 2008;3: e2280.","journal-title":"PLoS ONE"},{"key":"1352_CR58","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1111\/imr.12828","volume":"293","author":"RM de Jong","year":"2020","unstructured":"de Jong RM, Tebeje SK, Meerstein-Kessel L, Tadesse FG, Jore MM, Stone W, et al. Immunity against sexual stage Plasmodium falciparum and Plasmodium vivax parasites. Immunol Rev. 2020;293:190\u2013215.","journal-title":"Immunol Rev"},{"key":"1352_CR59","doi-asserted-by":"publisher","first-page":"627","DOI":"10.1645\/GE-1052R.1","volume":"93","author":"FE McKenzie","year":"2007","unstructured":"McKenzie FE, Jeffery GM, Collins WE. Gametocytemia and fever in human malaria infections. J Parasitol. 2007;93:627\u201333.","journal-title":"J Parasitol"},{"key":"1352_CR60","doi-asserted-by":"publisher","first-page":"523","DOI":"10.4269\/ajtmh.2001.65.523","volume":"65","author":"L von Seidlein","year":"2001","unstructured":"von Seidlein L, Drakeley C, Greenwood B, Walraven G, Targett G. Risk factors for gametocyte carriage in Gambian children. Am J Trop Med Hyg. 2001;65:523\u20137.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR61","doi-asserted-by":"publisher","first-page":"74","DOI":"10.4269\/ajtmh.19-0660","volume":"103","author":"TR Porter","year":"2020","unstructured":"Porter TR, Finn TP, Silumbe K, Chalwe V, Hamainza B, Kooma E, et al. Recent travel history and Plasmodium falciparum malaria infection in a region of heterogenous transmission in Southern Province, Zambia. Am J Trop Med Hyg. 2020;103:74\u201381.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR62","doi-asserted-by":"publisher","DOI":"10.5772\/intechopen.99364","author":"D Kepple","year":"2021","unstructured":"Kepple D, Ford A, Little E, Kolesar G, Abagero BR, Blackwell AN, et al. From genes to biomarkers: understanding the biology of malaria gametocytes and their detection. Genetic Polymorph New Insights. 2021. https:\/\/doi.org\/10.5772\/intechopen.99364.","journal-title":"Genetic Polymorph New Insights"},{"key":"1352_CR63","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0123102","volume":"10","author":"L Grange","year":"2015","unstructured":"Grange L, Loucoubar C, Telle O, Tall A, Faye J, Sokhna C, et al. Risk factors for Plasmodium falciparum gametocyte positivity in a longitudinal cohort. PLoS ONE. 2015;10: e0123102.","journal-title":"PLoS ONE"},{"key":"1352_CR64","doi-asserted-by":"publisher","first-page":"626","DOI":"10.4269\/ajtmh.2007.76.626","volume":"76","author":"AL Ouedraogo","year":"2007","unstructured":"Ouedraogo AL, Schneider P, de Kruijf M, Nebie I, Verhave JP, Cuzin-Ouattara N, et al. Age-dependent distribution of Plasmodium falciparum gametocytes quantified by Pfs25 real-time QT-NASBA in a cross-sectional study in Burkina Faso. Am J Trop Med Hyg. 2007;76:626\u201330.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR65","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0126747","volume":"10","author":"C Koepfli","year":"2015","unstructured":"Koepfli C, Robinson LJ, Rarau P, Salib M, Sambale N, Wampfler R, et al. Blood-stage parasitaemia and age determine Plasmodium falciparum and P. vivax gametocytaemia in Papua New Guinea. PLoS ONE. 2015;10: e0126747.","journal-title":"PLoS ONE"},{"key":"1352_CR66","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1186\/s13071-018-2787-7","volume":"11","author":"ACG Almeida","year":"2018","unstructured":"Almeida ACG, Kuehn A, Castro AJM, Vitor-Silva S, Figueiredo EFG, Brasil LW, et al. High proportions of asymptomatic and submicroscopic Plasmodium vivax infections in a peri-urban area of low transmission in the Brazilian Amazon. Parasit Vectors. 2018;11:194.","journal-title":"Parasit Vectors"},{"key":"1352_CR67","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1093\/infdis\/jit261","volume":"208","author":"NM Douglas","year":"2013","unstructured":"Douglas NM, Simpson JA, Phyo AP, Siswantoro H, Hasugian AR, Kenangalem E, et al. Gametocyte dynamics and the role of drugs in reducing the transmission potential of Plasmodium vivax. J Infect Dis. 2013;208:801\u201312.","journal-title":"J Infect Dis"},{"issue":"Pt 2","key":"1352_CR68","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1017\/S0031182097001145","volume":"115","author":"LH Taylor","year":"1997","unstructured":"Taylor LH, Walliker D, Read AF. Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology. 1997;115(Pt 2):121\u201332.","journal-title":"Parasitology"},{"key":"1352_CR69","doi-asserted-by":"publisher","first-page":"1188","DOI":"10.1093\/infdis\/jiu236","volume":"210","author":"R Wampfler","year":"2014","unstructured":"Wampfler R, Timinao L, Beck HP, Soulama I, Tiono AB, Siba P, et al. Novel genotyping tools for investigating transmission dynamics of Plasmodium falciparum. J Infect Dis. 2014;210:1188\u201397.","journal-title":"J Infect Dis"},{"key":"1352_CR70","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1016\/j.ijpara.2004.10.014","volume":"35","author":"E Nassir","year":"2005","unstructured":"Nassir E, Abdel-Muhsin AM, Suliaman S, Kenyon F, Kheir A, Geha H, et al. Impact of genetic complexity on longevity and gametocytogenesis of Plasmodium falciparum during the dry and transmission-free season of eastern Sudan. Int J Parasitol. 2005;35:49\u201355.","journal-title":"Int J Parasitol"},{"key":"1352_CR71","doi-asserted-by":"publisher","first-page":"592","DOI":"10.1186\/s12936-016-1640-8","volume":"15","author":"R Ayanful-Torgby","year":"2016","unstructured":"Ayanful-Torgby R, Oppong A, Abankwa J, Acquah F, Williamson KC, Amoah LE. Plasmodium falciparum genotype and gametocyte prevalence in children with uncomplicated malaria in coastal Ghana. Malar J. 2016;15:592.","journal-title":"Malar J"},{"key":"1352_CR72","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/s13071-017-2607-5","volume":"11","author":"LE Amoah","year":"2018","unstructured":"Amoah LE, Acquah FK, Ayanful-Torgby R, Oppong A, Abankwa J, Obboh EK, et al. Dynamics of anti-MSP3 and Pfs230 antibody responses and multiplicity of infection in asymptomatic children from southern Ghana. Parasit Vectors. 2018;11:13.","journal-title":"Parasit Vectors"},{"key":"1352_CR73","doi-asserted-by":"publisher","first-page":"366","DOI":"10.4269\/ajtmh.2009.81.366","volume":"81","author":"M Beurskens","year":"2009","unstructured":"Beurskens M, Mens P, Schallig H, Syafruddin D, Asih PB, Hermsen R, et al. Quantitative determination of Plasmodium vivax gametocytes by real-time quantitative nucleic acid sequence-based amplification in clinical samples. Am J Trop Med Hyg. 2009;81:366\u20139.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR74","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1186\/1475-2875-11-190","volume":"11","author":"N Kuamsab","year":"2012","unstructured":"Kuamsab N, Putaporntip C, Pattanawong U, Jongwutiwes S. Simultaneous detection of Plasmodium vivax and Plasmodium falciparum gametocytes in clinical isolates by multiplex-nested RT-PCR. Malar J. 2012;11:190.","journal-title":"Malar J"},{"key":"1352_CR75","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/j.ijpara.2016.10.006","volume":"47","author":"K Kiattibutr","year":"2017","unstructured":"Kiattibutr K, Roobsoong W, Sriwichai P, Saeseu T, Rachaphaew N, Suansomjit C, et al. Infectivity of symptomatic and asymptomatic Plasmodium vivax infections to a Southeast Asian vector, Anopheles dirus. Int J Parasitol. 2017;47:163\u201370.","journal-title":"Int J Parasitol"},{"key":"1352_CR76","doi-asserted-by":"publisher","first-page":"864","DOI":"10.1186\/s12864-017-4260-y","volume":"18","author":"A Lerch","year":"2017","unstructured":"Lerch A, Koepfli C, Hofmann NE, Messerli C, Wilcox S, Kattenberg JH, et al. Development of amplicon deep sequencing markers and data analysis pipeline for genotyping multi-clonal malaria infections. BMC Genomics. 2017;18:864.","journal-title":"BMC Genomics"},{"key":"1352_CR77","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2021.725859","volume":"11","author":"X He","year":"2021","unstructured":"He X, Zhong D, Zou C, Pi L, Zhao L, Qin Y, et al. Unraveling the complexity of imported malaria infections by amplicon deep sequencing. Front Cell Infect Microbiol. 2021;11: 725859.","journal-title":"Front Cell Infect Microbiol"},{"key":"1352_CR78","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0004526","volume":"10","author":"LR Friedrich","year":"2016","unstructured":"Friedrich LR, Popovici J, Kim S, Dysoley L, Zimmerman PA, Menard D, et al. Complexity of infection and genetic diversity in Cambodian Plasmodium vivax. PLoS Negl Trop Dis. 2016;10: e0004526.","journal-title":"PLoS Negl Trop Dis"},{"key":"1352_CR79","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1186\/1475-2875-14-4","volume":"14","author":"K Galinsky","year":"2015","unstructured":"Galinsky K, Valim C, Salmier A, de Thoisy B, Musset L, Legrand E, et al. COIL: a methodology for evaluating malarial complexity of infection using likelihood from single nucleotide polymorphism data. Malar J. 2015;14:4.","journal-title":"Malar J"},{"key":"1352_CR80","doi-asserted-by":"publisher","first-page":"1605","DOI":"10.1086\/587645","volume":"197","author":"KI Barnes","year":"2008","unstructured":"Barnes KI, Little F, Mabuza A, Mngomezulu N, Govere J, Durrheim D, et al. Increased gametocytemia after treatment: an early parasitological indicator of emerging sulfadoxine-pyrimethamine resistance in falciparum malaria. J Infect Dis. 2008;197:1605\u201313.","journal-title":"J Infect Dis"},{"key":"1352_CR81","doi-asserted-by":"publisher","first-page":"442","DOI":"10.4269\/ajtmh.2008.78.442","volume":"78","author":"JT Bousema","year":"2008","unstructured":"Bousema JT, Drakeley CJ, Mens PF, Arens T, Houben R, Omar SA, et al. Increased Plasmodium falciparum gametocyte production in mixed infections with P. malariae. Am J Trop Med Hyg. 2008;78:442\u20138.","journal-title":"Am J Trop Med Hyg"},{"key":"1352_CR82","first-page":"1000278","volume":"9","author":"Y Sunbin","year":"2024","unstructured":"Sunbin Y. Understanding the impact of multi-species plasmodium infections on malaria transmission. J Infect Dis Diagn. 2024;9:1000278.","journal-title":"J Infect Dis Diagn."},{"key":"1352_CR83","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pmed.1001942","volume":"13","author":"I Chen","year":"2016","unstructured":"Chen I, Clarke SE, Gosling R, Hamainza B, Killeen G, Magill A, et al. \u201cAsymptomatic\u201d malaria: a chronic and debilitating infection that should be treated. PLoS Med. 2016;13: e1001942.","journal-title":"PLoS Med"},{"key":"1352_CR84","doi-asserted-by":"publisher","first-page":"1883","DOI":"10.1093\/cid\/cix1123","volume":"66","author":"FG Tadesse","year":"2018","unstructured":"Tadesse FG, Slater HC, Chali W, Teelen K, Lanke K, Belachew M, et al. The relative contribution of symptomatic and asymptomatic Plasmodium vivax and Plasmodium falciparum infections to the infectious reservoir in a low-endemic setting in Ethiopia. Clin Infect Dis. 2018;66:1883\u201391.","journal-title":"Clin Infect Dis"}],"container-title":["Infectious Diseases of Poverty"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40249-025-01352-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s40249-025-01352-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40249-025-01352-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,9,8]],"date-time":"2025-09-08T13:24:20Z","timestamp":1757337860000},"score":1,"resource":{"primary":{"URL":"https:\/\/idpjournal.biomedcentral.com\/articles\/10.1186\/s40249-025-01352-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,8,4]]},"references-count":84,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["1352"],"URL":"https:\/\/doi.org\/10.1186\/s40249-025-01352-2","relation":{},"ISSN":["2049-9957"],"issn-type":[{"value":"2049-9957","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,8,4]]},"assertion":[{"value":"11 April 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 July 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 August 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 August 2025","order":4,"name":"change_date","label":"Change Date","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Update","order":5,"name":"change_type","label":"Change Type","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The equal contributions statement was missing and has been added back to the article.","order":6,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Ethical approval for this project was obtained from the institutional review boards of China Medical University, China and University of South Florida, USA. Before conducting the study, all adult participants or legal guardians of children voluntarily signed the informed consent. All methods were carried out in accordance with relevant guidelines and regulations.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no conflict of interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"79"}}