{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T21:23:20Z","timestamp":1792790600557,"version":"4.5.0"},"update-to":[{"DOI":"10.1371\/journal.pntd.0009506","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,7,2]],"date-time":"2021-07-02T00:00:00Z","timestamp":1625184000000}}],"reference-count":47,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2021,6,17]],"date-time":"2021-06-17T00:00:00Z","timestamp":1623888000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Erasmus Universiteit Rotterdam","award":["EWIDAC Project from Travelling Doctors van Saint Lazare"],"award-info":[{"award-number":["EWIDAC Project from Travelling Doctors van Saint Lazare"]}]},{"DOI":"10.13039\/501100006378","name":"Universitas Indonesia","doi-asserted-by":"publisher","award":["1908\/UN2.R3.1\/HKP.05.00\/2019"],"award-info":[{"award-number":["1908\/UN2.R3.1\/HKP.05.00\/2019"]}],"id":[{"id":"10.13039\/501100006378","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006378","name":"Universitas Indonesia","doi-asserted-by":"crossref","award":["Hibah DAMAS PPI Q1 no.NKB-562\/UN2.RST\/HKP.05.00\/2021"],"award-info":[{"award-number":["Hibah DAMAS PPI Q1 no.NKB-562\/UN2.RST\/HKP.05.00\/2021"]}],"id":[{"id":"10.13039\/501100006378","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosntds.org"],"crossmark-restriction":false},"short-container-title":["PLoS Negl Trop Dis"],"abstract":"<jats:sec id=\"sec001\"><jats:title>Background<\/jats:title><jats:p>Soil-transmitted helminth (STH) infections are still prevalent in Indonesia, with roughly one-third of infected population being preschool-age children (PSC), which are generally at higher risk of morbidity such as malnutrition and anemia. This study aimed to investigate the association of STH infections with nutritional status and anemia among PSC in Nangapanda subdistrict, Ende, East Nusa Tenggara.<\/jats:p><\/jats:sec><jats:sec id=\"sec002\"><jats:title>Methods<\/jats:title><jats:p>A cross-sectional survey involving PSC ranging from 12 to 59 months old from Nangapanda subdistrict, Ende district, East Nusa Tenggara was performed. Socio-demographic, breastfeeding, and complementary feeding information was obtained from structured questionnaires, while nutritional and anemia status was determined from anthropometry and hemoglobin measurements, respectively. Anthropometric z-scores were calculated based on the World Health Organization 2006 standards and stool samples were examined using Kato-Katz method.<\/jats:p><\/jats:sec><jats:sec id=\"sec003\"><jats:title>Results<\/jats:title><jats:p>A total of 393 PSC randomly selected from 22 villages were examined. The prevalence of underweight, stunting, wasting, and anemia were 33.1%, 40.2%, 17.1%, and 60.3%, respectively. STH infection, predominated by<jats:italic>Ascaris lumbricoides<\/jats:italic>, was found in 160 (58.8%) PSC. Single STH infection, but not multiple infection, was independently associated with a lower risk of anemia (odds ratio [OR] 0.320, 95% confidence interval [CI]: 0.126\u20130.809, p = 0.016). Similar association with anemia was also found on mild STH infection (OR 0.318 [95% CI: 0.114\u20130.887], p = 0.029). On the other hand, younger children were found to have a higher risk of anemia and stunting. None of the examined variables were independently associated with underweight and wasting.<\/jats:p><\/jats:sec><jats:sec id=\"sec004\"><jats:title>Conclusion<\/jats:title><jats:p>STH infection as well as anemia and malnutrition were prevalent in this region. However in this study, current STH infections seemed to have minimal negative impact on children\u2019s nutritional status.<\/jats:p><\/jats:sec>","DOI":"10.1371\/journal.pntd.0009506","type":"journal-article","created":{"date-parts":[[2021,6,17]],"date-time":"2021-06-17T17:45:12Z","timestamp":1623951912000},"page":"e0009506","update-policy":"https:\/\/doi.org\/10.1371\/journal.pntd.corrections_policy","source":"Crossref","is-referenced-by-count":37,"title":["Soil-transmitted helminth infection, anemia, and malnutrition among preschool-age children in Nangapanda subdistrict, Indonesia"],"prefix":"10.1371","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2319-9481","authenticated-orcid":true,"given":"Yenny","family":"Djuardi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3605-6167","authenticated-orcid":true,"given":"Gilbert","family":"Lazarus","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Difa","family":"Stefanie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1403-6242","authenticated-orcid":true,"given":"Umi","family":"Fahmida","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Iwan","family":"Ariawan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1209-402X","authenticated-orcid":true,"given":"Taniawati","family":"Supali","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,6,17]]},"reference":[{"key":"pntd.0009506.ref001","first-page":"81","article-title":"Epidemiology and clinical features of soil-transmitted helminths","volume":"7","author":"SC Parija","year":"2017","journal-title":"Trop Parasitol"},{"key":"pntd.0009506.ref002","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pntd.0006606","article-title":"Toward the 2020 goal of soil-transmitted helminthiasis control and elimination","volume":"12","author":"SL Becker","year":"2018","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009506.ref003","volume-title":"Soil-transmitted helminthiases: number of children (pre-SAC and SAC) requiring preventive chemotherapy for soil-transmitted helminthiases: 2019","author":"World Health Organization","year":"2020"},{"key":"pntd.0009506.ref004","unstructured":"World Health Organization. Indonesia: communicable disease profile. In: World Health Organization [Internet]. 2016 [cited 2019 Oct 5]. Available from: https:\/\/www.who.int\/nmh\/countries\/idn_en.pdf?ua=1."},{"key":"pntd.0009506.ref005","doi-asserted-by":"crossref","first-page":"e0127746","DOI":"10.1371\/journal.pone.0127746","article-title":"Infection with soil-transmitted helminths is associated with increased insulin sensitivity","volume":"10","author":"AE Wiria","year":"2015","journal-title":"PLoS One"},{"key":"pntd.0009506.ref006","volume-title":"World Health Organization","author":"World Health Organization","year":"2012"},{"key":"pntd.0009506.ref007","first-page":"6706413","article-title":"Risk factors for soil-transmitted helminthiasis in preschool children living in farmland, North Sumatera","volume":"2018","author":"S Novianty","year":"2018","journal-title":"Indonesia. J Trop Med"},{"key":"pntd.0009506.ref008","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1186\/s12889-018-5124-3","article-title":"Risk factors for malnutrition among preschool children in rural Karnataka: a case-control study","volume":"18","author":"Ansuya","year":"2018","journal-title":"BMC Public Health"},{"key":"pntd.0009506.ref009","volume-title":"Hasil utama Riskesdas 2018","author":"Kementerian Kesehatan Republik Indonesia","year":"2018"},{"key":"pntd.0009506.ref010","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1186\/1471-2334-10-77","article-title":"Does treatment of intestinal helminth infections influence malaria? Background and methodology of a longitudinal study of clinical, parasitological and immunological parameters in Nangapanda, Flores, Indonesia (ImmunoSPIN Study)","volume":"10","author":"AE Wiria","year":"2010","journal-title":"BMC Infect Dis"},{"key":"pntd.0009506.ref011","first-page":"1","volume-title":"Adequacy of sample size in health studies","author":"World Health Organization","year":"1990"},{"key":"pntd.0009506.ref012","first-page":"212","volume-title":"Riset kesehatan dasar, RISKESDAS 2013","author":"Badan Penelitian dan Pengembangan Kesehatan","year":"2013"},{"key":"pntd.0009506.ref013","first-page":"106","volume-title":"The optimal duration of exclusive breastfeeding: report of an expert consultation","author":"World Health Organization","year":"2001"},{"key":"pntd.0009506.ref014","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1186\/s12887-018-0989-y","article-title":"Timely initiation of complementary feeding to children aged 6\u201323 months in rural Soro district of Southwest Ethiopia: a cross-sectional study","volume":"18","author":"B Yohannes","year":"2018","journal-title":"BMC Pediatr"},{"key":"pntd.0009506.ref015","volume-title":"Guiding principles for complementary feeding of the breastfed child","author":"Pan American Health Organization","year":"2003"},{"key":"pntd.0009506.ref016","volume-title":"WHO Anthro for personal computers, version 3.2.2, 2011: Software for assessing growth and development of the world\u2019s children","author":"World Health Organization","year":"2010"},{"key":"pntd.0009506.ref017","volume-title":"WHO child growth standards: length\/height-for-age, wieight-for-age, weight-for-length, weight-for-height, and body mass index-for-age: methods development","author":"WHO Multicentre Growth Reference Study Group","year":"2006"},{"key":"pntd.0009506.ref018","first-page":"1","volume-title":"Vitamin and Mineral Nutrition System","author":"World Health Organization","year":"2011"},{"key":"pntd.0009506.ref019","volume-title":"Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee","author":"WHO Expert Committee on the Control of Schistosomiasis","year":"2002"},{"issue":"Suppl 4","key":"pntd.0009506.ref020","doi-asserted-by":"crossref","first-page":"e12653","DOI":"10.1111\/mcn.12653","article-title":"Nutritional status and risk factors for stunting in preschool children in Bhutan","volume":"14","author":"Y Kang","year":"2018","journal-title":"Matern Child Nutr"},{"key":"pntd.0009506.ref021","doi-asserted-by":"crossref","first-page":"6438497","DOI":"10.1155\/2019\/6438497","article-title":"The effectiveness of triple dose albendazole in treating soil transmitted helminths infection","volume":"2019","author":"S Sungkar","year":"2019","journal-title":"J Parasitol Res"},{"key":"pntd.0009506.ref022","doi-asserted-by":"crossref","first-page":"329","DOI":"10.3347\/kjp.2019.57.4.329","article-title":"Current status of parasite infections in Indonesia: A literature review","volume":"57","author":"J Lee","year":"2019","journal-title":"Korean J Parasitol"},{"key":"pntd.0009506.ref023","doi-asserted-by":"crossref","DOI":"10.1186\/1756-3305-5-119","article-title":"The nutritional impacts of soil-transmitted helminths infections among Orang Asli schoolchildren in rural Malaysia","author":"A Ahmed","year":"2012","journal-title":"Parasit Vectors"},{"key":"pntd.0009506.ref024","article-title":"Prevalence, intensity and factors associated with soil-transmitted helminths infections among preschool-age children in Hoima district, rural western Uganda","author":"S Ojja","year":"2018","journal-title":"BMC Infect Dis"},{"key":"pntd.0009506.ref025","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.actatropica.2011.04.010","article-title":"From morbidity control to transmission control: Time to change tactics against helminths on Unguja Island","volume":"128","author":"S Knopp","year":"2013","journal-title":"Zanzibar. Acta Trop"},{"key":"pntd.0009506.ref026","volume-title":"World Health Organization","author":"M De Onis","year":"1997"},{"key":"pntd.0009506.ref027","doi-asserted-by":"crossref","first-page":"227","DOI":"10.3945\/an.111.001107","article-title":"Patterns of stunting and wasting: potential explanatory factors","volume":"3","author":"R Martorell","year":"2012","journal-title":"Adv Nutr"},{"key":"pntd.0009506.ref028","doi-asserted-by":"crossref","first-page":"e12617","DOI":"10.1111\/mcn.12617","article-title":"A review of child stunting determinants in Indonesia","volume":"14","author":"T Beal","year":"2018","journal-title":"Matern Child Nutr"},{"key":"pntd.0009506.ref029","article-title":"Prevalence of soil-transmitted helminthiases and schistosomiasis in preschool age children in Mwea Division, Kirinyaga South District, Kirinyaga County, and their potential effect on physical growth","author":"SSW Sakari","year":"2017","journal-title":"J Trop Med"},{"key":"pntd.0009506.ref030","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1186\/1756-3305-3-97","article-title":"Stunting and soil-transmitted-helminth infections among school-age pupils in rural areas of southern China","volume":"3","author":"Y Shang","year":"2010","journal-title":"Parasit Vectors"},{"key":"pntd.0009506.ref031","article-title":"Poly-helminth infection in east guatemalan school children","author":"WC Sorensen","year":"2011","journal-title":"J Glob Infect Dis"},{"key":"pntd.0009506.ref032","article-title":"Soil-transmitted helminth infections and nutritional status in school-age children from rural communities in Honduras","author":"AL Sanchez","year":"2013","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009506.ref033","doi-asserted-by":"crossref","first-page":"117","DOI":"10.5539\/gjhs.v11n5p117","article-title":"The impact of soil transmitted helminth (STH) towards anemia case in elementary school student in the district of Northwest Sumba","volume":"11","author":"R Paun","year":"2019","journal-title":"Glob J Health Sci"},{"key":"pntd.0009506.ref034","doi-asserted-by":"crossref","DOI":"10.13181\/mji.v27i4.2857","article-title":"The effect of albendazole toward anemia in children with soil-transmitted helminths infection in a remote and endemic area","volume":"27","author":"S Sungkar","year":"2018","journal-title":"Med J Indones"},{"key":"pntd.0009506.ref035","doi-asserted-by":"crossref","first-page":"168","DOI":"10.4103\/0019-5359.125878","article-title":"Prevalence and determining factors of anemia and malnutrition among Egyptian children.","volume":"67","author":"AA Barakat","year":"2013","journal-title":"Indian J Med Sci"},{"key":"pntd.0009506.ref036","doi-asserted-by":"crossref","first-page":"e0218961","DOI":"10.1371\/journal.pone.0218961","article-title":"Prevalence of anemia and its associated factors among children under five years of age attending at Guguftu Health Center, South Wollo, Northeast Ethiopia","volume":"14","author":"A Gebreweld","year":"2019","journal-title":"PLoS One"},{"key":"pntd.0009506.ref037","doi-asserted-by":"crossref","first-page":"95","DOI":"10.2149\/tmh.2011-13","article-title":"Anemia and Related Factors in Preschool Children in the Southern Rural Lao People\u2019s Democratic Republic","volume":"39","author":"S Kounnavong","year":"2011","journal-title":"Trop Med Health"},{"key":"pntd.0009506.ref038","doi-asserted-by":"crossref","first-page":"30","DOI":"10.4297\/najms.2011.330","article-title":"A significant association between intestinal helminth infection and anaemia burden in children in rural communities of Edo State","volume":"3","author":"F Osazuwa","year":"2011","journal-title":"Nigeria. N Am J Med Sci"},{"key":"pntd.0009506.ref039","doi-asserted-by":"crossref","first-page":"2160","DOI":"10.1086\/498219","article-title":"Functional significance of low-intensity polyparasite helminth infections in anemia","volume":"192","author":"AE Ezeamama","year":"2005","journal-title":"J Infect Dis"},{"key":"pntd.0009506.ref040","article-title":"Soil-transmitted helminths (STH) infection has no relations with anemia on children in SDN Barengan Sub-District, Teras, Boyolali [in Indonesian]","volume":"4","author":"AWT Salsabila","year":"2015","journal-title":"Nexus Biomedika."},{"key":"pntd.0009506.ref041","unstructured":"Lalangpuling IE O BY, A.W M, erdiana E. Hubungan infeksi soil transmitted helminths (STH) dengan status gizi dan anemia pada balita di Puskesmas Kokar Kabupaten Alor [thesis; in Indonesian]. Perpustakaan Universitas Gadjah Mada. Gadjah Mada University. 2017 [cited 2020 Nov 1]. Available from: http:\/\/etd.repository.ugm.ac.id\/penelitian\/detail\/112415."},{"key":"pntd.0009506.ref042","doi-asserted-by":"crossref","first-page":"e681","DOI":"10.1371\/journal.pntd.0000681","article-title":"Patterns and risk factors of helminthiasis and anemia in a rural and a peri-urban community in Zanzibar, in the context of helminth control programs","volume":"4","author":"S Knopp","year":"2010","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009506.ref043","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1016\/j.trstmh.2011.08.013","article-title":"Preventive chemotherapy in human helminthiasis: Theoretical and operational aspects","volume":"105","author":"AF Gabrielli","year":"2011","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"pntd.0009506.ref044","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-017-2084-x","article-title":"Investigations into the association between soil-transmitted helminth infections, haemoglobin and child development indices in Manufahi District, Timor-Leste","volume":"10","author":"SJ Campbell","year":"2017","journal-title":"Parasit Vectors"},{"key":"pntd.0009506.ref045","first-page":"41","volume-title":"Gizi dalam angka sampai dengan tahun 2003 [","author":"R Untoro","year":"2005"},{"key":"pntd.0009506.ref046","doi-asserted-by":"crossref","DOI":"10.1002\/ajhb.22952","article-title":"Improved nutrition in the first 1000 days and adult human capital and health","volume":"29","author":"R. Martorell","year":"2017","journal-title":"Am J Hum Biol"},{"key":"pntd.0009506.ref047","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/s12936-017-1691-5","article-title":"Effect of a short course of iron polymaltose on acquisition of malarial parasitaemia in anaemic Indonesian schoolchildren: a randomized trial","volume":"16","author":"MA Prasetyani","year":"2017","journal-title":"Malar J"}],"updated-by":[{"DOI":"10.1371\/journal.pntd.0009506","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,7,2]],"date-time":"2021-07-02T00:00:00Z","timestamp":1625184000000}}],"container-title":["PLOS Neglected Tropical Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0009506","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,5]],"date-time":"2023-11-05T01:30:29Z","timestamp":1699147829000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0009506"}},"subtitle":[],"editor":[{"given":"Maria Angeles","family":"G\u00f3mez-Morales","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,6,17]]},"references-count":47,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2021,6,17]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pntd.0009506","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pntd.0009506","asserted-by":"object"}]},"ISSN":["1935-2735"],"issn-type":[{"value":"1935-2735","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,17]]}}}