{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,30]],"date-time":"2026-10-30T03:54:10Z","timestamp":1793332450066,"version":"4.5.0"},"reference-count":66,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2013,12,17]],"date-time":"2013-12-17T00:00:00Z","timestamp":1387238400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosmedicine.org"],"crossmark-restriction":false},"short-container-title":["PLoS Med"],"DOI":"10.1371\/journal.pmed.1001575","type":"journal-article","created":{"date-parts":[[2013,12,17]],"date-time":"2013-12-17T21:41:38Z","timestamp":1387316498000},"page":"e1001575","update-policy":"https:\/\/doi.org\/10.1371\/journal.pmed.corrections_policy","source":"Crossref","is-referenced-by-count":131,"title":["Major Burden of Severe Anemia from Non-Falciparum Malaria Species in Southern Papua: A Hospital-Based Surveillance Study"],"prefix":"10.1371","volume":"10","author":[{"given":"Nicholas M.","family":"Douglas","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel A.","family":"Lampah","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Enny","family":"Kenangalem","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julie A.","family":"Simpson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeanne R.","family":"Poespoprodjo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paulus","family":"Sugiarto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas M.","family":"Anstey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ric N.","family":"Price","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2013,12,17]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1111\/j.1365-3156.2008.02076.x","article-title":"Estimates of the burden of malaria morbidity in Africa in children under the age of 5 years","volume":"13","author":"A Roca-Feltrer","year":"2008","journal-title":"Trop Med Int Health"},{"key":"ref2","unstructured":"Snow RW, Craig MH, Newton CRJC, Steketee RW (2003) The public health burden of Plasmodium falciparum<\/italic> malaria in Africa: deriving the numbers. BethesdaMaryland: Fogarty International Center, National Institutes of Health."},{"key":"ref3","doi-asserted-by":"crossref","first-page":"57","DOI":"10.4269\/ajtmh.2001.64.57","article-title":"Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy","volume":"64","author":"SC Murphy","year":"2001","journal-title":"Am J Trop Med Hyg"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"888","DOI":"10.1056\/NEJMoa072727","article-title":"Severe anemia in Malawian children","volume":"358","author":"JCJ Calis","year":"2008","journal-title":"N Engl J Med"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"1399","DOI":"10.1056\/NEJM199505253322102","article-title":"Indicators of life-threatening malaria in African children","volume":"332","author":"K Marsh","year":"1995","journal-title":"N Engl J Med"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"23","DOI":"10.4269\/ajtmh.77.6.suppl.23","article-title":"In-hospital morbidity and mortality due to severe malarial anemia in Western Kenya","volume":"77","author":"CO Obonyo","year":"2007","journal-title":"Am J Trop Med Hyg"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/0035-9203(94)90157-0","article-title":"In-hospital morbidity and mortality due to malaria-associated severe anaemia in two areas of Malawi with different patterns of malaria infection","volume":"88","author":"L Slutsker","year":"1994","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1111\/j.1365-3156.1996.tb00019.x","article-title":"Insecticide-treated bednets reduce mortality and severe morbidity from malaria among children on the Kenyan coast","volume":"1","author":"CG Nevill","year":"1996","journal-title":"Trop Med Int Health"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/0035-9203(93)90174-O","article-title":"A malaria control trial using insecticide-treated bed nets and targeted chemoprophylaxis in a rural area of The Gambia, West Africa. 6. The impact of the interventions on mortality and morbidity from malaria","volume":"87","author":"PL Alonso","year":"1993","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"1050","DOI":"10.1111\/j.1365-3156.2004.01317.x","article-title":"Impact of malaria control on childhood anaemia in Africa - a quantitative review","volume":"9","author":"EL Korenromp","year":"2004","journal-title":"Trop Med Int Health"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"636S","DOI":"10.1093\/jn\/131.2.636S","article-title":"An analysis of anemia and child mortality","volume":"131","author":"BJ Brabin","year":"2001","journal-title":"J Nutr"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1182\/blood-2010-04-202911","article-title":"The pathogenesis of Plasmodium falciparum<\/italic> malaria in humans: insights from splenic physiology","volume":"117","author":"PA Buffet","year":"2011","journal-title":"Blood"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1053\/beha.1999.0072","article-title":"Blood and bone marrow changes in malaria","volume":"13","author":"SN Wickramasinghe","year":"2000","journal-title":"Baillieres Best Pract Res Clin Haematol"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"1055","DOI":"10.1016\/S0140-6736(79)92952-0","article-title":"Cause of anaemia in malaria","volume":"1","author":"AW Woodruff","year":"1979","journal-title":"Lancet"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/S0035-9203(99)90180-3","article-title":"Evidence for erythrocyte lipid peroxidation in acute falciparum malaria","volume":"93","author":"BS Das","year":"1999","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1182\/asheducation-2009.1.87","article-title":"Malaria, erythrocytic infection, and anemia","author":"K Haldar","year":"2009","journal-title":"Hematology Am Soc Hematol Educ Program"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1111\/j.1365-2141.1980.tb05956.x","article-title":"The anaemia of P. falciparum<\/italic> malaria","volume":"46","author":"S Abdalla","year":"1980","journal-title":"Br J Haematol"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1128\/CDLI.8.6.1164-1170.2001","article-title":"Anemia and interleukin-10, tumor necrosis factor alpha, and erythropoietin levels among children with acute uncomplicated Plasmodium falciparum<\/italic> malaria","volume":"8","author":"V Nussenblatt","year":"2001","journal-title":"Clin Diagn Lab Immun"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"1501","DOI":"10.1016\/j.ijpara.2004.10.008","article-title":"Malarial anaemia: mechanisms and implications of insufficient erythropoiesis during blood-stage malaria","volume":"34","author":"K-H Chang","year":"2004","journal-title":"Int J Parasitol"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/0035-9203(87)90285-9","article-title":"Reduction in erythrocytic GSH level and stability in Plasmodium vivax<\/italic> malaria","volume":"81","author":"J Bhattacharya","year":"1987","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"151","DOI":"10.7883\/yoken1952.49.151","article-title":"Hematological impairments in recurrent Plasmodium vivax<\/italic> infected patients","volume":"49","author":"R Selvam","year":"1996","journal-title":"Jpn J Med Sci Biol"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1111\/j.1365-2141.1989.tb07658.x","article-title":"Dyserythropoiesis and ineffective erythropoiesis in Plasmodium vivax<\/italic> malaria","volume":"72","author":"SN Wickramasinghe","year":"1989","journal-title":"Br J Haematol"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1086\/596048","article-title":"High deformability of Plasmodium vivax<\/italic>-infected red blood cells under microfluidic conditions","volume":"199","author":"S Handayani","year":"2009","journal-title":"J Infect Dis"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1186\/1475-2875-11-135","article-title":"The anaemia of Plasmodium vivax<\/italic> malaria","volume":"11","author":"NM Douglas","year":"2012","journal-title":"Malar J"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/B978-0-12-397900-1.00003-7","article-title":"Plasmodium vivax<\/italic>: clinical spectrum, risk factors and pathogenesis","volume":"80","author":"NM Anstey","year":"2012","journal-title":"Adv Parasitol"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"e1972","DOI":"10.1371\/journal.pntd.0001972","article-title":"Severe anemia in papua new guinean children from a malaria-endemic area: a case-control etiologic study","volume":"6","author":"L Manning","year":"2012","journal-title":"PloS Negl Trop Dis"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"641","DOI":"10.4269\/ajtmh.1999.60.641","article-title":"Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission II. Descriptive epidemiology of malaria infection and disease among children","volume":"60","author":"PB Bloland","year":"1999","journal-title":"Am J Trop Med Hyg"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/S0169-4758(97)01061-2","article-title":"Plasmodium vivax<\/italic> and P. falciparum<\/italic>: biological interactions and the possibility of cross-species immunity","volume":"13","author":"K Maitland","year":"1997","journal-title":"Parasitol Today"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1016\/S0035-9203(96)90406-X","article-title":"The interaction between Plasmodium falciparum<\/italic> and P. vivax<\/italic> in children on Espiritu Santo Island, Vanuatu","volume":"90","author":"K Maitland","year":"1996","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"614","DOI":"10.4269\/ajtmh.2001.65.614","article-title":"Factors contributing to anemia after uncomplicated falciparum malaria","volume":"65","author":"RN Price","year":"2001","journal-title":"Am J Trop Med Hyg"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.pt.2004.03.006","article-title":"Mixed-species malaria infections in humans","volume":"20","author":"M Mayxay","year":"2004","journal-title":"Trends Parasitol"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"e35406","DOI":"10.1371\/journal.pone.0035406","article-title":"Risk factors and characterization of Plasmodium vivax<\/italic>-associated admissions to pediatric intensive care units in the Brazilian Amazon","volume":"7","author":"EF Lanca","year":"2012","journal-title":"PLoS ONE"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"e128","DOI":"10.1371\/journal.pmed.0050128","article-title":"Multidrug-resistant Plasmodium vivax<\/italic> associated with severe and fatal malaria: a prospective study in Papua, Indonesia","volume":"5","author":"E Tjitra","year":"2008","journal-title":"PLoS Med"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"e127","DOI":"10.1371\/journal.pmed.0050127","article-title":"Plasmodium vivax<\/italic> and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea","volume":"5","author":"B Genton","year":"2008","journal-title":"PLoS Med"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"984","DOI":"10.4269\/ajtmh.2007.77.984","article-title":"Demographic risk factors for severe and fatal vivax and falciparum malaria among hospital admissions in Northeastern Indonesian Papua","volume":"77","author":"MJ Barcus","year":"2007","journal-title":"Am J Trop Med Hyg"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"1374","DOI":"10.1086\/586743","article-title":"Adverse pregnancy outcomes in an area where multidrug-resistant Plasmodium vivax<\/italic> and Plasmodium falciparum<\/italic> infections are endemic","volume":"46","author":"JR Poespoprodjo","year":"2008","journal-title":"Clin Infect Dis"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1186\/1475-2875-7-148","article-title":"Epidemiology of multidrug resistant P. vivax<\/italic> and P. falciparum<\/italic> infection in Southern Papua, Indonesia","volume":"7","author":"M Karyana","year":"2008","journal-title":"Malar J"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"429","DOI":"10.2307\/2986270","article-title":"Regression using fractional polynomials of continuous covariates: parsimonious parametric modelling","volume":"43","author":"P Royston","year":"1994","journal-title":"Appl Statist"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"865","DOI":"10.2307\/2532206","article-title":"Maximum likelihood estimation of the attributable fraction from logistic models","volume":"49","author":"S Greenland","year":"1993","journal-title":"Biometrics"},{"key":"ref40","unstructured":"World Health Organization, United Nations Children's Fund (2004) Focusing on anaemia: towards an integrated approach for effective anaemia control. Joint statement by the World Health Organization and the United Nations Children's Fund. Geneva: World Health Organization."},{"key":"ref41","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1111\/j.1365-3156.2006.01635.x","article-title":"Stronger host response per parasitized erythrocyte in Plasmodium vivax<\/italic> or ovale<\/italic> then in Plasmodium falciparum<\/italic> malaria","volume":"11","author":"CJ Hemmer","year":"2006","journal-title":"Trop Med Int Health"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1086\/653211","article-title":"Greater endothelial activation, Weibel-Palade body release and host inflammatory response to Plasmodium vivax<\/italic>, compared with Plasmodium falciparum<\/italic>: a prospective study in Papua, Indonesia","volume":"202","author":"TW Yeo","year":"2010","journal-title":"J Infect Dis"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1016\/S0022-3476(96)70331-1","article-title":"Serum erythropoietin levels during infancy: associations with erythropoiesis","volume":"128","author":"PJ Kling","year":"1996","journal-title":"J Pediatr"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1038\/415680a","article-title":"The economic and social burden of malaria","volume":"415","author":"J Sachs","year":"2002","journal-title":"Nature"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"626","DOI":"10.2307\/3285103","article-title":"Plasmodium malariae<\/italic> blood-stage dynamics","volume":"87","author":"FE McKenzie","year":"2001","journal-title":"J Parasitol"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/s12551-010-0034-3","article-title":"Population dynamics of a pathogen: the conundrum of vivax malaria","volume":"2","author":"PG McQueen","year":"2010","journal-title":"Biophys Rev"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1016\/j.pt.2007.04.009","article-title":"Plasmodium malariae<\/italic> and Plasmodium ovale<\/italic>\u2013the \u201cbashful\u201d malaria parasites","volume":"23","author":"I Mueller","year":"2007","journal-title":"Trends Parasitol"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1086\/589884","article-title":"Alpha+ -thalassemia protects against anemia associated with asymptomatic malaria: evidence from community-based surveys in Tanzania and Kenya","volume":"198","author":"J Veenemans","year":"2008","journal-title":"J Infect Dis"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1016\/j.pt.2008.07.006","article-title":"Alpha+-thalassaemia and malarial anaemia","volume":"24","author":"I Danquah","year":"2008","journal-title":"Trends Parasitol"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"e56","DOI":"10.1371\/journal.pmed.0050056","article-title":"Increased microerythrocyte count in homozygous alpha+-thalassaemia contributes to protection against severe malarial anaemia","volume":"5","author":"FJI Fowkes","year":"2008","journal-title":"PLoS Med"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1038\/383522a0","article-title":"High incidence of malaria in alpha-thalassaemic children","volume":"383","author":"TN Williams","year":"1996","journal-title":"Nature"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1016\/S0140-6736(62)90956-X","article-title":"Erythrocyte glucose-6-phosphate dehydrogenase and malaria in Thailand","volume":"2","author":"M Kruatrachue","year":"1962","journal-title":"Lancet"},{"key":"ref53","first-page":"4","article-title":"Malaria species and Southeast Asian ovalocytosis defined by a 27-bp deletion in the erythrocyte band 3 gene","volume":"33","author":"M Kimura","year":"2002","journal-title":"Southeast Asian J Trop Med Public Health"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"271","DOI":"10.4269\/ajtmh.1992.47.271","article-title":"Ovalocytosis protects against severe malaria parasitemia in the Malayan aborigines","volume":"47","author":"LC Foo","year":"1992","journal-title":"Am J Trop Med Hyg"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1007\/s10038-005-0271-7","article-title":"Glucose-6-phosphate dehydrogenase deficiency and Southeast Asian ovalocytosis in asymptomatic Plasmodium<\/italic> carriers in Sumba Island, Indonesia","volume":"50","author":"H Shimizu","year":"2005","journal-title":"J Hum Genet"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1007\/BF00393579","article-title":"Malaria and hereditary ovalocytosis","volume":"37","author":"S Serjeantson","year":"1977","journal-title":"Hum Genet"},{"key":"ref57","unstructured":"Kitchen SF (1939) Malariology. London: W.B. Saunders."},{"key":"ref58","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1086\/589512","article-title":"Decreased susceptibility to Plasmodium falciparum<\/italic> infection in pregnant women with iron deficiency","volume":"198","author":"ER Kabyemela","year":"2008","journal-title":"J Infect Dis"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"88","DOI":"10.4269\/ajtmh.2007.77.88","article-title":"Epidemiology of Plasmodium<\/italic>-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control","volume":"77","author":"S Brooker","year":"2007","journal-title":"Am J Trop Med Hyg"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1645\/0022-3395(2002)088[0055:IHIAAW]2.0.CO;2","article-title":"Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum<\/italic> malaria in Thailand","volume":"88","author":"M Nacher","year":"2002","journal-title":"J Parasitol"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/S0035-9203(03)90117-9","article-title":"Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum<\/italic> malaria","volume":"97","author":"A Spiegel","year":"2003","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"e887","DOI":"10.1371\/journal.pntd.0000887","article-title":"Complex interactions between soil-transmitted helminths and malaria in pregnant women on the Thai-Burmese border","volume":"4","author":"M Boel","year":"2010","journal-title":"PloS Negl Trop Dis"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"e11206","DOI":"10.1371\/journal.pone.0011206","article-title":"Concurrent helminthic infection protects schoolchildren with Plasmodium vivax<\/italic> from anemia","volume":"5","author":"GC Melo","year":"2010","journal-title":"PLoS ONE"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"1724","DOI":"10.1093\/jn\/130.7.1724","article-title":"Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0- to 5-y old Zanzibari children and these relationships change with age","volume":"130","author":"RJ Stoltzfus","year":"2000","journal-title":"J Nutr"},{"key":"ref65","unstructured":"Brabin BJ (1991) The risks and severity of malaria in pregnant women. Geneva: World Health Organization."},{"key":"ref66","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1016\/0035-9203(91)90205-D","article-title":"Malaria during pregnancy in an area of unstable endemicity","volume":"85","author":"F Nosten","year":"1991","journal-title":"Trans R Soc Trop Med Hyg"}],"container-title":["PLoS Medicine"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pmed.1001575","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,20]],"date-time":"2022-03-20T00:13:04Z","timestamp":1647735184000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pmed.1001575"}},"subtitle":[],"editor":[{"given":"Lars","family":"Hviid","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2013,12,17]]},"references-count":66,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2013,12,17]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pmed.1001575","relation":{},"ISSN":["1549-1676"],"issn-type":[{"value":"1549-1676","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,12,17]]}}}