Major Burden of Severe Anemia from Non-Falciparum Malaria Species in Southern Papua: A Hospital-Based Surveillance Study

PLoS Medicine

Volumn 10, Issue 12, 2013, Pages 1-17

  Douglas, Nicholas M ^a,b   Lampah, Daniel A ^c   Kenangalem, Enny ^c,d   Simpson, Julie A ^e   Poespoprodjo, Jeanne R ^a,c,d   Sugiarto, Paulus ^f   Anstey, Nicholas M ^a,g   Price, Ric N ^a,b  

^a MENZIES SCHOOL OF HEALTH RESEARCH   (Australia)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c Papuan Health and Community Development Foundation   (Indonesia)

^d Mimika District Health Authority   (India)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f Rumah Sakit Mitra Masyarakat ^*  (India)

^g ROYAL DARWIN HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN;

ADOLESCENT; ADULT; ANEMIA; ARTICLE; CHILD; COMPARATIVE STUDY; DEATH; FEMALE; HOSPITALIZATION; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALARIA; MALE; MIDDLE AGED; MIXED INFECTION; MORTALITY; PAPUA NEW GUINEA; PLASMODIUM FALCIPARUM; PLASMODIUM MALARIAE; PLASMODIUM VIVAX; PRESCHOOL CHILD; RISK; SCHOOL CHILD; YOUNG ADULT; AGED; INDONESIA; METABOLISM; NEWBORN; PATHOGENICITY; RISK FACTOR;

ADOLESCENT; ADULT; AGED; ANEMIA; CHILD; CHILD, PRESCHOOL; FEMALE; HEMOGLOBINS; HUMANS; INDONESIA; INFANT; INFANT, NEWBORN; MALARIA; MALE; MIDDLE AGED; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; RISK FACTORS; YOUNG ADULT;

EID: 84892854787     PISSN: 15491277     EISSN: 15491676     Source Type: Journal    
DOI: 10.1371/journal.pmed.1001575     Document Type: Article

References (66)

1. Roca-Feltrer A, Carneiro I, Armstrong Schellenberg JR, (2008) Estimates of the burden of malaria morbidity in Africa in children under the age of 5 years. Trop Med Int Health 13: 771-783.
2. Snow RW, Craig MH, Newton CRJC, Steketee RW (2003) The public health burden of Plasmodium falciparum malaria in Africa: deriving the numbers. BethesdaMaryland: Fogarty International Center, National Institutes of Health.
3. Murphy SC, Breman JG, (2001) Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am J Trop Med Hyg 64: 57-67.
4. Calis JCJ, Phiri KS, Faragher EB, Brabin BJ, Bates I, et al. (2008) Severe anemia in Malawian children. N Engl J Med 358: 888-899.
5. Marsh K, Forster D, Waruiru C, Mwangi I, Winstanley P, et al. (1995) Indicators of life-threatening malaria in African children. N Engl J Med 332: 1399-1404.
6. Obonyo CO, Vulule J, Akhwale WS, Grobbee DE, (2007) In-hospital morbidity and mortality due to severe malarial anemia in Western Kenya. Am J Trop Med Hyg 77: 23-28.
7. Slutsker L, Taylor TE, Wirima JJ, Steketee RW, (1994) In-hospital morbidity and mortality due to malaria-associated severe anaemia in two areas of Malawi with different patterns of malaria infection. Trans R Soc Trop Med Hyg 88: 548-551.
8. Nevill CG, Some ES, Mung'ala VO, Mutemi W, New L, et al. (1996) Insecticide-treated bednets reduce mortality and severe morbidity from malaria among children on the Kenyan coast. Trop Med Int Health 1: 139-146.
9. Alonso PL, Lindsay SW, Armstrong Schellenberg JR, Keita K, Gomez P, et al. (1993) 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. Trans R Soc Trop Med Hyg 87: 37-44.
10. Korenromp EL, Armstrong-Schellenberg JRM, Williams BG, Nahlen BL, Snow RW, (2004) Impact of malaria control on childhood anaemia in Africa- a quantitative review. Trop Med Int Health 9: 1050-1065.
11. Brabin BJ, Premji Z, Verhoeff F, (2001) An analysis of anemia and child mortality. J Nutr 131: 636S-645S; discussion 646S-648S.
12. Buffet PA, Safeukui I, Deplaine G, Brousse V, Prendki V, et al. (2011) The pathogenesis of Plasmodium falciparum malaria in humans: insights from splenic physiology. Blood 117: 381-392.
13. Wickramasinghe SN, Abdalla SH, (2000) Blood and bone marrow changes in malaria. Baillieres Best Pract Res Clin Haematol 13: 277-299.
14. Woodruff AW, Ansdell VE, Pettitt LE, (1979) Cause of anaemia in malaria. Lancet 1: 1055-1057.
15. Das BS, Nanda NK, (1999) Evidence for erythrocyte lipid peroxidation in acute falciparum malaria. Trans R Soc Trop Med Hyg 93: 58-62.
16. Haldar K, Mohandas N, (2009) Malaria, erythrocytic infection, and anemia. Hematology Am Soc Hematol Educ Program pp. 87-93.
17. Abdalla S, Weatherall DJ, Wickramasinghe SN, Hughes M, (1980) The anaemia of P. falciparum malaria. Br J Haematol 46: 171-183.
18. Nussenblatt V, Mukasa G, Metzger A, Ndeezi G, Garrett E, et al. (2001) Anemia and interleukin-10, tumor necrosis factor alpha, and erythropoietin levels among children with acute uncomplicated Plasmodium falciparum malaria. Clin Diagn Lab Immun 8: 1164-1170.
19. Chang K-H, Stevenson MM, (2004) Malarial anaemia: mechanisms and implications of insufficient erythropoiesis during blood-stage malaria. Int J Parasitol 34: 1501-1516.
20. Bhattacharya J, Swarup-Mitra S, (1987) Reduction in erythrocytic GSH level and stability in Plasmodium vivax malaria. Trans R Soc Trop Med Hyg 81: 64-66.
21. Selvam R, Baskaran G, (1996) Hematological impairments in recurrent Plasmodium vivax infected patients. Jpn J Med Sci Biol 49: 151-165.
22. Wickramasinghe SN, Looareesuwan S, Nagachinta B, White NJ, (1989) Dyserythropoiesis and ineffective erythropoiesis in Plasmodium vivax malaria. Br J Haematol 72: 91-99.
23. Handayani S, Chiu DT, Tjitra E, Kuo JS, Lampah D, et al. (2009) High deformability of Plasmodium vivax-infected red blood cells under microfluidic conditions. J Infect Dis 199: 445-450.
24. Douglas NM, Anstey NM, Buffet PA, Poespoprodjo JR, Yeo TW, et al. (2012) The anaemia of Plasmodium vivax malaria. Malar J 11: 135.
25. Anstey NM, Douglas NM, Poespoprodjo JR, Price RN, (2012) Plasmodium vivax: clinical spectrum, risk factors and pathogenesis. Adv Parasitol 80: 151-201.
26. Manning L, Laman M, Rosanas-Urgell A, Michon P, Aipit S, et al. (2012) Severe anemia in papua new guinean children from a malaria-endemic area: a case-control etiologic study. PloS Negl Trop Dis 6: e1972 doi:10.1371/journal.pntd.0001972.
27. Bloland PB, Boriga DA, Ruebush TK, McCormick JB, Roberts JM, et al. (1999) 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. Am J Trop Med Hyg 60: 641-648.
28. Maitland K, Williams TN, Newbold CI, (1997) Plasmodium vivax and P. falciparum: biological interactions and the possibility of cross-species immunity. Parasitol Today 13: 227-231.
29. Maitland K, Williams TN, Bennett S, Newbold CI, Peto TEA, et al. (1996) The interaction between Plasmodium falciparum and P. vivax in children on Espiritu Santo Island, Vanuatu. Trans R Soc Trop Med Hyg 90: 614-620.
30. Price RN, Simpson JA, Nosten F, Luxemburger C, Hkirijaroen L, et al. (2001) Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg 65: 614-622.
31. Mayxay M, Pukrittayakamee S, Newton PN, White NJ, (2004) Mixed-species malaria infections in humans. Trends Parasitol 20: 233-240.
32. Lanca EF, Magalhaes BM, Vitor-Silva S, Siqueira AM, Benzecry SG, et al. (2012) Risk factors and characterization of Plasmodium vivax-associated admissions to pediatric intensive care units in the Brazilian Amazon. PLoS ONE 7: e35406 doi:10.1371/journal.pone.0035406.
33. Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, et al. (2008) Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med 5: e128 doi:10.1371/journal.pmed.0050128.
34. Genton B, D'Acremont V, Rare L, Baea K, Reeder JC, et al. (2008) Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med 5: e127 doi:10.1371/journal.pmed.0050127.
35. Barcus MJ, Basri H, Picarima H, Manyakori C, Sekartuti, et al. (2007) Demographic risk factors for severe and fatal vivax and falciparum malaria among hospital admissions in Northeastern Indonesian Papua. Am J Trop Med Hyg 77: 984-991.
36. Poespoprodjo JR, Fobia W, Kenangalem E, Lampah DA, Warikar N, et al. (2008) Adverse pregnancy outcomes in an area where multidrug-resistant Plasmodium vivax and Plasmodium falciparum infections are endemic. Clin Infect Dis 46: 1374-1381.
37. Karyana M, Burdarm L, Yeung S, Kenangalem E, Wariker N, et al. (2008) Epidemiology of multidrug resistant P. vivax and P. falciparum infection in Southern Papua, Indonesia. Malar J 7: 148.
38. Royston P, Altman D, (1994) Regression using fractional polynomials of continuous covariates: parsimonious parametric modelling. Appl Statist 43: 429-467.
39. Greenland S, Drescher K, (1993) Maximum likelihood estimation of the attributable fraction from logistic models. Biometrics 49: 865-872.
40. 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.
41. Hemmer CJ, Holst FGE, Kern P, Chiwakata CB, Dietrich M, et al. (2006) Stronger host response per parasitized erythrocyte in Plasmodium vivax or ovale then in Plasmodium falciparum malaria. Trop Med Int Health 11: 817-823.
42. Yeo TW, Lampah DA, Tjitra E, Piera K, Gitawati R, et al. (2010) Greater endothelial activation, Weibel-Palade body release and host inflammatory response to Plasmodium vivax, compared with Plasmodium falciparum: a prospective study in Papua, Indonesia. J Infect Dis 202: 109-112.
43. Kling PJ, Schmidt RL, Roberts RA, Widness JA, (1996) Serum erythropoietin levels during infancy: associations with erythropoiesis. J Pediatr 128: 791-796.
44. Sachs J, Malaney P, (2002) The economic and social burden of malaria. Nature 415: 680-685.
45. McKenzie FE, Jeffery GM, Collins WE, (2001) Plasmodium malariae blood-stage dynamics. J Parasitol 87: 626-637.
46. McQueen PG, (2010) Population dynamics of a pathogen: the conundrum of vivax malaria. Biophys Rev 2: 111-120.
47. Mueller I, Zimmerman PA, Reeder JC, (2007) Plasmodium malariae and Plasmodium ovale-the "bashful" malaria parasites. Trends Parasitol 23: 278-283.
48. Veenemans J, Andang'o PEA, Mbugi EV, Kraaijenhagen RJ, Mwaniki DL, et al. (2008) Alpha+-thalassemia protects against anemia associated with asymptomatic malaria: evidence from community-based surveys in Tanzania and Kenya. J Infect Dis 198: 401-408.
49. Danquah I, Mockenhaupt FP, (2008) Alpha+-thalassaemia and malarial anaemia. Trends Parasitol 24: 479-481.
50. Fowkes FJI, Allen S, Allen A, Alpers MP, Weatherall DJ, et al. (2008) Increased microerythrocyte count in homozygous alpha+-thalassaemia contributes to protection against severe malarial anaemia. PLoS Med 5: e56 doi:10.1371/journal.pmed.0050056.
51. Williams TN, Maitland K, Bennett S, Ganczakowski M, Peto TE, et al. (1996) High incidence of malaria in alpha-thalassaemic children. Nature 383: 522-525.
52. Kruatrachue M, Charoenlarp P, Chongsuphajaisiddhi T, Harinasuta C, (1962) Erythrocyte glucose-6-phosphate dehydrogenase and malaria in Thailand. Lancet 2: 1183-1186.
53. Kimura M, Soemantri A, Ishida T, (2002) Malaria species and Southeast Asian ovalocytosis defined by a 27-bp deletion in the erythrocyte band 3 gene. Southeast Asian J Trop Med Public Health 33: 4-6.
54. Foo LC, Rekhraj V, Chiang GL, Mak JW, (1992) Ovalocytosis protects against severe malaria parasitemia in the Malayan aborigines. Am J Trop Med Hyg 47: 271-275.
55. Shimizu H, Tamam M, Soemantri A, Ishida T, (2005) Glucose-6-phosphate dehydrogenase deficiency and Southeast Asian ovalocytosis in asymptomatic Plasmodium carriers in Sumba Island, Indonesia. J Hum Genet 50: 420-424.
56. Serjeantson S, Bryson K, Amato D, Babona D, (1977) Malaria and hereditary ovalocytosis. Hum Genet 37: 161-167.
57. Kitchen SF (1939) Malariology. London: W.B. Saunders.
58. Kabyemela ER, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE, (2008) Decreased susceptibility to Plasmodium falciparum infection in pregnant women with iron deficiency. J Infect Dis 198: 163-166.
59. Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, et al. (2007) Epidemiology of Plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 77: 88-98.
60. Nacher M, Singhasivanon P, Yimsamran S, Manibunyong W, Thanyavanich N, et al. (2002) Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J Parasitol 88: 55-58.
61. Spiegel A, Tall A, Raphenon G, Trape JF, Druilhe P, (2003) Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 97: 198-199.
62. Boel M, Carrara VI, Rijken M, Proux S, Nacher M, et al. (2010) Complex interactions between soil-transmitted helminths and malaria in pregnant women on the Thai-Burmese border. PloS Negl Trop Dis 4: e887 doi:10.1371/journal.pntd.0000887.
63. Melo GC, Reyes-Lecca RC, Vitor-Silva S, Monteiro WM, Martins M, et al. (2010) Concurrent helminthic infection protects schoolchildren with Plasmodium vivax from anemia. PLoS ONE 5: e11206 doi:10.1371/journal.pone.0011206.
64. Stoltzfus RJ, Chwaya HM, Montresor A, Albonico M, Savioli L, et al. (2000) 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. J Nutr 130: 1724-1733.
65. Brabin BJ (1991) The risks and severity of malaria in pregnant women. Geneva: World Health Organization.
66. Nosten F, ter Kuile F, Maelankirri L, Decludt B, White NJ, (1991) Malaria during pregnancy in an area of unstable endemicity. Trans R Soc Trop Med Hyg 85: 424-429.