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Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Research

Haemoglobin dynamics in Papuan and non-Papuan adults in northeast Papua, Indonesia, with acute, uncomplicated vivax or falciparum malaria

Authors: Walter RJ Taylor, Hendra Widjaja, Hasan Basri, Emiliana Tjitra, Colin Ohrt, Taufik Taufik, Samuel Baso, Stephen L Hoffman, Thomas L Richie

Published in: Malaria Journal | Issue 1/2013

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Abstract

Background

Haemoglobin (Hb) recovers slowly in malaria and may be influenced by naturally acquired immunity. Hb recovery was compared in malaria immune, indigenous Papuan and non-Papuan adults with limited malaria exposure.

Methods

Hb concentrations were measured on Days (D) 0, 3, 7, and 28 in 57 Papuans and 105 non-Papuans treated with chloroquine, doxycycline or both drugs for acute, uncomplicated Plasmodium vivax (n?=?64) or Plasmodium falciparum (n?=?98).

Results

Mean (SD, range) D0 Hb was 12.7 (2.2, 7–21.3) g/dL and was similar in P. falciparum infected Papuans and non-Papuans: 12.2 vs. 12.8 g/dL (P?=?0.15) but significantly lower in: (i) P. vivax-infected Papuans vs. P. vivax-infected non-Papuans: 11.4 vs. 13.47 g/dL [∆?=?−2.07 (95% CI: –3.3 – –0.8), P?=?0.0018], (ii) all patients with splenomegaly (vs. those without splenomegaly): 12.16 vs. 13.01 g/dL [∆?=?−0.85 (−1.6– –0.085), P?=?0.029], and (iii) all females vs. all males: 10.18 vs. 13.01 g/dL [∆?=?−2.82 (−3.97 – –1.67), P?<?0.0001].Multiple regression identified female sex (P?=?0.000), longer illness duration (P?=?0.015) (P. falciparum patients) and Papuan ethnicity (P?=?0.017) (P. vivax patients) as significant factors for a lower D0 Hb.
Mean D28 Hb increased to 13.6 g/dL [∆?=?1.01 (0.5-1.5) vs. D0 Hb, P?=?0.0001]. It was: (i) positively correlated with the D0 Hb (adjusted R2?=?0.24, P?=?0.000), and was significantly lower in P. vivax infected Papuans vs. non-Papuans: 12.71 vs. 14.46 g/dL [∆?=?−1.7 (−2.95– –0.5, P?=?0.006).

Conclusions

Haemoglobin recovery was related to baseline Hb. Vivax-infected malaria immune Papuans had persistently lower Hb concentrations compared to non-Papuans with limited malaria exposure. This haematological disadvantage remains unexplained.
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Literature
1.
go back to reference Wickramasinghe SN, Abdalla SH: Blood and bone marrow changes in malaria. Baillieres Best Pract Res Clin Haematol. 2000, 13: 277-299. 10.1053/beha.1999.0072.CrossRefPubMed Wickramasinghe SN, Abdalla SH: Blood and bone marrow changes in malaria. Baillieres Best Pract Res Clin Haematol. 2000, 13: 277-299. 10.1053/beha.1999.0072.CrossRefPubMed
2.
go back to reference Price RN, Simpson JA, Nosten F, Luxemburger C, Hkirjaroen L, ter Kuile F, Chongsuphajaisiddhi T, White NJ: Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg. 2001, 65: 614-622.PubMedCentralPubMed Price RN, Simpson JA, Nosten F, Luxemburger C, Hkirjaroen L, ter Kuile F, Chongsuphajaisiddhi T, White NJ: Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg. 2001, 65: 614-622.PubMedCentralPubMed
3.
go back to reference Bruneel F, Gachot B, Wolff M, Regnier B, Danis M, Vachon F: Resurgence of blackwater fever in long-term European expatriates in Africa: report of 21 cases and review. Clin Infect Dis. 2001, 32: 1133-1140. 10.1086/319743.CrossRefPubMed Bruneel F, Gachot B, Wolff M, Regnier B, Danis M, Vachon F: Resurgence of blackwater fever in long-term European expatriates in Africa: report of 21 cases and review. Clin Infect Dis. 2001, 32: 1133-1140. 10.1086/319743.CrossRefPubMed
4.
go back to reference van Eijk AM, Ayisi JG, Ter erKuile FO, Misore AO, Otieno JA, Kolczak MS, Kager PA, Steketee RW, Nahlen BL: Malaria and human immunodeficiency virus infection as risk factors for anemia in infants in Kisumu, western Kenya. Am J Trop Med Hyg. 2002, 67: 44-53.PubMed van Eijk AM, Ayisi JG, Ter erKuile FO, Misore AO, Otieno JA, Kolczak MS, Kager PA, Steketee RW, Nahlen BL: Malaria and human immunodeficiency virus infection as risk factors for anemia in infants in Kisumu, western Kenya. Am J Trop Med Hyg. 2002, 67: 44-53.PubMed
5.
go back to reference Dreyfuss ML, Stoltzfus RJ, Shrestha JB, Pradhan EK, LeClerq SC, Khatry SK, Shrestha SR, Katz J, Albonico M, West KP: Hookworms, malaria and vitamin A deficiency contribute to anemia and iron deficiency among pregnant women in the plains of Nepal. J Nutr. 2000, 130: 2527-2536.PubMed Dreyfuss ML, Stoltzfus RJ, Shrestha JB, Pradhan EK, LeClerq SC, Khatry SK, Shrestha SR, Katz J, Albonico M, West KP: Hookworms, malaria and vitamin A deficiency contribute to anemia and iron deficiency among pregnant women in the plains of Nepal. J Nutr. 2000, 130: 2527-2536.PubMed
6.
go back to reference Looareesuwan S, Davis TM, Pukrittayakamee S, Supanaranond W, Desakorn V, Silamut K, Krishna S, Boonamrung S, White NJ: Erythrocyte survival in severe falciparum malaria. Acta Trop. 1991, 48: 263-270. 10.1016/0001-706X(91)90014-B.CrossRefPubMed Looareesuwan S, Davis TM, Pukrittayakamee S, Supanaranond W, Desakorn V, Silamut K, Krishna S, Boonamrung S, White NJ: Erythrocyte survival in severe falciparum malaria. Acta Trop. 1991, 48: 263-270. 10.1016/0001-706X(91)90014-B.CrossRefPubMed
7.
go back to reference Anstey NM, Russell B, Yeo TW, Price RN: The pathophysiology of vivax malaria. Trends Parasitol. 2009, 25: 220-227. 10.1016/j.pt.2009.02.003.CrossRefPubMed Anstey NM, Russell B, Yeo TW, Price RN: The pathophysiology of vivax malaria. Trends Parasitol. 2009, 25: 220-227. 10.1016/j.pt.2009.02.003.CrossRefPubMed
8.
go back to reference Hue NT, Charlieu JP, Chau TT, Day N, Farrar JJ, Hien TT, Dunstan SJ: Glucose-6-phosphate dehydrogenase (G6PD) mutations and haemoglobinuria syndrome in the Vietnamese population. Malar J. 2009, 8: 152-10.1186/1475-2875-8-152.PubMedCentralCrossRefPubMed Hue NT, Charlieu JP, Chau TT, Day N, Farrar JJ, Hien TT, Dunstan SJ: Glucose-6-phosphate dehydrogenase (G6PD) mutations and haemoglobinuria syndrome in the Vietnamese population. Malar J. 2009, 8: 152-10.1186/1475-2875-8-152.PubMedCentralCrossRefPubMed
9.
go back to reference Luzzatto L: The rise and fall of the antimalarial Lapdap: a lesson in pharmacogenetics. Lancet. 2010, 376: 739-741. 10.1016/S0140-6736(10)60396-0.CrossRefPubMed Luzzatto L: The rise and fall of the antimalarial Lapdap: a lesson in pharmacogenetics. Lancet. 2010, 376: 739-741. 10.1016/S0140-6736(10)60396-0.CrossRefPubMed
10.
go back to reference Collins WE, Jeffery GM, Roberts JM: A retrospective examination of anemia during infection of humans with Plasmodium vivax. Am J Trop Med Hyg. 2003, 68: 410-412.PubMed Collins WE, Jeffery GM, Roberts JM: A retrospective examination of anemia during infection of humans with Plasmodium vivax. Am J Trop Med Hyg. 2003, 68: 410-412.PubMed
11.
go back to reference Jakeman GN, Saul A, Hogarth WL, Collins WE: Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology. 1999, 119 (Pt 2): 127-133.CrossRefPubMed Jakeman GN, Saul A, Hogarth WL, Collins WE: Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology. 1999, 119 (Pt 2): 127-133.CrossRefPubMed
12.
go back to reference Looareesuwan S, Ho M, Wattanagoon Y, White NJ, Warrell DA, Bunnag D, Harinasuta T, Wyler DJ: Dynamic alteration in splenic function during acute falciparum malaria. N Engl J Med. 1987, 317: 675-679. 10.1056/NEJM198709103171105.CrossRefPubMed Looareesuwan S, Ho M, Wattanagoon Y, White NJ, Warrell DA, Bunnag D, Harinasuta T, Wyler DJ: Dynamic alteration in splenic function during acute falciparum malaria. N Engl J Med. 1987, 317: 675-679. 10.1056/NEJM198709103171105.CrossRefPubMed
13.
14.
go back to reference Lamikanra AA, Brown D, Potocnik A, Casals-Pascual C, Langhorne J, Roberts DJ: Malarial anemia: of mice and men. Blood. 2007, 110: 18-28. 10.1182/blood-2006-09-018069.CrossRefPubMed Lamikanra AA, Brown D, Potocnik A, Casals-Pascual C, Langhorne J, Roberts DJ: Malarial anemia: of mice and men. Blood. 2007, 110: 18-28. 10.1182/blood-2006-09-018069.CrossRefPubMed
15.
go back to reference Dondorp AM, Nyanoti M, Kager PA, Mithwani S, Vreeken J, Marsh K: The role of reduced red cell deformability in the pathogenesis of severe falciparum malaria and its restoration by blood transfusion. Trans R Soc Trop Med Hyg. 2002, 96: 282-286. 10.1016/S0035-9203(02)90100-8.CrossRefPubMed Dondorp AM, Nyanoti M, Kager PA, Mithwani S, Vreeken J, Marsh K: The role of reduced red cell deformability in the pathogenesis of severe falciparum malaria and its restoration by blood transfusion. Trans R Soc Trop Med Hyg. 2002, 96: 282-286. 10.1016/S0035-9203(02)90100-8.CrossRefPubMed
16.
go back to reference Dondorp AM, Angus BJ, Chotivanich K, Silamut K, Ruangveerayuth R, Hardeman MR, Kager PA, Vreeken J, White NJ: Red blood cell deformability as a predictor of anemia in severe falciparum malaria. Am J Trop Med Hyg. 1999, 60: 733-737.PubMed Dondorp AM, Angus BJ, Chotivanich K, Silamut K, Ruangveerayuth R, Hardeman MR, Kager PA, Vreeken J, White NJ: Red blood cell deformability as a predictor of anemia in severe falciparum malaria. Am J Trop Med Hyg. 1999, 60: 733-737.PubMed
17.
go back to reference Handayani S, Chiu DT, Tjitra E, Kuo JS, Lampah D, Kenangalem E, Renia L, Snounou G, Price RN, Anstey NM, Russell B: High deformability of Plasmodium vivax-infected red blood cells under micro fluidic conditions. J Infect Dis. 2009, 199: 445-450. 10.1086/596048.PubMedCentralCrossRefPubMed Handayani S, Chiu DT, Tjitra E, Kuo JS, Lampah D, Kenangalem E, Renia L, Snounou G, Price RN, Anstey NM, Russell B: High deformability of Plasmodium vivax-infected red blood cells under micro fluidic conditions. J Infect Dis. 2009, 199: 445-450. 10.1086/596048.PubMedCentralCrossRefPubMed
18.
go back to reference Angus BJ, Chotivanich K, Udomsangpetch R, White NJ: In vivo removal of malaria parasites from red blood cells without their destruction in acute falciparum malaria. Blood. 1997, 90: 2037-2040.PubMed Angus BJ, Chotivanich K, Udomsangpetch R, White NJ: In vivo removal of malaria parasites from red blood cells without their destruction in acute falciparum malaria. Blood. 1997, 90: 2037-2040.PubMed
19.
go back to reference Newton PN, Chotivanich K, Chierakul W, Ruangveerayuth R, Teerapong P, Silamut K, Looareesuwan S, White NJ: A comparison of the in vivo kinetics of Plasmodium falciparum ring-infected erythrocyte surface antigen-positive and -negative erythrocytes. Blood. 2001, 98: 450-457. 10.1182/blood.V98.2.450.CrossRefPubMed Newton PN, Chotivanich K, Chierakul W, Ruangveerayuth R, Teerapong P, Silamut K, Looareesuwan S, White NJ: A comparison of the in vivo kinetics of Plasmodium falciparum ring-infected erythrocyte surface antigen-positive and -negative erythrocytes. Blood. 2001, 98: 450-457. 10.1182/blood.V98.2.450.CrossRefPubMed
20.
go back to reference Phillips RE, Looareesuwan S, Warrell DA, Lee SH, Karbwang J, Warrell MJ, White NJ, Swasdichai C, Weatherall DJ: The importance of anaemia in cerebral and uncomplicated falciparum malaria: role of complications, dyserythropoiesis and iron sequestration. Q J Med. 1986, 58: 305-323.PubMed Phillips RE, Looareesuwan S, Warrell DA, Lee SH, Karbwang J, Warrell MJ, White NJ, Swasdichai C, Weatherall DJ: The importance of anaemia in cerebral and uncomplicated falciparum malaria: role of complications, dyserythropoiesis and iron sequestration. Q J Med. 1986, 58: 305-323.PubMed
21.
go back to reference Clark IA, Chaudhri G: Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythro phagocytosis. Br J Haematol. 1988, 70: 99-103. 10.1111/j.1365-2141.1988.tb02440.x.CrossRefPubMed Clark IA, Chaudhri G: Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythro phagocytosis. Br J Haematol. 1988, 70: 99-103. 10.1111/j.1365-2141.1988.tb02440.x.CrossRefPubMed
22.
go back to reference Othoro C, Lal AA, Nahlen B, Koech D, Orago AS, Udhayakumar V: A low interleukin-10 tumor necrosis factor-alpha ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya. J Infect Dis. 1999, 179: 279-282. 10.1086/314548.CrossRefPubMed Othoro C, Lal AA, Nahlen B, Koech D, Orago AS, Udhayakumar V: A low interleukin-10 tumor necrosis factor-alpha ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya. J Infect Dis. 1999, 179: 279-282. 10.1086/314548.CrossRefPubMed
23.
go back to reference Casals-Pascual C, Kai O, Cheung JO, Williams S, Lowe B, Nyanoti M, Williams TN, Maitland K, Molyneux M, Newton CR, Peshu N, Watt SM, Roberts DJ: Suppression of erythropoiesis in malarial anemia is associated with hemozoin in vitro and in vivo. Blood. 2006, 108: 2569-2577. 10.1182/blood-2006-05-018697.CrossRefPubMed Casals-Pascual C, Kai O, Cheung JO, Williams S, Lowe B, Nyanoti M, Williams TN, Maitland K, Molyneux M, Newton CR, Peshu N, Watt SM, Roberts DJ: Suppression of erythropoiesis in malarial anemia is associated with hemozoin in vitro and in vivo. Blood. 2006, 108: 2569-2577. 10.1182/blood-2006-05-018697.CrossRefPubMed
24.
go back to reference Kurtzhals JA, Rodrigues O, Addae M, Commey JO, Nkrumah FK, Hviid L: Reversible suppression of bone marrow response to erythropoietin in Plasmodium falciparum malaria. Br J Haematol. 1997, 97: 169-174. 10.1046/j.1365-2141.1997.82654.x.CrossRefPubMed Kurtzhals JA, Rodrigues O, Addae M, Commey JO, Nkrumah FK, Hviid L: Reversible suppression of bone marrow response to erythropoietin in Plasmodium falciparum malaria. Br J Haematol. 1997, 97: 169-174. 10.1046/j.1365-2141.1997.82654.x.CrossRefPubMed
25.
go back to reference Burgmann H, Looareesuwan S, Kapiotis S, Viravan C, Vanijanonta S, Hollenstein U, Wiesinger E, Presterl E, Winkler S, Graninger W: Serum levels of erythropoietin in acute Plasmodium falciparum malaria. Am J Trop Med Hyg. 1996, 54: 280-283.PubMed Burgmann H, Looareesuwan S, Kapiotis S, Viravan C, Vanijanonta S, Hollenstein U, Wiesinger E, Presterl E, Winkler S, Graninger W: Serum levels of erythropoietin in acute Plasmodium falciparum malaria. Am J Trop Med Hyg. 1996, 54: 280-283.PubMed
26.
go back to reference Nussenblatt V, Mukasa G, Metzger A, Ndeezi G, Garrett E, Semba RD: Anemia and interleukin-10, tumor necrosis factor alpha, and erythropoietin levels among children with acute, uncomplicated Plasmodium falciparum malaria. Clin Diagn Lab Immunol. 2001, 8: 1164-1170.PubMedCentralPubMed Nussenblatt V, Mukasa G, Metzger A, Ndeezi G, Garrett E, Semba RD: Anemia and interleukin-10, tumor necrosis factor alpha, and erythropoietin levels among children with acute, uncomplicated Plasmodium falciparum malaria. Clin Diagn Lab Immunol. 2001, 8: 1164-1170.PubMedCentralPubMed
27.
go back to reference Camacho LH, Gordeuk VR, Wilairatana P, Pootrakul P, Brittenham GM, Looareesuwan S: The course of anaemia after the treatment of acute, falciparum malaria. Ann Trop Med Parasitol. 1998, 92: 525-537. 10.1080/00034989859221.CrossRefPubMed Camacho LH, Gordeuk VR, Wilairatana P, Pootrakul P, Brittenham GM, Looareesuwan S: The course of anaemia after the treatment of acute, falciparum malaria. Ann Trop Med Parasitol. 1998, 92: 525-537. 10.1080/00034989859221.CrossRefPubMed
28.
go back to reference Mayxay M, Khanthavong M, Lindegardh N, Keola S, Barends M, Pongvongsa T, Yapom R, Annerberg A, Phompida S, Phetsouvanh R, White NJ, Newton PN: Randomized comparison of chloroquine plus sulfadoxine-pyrimethamine versus artesunate plus mefloquine versus artemether-lumefantrine in the treatment of uncomplicated falciparum malaria in the Lao People's Democratic Republic. Clin Infect Dis. 2004, 39: 1139-1147. 10.1086/424512.CrossRefPubMed Mayxay M, Khanthavong M, Lindegardh N, Keola S, Barends M, Pongvongsa T, Yapom R, Annerberg A, Phompida S, Phetsouvanh R, White NJ, Newton PN: Randomized comparison of chloroquine plus sulfadoxine-pyrimethamine versus artesunate plus mefloquine versus artemether-lumefantrine in the treatment of uncomplicated falciparum malaria in the Lao People's Democratic Republic. Clin Infect Dis. 2004, 39: 1139-1147. 10.1086/424512.CrossRefPubMed
29.
go back to reference Srichaikul T, Panikbutr N, Jeumtrakul P: Bone-marrow changes in human malaria. Ann Trop Med Parasitol. 1967, 61: 40-51.PubMed Srichaikul T, Panikbutr N, Jeumtrakul P: Bone-marrow changes in human malaria. Ann Trop Med Parasitol. 1967, 61: 40-51.PubMed
30.
go back to reference Premji Z, Hamisi Y, Shiff C, Minjas J, Lubega P, Makwaya C: Anaemia and Plasmodium falciparum infections among young children in an holoendemic area, Bagamoyo, Tanzania. Acta Trop. 1995, 59: 55-64. 10.1016/0001-706X(94)00079-G.CrossRefPubMed Premji Z, Hamisi Y, Shiff C, Minjas J, Lubega P, Makwaya C: Anaemia and Plasmodium falciparum infections among young children in an holoendemic area, Bagamoyo, Tanzania. Acta Trop. 1995, 59: 55-64. 10.1016/0001-706X(94)00079-G.CrossRefPubMed
31.
go back to reference Bloland PB, Boriga DA, Ruebush TK, McCormick JB, Roberts JM, Oloo AJ, Hawley W, Lal A, Nahlen B, Campbell CC: 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. 1999, 60: 641-648.PubMed Bloland PB, Boriga DA, Ruebush TK, McCormick JB, Roberts JM, Oloo AJ, Hawley W, Lal A, Nahlen B, Campbell CC: 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. 1999, 60: 641-648.PubMed
32.
go back to reference Baird JK, Purnomo , Basri H, Bangs MJ, Andersen EM, Jones TR, Masbar S, Harjosuwarno S, Subianto B, Arbani PR: Age-specific prevalence of Plasmodium falciparum among six populations with limited histories of exposure to endemic malaria. Am J Trop Med Hyg. 1993, 49: 707-719.PubMed Baird JK, Purnomo , Basri H, Bangs MJ, Andersen EM, Jones TR, Masbar S, Harjosuwarno S, Subianto B, Arbani PR: Age-specific prevalence of Plasmodium falciparum among six populations with limited histories of exposure to endemic malaria. Am J Trop Med Hyg. 1993, 49: 707-719.PubMed
33.
go back to reference Baird JK, Jones TR, Danudirgo EW, Annis BA, Bangs MJ, Basri H, Purnomo , Masbar S: Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. AmJTrop Med Hyg. 1991, 45: 65-76. Baird JK, Jones TR, Danudirgo EW, Annis BA, Bangs MJ, Basri H, Purnomo , Masbar S: Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. AmJTrop Med Hyg. 1991, 45: 65-76.
34.
go back to reference Taylor WR, Widjaja H, Richie TL, Basri H, Ohrt C, Tjitra , Taufik E, Jones TR, Kain KC, Hoffman SL: Chloroquine/doxycycline combination versus chloroquine alone, and doxycycline alone for the treatment of Plasmodium falciparum and Plasmodium vivax malaria in northeastern Irian Jaya, Indonesia. AmJTrop Med Hyg. 2001, 64: 223-228. Taylor WR, Widjaja H, Richie TL, Basri H, Ohrt C, Tjitra , Taufik E, Jones TR, Kain KC, Hoffman SL: Chloroquine/doxycycline combination versus chloroquine alone, and doxycycline alone for the treatment of Plasmodium falciparum and Plasmodium vivax malaria in northeastern Irian Jaya, Indonesia. AmJTrop Med Hyg. 2001, 64: 223-228.
35.
go back to reference Taylor WR, Widjaja H, Basri H, Ohrt C, Taufik T, Tjitra E, Baso S, Fryauff D, Hoffman SL, Richie TL: Changes in the total leukocyte and platelet counts in Papuan and non Papuan adults from northeast Papua infected with acute Plasmodium vivax or uncomplicated Plasmodium falciparum malaria. Malar J. 2008, 7: 259-10.1186/1475-2875-7-259.PubMedCentralCrossRefPubMed Taylor WR, Widjaja H, Basri H, Ohrt C, Taufik T, Tjitra E, Baso S, Fryauff D, Hoffman SL, Richie TL: Changes in the total leukocyte and platelet counts in Papuan and non Papuan adults from northeast Papua infected with acute Plasmodium vivax or uncomplicated Plasmodium falciparum malaria. Malar J. 2008, 7: 259-10.1186/1475-2875-7-259.PubMedCentralCrossRefPubMed
36.
go back to reference Jones TR, Baird JK, Basri H, Purnomo , Danudirgo EW: Prevalence of malaria in native and transmigrant populations. Effects of age and history of exposure. Trop Geogr Med. 1991, 43: 1-6.PubMed Jones TR, Baird JK, Basri H, Purnomo , Danudirgo EW: Prevalence of malaria in native and transmigrant populations. Effects of age and history of exposure. Trop Geogr Med. 1991, 43: 1-6.PubMed
37.
go back to reference WHO: Iron deficiency anaemia: assessment, prevention and control: a guide for programme managers. 2001, Geneva: World Health Organization WHO: Iron deficiency anaemia: assessment, prevention and control: a guide for programme managers. 2001, Geneva: World Health Organization
38.
go back to reference Poravuth Y, Socheat D, Rueangweerayut R, Uthaisin C, Pyae Phyo A, Valecha N, Rao BH, Tjitra E, Purnama A, Borghini-Fuhrer I, Duparc S, Shin CS, Fleckenstein L: Pyronaridine-artesunate versus chloroquine in patients with acute Plasmodium vivax malaria: a randomized, double-blind, non-inferiority trial. PLoS One. 2011, 6: e14501-10.1371/journal.pone.0014501.PubMedCentralCrossRefPubMed Poravuth Y, Socheat D, Rueangweerayut R, Uthaisin C, Pyae Phyo A, Valecha N, Rao BH, Tjitra E, Purnama A, Borghini-Fuhrer I, Duparc S, Shin CS, Fleckenstein L: Pyronaridine-artesunate versus chloroquine in patients with acute Plasmodium vivax malaria: a randomized, double-blind, non-inferiority trial. PLoS One. 2011, 6: e14501-10.1371/journal.pone.0014501.PubMedCentralCrossRefPubMed
39.
go back to reference Douglas NM, Anstey NM, Buffet PA, Poespoprodjo JR, Yeo TW, White NJ, Price RN: The anaemia of Plasmodium vivax malaria. Malar J. 2012, 11: 135-10.1186/1475-2875-11-135.PubMedCentralCrossRefPubMed Douglas NM, Anstey NM, Buffet PA, Poespoprodjo JR, Yeo TW, White NJ, Price RN: The anaemia of Plasmodium vivax malaria. Malar J. 2012, 11: 135-10.1186/1475-2875-11-135.PubMedCentralCrossRefPubMed
Metadata
Title
Haemoglobin dynamics in Papuan and non-Papuan adults in northeast Papua, Indonesia, with acute, uncomplicated vivax or falciparum malaria
Authors
Walter RJ Taylor
Hendra Widjaja
Hasan Basri
Emiliana Tjitra
Colin Ohrt
Taufik Taufik
Samuel Baso
Stephen L Hoffman
Thomas L Richie
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-209

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