Clinical predictors of severe malarial anaemia in a holoendemic Plasmodium falciparum transmission area: Research paper

British Journal of Haematology

Volumn 149, Issue 5, 2010, Pages 711-721

  Novelli, Enrico M ^a   Hittner, James B ^b   Davenport, Gregory C ^c,d   Ouma, Collins ^d,e   Were, Tom ^d   Obaro, Stephen ^f   Kaplan, Sandra ^a   Ong'Echa, John M ^d,g   Perkins, Douglas J ^d,g  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b School of Business   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF NEW MEXICO   (United States)

^e MASENO UNIVERSITY   (Kenya)

^f MICHIGAN STATE UNIVERSITY   (United States)

^g UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Anaemia; Malaria; Pallor; Plasmodium falciparum; Respiratory distress

Indexed keywords

ANTIANEMIC AGENT; ARTEMETHER PLUS BENFLUMETOL; HEMOGLOBIN; QUININE;

AGE; ANEMIA; ARTICLE; BLOOD TRANSFUSION; CHILD; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; FEVER; HEMOGLOBIN BLOOD LEVEL; HUMAN; INFANT; KENYA; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; MALNUTRITION; MONOCYTOSIS; PALLOR; PARASITE TRANSMISSION; PREDICTION; PRESCHOOL CHILD; PRIORITY JOURNAL; RESPIRATORY DISTRESS; RETICULOCYTOSIS; RISK FACTOR; SPLENOMEGALY; THROMBOCYTOPENIA; VOMITING;

ANEMIA; CHILD, PRESCHOOL; ENDEMIC DISEASES; FEMALE; HUMANS; INFANT; KENYA; MALARIA, FALCIPARUM; MALE; PALLOR; PHYSICAL EXAMINATION; PLATELET COUNT; RETICULOCYTE COUNT; RISK FACTORS;

EID: 77952595648     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2010.08147.x     Document Type: Article

References (60)

1. Abdalla, S. Pasvol, G. (2004) Malaria: a Haematological Perspective. Imperial College Press
2. Aidoo, M., Terlouw, D.J., Kolczak, M.S., McElroy, P.D., ter Kuile, F.O., Kariuki, S., Nahlen, B.L., Lal, A.A. Udhayakumar, V. (2002) Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet, 359, 1311 1312.
3. Akman-Anderson, L., Olivier, M. Luckhart, S. (2007) Induction of nitric oxide synthase and activation of signaling proteins in Anopheles mosquitoes by the malaria pigment, hemozoin. Infection and Immunity, 75, 4012 4019.
4. Awandare, G.A., Ouma, C., Keller, C.C., Were, T., Otieno, R., Ouma, Y., Davenport, G.C., Hittner, J.B., Ong'echa, J.M., Ferrell, R. Perkins, D.J. (2006) A macrophage migration inhibitory factor promoter polymorphism is associated with high-density parasitaemia in children with malaria. Genes and Immunity, 7, 568 575.
5. Awandare, G.A., Ouma, Y., Ouma, C., Were, T., Otieno, R., Keller, C.C., Davenport, G.C., Hittner, J.B., Vulule, J., Ferrell, R., Ong'echa, J.M. Perkins, D.J. (2007) Role of monocyte-acquired haemozoin in suppression of macrophage migration inhibitory factor in children with severe malarial anaemia. Infection and Immunity, 75, 201 210.
6. Beier, J.C., Oster, C.N., Onyango, F.K., Bales, J.D., Sherwood, J.A., Perkins, P.V., Chumo, D.K., Koech, D.V., Whitmire, R.E., Roberts, C.R., Diggs, C.L. Hoffman, S.L. (1994) Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. American Journal of Tropical Medicine and Hygiene, 50, 529 536.
7. Berkley, J., Mwarumba, S., Bramham, K., Lowe, B. Marsh, K. (1999) Bacteraemia complicating severe malaria in children. Transactions of the Royal Society of Tropical Medicine and Hygiene, 93, 283 286.
8. Berkley, J.A., Lowe, B.S., Mwangi, I., Williams, T., Bauni, E., Mwarumba, S., Ngetsa, C., Slack, M.P., Njenga, S., Hart, C.A., Maitland, K., English, M., Marsh, K. Scott, J.A. (2005a) Bacteraemia among children admitted to a rural hospital in Kenya. New England Journal of Medicine, 352, 39 47. (Pubitemid 40075679)
9. Berkley, J., Mwangi, I., Griffiths, K., Ahmed, I., Mithwani, S., English, M., Newton, C. Maitland, K. (2005b) Assessment of severe malnutrition among hospitalized children in rural Kenya: comparison of weight for height and mid upper arm circumference.[see comment]. Journal of the American Medical Association, 294, 591 597.
10. Bienzle, U., Guggenmoos-Holzmann, I. Luzzatto, L. (1979) Malaria and erythrocyte glucose-6-phosphate dehydrogenase variants in West Africa. American Journal of Tropical Medicine and Hygiene, 28, 619 621.
11. Bloland, P.B., Boriga, D.A., Ruebush, T.K., McCormick, J.B., Roberts, J.M., Oloo, A.J., Hawley, W., Lal, A., Nahlen, B. Campbell, C.C. (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. American Journal of Tropical Medicine and Hygiene, 60, 641 648. (Pubitemid 29233123)
12. Breman, J.G., Egan, A. Keusch, G.T. (2001) The intolerable burden of malaria: a new look at the numbers. American Journal of Tropical Medicine and Hygiene, 64, iv vii.
13. Calis, J.C., Phiri, K.S., Faragher, E.B., Brabin, B.J., Bates, I., Cuevas, L.E., de Haan, R.J., Phiri, A.I., Malange, P., Khoka, M., Hulshof, P.J., van Lieshout, L., Beld, M.G., Teo, Y.Y., Rockett, K.A., Richardson, A., Kwiatkowski, D.P., Molyneux, M.E. van Hensbroek, M.B. (2008) Severe anaemia in Malawian children. New England Journal of Medicine, 358, 888 899.
14. Casals-Pascual, C., Kai, O., Cheung, J.O., Williams, S., Lowe, B., Nyanoti, M., Williams, T.N., Maitland, K., Molyneux, M., Newton, C.R., Peshu, N., Watt, S.M. Roberts, D.J. (2006) Suppression of erythropoiesis in malarial anaemia is associated with haemozoin in vitro and in vivo. Blood, 108, 2569 2577.
15. Chalco, J.P., Huicho, L., Alamo, C., Carreazo, N.Y. Bada, C.A. (2005) Accuracy of clinical pallor in the diagnosis of anaemia in children: a meta-analysis. BMC Pediatrics, 5, 46.
16. Diemert, D.J., Bethony, J.M. Hotez, P.J. (2008) Hookworm vaccines. Clinical Infectious Diseases, 46, 282 288.
17. Dzeing-Ella, A., Nze Obiang, P.C., Tchoua, R., Planche, T., Mboza, B., Mbounja, M., Muller-Roemer, U., Jarvis, J., Kendjo, E., Ngou-Milama, E., Kremsner, P.G., Krishna, S. Kombila, M. (2005) Severe falciparum malaria in Gabonese children: clinical and laboratory features. Malaria Journal, 4, 1.
18. English, M., Wale, S., Binns, G., Mwangi, I., Sauerwein, H. Marsh, K. (1998) Hypoglycaemia on and after admission in Kenyan children with severe malaria. Quarterly Journal of Medicine, 91, 191 197.
19. Friedman, J.F., Kwena, A.M., Mirel, L.B., Kariuki, S.K., Terlouw, D.J., Phillips-Howard, P.A., Hawley, W.A., Nahlen, B.L., Shi, Y.P. ter Kuile, F.O. (2005) Malaria and nutritional status among pre-school children: results from cross-sectional surveys in western Kenya. American Journal of Tropical Medicine and Hygiene, 73, 698 704.
20. Graham, S.M., Walsh, A.L., Molyneux, E.M., Phiri, A.J. Molyneux, M.E. (2000) Clinical presentation of non-typhoidal Salmonella bacteraemia in Malawian children. Transactions of the Royal Society of Tropical Medicine and Hygiene, 94, 310 314.
21. Hillman, R.S. Finch, C.A. (1996) Red Cell Manual. F.A. Davis
22. Kahigwa, E., Schellenberg, D., Schellenberg, J.A., Aponte, J.J., Alonso, P.L. Menendez, C. (2002) Inter-observer variation in the assessment of clinical signs in sick Tanzanian children. Transactions of the Royal Society of Tropical Medicine and Hygiene, 96, 162 166.
23. Keller, C.C., Ouma, C., Ouma, Y., Awandare, G.A., Davenport, G.C., Were, T., Hittner, J.B., Vulule, J.M., Ong'Echa, J.M. Perkins, D.J. (2009) Suppression of a novel hematopoietic mediator in children with severe malarial anaemia. Infection and Immunity, 77, 3864 3871.
24. Khanna-Gupta, A. Berliner, N. (2008) Granulocytopoiesis and monocytopoiesis. In : Hematology: Basic Principles and Practice (ed. by R. Hoffman, E.J. Benz, S.J. Shattil, B. Furie, L.E. Silberstein, P. McGlave H. Heslop). Churchill Livingstone/Elsevier
25. Kueh, Y.K. Yeo, K.L. (1982) Haematological alterations in acute malaria. Scandinavian Journal of Haematology, 29, 147 152.
26. Ladhani, S., Lowe, B., Cole, A.O., Kowuondo, K. Newton, C.R. (2002) Changes in white blood cells and platelets in children with falciparum malaria: relationship to disease outcome. British Journal of Haematology, 119, 839 847.
27. Luckner, D., Lell, B., Greve, B., Lehman, L.G., Schmidt- Ott, R.J., Matousek, P., Herbich, K., Schmid, D., Mba, R. Kremsner, P.G. (1998) No influence of socioeconomic factors on severe malarial anaemia, hyperparasitaemia or reinfection. Transactions of the Royal Society of Tropical Medicine and Hygiene, 92, 478 481.
28. Lyke, K.E., Diallo, D.A., Dicko, A., Kone, A., Coulibaly, D., Guindo, A., Cissoko, Y., Sangare, L., Coulibaly, S., Dakouo, B., Taylor, T.E., Doumbo, O.K. Plowe, C.V. (2003) Association of intraleukocytic Plasmodium falciparum malaria pigment with disease severity, clinical manifestations, and prognosis in severe malaria. American Journal of Tropical Medicine and Hygiene, 69, 253 259.
29. Marsh, K., Forster, D., Waruiru, C., Mwangi, I., Winstanley, M., Marsh, V., Newton, C., Winstanley, P., Warn, P., Peshu, N., Pasvol, G. Snow, R. (1995) Indicators of life-threatening malaria in African children.[see comment]. New England Journal of Medicine, 332, 1399 1404.
30. Marx, J. (2002) Rosen's Emergency Medicine: Concepts and Clinical Practice. C.V. Mosby
31. McElroy, P.D., Lal, A.A., Hawley, W.A., Bloland, P.B., Kuile, F.O., Oloo, A.J., Harlow, S.D., Lin, X. Nahlen, B.L. (1999) Analysis of repeated hemoglobin measures in full-term, normal birth weight Kenyan children between birth and four years of age III. The Asemobo Bay Cohort Project. American Journal of Tropical Medicine and Hygiene, 61, 932 940.
32. McElroy, P.D., ter Kuile, F.O., Lal, A.A., Bloland, P.B., Hawley, W.A., Oloo, A.J., Monto, A.S., Meshnick, S.R. Nahlen, B.L. (2000) Effect of Plasmodium falciparum parasitaemia density on haemoglobin concentrations among full-term, normal birth weight children in western Kenya, IV. The Asembo Bay Cohort Project. American Journal of Tropical Medicine and Hygiene, 62, 504 512.
33. McGregor, I.A. (1982) Malaria: nutritional implications. Reviews in Infectious Diseases, 4, 798 804.
34. Metzger, W.G., Mordmuller, B.G. Kremsner, P.G. (1995) Malaria pigment in leucocytes. Transactions of the Royal Society of Tropical Medicine and Hygiene, 89, 637 638.
35. Mockenhaupt, F.P., Ehrhardt, S., Burkhardt, J., Bosomtwe, S.Y., Laryea, S., Anemana, S.D., Otchwemah, R.N., Cramer, J.P., Dietz, E., Gellert, S. Bienzle, U. (2004) Manifestation and outcome of severe malaria in children in northern Ghana. American Journal of Tropical Medicine and Hygiene, 71, 167 172.
36. Mulenga, M., Malunga, P., Bennett, S., Thuma, P.E., Shulman, C., Fielding, K. Greenwood, B.M. (2005) Factors associated with severe anaemia in Zambian children admitted with Plasmodium falciparum malarial anaemia. Annals of Tropical Paediatrics, 25, 87 90.
37. Nguyen, P.H., Day, N., Pram, T.D., Ferguson, D.J. White, N.J. (1995) Intraleucocytic malaria pigment and prognosis in severe malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 89, 200 204.
38. Obonyo, C., Taylor, W., Ogutu, B., Vulule, J. Grobbee, D. (2006) Prevalence of and Risk Factors for Malaria-Associated Anaemia in Young Kenyan Children. University of Utrecht
39. Obonyo, C.O., Vulule, J., Akhwale, W.S. Grobbee, D.E. (2007) In-hospital morbidity and mortality due to severe malarial anaemia in western Kenya. American Journal of Tropical Medicine and Hygiene, 77, 23 28.
40. Ong'echa, J.M., Keller, C.C., Were, T., Ouma, C., Otieno, R.O., Landis-Lewis, Z., Ochiel, D., Slingluff, J.L., Mogere, S., Ogonji, G.A., Orago, A.S., Vulule, J.M., Kaplan, S.S., Day, R.D. Perkins, D.J. (2006) Parasitaemia, anaemia, and malarial anaemia in infants and young children in a rural holoendemic Plasmodium falciparum transmission area. American Journal of Tropical Medicine and Hygiene, 74, 376 385.
41. Otieno, R.O., Ouma, C., Ong'echa, J.M., Keller, C.C., Were, T., Waindi, E.N., Michaels, M.G., Day, R.D., Vulule, J.M. Perkins, D.J. (2006) Increased severe anaemia in HIV-1-exposed and HIV-1-positive infants and children during acute malaria. AIDS, 20, 275 280.
42. Ouedraogo, H.Z., Zeba, A., Dramaix-Wilmet, M. Donnen, P. (2008) Moderate-to-severe anaemia due to afebrile Plasmodium falciparum infection in children aged 6-23 months from the rural district of Kongoussi, Burkina Faso. Journal of Tropical Pediatrics, 54, 395 400.
43. Ouma, C., Keller, C.C., Opondo, D.A., Were, T., Otieno, R.O., Otieno, M.F., Orago, A.S., Ong'Echa, J.M., Vulule, J.M., Ferrell, R.E. Perkins, D.J. (2006) Association of FCgamma receptor IIA (CD32) polymorphism with malarial anemia and high-density parasitemia in infants and young children. American Journal of Tropical Medicine and Hygiene, 74, 573 577.
44. Ouma, C., Davenport, G.C., Were, T., Otieno, M.F., Hittner, J.B., Vulule, J.M., Martinson, J., Ong'echa, J.M., Ferrell, R.E. Perkins, D.J. (2008) Haplotypes of IL-10 promoter variants are associated with susceptibility to severe malarial anaemia and functional changes in IL-10 production. Human Genetics, 124, 515 524.
45. Ouma, C., Keller, C.C., Davenport, G.C., Were, T., Konah, S., Otieno, M.F., Hittner, J.B., Vulule, J.M., Martinson, J., Ong'echa, J.M., Ferrell, R.E. Perkins, D.J. (2010) A novel functional variant in the stem cell growth factor promoter protects against severe malarial anemia. Infection and Immunity, 78, 453 460.
46. Pathirana, S.L., Alles, H.K., Bandara, S., Phone-Kyaw, M., Perera, M.K., Wickremasinghe, A.R., Mendis, K.N. Handunnetti, S.M. (2005) ABO-blood-group types and protection against severe, Plasmodium falciparum malaria. Annals of Tropical Medicine and Parasitology, 99, 119 124.
47. Prato, M., Gallo, V., Giribaldi, G. Arese, P. (2008) Phagocytosis of haemozoin (malarial pigment) enhances metalloproteinase-9 activity in human adherent monocytes: role of IL-1beta and 15-HETE. Malaria Journal, 7, 157.
48. Raper, A.B. (1955) Malaria and the sickling trait. British Medical Journal, 1, 1186 1189.
49. Rowe, J.A., Handel, I.G., Thera, M.A., Deans, A.-M., Lyke, K.E., Kone, A., Diallo, D.A., Raza, A., Kai, O., Marsh, K., Plowe, C.V., Doumbo, O.K. Moulds, J.M. (2007) Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proceedings of the National Academy of Sciences of the United States of America, 104, 17471 17476.
50. Snow, R.W., Craig, M.H., Deichmann, U. le Sueur, D. (1999a) A preliminary continental risk map for malaria mortality among African children. Parasitology Today, 15, 99 104.
51. Snow, R.W., Craig, M., Deichmann, U. Marsh, K. (1999b) Estimating mortality, morbidity and disability due to malaria among Africa's non-pregnant population. Bulletin of the World Health Organization, 77, 624 640.
52. Verhoef, H., West, C.E., Veenemans, J., Beguin, Y. Kok, F.J. (2002) Stunting may determine the severity of malaria-associated anaemia in African children. Pediatrics, 110, e48.
53. Walsh, A.L., Phiri, A.J., Graham, S.M., Molyneux, E.M. Molyneux, M.E. (2000) Bacteraemia in febrile Malawian children: clinical and microbiologic features. Pediatric Infectious Disease Journal, 19, 312 318.
54. Warrell, D., Molyneux, M. Beales, P. (1990) Severe and complicated malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 84, 1 65.
55. Were, T., Hittner, J.B., Ouma, C., Otieno, R.O., Orago, A.S.S., Ong'echa, J.M., Vulule, J.M., Keller, C.C. Perkins, D.J. (2006) Suppression of RANTES in children with Plasmodium falciparum malaria. [erratum appears in Haematologica. 2007 Jan;92(1):136 Note: Hittner, J B [added]]. Haematologica, 91, 1396 1399.
56. Were, T., Davenport, G.C., Yamo, E.O., Hittner, J.B., Awandare, G.A., Otieno, M.F., Ouma, C., Orago, A.S., Vulule, J.M., Ong'echa, J.M. Perkins, D.J. (2009) Naturally acquired haemozoin by monocytes promotes suppression of RANTES in children with malarial anaemia through an IL-10-dependent mechanism. Microbes and Infection, 11, 811 819.
57. Whitelaw, D.M. (1966) The intravascular lifespan of monocytes. Blood, 28, 455 464.
58. WHO (2000) Severe falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 94 (Suppl. 1 S1 S90.
59. WHO (2005) WHO. World Malaria Report 2005. World Health Organization/United Nations Children's Fund
60. Zamora, F., Ramirez, O., Vergara, J., Arevalo-Herrera, M. Herrera, S. (2005) Haemoglobin levels related to days of illness, race, and Plasmodium species in Colombian patients with uncomplicated malaria. American Journal of Tropical Medicine and Hygiene, 73, 50 54.