Severity of anaemia is associated with bone marrow haemozoin in children exposed to Plasmodium falciparum

British Journal of Haematology

Volumn 164, Issue 6, 2014, Pages 877-887

  Aguilar, Ruth ^a,b,c   Moraleda, Cinta ^a,c   Achtman, Ariel H ^d,e   Mayor, Alfredo ^a,b   Quintó, Llorenç ^a   Cisteró, Pau ^a   Nhabomba, Augusto ^c   Macete, Eusebio ^c   Schofield, Louis ^d,e   Alonso, Pedro L ^a,c   Menéndez, Clara ^a,c  

^a CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^b CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^c Manhiça Health Research Center   (Mozambique)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Anaemia; Bone marrow; Dyserythropoiesis; Haemozoin; Plasmodium falciparum

Indexed keywords

HEMOGLOBIN; HEMOZOIN;

ANEMIA; ARTICLE; BLOODSTREAM INFECTION; BONE MARROW EXAMINATION; CHILD; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; DRUG TARGETING; DYSERYTHROPOIESIS; EX VIVO STUDY; EXPOSURE; FEMALE; GAMETOCYTE; HEMOGLOBIN BLOOD LEVEL; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; MICROSCOPY; MOZAMBIQUE; NONHUMAN; PARASITE EXAMINATION; PARASITEMIA; PATHOGENESIS; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SCHIZONT; TROPHOZOITE;

ANAEMIA; BONE MARROW; DYSERYTHROPOIESIS; HAEMOZOIN; PLASMODIUM FALCIPARUM;

ADULT; ANEMIA; BONE MARROW; CASE-CONTROL STUDIES; FEMALE; HEMEPROTEINS; HUMANS; MALARIA, FALCIPARUM; MALE; PLASMODIUM FALCIPARUM; YOUNG ADULT;

EID: 84896715750     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12716     Document Type: Article

References (56)

1. Abdalla, S.H. (1990) Hematopoiesis in human malaria. Blood Cells, 16, 401-416. discussion 417-409.
2. Abdalla, S., Weatherall, D.J., Wickramasinghe, S.N. & Hughes, M. (1980) The anaemia of P. falciparum malaria. British Journal of Haematology, 46, 171-183.
3. Abdulsalam, A.H., Sabeeh, N. & Bain, B.J. (2010) Immature Plasmodium falciparum gametocytes in bone marrow. American Journal of Hematology, 85, 943.
4. Aguilar, R., Moraleda, C., Quinto, L., Renom, M., Mussacate, L., Macete, E., Aguilar, J.L., Alonso, P.L. & Menendez, C. (2012) Challenges in the diagnosis of iron deficiency in children exposed to high prevalence of infections. PLoS One, 7, e50584.
5. Akinosoglou, K.S., Solomou, E.E. & Gogos, C.A. (2012) Malaria: a haematological disease. Hematology, 17, 106-114.
6. Alano, P. (2007) Plasmodium falciparum gametocytes: still many secrets of a hidden life. Molecular Microbiology, 66, 291-302.
7. Alonso, P.L., Smith, T., Schellenberg, J.R., Masanja, H., Mwankusye, S., Urassa, H., Bastos de Azevedo, I., Chongela, J., Kobero, S., Menendez, C., Hurt, N., Thomas, M.C., Lyimo, E., Weiss, N.A., Hayes, R., Kitua, A.Y., López, M.C., Kilama, W.L., Teuscher, T. & Tanner, M. (1994) Randomised trial of efficacy of SPf66 vaccine against Plasmodium falciparum malaria in children in southern Tanzania. Lancet, 344, 1175-1181.
8. Alonso, P., Saute, F., Aponte, J.J., Gomez-Olive, F.X., Nhacolo, A., Thomson, R., Macete, E., Abacassamo, F., Ventura, P.J., Bosch, X., Menendez, C. & Dgedge, M. (2001) Population, Health and Survival at INDEPTH Sites, Vol. 1. Manhica DSS, Mozambique, pp. 189-195. International Development Research Centre, Ottawa, Ontario, Canada.
9. 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 hemozoin in suppression of macrophage migration inhibitory factor in children with severe malarial anemia. Infection and Immunity, 75, 201-210.
10. Awandare, G.A., Kempaiah, P., Ochiel, D.O., Piazza, P., Keller, C.C. & Perkins, D.J. (2011) Mechanisms of erythropoiesis inhibition by malarial pigment and malaria-induced proinflammatory mediators in an in vitro model. American Journal of Hematology, 86, 155-162.
11. Bain, B.J. (2001) Bone marrow aspiration. Journal of Clinical Pathology, 54, 657-663.
12. Beeson, J.G. & Brown, G.V. (2002) Pathogenesis of Plasmodium falciparum malaria: the roles of parasite adhesion and antigenic variation. Cellular and Molecular Life Sciences, 59, 258-271.
13. Beeson, J.G., Amin, N., Kanjala, M. & Rogerson, S.J. (2002) Selective accumulation of mature asexual stages of Plasmodium falciparum-infected erythrocytes in the placenta. Infection and Immunity, 70, 5412-5415.
14. Beutler, E., Blume, K.G., Kaplan, J.C., Lohr, G.W., Ramot, B. & Valentine, W.N. (1979) International Committee for Standardization in Haematology: recommended screening test for glucose-6-phosphate dehydrogenase (G-6-PD) deficiency. British Journal of Haematology, 43, 465-467.
15. Calenda, V. & Chermann, J.C. (1992) The effects of HIV on hematopoiesis. European Journal of Haematology, 48, 181-186.
16. Carpenter, S.L., Zimmerman, S.A. & Ware, R.E. (2004) Acute parvovirus B19 infection mimicking congenital dyserythropoietic anemia. Journal of Pediatric Hematology/oncology, 26, 133-135.
17. 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 anemia is associated with hemozoin in vitro and in vivo. Blood, 108, 2569-2577.
18. Coban, C., Ishii, K.J., Kawai, T., Hemmi, H., Sato, S., Uematsu, S., Yamamoto, M., Takeuchi, O., Itagaki, S., Kumar, N., Horii, T. & Akira, S. (2005) Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. Journal of Experimental Medicine, 201, 19-25.
19. Dasari, P. & Bhakdi, S. (2012) Pathogenesis of malaria revisited. Medical Microbiology and Immunology, 201, 599-604.
20. Dasari, P., Reiss, K., Lingelbach, K., Baumeister, S., Lucius, R., Udomsangpetch, R., Bhakdi, S.C. & Bhakdi, S. (2011) Digestive vacuoles of Plasmodium falciparum are selectively phagocytosed by and impair killing function of polymorphonuclear leukocytes. Blood, 118, 4946-4956.
21. Dasari, P., Heber, S.D., Beisele, M., Torzewski, M., Reifenberg, K., Orning, C., Fries, A., Zapf, A.L., Baumeister, S., Lingelbach, K., Udomsangpetch, R., Bhakdi, S.C., Reiss, K. & Bhakdi, S. (2012) Digestive vacuole of Plasmodium falciparum released during erythrocyte rupture dually activates complement and coagulation. Blood, 119, 4301-4310.
22. Deroost, K., Lays, N., Noppen, S., Martens, E., Opdenakker, G. & Van den Steen, P.E. (2012) Improved methods for haemozoin quantification in tissues yield organ-and parasite-specific information in malaria-infected mice. Malaria Journal, 11, 166.
23. Deshpande, P. & Shastry, P. (2004) Modulation of cytokine profiles by malaria pigment-hemozoin: role of IL-10 in suppression of proliferative responses of mitogen stimulated human PBMC. Cytokine, 28, 205-213.
24. Farfour, E., Charlotte, F., Settegrana, C., Miyara, M. & Buffet, P. (2012) The extravascular compartment of the bone marrow: a niche for Plasmodium falciparum gametocyte maturation? Malaria Journal, 11, 285.
25. Frita, R., Carapau, D., Mota, M.M. & Hanscheid, T. (2012) In Vivo hemozoin kinetics after clearance of plasmodium berghei infection in mice. Malaria Research and Treatment, 2012, 373086.
26. Giribaldi, G., Ulliers, D., Schwarzer, E., Roberts, I., Piacibello, W. & Arese, P. (2004) Hemozoin- and 4-hydroxynonenal-mediated inhibition of erythropoiesis. Possible role in malarial dyserythropoiesis and anemia. Haematologica, 89, 492-493.
27. Guinovart, C., Bassat, Q., Sigauque, B., Aide, P., Sacarlal, J., Nhampossa, T., Bardaji, A., Nhacolo, A., Macete, E., Mandomando, I., Aponte, J.J., Menendez, C. & Alonso, P.L. (2008) Malaria in rural Mozambique. Part I: children attending the outpatient clinic. Malaria Journal, 7, 36.
28. Imirzalioglu, C., Soydan, N., Schaller, M., Bretzel, R.G., Chakraborty, T. & Domann, E. (2006) Diagnosis of mixed Plasmodium malariae and P. vivax infection in a development aid volunteer by examination of bone-marrow specimens by real-time PCR. Journal of Clinical Microbiology, 44, 2307-2310.
29. Ismail, M.R., Ordi, J., Menendez, C., Ventura, P.J., Aponte, J.J., Kahigwa, E., Hirt, R., Cardesa, A. & Alonso, P.L. (2000) Placental pathology in malaria: a histological, immunohistochemical, and quantitative study. Human Pathology, 31, 85-93.
30. Keller, C.C., Kremsner, P.G., Hittner, J.B., Misukonis, M.A., Weinberg, J.B. & Perkins, D.J. (2004) Elevated nitric oxide production in children with malarial anemia: hemozoin-induced nitric oxide synthase type 2 transcripts and nitric oxide in blood mononuclear cells. Infection and Immunity, 72, 4868-4873.
31. 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 anemia. Infection and Immunity, 77, 3864-3871.
32. Klco, J.M., Geng, B., Brunt, E.M., Hassan, A., Nguyen, T.D., Kreisel, F.H., Lisker-Melman, M. & Frater, J.L. (2010) Bone marrow biopsy in patients with hepatitis C virus infection: spectrum of findings and diagnostic utility. American Journal of Hematology, 85, 106-110.
33. Lamikanra, A.A., Theron, M., Kooij, T.W. & Roberts, D.J. (2009) Hemozoin (malarial pigment) directly promotes apoptosis of erythroid precursors. PLoS One, 4, e8446.
34. Lee, S.H., Erber, W.N., Porwit, A., Tomonaga, M. & Peterson, L.C. (2008) ICSH guidelines for the standardization of bone marrow specimens and reports. International Journal of Laboratory Hematology, 30, 349-364.
35. Mayor, A., Serra-Casas, E., Bardaji, A., Sanz, S., Puyol, L., Cistero, P., Sigauque, B., Mandomando, I., Aponte, J.J., Alonso, P.L. & Menendez, C. (2009) Sub-microscopic infections and long-term recrudescence of Plasmodium falciparum in Mozambican pregnant women. Malaria Journal, 8, 9.
36. McDevitt, M.A., Xie, J., Gordeuk, V. & Bucala, R. (2004) The anemia of malaria infection: role of inflammatory cytokines. Current Hematology Reports, 3, 97-106.
37. Newton, C.R., Chokwe, T., Schellenberg, J.A., Winstanley, P.A., Forster, D., Peshu, N., Kirkham, F.J. & Marsh, K. (1997) Coma scales for children with severe falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 91, 161-165.
38. Nuchsongsin, F., Chotivanich, K., Charunwatthana, P., Omodeo-Sale, F., Taramelli, D., Day, N.P., White, N.J. & Dondorp, A.M. (2007) Effects of malaria heme products on red blood cell deformability. American Journal of Tropical Medicine and Hygiene, 77, 617-622.
39. 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.
40. Phillips, R.E., Looareesuwan, S., Warrell, D.A., Lee, S.H., Karbwang, J., Warrell, M.J., White, N.J., Swasdichai, C. & Weatherall, D.J. (1986) The importance of anaemia in cerebral and uncomplicated falciparum malaria: role of complications, dyserythropoiesis and iron sequestration. The Quarterly Journal of Medicine, 58, 305-323.
41. Phiri, K.S., Calis, J.C., Kachala, D., Borgstein, E., Waluza, J., Bates, I., Brabin, B. & van Hensbroek, M.B. (2009) Improved method for assessing iron stores in the bone marrow. Journal of Clinical Pathology, 62, 685-689.
42. Romagosa, C., Menendez, C., Ismail, M.R., Quinto, L., Ferrer, B., Alonso, P.L. & Ordi, J. (2004) Polarisation microscopy increases the sensitivity of hemozoin and Plasmodium detection in the histological assessment of placental malaria. Acta Tropica, 90, 277-284.
43. Rozman, M., Masat, T., Feliu, E. & Rozman, C. (1992) Dyserythropoiesis in iron-deficiency anemia: ultrastructural reassessment. American Journal of Hematology, 41, 147-150.
44. Schrimpe, A.C. & Wright, D.W. (2009) Comparative analysis of gene expression changes mediated by individual constituents of hemozoin. Chemical Research in Toxicology, 22, 433-445.
45. Schwarzer, E., Turrini, F., Ulliers, D., Giribaldi, G., Ginsburg, H. & Arese, P. (1992) Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. Journal of Experimental Medicine, 176, 1033-1041.
46. Schwarzer, E., Kuhn, H., Valente, E. & Arese, P. (2003) Malaria-parasitized erythrocytes and hemozoin nonenzymatically generate large amounts of hydroxy fatty acids that inhibit monocyte functions. Blood, 101, 722-728.
47. Sherry, B.A., Alava, G., Tracey, K.J., Martiney, J., Cerami, A. & Slater, A.F. (1995) Malaria-specific metabolite hemozoin mediates the release of several potent endogenous pyrogens (TNF, MIP-1 alpha, and MIP-1 beta) in vitro, and altered thermoregulation in vivo. Journal of Inflammation, 45, 85-96.
48. Silvestrini, F., Alano, P. & Williams, J.L. (2000) Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology, 121, 465-471.
49. Skorokhod, O.A., Alessio, M., Mordmuller, B., Arese, P. & Schwarzer, E. (2004) Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect. Journal of Immunology (Baltimore, Md. : 1950), 173, 4066-4074.
50. Skorokhod, A., Schwarzer, E., Gremo, G. & Arese, P. (2007) HNE produced by the malaria parasite Plasmodium falciparum generates HNE-protein adducts and decreases erythrocyte deformability. Redox Report, 12, 73-75.
51. Skorokhod, O.A., Caione, L., Marrocco, T., Migliardi, G., Barrera, V., Arese, P., Piacibello, W. & Schwarzer, E. (2010) Inhibition of erythropoiesis in malaria anemia: role of hemozoin and hemozoin-generated 4-hydroxynonenal. Blood, 116, 4328-4337.
52. Smalley, M.E. & Brown, J. (1980) The distribution of Plasmodium falciparum gametocytes in the internal organs and peripheral circulation. Transactions of the Royal Society of Tropical Medicine and Hygiene, 75, 103-105.
53. Smalley, M.E., Abdalla, S. & Brown, J. (1981) The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Transactions of the Royal Society of Tropical Medicine and Hygiene, 75, 103-105.
54. Were, T., Hittner, J.B., Ouma, C., Otieno, R.O., Orago, A.S., Ong'echa, J.M., Vulule, J.M., Keller, C.C. & Perkins, D.J. (2006) Suppression of RANTES in children with Plasmodium falciparum malaria. Haematologica, 91, 1396-1399.
55. Wickramasinghe, S.N. (1997) Dyserythropoiesis and congenital dyserythropoietic anaemias. British Journal of Haematology, 98, 785-797.
56. Wickramasinghe, S.N., Phillips, R.E., Looareesuwan, S., Warrell, D.A. & Hughes, M. (1987) The bone marrow in human cerebral malaria: parasite sequestration within sinusoids. British Journal of Haematology, 66, 295-306.