Erythropoiesis, red cells, and the approach to anemia

doi:10.1017/CBO9780511545306.005

3 - Erythropoiesis, red cells, and the approach to anemia

Published online by Cambridge University Press: 10 August 2009

Pedro A. De Alarcón ,

M. Cris Johnson and

Eric J. Werner

Edited by

Pedro A. de Alarcón and

Eric J. Werner

Foreword by

J. Lawrence Naiman

Show author details

Pedro A. De Alarcón: Affiliation:
St Jude Children's Research Center, Memphis, TN, USA
M. Cris Johnson: Affiliation:
Children's Hospital Central California, Madera, CA, USA
Eric J. Werner: Affiliation:
Children's Hospital of the King's Daughters, Norfolk, VA, USA
Pedro A. de Alarcón: Affiliation:
University of Tennessee
Eric J. Werner: Affiliation:
Eastern Virginia Medical School
J. Lawrence Naiman: Affiliation:
Stanford University School of Medicine, California

Book contents

Get access

Summary

Neonatal erythropoiesis

Neonatal erythropoiesis differs significantly from that in older children and adults. The birthing process with the rapid changes in oxygen concentration precipitates drastic changes in the newborn's erythroid system. To understand neonatal erythropoiesis, one needs to understand the ontogeny of erythropoiesis, from the embryo through the fetus to the newborn.

The current hypothesis of hematopoiesis is that there is a pleuripotent hematopoietic stem cell that gives rise to all hematopoietic lineages (Fig. 3.1). The ability of bone-marrow cells to reconstitute the hematopoietic system of lethally irradiated mice documented the existence of the stem cell [1]. In vitro clonogenic culture assays of bone-marrow cells documented the existence of a cascade of pluripotent and committed progenitor cells [2–6]. The commitment of the stem cell to differentiation may be a stochastic (random) or deterministic event, or a combination of both [7]. As stem cells differentiate, they lose their ability for self-renewal. Proliferation, differentiation, and survival of erythroid progenitors are dependent on the hormone erythropoietin [8]. The cascade of differentiation from the stem cell proceeds through a multipotent progenitor cell identified in vitro as colony-forming unit-granulocyte erythroid macrophage megakaryocyte (CFU-GEMM). The first recognizable pure erythroid progenitor is the burst-forming unit-erythroid (BFU-E), which then matures into the colony-forming unit-erythroid (CFU-E). The hormone erythropoietin is necessary for terminal maturation of the CFU-E. It also has an antiapoptotic effect on progenitor cells. Early progenitors depend on several cytokine mixtures for their proliferation and maturation. In utero hematopoiesis is primarily erythroid.

Information

Type: Chapter
Information: Neonatal Hematology , pp. 40 - 57

DOI: https://doi.org/10.1017/CBO9780511545306.005 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Book purchase

Temporarily unavailable

References

Till, J. E., McCulloch, E. A.A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 1961; 14: 213–222CrossRef Google Scholar PubMed

Bradley, J. R., Metcalf, D.The growth of mouse bone marrow cells in vitro. Aust J Exp Biol Med Sci 1966; 44: 287–300CrossRef Google Scholar PubMed

Moore, M. A., Williams, N., Metcalf, D.In vitro colony formation by normal and leukemic human hematopoietic cells: characterization of the colony-forming cells. J Natl Cancer Inst 1973; 50: 603–623CrossRef Google Scholar PubMed

Nakahata, T., Tsuji, K., Ishiguro, A., et al.Single-cell origin of human mixed hemopoietic colonies expressing various combinations of cell lineages. Blood 1985; 65: 1010–1016Google Scholar PubMed

Stephenson, J. R., Axelrad, A. A., McLeod, D. L., Shreeve, M. M.Induction of colonies of hemoglobin-synthesizing cells by erythropoietin in vitro. Proc Natl Acad Sci USA 1971; 68: 1542–1546CrossRef Google Scholar PubMed

Suda, T., Suda, J., Ogawa, M.Single-cell origin of mouse hemopoietic colonies expressing multiple lineages in variable combinations. Proc Natl Acad Sci USA 1983; 80: 6689–6693CrossRef Google Scholar PubMed

Metcalf, D.Stem cells, pre-progenitor cells and lineage-committed cells: are our dogmas correct?Ann N Y Acad Sci 1999; 872: 289–303, 303–304CrossRef Google Scholar PubMed

Fisher, J. W.Erythropoietin: physiology and pharmacology update. Exp Biol Med 2003; 228: 1–14CrossRef Google Scholar PubMed

Wyrsch, A., dalle Carbonare, V., Jansen, W., et al.Umbilical cord blood from preterm human fetuses is rich in committed and primitive hematopoietic progenitors with high proliferative and self-renewal capacity. Exp Hematol 1999; 27: 1338–1345CrossRef Google Scholar

Shannon, K. M., Naylor, G. S., Torkildson, J. C., et al.Circulating erythroid progenitors in the anemia of prematurity. N Engl J Med 1987; 317: 728–733CrossRef Google Scholar PubMed

Palis, J., Robertson, S., Kennedy, M., Wall, C., Keller, G.Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 1999; 126: 5073–5084Google Scholar PubMed

Keller, G., Lacaud, G., Robertson, S.Development of the hematopoietic system in the mouse. Exp Hematol 1999; 27: 777–787CrossRef Google Scholar PubMed

Palis, J., Yoder, M. C.Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol 2001; 29: 927–936CrossRef Google Scholar PubMed

Dieterlen-Lievre, F., Pardanaud, L., Bollerot, K., Jaffredo, T.Hemangioblasts and hemopoietic stem cells during ontogeny. C R Biol 2002; 325: 1013–1020CrossRef Google Scholar PubMed

Jaffredo, T., Gautier, R., Brajeul, V., Dieterlen-Lievre, F.Tracing the progeny of the aortic hemangioblast in the avian embryo. Dev Biol 2000; 224: 204–214CrossRef Google Scholar PubMed

Jaffredo, T., Gautier, R., Eichmann, A., Dieterlen-Lievre, F.Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 1998; 125: 4575–4583Google Scholar PubMed

Dieterlen-Lievre, F., Godin, I., Pardanaud, L.Where do hematopoietic stem cells come from?Int Arch Allergy Immunol 1997; 112: 3–8CrossRef Google Scholar

, Kelemen E., Calvo, W., Fliedner, T. M.Atlas of Human Hematopoietic Development. Berlin, Springer-Verlag, 1979Google Scholar

Emura, I., Sekiya, M., Ohnishi, Y.Ultrastructural identification of the hemopoietic inductive microenvironment in the human embryonic liver. Arch Histol Jpn 1984; 47: 95–112CrossRef Google Scholar PubMed

Emura, I., Sekiya, M., Ohnishi, Y.Four types of presumptive hemopoietic stem cells in the human fetal liver. Arch Histol Jpn 1983; 46: 645–662CrossRef Google Scholar PubMed

Emura, I., Sekiya, M., Ohnishi, Y.Two types of immature erythrocytic series in the human fetal liver. Arch Histol Jpn 1983; 46: 631–643CrossRef Google Scholar PubMed

Fukuda, T.Fetal hemopoiesis. I. Electron microscopic studies on human yolk sac hemopoiesis. Virchows Arch B Cell Pathol 1973; 14: 197–213Google Scholar PubMed

Zamboni, L.Electron microscopic studies of blood embryogenesis in humans. II. The hemopoietic activity in the fetal liver. J Ultrastruct Res 1965; 12: 525–541CrossRef Google Scholar PubMed

Gilmour, J. R.Normal haemopoiesis in intra-uterine and neonatal life. J Pathol 1941; 52: 25–55CrossRef Google Scholar

Eichmann, A., Corbel, C., Nataf, V., et al.Ligand-dependent development of the endothelial and hemopoietic lineages from embryonic mesodermal cells expressing vascular endothelial growth factor receptor 2. Proc Natl Acad Sci USA 1997; 94: 5141–5146CrossRef Google Scholar PubMed

Takashina, T.Haemopoiesis in the human yolk sac. J Anat 1987; 151: 125–35Google Scholar PubMed

Fukuda, T.Fetal hemopoiesis. II. Electron microscopic studies on human hepatic hemopoiesis. Virchows Arch B Cell Pathol 1974; 16: 249–270CrossRef Google Scholar PubMed

Moore, M. A., Metcalf, D.Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 1970; 18: 279–296CrossRef Google Scholar PubMed

Delassus, S., Titley, I., Enver, T.Functional and molecular analysis of hematopoietic progenitors derived from the aorta-gonad-mesonephros region of the mouse embryo. Blood 1999; 94: 1495–1503Google Scholar PubMed

Yoder, M. C., Cumming, J. G., Hiatt, K., Mukherjee, P., Williams, D. A.A novel method of myeloablation to enhance engraftment of adult bone marrow cells in newborn mice. Biol Blood Marrow Transplant 1996; 2: 59–67Google Scholar PubMed

Yoder, M. C., Hiatt, K.Engraftment of embryonic hematopoietic cells in conditioned newborn recipients. Blood 1997; 89: 2176–2183Google Scholar PubMed

Stockman, J. A., Pochedly, C.Developmental and Neonatal Hematology.New York: Raven Press, 1988Google Scholar

Lee, G. R., Foerster, J., Lukens, J., et al.Wintrobe's Clinical Hematology, 10th edn. Philadelphia: Lippincott Williams & Wilkins, 1999Google Scholar

Nathan, D. G., Orkin, S. H.Hematology of Infancy and Childhood, 5th edn. Philadelphia: W. B. Saunders Co., 1998Google Scholar

Gross, G. P., Hathaway, W. E.Fetal erythrocyte deformability. Pediatr Res 1972; 6: 593–599Google Scholar PubMed

Tillman, W., Wagner, D., Schroter, W.Decreased flexibility of newborn infant erythrocytes. Blut 1977; 34: 281–288Google Scholar

Buchan, P. C.Evaluation and modification of whole blood filtration in the measurement of erythrocyte deformability in preganacy and the newborn. Br J Haematol 1980; 45: 97–105CrossRef Google Scholar

Landaw, S. A., Rathbun, S. C., Guancial, R. L.Evidence for a tightly linked spectrin lattice in red blood cells of newborn man. Prog Soc Pediatr Res 1982; 16 (2): 208A, abstract 776Google Scholar

Neerhout, R. C.Erythrocyte lipids in the neonate. Pediatr Res 1968; 2: 172–178CrossRef Google Scholar PubMed

Crowley, J., Ways, P., Jones, J. W.Human fetal erythrocyte and plasma lipids. J Clin Invest 1965; 44: 989–998CrossRef Google Scholar PubMed

Delaunay, J.Red cell membrane and erythropoiesis genetic defects. Hematol J 2003; 4 (4): 225–232CrossRef Google Scholar PubMed

Hoffman, R.Hematology: Basic Principles and Practice, 3rd edn. New York: Churchill Livingstone, 2000Google Scholar

Oski, F. A., Naiman, J. L.Red cell metabolism in the premature infant. I. Adenosine triphosphate levels, adenosine triphosphate stability and glucose consumption. Pediatrics 1965; 36: 104–112Google Scholar PubMed

Ng, W. G., Bergren, W. R., Donnell, G. N., Hodgman, J. E., et al.Galactose-1 phosphate uridyl transferase activity in hemolysates of newborn infants. Pediatrics 1967; 39 (2): 293–294Google Scholar

Travis, S. F., Kumar, S. P., Paez, P. C., Delivoria-Papadopoulous, M.Red cell metabolic alterations and postnatal life in term infants: glycolytic enzymes and glucose-6-phosphate dehydrogenase. Pediatr Res 1980; 14: 1349–1352CrossRef Google Scholar PubMed

Konrad, P. N., Valentine, W. N., Paglia, D. E.Enzymatic activities and glutathione content of erythrocytes in the newborn: comparison with red cells of older subjects and those with comparable reticulocytosis. Acta Haematol 1972; 48: 193CrossRef Google Scholar PubMed

Gross, R. T., Schroeder, E. A., Brounstein, S. A.Energy metabolism in the erythrocytes of premature infants compared to full term newborn infants and adults. Blood 1963; 21: 755–765Google Scholar PubMed

Whittam, R.Control of membrane permeability to potassium in red blood cells. Nature 1968; 219 (154): 610CrossRef Google Scholar PubMed

Stave, U., Hintz, H.On erythrocytes in newborn infants. Hematological and enzymological studies in the 1st year of life. Z Kinderheinkd 1961; 86: 184–197CrossRef Google Scholar PubMed

Luca, C., Stevenson, J. H. Jr, Kaplan, E.Simultaneous multiple-column chromatography: its application to the separation of the adenine nucleotides of human erythrocytes. Anal Biochem 1962; 4: 39–45CrossRef Google Scholar

Schroter, W., Tillman, W.Heinz body susceptibility of red cells and exchange transfusion. Acta Haematol 1973; 49: 74–79CrossRef Google Scholar PubMed

Tillman, W., Menke, J., Schroter, W.The formation of Heinz bodies in ghosts of human erythrocytes of adults and newborn infants. Clin Wochenschr 1973; 51: 201–203CrossRef Google Scholar

Stockman, J. A., Clark, D. A.Diminished antioxidant activity of newborn infants. Pediatr Res 1981; 15: 684. Abstract 1444Google Scholar

Carrell, R. W., Winterbourn, C. C., Rachmilewitz, E. A.Activated oxygen and hemolysis. Br J Haematol 1975; 30: 259–264CrossRef Google Scholar

Stockman, J. A.Newborn red cells, the nature of oxidant injury. Pediatr Res 1977; 11: 41CrossRef Google Scholar

Bunn, H. F. Human hemoglobins: normal and abnormal. In Nathan, D. G., Orkin, S. H., eds. Hematology of Infancy and Childhood, 5th edn. Philadelphia: W. B. Saunders Co., 1998: 729–762Google Scholar

Hann, I. M. The normal blood picture in neonates. In Hann, I. M., Gibson, B. E. S., Letsky, E. A., eds. Fetal and Neonatal Hematology. London: Bailliere Tindall, 1991: 29–50Google Scholar

Stockman, J. A., 3rd, Garcia, J. F., Oski, F. A.The anemia of prematurity. Factors governing the erythropoietin response. N Engl J Med 1977; 296: 647–650CrossRef Google Scholar PubMed

Delivoria-Papadopoulos, M., Roncevic, , Oski, N. P., , F. A.Postnatal changes in oxygen transport of term, preterm and sick infants: the role of red cell 2,3-diphosphoglycerate and adult hemoglobin. Pediatr Res 1971; 5: 235–245CrossRef Google Scholar

Bifano, E. M., Smith, F., Borer, J.Relationship between determinants of oxygen delivery and respiratory abnormalities in preterm infants with anemia. J Pediatr 1992; 120: 292–296CrossRef Google Scholar PubMed

Izraeli, S., Ben-Sira, L., Harell, D., et al.Lactic acid as a predictor for erythrocyte transfusion in healthy preterm infants with anemia of prematurity. J Pediatr 1993; 122: 629–631CrossRef Google Scholar PubMed

Stockman, J. A., 3rd, Clark, D. A.Weight gain: a response to transfusion in selected preterm infants. Am J Dis Child 1984; 138: 828–830Google Scholar PubMed

Delivoria-Papadopoulos, M., Roncevic, N. P., Oski, F. A.Postnatal changes in oxygen transport of term, preterm and sick infants: the role of red cell 2, 3-diphosphoglycerate and adult hemoglobin. Pediatr Res 1971; 5: 235–245CrossRef Google Scholar

Forestier, F., Daffos, F., Glacteros, F., et al.Hematological values of 163 normal fetuses between 18 and 30 weeks of gestation. Pediatr Res 1986; 20: 342–346CrossRef Google Scholar PubMed

Saltzman, D. H., Frigoletto, F. D., Harlow, B. L., Barss, V. A., Benacerraf, B. R.Sonographic evaluation of hydrops fetalis. Obstet Gynecol 1989; 74: 106–111Google Scholar PubMed

Burman, D., Morris, A. F.Cord haemoglobin in low birthweight infants. Arch Dis Child 1974; 49: 382–385CrossRef Google Scholar PubMed

Rivera, L. M., Rudolph, N.Postnatal persistence of capillary-venous differences in hematocrit and hemoglobin values in low-birth-weight and term infants. Pediatrics 1982; 70: 956–957Google Scholar PubMed

Thurlbeck, S. M., McIntosh, N.Preterm blood counts vary with sampling site. Arch Dis Child 1987; 62: 74–75CrossRef Google Scholar PubMed

Stockman, J. A. III, Oski, F. A.Physiological anaemia of infancy and the anaemia of prematurity. Clin Haematol 1978; 7: 3–18Google Scholar PubMed

O'Brien, R. T., Pearson, H. A.Physiologic anemia of the newborn infant. J Pediatr 1971; 79: 132–138CrossRef Google Scholar PubMed

Stockman, J. A. III, Garcia, J. F., Oski, F. A.The anemia of prematurity: factors governing the erythropoietin response. N Engl J Med 1977; 296: 647–650CrossRef Google Scholar PubMed

Lin, J. C., Strauss, R. G., Kulhavy, J. C., et al.Phlebotomy overdraw in the neonatal intensive care nursery. Pediatrics 2000; 106: E19CrossRef Google Scholar PubMed

Stockman, J. A. III, Alarcon, P. A.Overview of the state of the art of Rh disease: history, current clinical management, and recent progress. J Pediatr Hematol Oncol 2001; 23: 385–393CrossRef Google Scholar PubMed

Hariharan, D., Manno, C. S., Seri, I.Neonatal lupus erythematosus with microvascular hemolysis. J Pediatr Hematol Oncol 2000; 22: 351–354CrossRef Google Scholar PubMed

Passi, G. R., Kriplani, A., Pati, H. P., Choudhry, V. P.Isoimmune hemolysis in an infant due to maternal Evans' syndrome. Indian J Pediatr 1997; 64: 893–895CrossRef Google Scholar

Sokol, R. J., Hewitt, S., Stamps, B. K.Erythrocyte autoantibodies, autoimmune haemolysis and pregnancy. Vox Sang 1982; 43: 169–176CrossRef Google Scholar

Sacks, D. A., Platt, L. D., Johnson, C. S.Autoimmune hemolytic disease during pregnancy. Am J Obstet Gynecol 1981; 140: 942–946CrossRef Google Scholar PubMed

Kitzmiller, J. L.Autoimmune disorders: maternal, fetal, and neonatal risks. Clin Obstet Gynecol 1978; 21: 385–396CrossRef Google Scholar PubMed

Chaplin, H. Jr, Cohen, R., Bloomberg, G., et al.Pregnancy and idiopathic autoimmune haemolytic anaemia: a prospective study during 6 months gestation and 3 months post-partum. Br J Haematol 1973; 24: 219–229CrossRef Google Scholar PubMed

Baumann, R., Rubin, H.Autoimmune hemolytic anemia during pregnancy with hemolytic disease in the newborn. Blood 1973; 41: 293–297Google Scholar PubMed

Gilsanz, F., Vega, M. A., Gomez-Castillo, E., Ruiz-Balda, J. A., Omenaca, F.Fetal anaemia due to pyruvate kinase deficiency. Arch Dis Child 1993; 69: 523–524CrossRef Google Scholar PubMed

Hennekam, R. C., Beemer, F. A., Cats, B. P., Jansen, G., Staal, G. E.Hydrops fetalis associated with red cell pyruvate kinase deficiency. Genet Couns 1990; 1: 75–79Google Scholar PubMed

Whitelaw, A. G., Rogers, P. A., Hopkinson, D. A., et al.Congenital haemolytic anaemia resulting from glucose phosphate isomerase deficiency: genetics, clinical picture, and prenatal diagnosis. J Med Genet 1979; 16: 189–196CrossRef Google Scholar PubMed

Gallagher, P. G., Petruzzi, M. J., Weed, S. A., et al.Mutation of a highly conserved residue of betaI spectrin associated with fatal and near-fatal neonatal hemolytic anemia. J Clin Invest 1997; 99: 267–277CrossRef Google Scholar PubMed

Gallagher, P. G., Weed, S. A., Tse, W. T., et al.Recurrent fatal hydrops fetalis associated with a nucleotide substitution in the erythrocyte beta-spectrin gene. J Clin Invest 1995; 95: 1174–1182CrossRef Google Scholar PubMed

Whitfield, C. F., Follweiler, J. B., Lopresti-Morrow, L., Miller, B. A.Deficiency of alpha-spectrin synthesis in burst-forming units-erythroid in lethal hereditary spherocytosis. Blood 1991; 78: 3043–3051Google Scholar PubMed

Delhommeau, F., Cynober, T., Schischmanoff, P. O., et al.Natural history of hereditary spherocytosis during the first year of life. Blood 2000; 95: 393–397Google Scholar PubMed

Kaplan, M., Hammerman, C.Glucose-6-phosphate dehydrogenase deficiency: a potential source of severe neonatal hyperbilirubinaemia and kernicterus. Semin Neonatol 2002; 7: 121–128CrossRef Google Scholar PubMed

Herschel, M., Ryan, M., Gelbart, T., Kaplan, M.Hemolysis and hyperbilirubinemia in an African American neonate heterozygous for glucose-6-phosphate dehydrogenase deficiency. J Perinatol 2002; 22: 577–579CrossRef Google Scholar

Kaplan, M., Abramov, A.Neonatal hyperbilirubinemia associated with glucose-6-phosphate dehydrogenase deficiency in Sephardic-Jewish neonates: incidence, severity, and the effect of phototherapy. Pediatrics 1992; 90: 401–405Google Scholar PubMed

Lu, T. C., Wei, H., Blackwell, R. Q.Increased incidence of severe hyperbilirubinemia among newborn Chinese infants with G-6-P D deficiency. Pediatrics 1966; 37: 994–999Google Scholar PubMed

Missiou-Tsagaraki, S.Screening for glucose-6-phosphate dehydrogenase deficiency as a preventive measure: prevalence among 1,286,000 Greek newborn infants. J Pediatr 1991; 119: 293–299CrossRef Google Scholar PubMed

Kaplan, M., Renbaum, P., Levy-Lahad, E., et al.Gilbert syndrome and glucose-6-phosphate dehydrogenase deficiency: a dose-dependent genetic interaction crucial to neonatal hyperbilirubinemia. Proc Natl Acad Sci USA 1997; 94: 12128–12132CrossRef Google Scholar PubMed

Slusher, T. M., Vreman, H. J., McLaren, D. W., et al.Glucose-6-phosphate dehydrogenase deficiency and carboxyhemoglobin concentrations associated with bilirubin-related morbidity and death in Nigerian infants. J Pediatr 1995; 126: 102–108CrossRef Google Scholar PubMed

Kaplan, M., Hammerman, C., Vreman, H. J., Stevenson, D. K., Beutler, E.Acute hemolysis and severe neonatal hyperbilirubinemia in glucose-6-phosphate dehydrogenase-deficient heterozygotes. J Pediatr 2001; 139: 137–140CrossRef Google Scholar PubMed

Sarihan, H., Mocan, H., Abeys, M., et al.Kasabach–Merrit syndrome in infants. Panminerva Med 1998; 40: 128–131

Bjerke, H. S., Kelly, R. E. J., Foglia, R. P., Barcliff, L., Petz, L.Decreasing transfusion exposure risk during extracorporeal membrane oxygenation (ECMO). Transfus Med 1992; 2: 43–49CrossRef Google Scholar

Sartori, P. C., Enayat, M. S., Darbyshire, P. J.Congenital microangiopathic haemolytic anemia: a variant of thrombotic thrombocytopenic purpura?Pediatr Hematol Oncol 1993; 10: 271–277CrossRef Google Scholar PubMed

Kling, P. J., Schmidt, R. L., Roberts, R. A., Widness, J. A.Serum erythropoietin levels during infancy: associations with erythropoiesis. J Pediatr 1996; 128: 791–796CrossRef Google Scholar PubMed

Kanto, W. P. Jr, Marino, B., Godwin, A. S., Bunyapen, C.ABO hemolytic disease: a comparative study of clinical severity and delayed anemia. Pediatrics 1978; 62: 365–369Google Scholar PubMed

Strand, C., Polesky, H. F.Delayed anemia in erythroblastosis fetalis. Minn Med 1972; 55: 439–441Google Scholar PubMed

Scaradavou, A., Inglis, S., Peterson, P., et al.Suppression of erythropoiesis by intrauterine transfusions in hemolytic disease of the newborn: use of erythropoietin to treat the late anemia. J Pediatr 1993; 123: 279–284CrossRef Google Scholar PubMed

Ohls, R. K., Hunter, D. D., Christensen, R. D.A randomized, double-blind, placebo-controlled trial of recombinant erythropoietin in treatment of the anemia of bronchopulmonary dysplasia. J Pediatr 1993; 123: 996–1000CrossRef Google Scholar PubMed

Christensen, R. D., Hunter, D. D., Goodell, H., Rothstein, G.Evaluation of the mechanism causing anemia in infants with bronchopulmonary dysplasia. J Pediatr 1992; 120: 593–598CrossRef Google Scholar PubMed

Sood, S. K., Ramachandran, K., Mathur, M., et al.W.H.O. sponsored collaborative studies on nutritional anaemia in India. 1. The effects of supplemental oral iron administration to pregnant women. Q J Med 1975; 44: 241–258Google Scholar PubMed

Chan, S., Gerson, B., Subramaniam, S.The role of copper, molybdenum, selenium, and zinc in nutrition and health. Clin Lab Med 1998; 18: 673–685Google Scholar PubMed

Oski, F. A.Nutritional anemias. Semin Perinatol 1979; 3: 381–395Google Scholar PubMed

Ashkenazi, A., Levin, S., Djaldetti, M., Fishel, E., Benvenisti, D.The syndrome of neonatal copper deficiency. Pediatrics 1973; 52: 525–533Google Scholar PubMed

Karpel, J. T., Peden, V. H.Copper deficiency in long-term parenteral nutrition. J Pediatr 1972; 80: 32–36CrossRef Google Scholar PubMed

Krasinski, K., Perkin, R., Rutledge, J.Gray baby syndrome revisited. Clin Pediatr (Phila) 1982; 21: 571–572CrossRef Google Scholar PubMed

Stahl, M. M., Neiderud, J., Vinge, E.Thrombocytopenic purpura and anemia in a breast-fed infant whose mother was treated with valproic acid. J Pediatr 1997; 130: 1001–1003CrossRef Google Scholar

Ramaekers, L. H., The, T. S. Maternal anticonvulsants and perinatal risk. Eur J Obstet Gynecol Reprod Biol 1975; 5: 277–282CrossRef Google Scholar

Widness, J. A., Seward, V. J., Kromer, I. J., et al.Changing patterns of red blood cell transfusion in very low birth weight infants. J Pediatr 1996; 129: 680–687CrossRef Google Scholar PubMed

Fain, J., Hilsenrath, P., Widness, J. A., Strauss, R. G., Mutnick, A. H.A cost analysis comparing erythropoietin and red cell transfusions in the treatment of anemia of prematurity. Transfusion 1995; 35: 936–943CrossRef Google Scholar PubMed

Stockman, J. A. III.Anemia in children. Differential Insight 1979; 1: 13–20Google Scholar

Accessibility standard: Unknown

Accessibility compliance for the PDF of this book is currently unknown and may be updated in the future.