Williams Hematology


Other Infections
Chapter References

Hemolytic anemia is a prominent part of the clinical presentation of patients infected with organisms, such as the malaria parasites, Babesia, and Bartonella, that directly invade the erythrocyte. Malaria is probably the most common cause of hemolytic anemia on a worldwide basis, and much has been learned about how the parasite enters the erythrocyte. Falciparum malaria, in particular, can cause severe and sometimes fatal hemolysis (blackwater fever). Other organisms cause hemolytic anemia by producing a hemolysin (e.g., Clostridium welchii), by stimulating an immune response (e.g., Mycoplasma pneumoniae), by enhancing macrophage recognition and hemophagocytosis, or by as yet unknown mechanisms. The many different infections that have been associated with hemolytic anemia are tabulated, and references to the original studies provided.

Acronyms and abbreviations that appear in this chapter include: CMV, cytomegalovirus; G-6-PD, glucose-6-phosphate dehydrogenase; HIV, human immunodeficiency virus; ICAM, intercellular adhesion molecule; VCAM, vascular cell adhesion molecule.

Shortening of erythrocyte life span occurs commonly in the course of inflammatory and infectious diseases. This may occur particularly in patients with glucose-6-phosphate dehydrogenase (G-6-PD) deficiency (Chap. 45), splenomegaly (Chap. 60), and the microvascular fragmentation syndrome (Chap. 41 and Chap. 126). In some infections, however, rapid destruction of erythrocytes represents a prominent part of the overall clinical picture (Table 54-1). This chapter deals only with the latter states.


Several distinct mechanisms may lead to hemolysis during infections.1 These include direct invasion of erythrocytes by the infecting organism, as in malaria, babesiosis, and bartonellosis; elaboration of hemolytic toxins, as by Clostridium perfringens; development of antibodies or autoantibodies against red cell antigens; or deposition of microbial antigens or immune complexes on erythrocytes.2
Known since antiquity, malaria is the world’s most common cause of hemolytic anemia.3 After the host is bitten by an infected female Anopheles mosquito, the sporozoites invade the liver and possibly other internal organs in the asymptomatic tissue stage of malaria. Merozoites, emerging at first from the tissues and later from previously parasitized red cells, bind to glyocophorin A and B by means of a 175-kD protein that has been designated the erythrocyte-binding antigen.4,5 and 6 A complex series of events, not yet fully understood, eventuates in invasion of the interior of the red cell by the parasite.4 Having entered the erythrocyte, the parasite grows intracellularly, nourished by the cell’s contents. Erythrocytes infected with Plasmodium falciparum develop surface knobs7,8 that contain receptors, especially the P. falciparum erthrocyte membrane protein 1, for endothelial proteins. All parasites bind to CD36 antigen and thrombospondin found on endothelial surfaces, while some bind to the intercellular adhesion molecule 1(ICAM-1), and a few bind to vascular cell adhesion molecule (VCAM)9,10,11,12 and 13 and mediate the adherence of parasitized cells to endothelium. Rosetting of parasitized cells with unparasitized cells also occurs through another undefined mechanism.4 One of the membrane proteins of the P. falciparum binds specifically to the spectrin on the inner surface of the red cell membrane.14 A large number of genetic polymorphisms that interfere with invasion of erythrocytes by parasites and their proliferation have developed in areas where malaria has been a leading cause of death for many generations.15 These include G-6-PD deficiency, Southeast Asian ovalocytosis, thalassemias, and hemoglobinopathies.
The degree to which anemia develops often seems to be out of proportion to the number of cells infected with the parasite; the reason for this apparent destruction of uninvaded cells is not clear. Osmotic fragility is increased in nonparasitized cells as well as cells containing plasmodia.16 The erythrocyte cation permeability is altered in monkeys with malaria.17 Positive Coombs’ test results have been reported, but the role of antibodies in the etiology of the anemia is not clear.18 It has been suggested that oxidative damage to red cell lipids occurs19,20 and that there is an abnormality in the phosphorylation of membranes of parasitized red cells.21 Plasmodium falciparum–infected red cells have a highly irregular surface defect. This may be produced by the intracellular growth of the plasmodium, or it could represent the site of parasite entry. Nonparasitized cells often have similar surface defects,22 suggesting a phenomenon known to occur in simian malaria,23 the “pitting” of parasites from an infected cell.
Destruction of parasitized red cell appears to occur largely in the spleen, and splenomegaly is typically present in chronic malarial infection. The “pitting” of parasites from infected erythrocytes may also occur in the spleen.24 The fever associated with malaria is characteristically cyclic, varying in frequency according to the malaria type. Although classic periodicity is often absent, febrile paroxysms of Plasmodium vivax malaria tend to occur every 48 h, those of Plasmodium malariae infection every 72 h, and those of P. falciparum malaria daily. Falciparum malaria is occasionally associated with particularly severe hemolysis and may result in the passage of dark, almost black, urine. This disorder, also called blackwater fever, is no longer common. At one time it was seen frequently among Europeans in Africa and in India, usually after quinine was given to treat malaria. The relative roles of the malarial infection and of the drug have never been clarified.25
Diagnosis of malaria depends upon demonstration of the parasites on the blood film26 (Plate I-11, Plate I-12) or demonstration of the appropriate DNA sequences in the blood.27,28 The morphological distinction of P. falciparum from other forms of malaria, principally P. vivax, is clinically important, since P. falciparum infection may constitute a clinical emergency. If more than 5 percent of the red cells infected contain parasites, the infection is almost certainly with P. falciparum. In an infection with this organism, rings are practically the only form of parasite evident on the blood film. The finding of two or more rings within the same red cells is regarded as pathognomic of P. falciparum.28
Eradication of blood forms is achieved with quinine, chloroquine, or various sulfones or sulfonamides given together with pyrimethamine. Tissue stages of vivax malaria are effectively treated with primaquine. This drug, as well as certain sulfones used in the treatment of malaria, produces severe hemolysis in patients with G-6-PD deficiency (see Chap. 45).
When acute, unusually severe hemolysis occurs in the course of falciparum malaria (blackwater fever), the physician should be certain that a hemolytic drug is not being administered to a G-6-PD–deficient individual. Transfusions may be needed with severe hemolysis, and if renal failure occurs, extracorporeal dialysis may be required. With early institution of therapy, the prognosis in malaria is excellent. However, when treatment is delayed or the strain is resistant to the administered agent, falciparum malaria may follow a rapid fatal course.
In 1885, Daniel A. Carrón, a medical student, inoculated himself with blood obtained from a verrucous node of the skin of a patient with verruca peruviana. He developed a fatal hemolytic anemia with the characteristics of Oroya fever, a disease that had first been observed some years earlier among workers in a railroad construction project near the city of Oroya in the Peruvian Andes. This fatal self-experiment established the identity of the verrucous form and the hemolytic phase of human bartonellosis, an infection that now bears the name Carrión’s disease.29 Human bartonellosis is transmitted by the sand fly. The red blood cells become infected with Bartonella bacilliformis. It is believed that the organism does not grow within the red cell but, rather, adheres to its exterior surface: when infected red cells are washed with citrated plasma, free organisms are found but the red cells are not hemolyzed. In hanging-drop cultures, masses of organisms are clearly seen outside the erythrocytes, while the cells themselves are intact.30 The osmotic fragility of the red cells is normal.29 They are rapidly removed from the circulation, apparently both by liver and spleen. Normal red cells transfused into patients with bartonellosis meet a similar fate.31 A 130-kD bartonella protein that causes erythrocytes to acquire trenches, indentations, and invaginations has been purified from culture broths and has been called deformin.32 In addition, two B. bacillformis genes, designated ialA and ialB, predicted to code for polypeptides of 170 amino acids (20.1 kDa) and 186 amino acids (19.9 kDa), respectively, have been shown to greatly enhance the ability of Escherichia coli to invade erythrocytes.33
As demonstrated by Carrión’s experiment, bartonellosis has two clinical stages. The acute hemolytic anemia, Oroya fever, represents the early, invasive stage of a chronic granulomatous disorder, the late stage of which is designated verruca peruviana. Most patients manifest no clinical symptoms during the Oroya fever phase, but when anemia does occur, its onset is dramatic. Red counts as low as 750,000/µl have been documented.34 In addition to symptoms of anemia, patients manifest thirst, anorexia, sweating, and generalized lymphadenopathy. Spleen and liver enlargement is unusual. Large numbers of nucleated red cells appear in the blood smear, and reticulocytosis is often striking. The white cell count is variable. Diagnosis is established by demonstrating the presence of the organism B. bacilliformis on the erythrocytes. Giemsa-stained blood films reveal red-violet rods varying in length from 1 to 3 µm and in width from 0.25 to 0.2 µm.
The mortality rate among untreated patients is very high, but those who do survive undergo a sudden transitional period in which the bartonellae change from an elongated to a coccoid form, the number of parasitized cells decreases, and the red cell count increases. Lymphocytosis and a right shift in the granulocyte series are observed with disappearance of the fever and abatement of other symptoms. Oroya fever responds well to treatment with penicillin, streptomycin, chloramphenicol, and the tetracyclines. The second stage of Bartonella infection, verruca peruviana, is a nonhematologic disorder characterized by an eruption over the face and extremities developing into bleeding warty tumors.
Babesia are intraerythrocytic protozoa known as piroplasms transmitted by ticks that may infect many species of wild and domestic animals. Humans occasionally become infected with Babesia microti or Babesia divergens, species that normally parasitize rodents and cattle, respectively.35 Other babesia-like piroplasms, such as WA1, first isolated from a patient in the state of Washington, are also becoming recognized.36,37 Once thought to be rare, babesiosis is being recognized with increasing frequency.38 The disease is usually tick-borne in man but has apparently also been transmitted by transfusion.37,39,40 Presumably because of the distribution of the vector, in the United States the disease is most common in the northeastern coastal region, where it became known as “Nantucket fever,” but it has also been encountered in the Midwest.41 Infections with B. divergens usually occur in splenectomized patients, but this is not the case with B. microti infections.38
The disease generally has a gradual onset with malaise, anorexia, and fatigue, followed by fever, sweats, and muscle and joint pains. Parasites can be seen in the red cells in Giemsa-stained thin blood films (Plate I-10). Serologic tests for antibodies to Babesia have been described,42 and PCR-based diagnostic tests are also available.38 It has responded to chemotherapy with clindamycin and quinine,43 but failure to respond to antibiotics has also been encountered.40 Whole-blood exchange was used with a marked improvement.39
Clostridium perfringens (welchii) sepsis is most likely to occur in patients who have undergone septic abortion. It has also been observed following acute cholecystitis.44 The a toxin of C. welchii is a lecithinase that may react with lipoprotein complexes at cell surfaces, liberating potent hemolytic substances, lysolecithins (see Chap. 38). It has also been suggested that erythrocyte membrane proteolysis plays an important role in hemolysis.45 Severe, often fatal hemolysis occurs in patients with C. welchii septicemia. Striking hemoglobinemia and hemoglobinuria occur. The serum may become a brilliant red, and the urine is a dark-brown mahogany color. The high plasma hemoglobin level may produce a marked dissociation between the blood hemoglobin and hematocrit levels. Microspherocytosis is prominent, and leukocytosis with a left shift and thrombocytopenia are often present. Acute renal and hepatic failure usually develop, and the prognosis is grave; more than half of the patients die, even with extensive treatment (see Chap. 126).46,47 Therapy consists of high-dose penicillin and surgical debridement.48
A variety of other infections have occasionally been associated with hemolytic anemia. The mechanisms involved vary. Some organisms, among them such common pathogens as Haemophilus influenzae, E. coli, and Salmonella species, can produce red cell agglutination in vitro, but it is not known whether this phenomenon is important in initiating in vivo hemolysis.49 Bacteria may also produce destruction of red cells indirectly when bacterial polysaccharides are adsorbed onto erythrocytes. Action of an antibody directed against the antigen-coated cells results in their agglutination50 or in complement-mediated lysis.51 The unmasking of T-type antigens by bacteria renders the cell polyagglutinable. This may be a rare cause of hemolysis occurring in the course of bacterial infections.52,53
Many different types of microorganisms may play a role in precipitating autoimmune hemolytic disease (see Chap. 63). In one study of 234 patients,54 55 were found to have an antecedent bacterial infection, 18 of these exhibiting an “unequivocal etiologic relationship” of infection to anemia. However, the principal evidence for such a relationship was a temporal one. A number of viral agents, including measles, cytomegalovirus (CMV), varicella, herpes simplex, influenza A and B, Epstein-Barr, human immunodeficiency virus (HIV), and coxsackievirus, have also been associated with immune hemolytic disease.54,55 Various mechanisms have been postulated, including absorption of immune complexes and complement, cross-reacting antigen, and a true autoimmune state with possible loss of tolerance secondary to the infectious organism.54 Histopathologic and sometimes virologic evidence of infection with cytomegalovirus has been reported in a high percentage of children with lymphadenopathy and hemolytic anemia.56 A positive antiglobulin reaction was demonstrated in some of these patients, and it has been suggested that some cases of “idiopathic autoimmune hemolytic anemia” are in reality due to cytomegalovirus infection.56
The high cold agglutinin titer that sometimes develops in the course of Mycoplasma pneumoniae pneumonia (see Chap. 56) may occasionally result in hemolytic anemia57,58 or compensated hemolysis, although most patients with high cold agglutinin titers do not become anemic. The red cells of a number of patients with kala-azar were found to be agglutinated with anticomplement and anti–non-g-globulin serum.59 Both splenic and hepatic sequestration of red cells appears to occur in this disease.60
Microangiopathic hemolytic anemia is discussed in detail in Chap. 51. This disorder may be triggered by a variety of infections, some of which are caused by well-characterized organisms, such as species of Shigella,61,62 Campylobacter,63 and Aspergillus.57

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Copyright © 2001 McGraw-Hill
Ernest Beutler, Marshall A. Lichtman, Barry S. Coller, Thomas J. Kipps, and Uri Seligsohn
Williams Hematology


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