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Hemolytic Uremic Syndrome
Hemolytic uremic syndrome HUS is a disease of nonimmune Coombs negative hemolytic anemia, low platelet count, and renal impairment 1. Anemia is severe and microangiopathic in nature, with fragmented red blood cells schistocytes in the peripheral smear, high serum lactate dehydrogenase LDH , circulating free hemoglobin, and reticulocytes.
In children, the disease is most commonly triggered by Shiga-like toxin Stx -producing Escherichia coli Stx- E. Cases of Stx- E.
Non—Shiga toxin-associated HUS non—Stx-HUS comprises a heterogeneous group of patients in whom an infection by Stx-producing bacteria could be excluded as cause of the disease. It can be sporadic or familial i. Collectively, non—Stx-HUS forms have a poor outcome.
Genetic studies have recently documented that the familial form is associated with genetic abnormalities of complement regulatory proteins, and evidence is now emerging that similar genetic alterations can predispose to sporadic cases of non—Stx-HUS as well.
Microvascular lesion of HUS consists of vessel wall thickening with endothelial swelling and accumulation of proteins and cell debris in the subendothelial layer, creating a space between endothelial cells and the underlying basement membrane of affected microvessels 1 , 3.
In Stx-HUS, the lesion is mainly confined to the glomerular tuft and is noted in an early phase of the disease. Arterial thrombosis does occur but is uncommon and seems to be a proximal extension of the glomerular lesion 11 , H7 13 — This serotype has a unique biochemical property lack of sorbitol fermentation as to render it readily distinguishable from other fecal E.
However, many other E. Infection by Stx-producing Shigella dysenteriae serotype 1 has been commonly linked to Stx-HUS in developing countries of Asia 24 and Africa 25 but rarely in industrialized countries After exposure to Stx- E. The overall incidence of Stx-HUS is estimated to be 2. The incidence of the disease parallels the seasonal fluctuation of E. H7 infections with a peak in warmer months, between June and September. In Argentina and Uruguay, E. An association between traditional extensive production of cattle with endemic HUS in Argentina has been proposed, as supported by detection of Stx-producing E.
They are found in manure and water troughs in farms, which explains the increased risk for infection in people who live in rural areas. Meat is contaminated at slaughter. Internalization of the microorganism during grinding renders it capable of surviving cooking Fruits and vegetables may also be contaminated, including radish sprouts, lettuce, and apple cider. Unpasteurized apple juice has been implicated in several outbreaks Person-to-person transmission has been reported in child care and long-term care facilities The disease is characterized by prodromal diarrhea followed by acute renal failure.
The average interval between E. HUS is usually diagnosed 6 d after the onset of diarrhea 1. After infection, Stx- E. Diagnosis rests on detection of Stx- E.
Serologic tests for antibodies to Stx and O LPS can be done in research laboratories, and tests are being developed for rapid detection of E. H7 and Stx in stools. Bloody diarrhea, fever, vomiting, elevated leukocyte count, extremes of age, and female gender as well as the use of antimotility agents 37 have been associated with an increased risk of HUS after E.
Stx-HUS is not a benign disease. A recent meta-analysis of 49 published studies patients, mean follow-up of 4. The severity of acute illness, particularly central nervous system symptoms, and the need for initial dialysis were strongly associated with a worse long-term prognosis 4 , Stx-HUS that is precipitated by S.
In , Albert Adam first reported an epidemia of bloody diarrhea of infants caused by a special type of Bacterium coli. Such bacterium was biochemically unique in that fermentation properties were different from known E.
In , the E. A filterable agent—we now know that this was likely Stx—that caused diarrhea in calves and was lethal to mice was isolated from the stools of these children. A few years later, it was found that most severe cases of O B4-induced epidemic diarrhea were associated with purpura, anuria, and neurologic signs. Autopsy material revealed thrombosis of capillary and precapillary arterioles in lungs, liver, brain, and kidneys, as well as glomerular tuft occlusion by fibrin thrombi These early findings were taken to indicate that a toxin, possibly released by the E.
Several years later, in , Konowalciuck et al. H7 infection an had received a diagnosis of HUS. The Stx associated with E. Stx-1 is almost identical to Stx from S. Despite their similar sequences, Stx-1 and Stx-2 cause different degrees and types of tissue damage as documented by the higher pathogenicity of strains of E.
In a recent study in children who become infected by Stx- E. This is also true in mice and baboons 45 , It is interesting that a new AB5 toxin that comprises a single kD A subunit and a pentamer of kD B subunits has been recently isolated from a highly virulent E.
H21 that was responsible for an outbreak of HUS 53 , which may represent the prototype of a new class of toxins, accounting for HUS associated with strains of E. Binding and mechanism of action of Shiga-like toxin. The B subunits of Shiga toxin Stx molecules attach to galactose gal disaccharides of globotriaosylceramide Gb3 receptors on the membrane of monocytes, polymorphonuclear cells, platelets, glomerular endothelial cells, and tubular epithelial cells. The toxin is internalized via retrograde transport through the Golgi complex.
Then the A and B subunits dissociate, and the A subunit is translocated to the cytosol. After oral ingestion, Stx- E. Stx then are picked up by polarized gastrointestinal cells via transcellular pathways 55 and translocate into the circulation, probably facilitated by the transmigration of neutrophils PMN 56 , which increase paracellular permeability.
The route of transport of Stx from the intestine to the kidney has been greatly debated. In vitro experiments have shown that Stx can bind to human erythrocytes 57 , platelets 58 , and activated monocytes However, more recent studies have underpinned a role for PMN in Stx transfer in the blood because Stx rapidly and completely bind to PMN when incubated with human blood The Stx receptor on PMN has a fold lower affinity than the high-affinity receptor expressed on glomerular endothelial cells.
In vitro , in co-cultures, PMN loaded with Stx transfer the ligand to glomerular endothelial cells so that at the end of the incubation, Stx molecules were found on glomerular endothelial cells but no more on PMN Binding of Stx to target cells is dependent on B subunits and occurs via the terminal digalactose moiety of the glycolipid cell surface receptor globotriaosylceramide Gb3 Figure 1. Stx-1 and Stx-2 bind to different epitopes on the Gb3 molecule, and they also differ in binding affinity and kinetics Surface plasmon resonance analysis showed that Stx-1 easily binds to and detaches from Gb3, in contrast to Stx-2, which binds slowly but also dissociates very slowly, thus staying on the cells long enough to be incorporated The latter could explain why Stx-2 is fold more toxic than Stx-1 on human endothelial cells in vitro Cultured human microvascular endothelial cells are more susceptible to the toxic effects of Stx than large-vessel endothelium This is consistent with data that the number of Gb3 receptors expressed on human microvascular endothelial cells is fold higher than in endothelial cells from human umbilical veins Altogether these data provide the biochemical basis for the preferential localization of microangiopathic lesions to renal vasculature in HUS in humans.
After internalization by receptor-mediated endocytosis, Stx are carried by retrograde transport through the Golgi complex to the endoplasmic reticulum, where the A and B subunits likely dissociate Figure 1.
Then the A subunit is translocated to the cytosol and nuclear envelope, where it enzymatically blocks protein synthesis 67 Figure 1. Stx-1 and Stx-2 also induce endothelial apoptosis 68 , 69 possibly by inhibiting the expression of the antiapoptotic Bcl-2 family member, Mcl-1 For many years, it was assumed that the only relevant biologic activity of Stx was the block of protein synthesis and destruction of endothelial cells.
Chemokines and cytokines are likely involved in the chemoattraction and activation of neutrophils. Adhesion molecules seem to play a critical role in mediating binding of inflammatory cells to the endothelium. This is supported by adhesion experiments under flow showing that Stx-2 treatment enhanced the number of leukocytes that adhere and migrate across a monolayer of human endothelial cells Taken together, these findings indicate that Stx, by altering endothelial cell adhesion properties and metabolism, favor leukocyte-dependent inflammation.
The latter activates endothelial cells that lose thromboresistance, which ultimately leads to microvascular thrombosis. Evidence for such sequence of events has been obtained in experiments of whole blood flowing on human microvascular endothelial cells, pre-exposed to Stx-1, at high shear stress Finding that in such circumstances early platelet activation and adhesion takes place, followed by the formation of organized thrombi dependent on endothelial P-selectin and PECAM-1, offers a plausible pathophysiologic pathway for microvascular thrombosis in HUS.
The above report could also be taken as a demonstration of a link between bacteria and their products and arterial thrombosis, as suggested in the accompanying commentary In vivo evidence of coagulation disturbances, i.
Although early studies suggested that fibrinolysis is augmented in Stx-HUS 76 , more recent work revealed the presence of higher-than-normal levels of plasminogen-activator inhibitor type 1, indicating that fibrinolysis is substantially inhibited There is no treatment of proven value, and care during the acute phase of the illness is still merely supportive with no substantial changes as compared with the past Table 2.
There is no clear consensus on whether antibiotics should be administered to treat Stx- E. It was postulated that antibiotic-induced injury to the bacterial membrane might favor the acute release of large amounts of toxins. However, a recent meta-analysis on 26 reports failed to show a higher risk for HUS associated with antibiotic administration Of note, in the study by Wong et al.
However, a recent report of an adult patient with E. H7—induced HUS with bacteremia and urinary tract infection showed that early antibiotic therapy rapidly resolved hematologic and renal abnormalities On the basis of available data, we suggest that in patients with Stx- E.
Most treatments, including plasma therapy, intravenous IgG, fibrinolytic agents, antiplatelet drugs, corticosteroids, and antioxidants 38 , have been shown to be ineffective in controlled clinical trials in the acute phase of the disease Careful BP control and renin-angiotensin system blockade may be particularly beneficial on the long term for patients who experience chronic renal disease after an episode of Stx-HUS. Finally, kidney transplant should be considered as an effective and safe treatment for children who progress to ESRD.
Hemolytic Uremic Syndrome
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