Pathophysiology and treatment of typical and atypical hemolytic uremic syndrome

Pathologie Biologie

Volumn 63, Issue 3, 2015, Pages 136-143

  Picard, C ^a   Burtey, S ^b   Bornet, C ^b   Curti, C ^c,d   Montana, M ^c,d   Vanelle, P ^c,d  

^a TIMONE HOSPITAL   (France)

^b HÔPITAL DE LA CONCEPTION   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Eculizumab; Hemolytic uremic syndrome; Shiga toxin receptor analogues; Urtoxazumab

Indexed keywords

ANTIBIOTIC AGENT; ANTICOAGULANT AGENT; ANTIINFLAMMATORY AGENT; BEVACIZUMAB; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; CIPROFLOXACIN; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5A; DIURETIC AGENT; ECULIZUMAB; ERYTHROPOIETIN; GB3 RECEPTOR; GLYCOSIDASE; MANGANESE; MONOCLONAL ANTIBODY; PADGEM PROTEIN; PROTEIN DERIVATIVE; RECOMBINANT THROMBOMODULIN; SHIGA TOXIN ANTIBODY; SHIGA TOXIN RECEPTOR DERIVATIVE; STROMAL CELL DERIVED FACTOR 1; SYNSORB PK; TETRAVALENT PEPTIDE; THROMBOMODULIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; URTOXAZUMAB; VASCULOTROPIN ANTIBODY; VEROTOXIN 1; VEROTOXIN 2; ANTIINFECTIVE AGENT; BACTERIAL TOXIN; COMPLEMENT; PLASMA SUBSTITUTE; SHIGA TOXIN; VASCULOTROPIN A;

ANTICOAGULATION; ANTIINFLAMMATORY ACTIVITY; BACTERIAL VIRULENCE; BLOOD TRANSFUSION; CFH GENE; CHRONIC KIDNEY DISEASE; CONSERVATIVE TREATMENT; DISSEMINATED INTRAVASCULAR CLOTTING; DRUG EFFICACY; DRUG TOLERABILITY; GENE; HEMOLYTIC UREMIC SYNDROME; HUMAN; KIDNEY TRANSPLANTATION; LIVING DONOR; MUTATIONAL ANALYSIS; NONHUMAN; PATHOPHYSIOLOGY; PHASE 1 CLINICAL TRIAL (TOPIC); PLASMA THERAPY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SHIGELLA DYSENTERIAE; SOCIAL SUPPORT; STREPTOCOCCUS PNEUMONIAE; THROMBOTIC THROMBOCYTOPENIC PURPURA; TREATMENT CONTRAINDICATION; TREATMENT INDICATION; TYPICAL HEMOLYTIC UREMIC SYNDROME; UREMIA; ANIMAL; BABOON; BACTERIAL INFECTION; CLASSIFICATION; CLINICAL TRIAL (TOPIC); COMPLICATION; DISEASE MODEL; ESCHERICHIA COLI INFECTION; FORECASTING; GENETIC PREDISPOSITION; GENETICS; HEMOLYTIC-UREMIC SYNDROME; IMMUNOLOGY; LIVER TRANSPLANTATION; MICROBIOLOGY; MOUSE; PATHOGENICITY; PHYSIOLOGY; PLASMA; PRECLINICAL STUDY; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; THROMBOPHILIA;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBODIES, MONOCLONAL, HUMANIZED; BACTERIAL INFECTIONS; BACTERIAL TOXINS; CLINICAL TRIALS AS TOPIC; COMPLEMENT SYSTEM PROTEINS; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; ESCHERICHIA COLI INFECTIONS; FORECASTING; GENETIC PREDISPOSITION TO DISEASE; HEMOLYTIC-UREMIC SYNDROME; HUMANS; KIDNEY TRANSPLANTATION; LIVER TRANSPLANTATION; MICE; PAPIO; PLASMA; PLASMA SUBSTITUTES; SHIGA TOXIN; SHIGA-TOXIGENIC ESCHERICHIA COLI; THROMBOPHILIA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84930474152     PISSN: 03698114     EISSN: 17683114     Source Type: Journal    
DOI: 10.1016/j.patbio.2015.03.001     Document Type: Review

References (91)

1. Bertholet-Thomas A., Ranchin B., King L.A., Bacchetta J., Belot A., Gillet Y., et al. Syndrome hémolytique et urémique post-diarrhéique: quand y penser? Quel suivi?. Arch Pediatr 2011, 18(7):823-830.
2. Schifferli A., Von Vigier R.O., Fontana M., Spartà G., Schmid H., Bianchetti M.G., et al. Hemolytic-uremic syndrome in Switzerland: a nationwide surveillance 1997-2003. Eur J Pediatr 2010, 169(5):591-598.
3. Fisher Walker C.L., Applegate J.A., Black R.E. Haemolytic-uraemic syndrome as a sequela of diarrhoeal disease. J Health Popul Nutr 2012, 30(3):257-261.
4. Blaser M.J. Deconstructing a lethal foodborne epidemic. N Engl J Med 2011, 365:1835-1836.
5. Loirat C., Saland J., Bitzan M. Management of hemolytic uremic syndrome. Presse Med 2012, 41(3 Pt 2):e115-e135.
6. Orth D., Würzner R. What makes an enterohemorrhagic Escherichia coli?. Clin Infect Dis 2006, 43:1168-1169.
7. Mariani-Kurkdjian P., Bingen E. Syndrome hémolytique et urémique: aspects microbiologiques. Arch Pediatr 2001, 8(S4):785-791.
8. Liu F., Huang J., Sadler J.E. Shiga toxin (Stx) 1B and Stx 2B induce von Willebrand factor secretion from human umbilical vein endothelial cells through different signaling pathways. Blood 2011, 118(12):3392-3398.
9. Acheson D.W., Moore R., De Breucker S. Translocation of Shiga toxin across polarized intestinal cells in tissue culture. Infect Immun 1996, 64(8):3294-3300.
10. MacLeod D.L., Gyles C.L., Wilcock B.P. Reproduction of edema disease of swine with purified Shiga-like toxin II variant. Vet Pathol 1991, 28(1):66-73.
11. Brigotti M., Carnicelli D., Ravanelli E., Barbieri S., Ricci F., Bontadini A., et al. Interactions between Shiga toxins and human polymorphonuclear leukocytes. J Leukoc Biol 2008, 84(4):1019-1027.
12. Exeni R.A., Fernandez G.C., Palermo M.S. Role of polymorphonuclear leukocytes in the pathophysiology of typical hemolitic uremic syndrome. Sci World J 2007, 7:1155-1164.
13. Griener T., Mulvey G.L., Marcato P., Armstrong G.D. Differential binding of Shiga toxin 2 to human and murine neutrophils. J Med Microbiol 2007, 56(11):1423-1430.
14. Te Loo D., Monnens L., van der Velden T., Vermeer M.A., Preyers F., Demacker P.N., et al. Binding and transfer of verocytotoxin by polymorphonuclear leukocytes in hemolytic uremic syndrome. Blood 2000, 95(11):3396-3402.
15. Geelen J.M., Van der Velden T., Van den Heuvel L., Monnens L.A. Interactions of Shiga-like toxin with human peripheral blood monocytes. Pediatr Nephrol 2007, 22(8):1181-1187.
16. Van Setten P.A., Monnens L.A., Verstraten R.G., van den Heuvel L.P., van Hinsbergh V.W. Effects of verocytotoxin on nonadherent human monocytes: binding characteristics, protein synthesis, and induction of cytokine release. Blood 1996, 88(1):174-183.
17. Keir L.S., Marks S.D., Kim J.J. Shiga toxin-associated hemolytic uremic syndrome: current molecular mechanisms and future therapies. Drug Des Dev Ther 2012, 6:195-208.
18. Ståhl A.L., Sartz L., Nelsson A., Békássy Z.D., Karpman D. Shiga toxin and lipopolysaccharide induce platelet-leukocyte aggregates and tissue factor release, a thrombotic mechanism in hemolytic uremic syndrome. PLoS One 2009, 4(9):e6990.
19. McGregor J.L. Rôle de la sélectine P (CD62P) dans les interactions des cellules endothéliales et des plaquettes activées avec les leucocytes. Hematologie 1995, 1(2):83-87.
20. Orth D., Würzner R. Complement in typical hemolitic uremic syndrome. Semin Thromb Hemost 2010, 36(6):620-624.
21. Ståhl A.L., Sartz L., Karpman Complement activation on platelet-leukocyte complexes and microparticles in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Blood 2011, 117(20):5503-5513.
22. Morigi M., Galbusera M., Gastoldi S., Locatelli M., Buelli S., Pezzotta A., et al. Alternative pathway activation of complement by Shiga toxin promotes exuberant C3a formation that triggers microvascular thrombosis. J Immunol 2011, 187(1):172-180.
23. Orth D., Khan A.B., Naim A., Grif K., Brockmeyer J., Karch H., et al. Shiga toxin activates complement and binds factor H: evidence for an active role of complement in hemolytic uremic syndrome. J Immunol 2009, 182(10):6394-6400.
24. Petruzziello-Pellegrini T.N., Yuen D.A., Page A.V., Patel S., Soltyk A.M., Matouk C.C., et al. The CXCR4/CXCR7/SDF-1 pathway contributes to the pathogenesis of Shiga toxin-associated hemolytic uremic syndrome in human and mice. J Clin Invest 2012, 122(2):759-776.
25. Ake J.A., Jelacic S., Ciol M.A., Watkins S.L., Murray K.F., Christie D.L., et al. Relative nephroprotection during Escherichia coli O157:H7 infections: association with intravenous volume expansion. Pediatrics 2005, 115:e673-e680.
26. Hickey C.A., Beattie T.J., Cowieso J., Miyashita Y., Strife C.F., Frem J.C., et al. Early volume expansion during diarrhea and relative nephroprotection during subsequent hemolytic uremic syndrome. Arch Pediatr Adolesc Med. 2011, 165(10):884-889.
27. Georges J.N. How I treat patients with thrombotic thrombocytopenic purpura: 2010. Blood 2010, 116(20):4060-4069.
28. Waters A.M., Licht C. aHUS caused by complement dysregulation: new therapies on the horizon. Pediatr Nephrol 2011, 26(1):41-57.
29. Kim J.J., Goodship T.H., Tizard J., Inward C. Plasma therapy for atypical haemolytic uraemic syndrome associated with heterozygous factor H mutations. Pediatr Nephrol 2011, 26(11):2073-2076.
30. Wong C.S., Mooney J.C., Brandt J.R., Staples A.O., Jelacic S., Boster D.R., et al. Risk factors for the hemolytic uremic syndrome in children infected with Escherichia coli O157. Clin Infect Dis 2012, 55(1):33-41.
31. McGannon C.M., Fuller C.A., Weiss A.A. Different classes of antibiotics differentially influence Shiga toxin production. Antimicrob Agents Chemother 2010, 54(9):3790-3798.
32. Corogeanu D., Willmes R., Wolke M., Plum G., Utermöhlen O., Krönke M. Therapeutic concentrations of antibiotics inhibit Shiga toxin release from enterohemorrhagic E.coli O104:H4 from the 2011 German outbreak. BMC Microbiol 2012, 12:160-170.
33. Nitschke M., Sayk F., Härtel C., Roseland R.T., Hauswaldt S., Steinhoff J., et al. Association between azithromycine therapy and duration of bacterial shedding among patients with Shiga toxin-producing enteroaggregative Escherichia coli O104:H4. JAMA 2012, 307(10):1046-1052.
34. Eremina V., Jefferson J.A., Kowalewska J., Hochster H., Haas M., Weisstuch J., et al. VEGF inhibition and renal trombotic microangiopathy. N Engl J Med 2008, 358(11):1129-1136.
35. Psotka M.A., Obata F., Kolling G.L., Gross L.K., Saleem M.A., Satchell S.C., et al. Shiga toxin 2 targets the murine renal collecting duct epithelium. Infect Immun 2009, 77(3):959-969.
36. Armstrong G.D., Rowe P.C., Goodyer P., Orrbine E., Klassen T.P., Wells G., et al. A phase I study of chemically synthesized verotoxin (Shiga-like toxin) Pk-trisaccharide receptors attached to chromosorb for preventing hemolytic-uremic syndrome. J Infect Dis 1995, 171(4):1042-1045.
37. Trachtman H., Cnaan A., Christen E., Gibbs K., Zhao S., Acheson D.W., et al. Effect of an oral Shiga toxin binding agent on diarrhea associated hemolytic uremic syndrome in children: a randomized controlled trial. JAMA 2003, 290(10):1337-1344.
38. Karmali M.A. Prospects for preventing serious systemic toxemic complications of Shiga toxin-producing Escherichia coli infections using Shiga toxin receptor analogues. J Infect Dis 2004, 189(3):355-359.
39. Nishikawa K., Watanabe M., Kita E., Igai K., Omata K., Yaffe M.B., et al. A multivalent peptide library approach identifies a novel Shiga toxin inhibitor that induces aberrant cellular transport of the toxin. FASEB J 2006, 20(14):E2077-E2086.
40. Stearns-Kurosawa D.J., Collins V., Freeman S., Debord D., Nishikawa K., Oh S.Y., et al. Rescue from lethal Shiga toxin 2-induced renal failure with a cell-permeable peptide. Pediatr Nephrol 2011, 26(11):2031-2039.
41. Mulvey G.L., Marcato P., Kitov P.I., Sadowska J., Bundle D.R., Armstrong G.D. Assessment in mice of the therapeutic potential of tailored, multivalent Shiga toxin carbohydrate ligands. J Infect Dis 2003, 187(4):640-649.
42. Mukherjee J., Chios K., Fishwild D., Hudson D., O'Donnell S., Rich S.M., et al. Human Stx2-specific monoclonal antibodies prevent systemic complications of Escherichia coli O157:H7 infection. Infect Immun 2002, 70(2):612-619.
43. Yamagami S., Motoki M., Kimura T., Izumi H., Takeda T., Katsuura Y., et al. Efficacy of postinfection treatment with anti-Shiga toxin (Stx) 2 humanized monoclonal antibody TMA-15 in mice lethally challenged with Stx-producing Escherichia coli. J Infect Dis 2001, 184(6):738-742.
44. Lopez E.L., Contrini M.M., Glatstein E., González Ayala S., Santoro R., Allende D., et al. Safety and pharmacokinetics of Urtoxazumab, a humanized monoclonal antibody, against Shiga-like toxin 2 in healthy adults and in pediatric patients infected with Shiga-like toxin-producing Escherichia coli. Antimicrob Agents Chemother 2010, 54(1):239-243.
45. Dowling T.C., Chavaillaz P.A., Young D.G., Melton-Celsa A., O'Brien A., Thuning-Roberson C., et al. Phase 1 safety and pharmacokinetic study of chimeric murine-human monoclonal antibody cαStx2 administered intravenously to healthy adult volunteers. Antimicrob Agents Chemother 2005, 49(5):1808-1812.
46. Bitzan M., Poole R., Mehran M., Sicard E., Brockus C., Thuning-Roberson C., et al. Safety and pharmacokinetic of chimeric anti-Shiga toxin 1 and anti-Shiga toxin 2 monoclonal antibodies in healthy volunteers. Antimicrob Agents Chemother 2009, 53(7):3081-3087.
47. Lapeyraque A.L., Malina M., Fremeaux-Bacchi V., Boppel T., Kirschfink M., Oualha M., et al. Eculizumab in severe Shiga toxin-associated HUS. N Engl J Med 2011, 364(26):2561-2563.
48. Kielstein J.T., Beutel G., Fleig S., Steinhoff J., Meyer T.N., Hafer C., et al. Best supportive care and therapeutic plasma exchange with or without Eculizumab in Shiga toxin-producing E.coli O104:H4 induced haemolytic-uraemic syndrome: an analysis of the German STEC-HUS registry. Nephrol Dial Transplant 2012, 27(10):3807-3815.
49. Delmas Y., Vendrely B., Clouzeau B., Bachir H., Bui H.N., Lacraz A., et al. Outbreak of Escherichia coli O104:H4 haemolytic uraemic syndrome in France: outcome with eculizumab. Nephrol Dial Transplant 2014, 29:565-572.
50. Honda T., Ogata S., Mineo E., Nagamori Y., Nakamura S., Bando Y., et al. A novel strategy for hemolytic uremic syndrome: successful treatment with thrombomodulin α. Pediatrics 2013, 131:e928-e933.
51. Kawasaki y, Suyama K., Ono A., Oikawa T., Ohara S., Suzuki Y., et al. Efficacy of recombinant human soluble thrombomodulin for childhood hemolytic uremic syndrome. Pediatr Int 2013, 55(5):e139-e142.
52. Mukhopadhyay S., Linstedt A.D. Manganese blocks intracellular trafficking of Shiga toxin and protects against Shiga toxicosis. Science 2012, 335(6066):332-335.
53. Gaston M.A., Pellino C.A., Weiss A.A. Failure of manganese to protect from Shiga toxin. PLoS One 2013, 8(7):e69823.
54. Mukhopadhyay S., Redler B., Linstedt A.D. Shiga toxin-binding site for host cell receptor GPP130 reveals unexpected divergence in toxin-trafficking mechanisms. Mol Biol Cell 2013, 24(15):2311-2318.
55. Tewari R., Jarvela T., Linstedt A.D. Manganese induces oligomerization to promote down-regulation of the intracellular trafficking receptor used by Shiga toxin. Mol Biol Cell 2014, 25(19):3049-3058.
56. Nester C.M., Thomas C.P. Atypical hemolytic uremic syndrome: what is it, how is it diagnosed, and how is it treated?. Hematology Am Soc Hematol Educ Program 2012, 2012:617-625.
57. Loirat C., Frémeaux-Bacchi V. Atypical hemolytic uremic syndrome. Orphanet J Rare Dis 2011, 6:60-90.
58. Maga T.K., Nishimura C.J., Weaver A.E., Frees K.L., Smith R.J. Mutations in alternative pathway complement proteins in American patients with atypical hemolytic uremic syndrome. Hum Mutat 2010, 31(6):E1445-E1460.
59. Salvadori M., Bertoni E. Update on hemolytic uremic syndrome: diagnostic and therapeutic recommendations. World J Nephrol 2013, 2(3):56-57.
60. Caprioli J., Noris M., Brioschi S., Pianetti G., Castelletti F., Bettinaglio P., et al. Genetics of HUS: the impact of MCP, CFH, and IF mutations on clinical presentation, response to treatment, and outcome. Blood 2006, 108(4):1267-1279.
61. Skerka C., Chen Q., Fremeaux-Bacchi V., Roumenina L.T. Complement factor H related proteins (CFHRs). Mol Immunol 2013, 56:170-180.
62. Caprioli J., Casteletti F., Bucchioni S., Bettinaglio P., Bresin E., Pianetti G., et al. Complement factor H mutations and gene polymorphisms in haemolytic uraemic syndrome: the C-257T, the A2089G and the G2881T polymorphisms are strongly associated with the disease. Hum Mol Genet 2003, 12(24):3385-3396.
63. Lemaire M., Frémeaux-Bacchi V., Schaefer F., Choi M., Tang W.H., Le Quintrec M., et al. Recessive mutations in DGKE cause atypical haemolytic-uremic syndrome. Nat Genet 2013, 45(5):531-536.
64. Al-Nouri Z.L., Reese J.A., Terell D.R., Vesely S.K., George J.N. Drug-induced thrombotic microangiopathy: a systematic review of published reports. Blood 2015, 125(4):616-618.
65. Loirat C., Garnier A., Sellier-Leclerc A.L., Kwon T. Plasmatherapy in atypical hemolytic and uremic syndrome. Semin Thromb Hemost 2010, 36(6):673-681.
66. Lapeyraque A.L., Wagner E., Phan V., Clermont M.J., Merouani A., Frémeaux-Bacchi V., et al. Efficacy of plasma therapy in atypical hemolytic uremic syndrome with complement factor H mutations. Pediatr Nephrol 2008, 23(8):1363-1366.
67. Loirat C., Noris M., Fremeaux-Bacchi V. Complement and the atypical hemolytic uremic syndrome in children. Pediatr Nephrol 2008, 23(11):1957-1972.
68. Nathanson S., Ulinski T., Frémeaux-Bacchi V., Deschênes G. Secondary failure of plasma therapy in factor H deficiency. Pediatr Nephrol 2006, 21(11):1769-1771.
69. Michon B., Moghrabi A., Winikoff R., Barrette S., Bernstein M.L., Champagne J., et al. Complication of apheresis in children. Transfusion 2007, 47(10):1837-1842.
70. Goicoechea de Jorge E., Macor P., Paixão-Cavalcante D., Rose K.L., Tedesco F., Cook H.T., et al. The development of atypical hemolytic uremic syndrome depends on complement C5. J Am Soc Nephrol 2011, 22(1):137-145.
71. Legendre C.M., Licht C., Muus P., Greenbaum L.A., Babu S., Bedrosian C., et al. Terminal complement inhibitor eculizumab in atypical haemolytic-uremic syndrome. N Engl J Med 2013, 368(23):2169-2181.
72. Zuber J., Fakhouri F., Roumenina L.T., Loirat C., Frémeaux-Bacchi V., French Study Group for aHUS/C3G Use of Eculizumab for atypical haemolytic uraemic syndrome and C3 glomerulopathies. Nat Rev Nephrol 2012, 8(11):643-657.
73. Ranch D., Crowther B., Arar M., Assanasen C. Prophylactic eculizumab for kidney transplantation in a child with atypical hemolytic uremic syndrome due to complement factor H mutation. Pediatr Transplantation 2014, 18(6):185-189.
74. Matar D., Naqvi F., Racusen L.C., Carter-Monroe N., Montgomery R.A., Alachkar N. Atypical hemolytic uremic syndrome recurrence after kidney transplantation. Transplantation 2014, 98(11):1205-1212.
75. Loirat C., Frémeaux-Bacchi V. Anti-factor H autoantibody-associated hemolytic uremic syndrome: the earlier diagnosed and treated, the better. Kidney Int 2014, 85(5):1019-1022.
76. Sinha A., Gulati A., Saini S., Blanc C., Gupta A., Gurjar B.S., et al. Prompt plasma exchanges and immunosuppressive treatment improves the outcomes of anti-factor H autoantibody-associated hemolytic uremic syndrome in children. Kidney Int 2014, 85(5):1151-1160.
77. Khandelwal P., Gupta A., Sinha A., Saini S., Hari P., Dragon-Durey M.A., et al. Effect of plasma exchange and immunosuppressive medications on antibody titers and outcome in anti-complement factor H antibody-associated haemolytic uremic syndrome. Pediatr Nephrol 2015, 30(3):451-457.
78. Boyer O., Balzamo E., Charbit M., Biebuyck-Gougé N., Salomon R., Dragon-Durey M.A., et al. Pulse cyclophosphamide therapy and clinical remission in atypical haemolytic uremic syndrome with anti-complement factor H autoantibodies. Am J Kidney Dis 2010, 55(5):923-927.
79. Taylor C.M., Machin S., Wigmore S.J., Goodship T.H. Clinical Practice Guidelines for the management of atypical Haemolytic Uraemic Syndrome in the United Kingdom. Br J Haematol 2009, 148(1):37-47.
80. Saland M., Ruggenenti P., Remuzzi G., Consensus Study Group Liver-kidney transplantation to cure atypical hemolytic uremic syndrome. J Am Soc Neprol 2009, 20(2):940-949.
81. Cheong H.I., Lee B.S., Kang H.G., Hahn H., Suh K.S., Ha I.S., et al. Attempted treatment of factor H deficiency by liver transplantation. Pediatr Nephrol 2004, 19(4):454-458.
82. Remuzzi G., Ruggenenti P., Colledan M., Gridelli B., Bertani A., Bettinaglio P., et al. Hemolytic uremic syndrome: a fatal outcome after kidney and liver transplantation performed to correct factor H gene mutation. Am J Transplant 2005, 5(5):1146-1150.
83. Koskinen A.R., Tukiainen E., Arola J., Nordin A., Höckerstedt H.K., Nilsson B., et al. Complement activation during liver transplantation-special emphasis on patients with atypical hemolytic uremic syndrome. Am J Transplant 2011, 11:1885-1895.
84. Wilson C., Torpey N., Jaques B., Strain L., Talbot D., Manas D., et al. Successful simultaneous liver-kidney transplant in an adult with atypical hemolytic uremic syndrome associated with a mutation in complement factor H. Am J Kidney Dis 2011, 58(1):109-112.
85. Saland J.M., Shneider B.L., Bromberg J.S., Shi P.A., Ward S.C., Magid M.S., et al. Successful split liver-kidney transplant for factor H associated hemolytic uremic syndrome. Clin J Am Soc Nephrol 2009, 4(1):201-206.
86. Jalanko H., Peltonen S., Koskinen A., Puntila J., Isoniemi H., Holmberg C., et al. Successful liver-kidney transplantation in two children with aHUS caused by a mutation in complement factor H. Am J Transplant 2008, 8(1):216-221.
87. Forbes T.A., Bradbury M.G., Goodship T.H., McKiernan P.J., Milford D.V. Changing strategies for organ transplantation in atypical haemolytic uraemic syndrome: a tertiary case series. Pediatr Transplant 2013, 17(3):e93-e99.
88. Nester C., Stewart Z., Myers D., Jetton J., Nair R., Reed A., et al. Pre-emptive Eculizumab and plasmapheresis for renal transplant in atypical hemolytic uremic syndrome. Clin J Am Soc Nephrol 2011, 6(6):1488-1494.
89. Weitz M., Amon O., Bassler D., Koenigsrainer A., Nadalin S. Prophylactic eculizumab prior to kidney transplantation for atypical hemolytic uremic syndrome. Pediatr Nephrol 2011, 26(8):1325-1329.
90. Haller W., Milford D.V., Goodship T.H.J., Sharif K., Mirza D.F., McKiernan P.J. Successful isolated liver transplantation in a child with atypical hemolytic uremic syndrome and a mutation in complement factor H. Am J Transplant 2010, 10(9):2142-2147.
91. Brandstätter H., Schulz P., Polunic I., Kannicht C., Kohla G., Römisch J. Purification and biochemical characterization of functional complement factor H from human plasma fractions. Vox Sang 2012, 103(3):201-212.