Abstract
We reviewed the literature to analyze the risk of recurrence of hemolytic uremic syndrome (HUS) after renal transplantation in children. Among 118 children transplanted after post-diarrheal (D+) HUS, 1 (0.8%) had recurrence with graft loss. Among 63 children transplanted after HUS not associated with a prodrome of diarrhea (D−) of unknown mechanism, 13 (21%) had recurrence with graft loss. Of 11 patients with HUS associated with factor H deficiency who were transplanted, 5 lost the graft because of recurrence. Of 7 patients with HUS associated with normal factor H concentration but mutations in factor H gene who were transplanted, probably 2 had recurrence. Three patients with HUS associated with low serum C3, but no factor H deficiency or mutation lost their graft because of recurrence. The risk of recurrence in the autosomal recessive forms of HUS of unknown mechanism is not documented in children, but is around 60% in adults. A similar risk has been reported in the autosomal dominant forms. The only transplant patient with a constitutional deficiency of von Willebrand factor-cleaving protease had recurrence. Further efforts to document the post-transplant course of patients with D− HUS and progress in the understanding of the mechanisms and genetics of the disease are needed to allow more accurate prediction of the recurrence risk and to define therapeutic approaches.
Similar content being viewed by others
References
Loirat C, Ehrich JHH, Geerlings W, Jones EHP, Landais P, Mallick NP, Margreiter R, Raine AEG, Salmela K, Selwood NH, Tufveson G, Valderrabano F (1994) Report on management of renal failure in children in Europe, XXIII, 1992. Nephrol Dial Transplant 9 [Suppl 1]:26–40
Leonard MB, Donaldson LA, Ho M, Geary DF (2003) A prospective cohort study of incident maintenance dialysis in children: an NAPRTC Study. Kidney Int 63:744–755
Gagnadoux MF, Habib R, Gubler MC, Bacri JL, Broyer M (1996) Long-term (15–25 years) outcome of childhood hemolytic uremic syndrome. Clin Nephrol 46:39–41
Repetto HA (1997) Epidemic hemolytic-uremic syndrome in children. Kidney Int 52:1708–1719
Huseman D, Gellermann J, Vollmer I, Ohde I, Devaux S, Ehrich JH, Filler G (1999) Long-term prognosis of hemolytic uremic syndrome and effective plasma flow. Pediatr Nephrol 13:672–677
Niaudet P, Gagnadoux MF, Broyer M, Salomon R (2000) Hemolytic-uremic syndrome: hereditary forms and forms associated with hereditary diseases. Adv Nephrol Necker Hosp 30:261–280
Ruggenenti P, Remuzzi G (2001) Thrombotic microangiopathy, hemolytic uremic syndrome, and thrombotic thrombocytopenic purpura. Kidney Int 60:831–846
Warwicker P, Goodship THJ, Donne RL, Pirson Y, Nicholls A, Ward RM, Turnpenny P, Goodship JA (1998) Genetic studies into inherited and sporadic hemolytic uremic syndrome. Kidney Int 53:836–844
Loo DM te, Levtchenko E, Furlan M, Roosendaal GP, Heuvel LP van den (2000) Autosomal recessive inheritance of von Willebrand factor-cleaving protease deficiency. Pediatr Nephrol 14:762–765
Veyradier A, Obert B, Haddad E, Cloarec S, Nivet H, Foulard M, Lesure F, Delattre P, Lakhdari M, Meyer D, Girma JP, Loirat C (2003) Severe deficiency of the specific von Willebrand factor-cleaving protease (ADAMTS 13) activity in a subgroup of children with atypical hemolytic uremic syndrome. J Pediatr 142:310–317
Ruggenenti P (2002) Post-transplant hemolytic-uremic syndrome. Kidney Int 62:1093–1104
Agarwal A, Mauer SM, Matas AJ, Nath KA (1995) Recurrent hemolytic uremic syndrome in an adult renal allograft recipient: current concepts and management. J Am Soc Nephrol 6:1160–1169
Mor E, Lustig S, Tovar A, Bar-Nathan N, Shharabani E, Shapira Z, Yusim A (2000) Thrombotic microangiopathy early after kidney transplantation: hemolytic uremic syndrome or vascular rejection? Transplant Proc 32:686–687
Mehls O, Rigden S, Ehrich JHH, Berthoux F, Jones EH, Valderrabano F (1996) Report on management of renal failure in Europe, XXV, 1994. The child-adult interface. The EDTA-ERA Registry. European Dialysis and Transplant Association-European Renal Association. Nephrol Dial Transplant 11 [Suppl 1]:22–36
Kashtan CE, McEnery PT, Tejani A, Stablein DM (1995) Renal allograft survival according to primary diagnosis: a report of the North American Pediatric Renal Transplant Cooperative Study. Pediatr Nephrol 9:679–684
Quan A, Sullivan EK, Alexander SR (2001) Recurrence of hemolytic uremic syndrome after renal transplantation in children. A report of the North American Pediatric Renal Transplant Cooperative Study. Transplantation 72:742–745
Ducloux D, Rebibou JM, Semhoun-Ducloux S, Jamali M, Fournier V, Bresson-Vautrin C, Chalopin JM (1998) Recurrence of hemolytic-uremic syndrome in renal transplant recipients. Transplantation 65:1405–1407
Lahlou A, Lang P, Charpentier B, Barrou B, Glotz D, Baron C, Hiesse C, Kreis H, Legendre C, Bedrossian J, Mougenot B, Sraer JD, Rondeau E (2000) Hemolytic uremic syndrome. Recurrence after renal transplantation. Groupe Cooperatif d'Ile-de-France. Medicine (Baltimore) 79:90–102
Pirson Y, Leclercq B, Squifflet JP, Alexandre GPJ, Van Ypersele De Strihou C (1986) Good prognosis of the hemolytic uremic syndrome after renal transplantation (abstract). Nephrol Dial Transplant 1:134
Gagnadoux MF, Habib R, Niaudet P, Broyer M (1996) Results of renal transplantation in childhood hemolytic-uremic syndrome (abstract). J Am Soc Nephrol 7:1908
Müller T, Sikora P, Offner G, Hoyer PF, Brodehl J (1998) Recurrence of renal disease after kidney transplantation in children: 24 years of experience in a single center. Clin Nephrol 49:82–90
Ferraris J, Ramirez JA, Ruiz S, Caletti MG, Vallejo G, Piantanida JJ, Araujo JL, Sojo ET (2002) Shiga toxin-associated hemolytic uremic syndrome: absence of recurrence after renal transplantation. Pediatr Nephrol 17:809–814
Eijenraam FJ, Donckerwolcke RA, Monnens LA, Proesmans W, Wolf ED, Van Damme B (1990) Renal transplantation in 20 children with hemolytic-uremic syndrome. Clin Nephrol 33:87–93
Miller RB, Burke BA, Schmidt WJ, Gillingham KJ, Matas AJ, Mauer M, Kashtan CE (1997) Recurrence of haemolytic-uremic syndrome in renal transplants: a single-centre report. Nephrol Dial Transplant 12:1425–1430
Fitzpatrick MM, Walters MDS, Trompeter RS, Dillon MJ, Barratt TM (1993) Atypical (non-diarrhea associated) hemolytic uremic syndrome in childhood. J Pediatr 122:532–537
Neuhaus TJ, Calonder S, Leumann EP (1997) Heterogeneity of atypical haemolytic uraemic syndrome. Arch Dis Child 76:518–521
Folman R, Arbus GS, Churchill B, Gaum L, Huber J (1978) Recurrence of the hemolytic uremic syndrome in a 3 1/2-year-old child, 4 months after second renal transplantation. Clin Nephrol 10:121–127
Case records of the Massachussetts General Hospital (1986) Renal disorder 13 months after renal transplantation for the hemolytic uremic syndrome. N Engl J Med 314:1032–1040
Springate J, Fildes R, Anthone S, Anthone R, Brentjens J, O'Shea M, Feld L (1988) Recurrent hemolytic uremic syndrome after renal transplantation. Transplant Proc 20:559–561
Goodman DJ, Walker RG, Birchall IE, Apice AJF d′, Powell HR, Kincaid-Smith P (1991) Recurrent haemolytic uremic syndrome in a transplant recipient on orthoclone (OKT3). Pediatr Nephrol 5:240–241
Mochon M, Kaiser BA, De Chadarevian JP, Polinsky MS, Baluarte HJ (1992) Cerebral infarct with recurrence of hemolytic-uremic syndrome in a child following renal transplantation. Pediatr Nephrol 6:550–552
Scantlebury VP, Shapiro R, McCauley J, Jordan M, Vivas C, Irish W, Tzakis A, Ellis D, Gilboa N, Starzl TE (1995) Renal transplantation under cyclosporine and FK506 for hemolytic uremic syndrome. Transplant Proc 27:842–843
Davin JC, Gruppen M, Bouts AH, Groothoff JW, Amstel SP van, Surachno J, Berge IJ ten, Weening JJ (1999) Relapse of atypical haemolytic uraemic syndrome after kidney transplantation: role of ATG and failure of mycophenolate mofetil as rescue therapy. Nephrol Dial Transplant 14:984–987
Florman S, Benchimol C, Lieberman K, Burrows L, Bromberg JS (2002) Fulminant recurrence of atypical hemolytic uremic syndrome during a calcineurin inhibitor-free immunosuppression regimen. Pediatr Transplant 6:352–355
Donne RL, Abbs I, Barany P, Elinder CG, Little M, Conlon P, Goodship TH (2002) Recurrence of hemolytic uremic syndrome after live related renal transplantation associated with subsequent de novo disease in the donor. Am J Kidney Dis 40:E22
Caprioli J, Bettinaglio P, Zipfel P, Amadei B, Daina E, Gamba S, Skerka C, Marziliano N, Remuzzi G, Noris M; Italian Registry of Familial and Recurrent HUS/TTP (2001) The molecular basis of familial hemolytic uremic syndrome: mutation analysis of factor H gene reveals a hot spot in short consensus report 20. J Am Soc Nephrol 12:297–307
Noris M, Ruggenenti P, Perna A, Orisio S, Caprioli J, Skerka C, Vasile B, Zipfel PF, Remuzzi G (1999). Hypocomplementemia discloses genetic predisposition to hemolytic uremic syndrome and thrombotic thrombocytopenic purpura: role of factor H abnormalities. Italian Registry of Familial and Recurrent Hemolytic Uremic Syndrome/Thrombotic Thrombocytopenic Purpura. J Am Soc Nephrol 10:281–293
Roodhooft AM, Mc Lean RH, Elst E, Van Acker KJ (1990) Recurrent hemolytic uremic syndrome and acquired hypomorphic variant of the third compoment of complement. Pediatr Nephrol 4:597–599
Warwicker P, Donne RL, Goodship JA, Goodship TH, Howie AJ, Kumararatne DS, Thompson RA, Taylor CM (1999) Familial relapsing haemolytic uraemic syndrome and complement factor H deficiency. Nephrol Dial Transplant 14:1229–1233
Landau D, Shalev H, Levy-Finer G, Polonsky A, Segev Y, Katchko L (2001) Familial hemolytic uremic syndrome associated with complement factor H deficiency. J Pediatr 138:412–417
Pirson Y, Lefebvre C, Arnout C, Ypersele De Strihou C van (1987) Hemolytic uremic syndrome in three adult siblings: a familial study and evolution. Clin Nephrol 28:250–255
Kaplan BS, Papadimitriou M, Brelin JH, Tomlanovich JJ, Zulkharnain (1997) Renal transplantation in adults with autosomal recessive inheritance of hemolytic uremic syndrome. Am J Kidney Dis 30:760–765
Kaplan BS, Leonard MB (2000) Autosomal dominant hemolytic uremic syndrome: variable phenotype and transplant results. Pediatr Nephrol 14:464–468
Deschenes G, Veyradier A, Cloarec S, Benoit S, Desbois I, Gruel Y, Nivet H (2002) Plasma therapy in von Willebrand factor protease deficiency. Pediatr Nephrol 17:867–870
Cheong HI, Lee BS, Kang HG, Hahn H, Ha IS, Choi Y, Seo KS (2001) Treatment of factor H (FH) deficiency-associated atypical hemolytic uremic syndrome (HUS) with liver transplantation—a case report (abstract). J Am Soc Nephrol 12:550A
Remuzzi G, Ruggenenti P, Codazzi D, Noris M, Caprioli J, Locatelli G, Gridelli B (2002) Combined kidney and liver transplantation for familial haemolytic uraemic syndrome. Lancet 359:1671–1672
Bergstein J, Michael A Jr, Kellstrand C, Simmons R, Najarian J (1974) Hemolytic-uremic syndrome in adult sisters. Transplantation 17:487–490
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Loirat, C., Niaudet, P. The risk of recurrence of hemolytic uremic syndrome after renal transplantation in children. Pediatr Nephrol 18, 1095–1101 (2003). https://doi.org/10.1007/s00467-003-1289-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00467-003-1289-8