Liver transplantation in monogenic diseases: clinical experience of the Petrovsky National Research Centre of Surgery
Abstract The group of monogenic diseases combines different hereditary conditions associated with single gene mutation. Any of these conditions is quite rare. At the same time, the morbidity and mortality rates in this group are quite high. This fact stimulates active search for effective methods of treatment. Despite the achievements of the last decades in pharmacology and gene therapy, liver transplantation remains one of the most important and effective treatment options for patients with monogenic liver diseases. This report provides a brief overview of the different monogenic diseases, determining the presence of the indications for liver transplantation. On the example of a six-year experience of Liver Transplantation Department of Russian Research Center of Surgery reviewed all clinical forms of monogenic diseases, which determined the indications for liver transplantation in this period. Each form of monogenic diseases [Wilson's disease (n=10), progres- sive familial intrahepatic cholestasis type I (n=6), glycogenosis type I (n=3), Alagille syndrome (n=4), primary hyperoxaluria type I (n=1), deficiency of α1-antitrypsin (n=1)] is illustrated with clinical case. Good long-term results of treatment with 6-year actuarial survival rate at 88% demonstrate the high efficiency of liver transplantation in the treatment of patients with monogenic diseases.
Keywords:liver transplantation, monogenic diseases, inborn metabolic diseases
Clin. Experiment. Surg. Petrovsky J. – 2015. – N 1. – Р. 22–35.
References
1. Kamoun A., Lakhoua R. End-stage renal disease of the Tunisian child: epidemiology, etiologies, and outcome // Pediatr. Nephrol. 1996. Vol. 10, N 4. P. 479-482.
2. Alagille D., Odie`vre M., Gautier M., Dommergues J.P. Hepatic ductular hypoplasia associated with characteristic facies, vertebral malformations, retarded physical, mental, and sexual development, and cardiac murmur // Pediatrics. 1975. Vol. 86. P. 63-71.
3. Al-Eisa A.A., Samhan S., Naseef M. End-stage renal disease in Kuwaiti children: an 8-year experience // Transplant. Proc. 2004. Vol. 36, N 6. P. 1788-1791.
4. Alissa F.T., Jaffe R., Shneider B.L. Update on progressive familial intrahepatic cholestasis // J. Pediatr. Gastroenterol. Nutr. 2008. Vol. 46. P. 241-252.
5. Arnon R., Annunziato R., Miloh T. et al. Orthotopic liver transplantation for children with Alagille syndrome // Pediatr. Transplant. 2010. Vol. 14. P. 622-628.
6. Bearn A.G. A genetical analysis of thirty families with Wil- son’s disease (hepatolenticular degeneration) // Ann. Hum. Genet. 1960. Vol. 24. P. 33-43.
7. Boers S., Visser G., Smit P., Fuchs S. Liver transplantation in glycogen storage disease type I // Orphanet J. Rare Dis. 2014. Vol. 9. P. 47. doi:10.1186/1750-1172-9-47.
8. Bordignon C., Notarangelo L.D., Nobili N. et al. Gene therapy in peripheral blood lymphocytes and bone marrow for ADA- immunodeficient patients // Science. 1995. Vol. 270. P. 470-475.
9. Brewer G.J., Askari F. Transplant livers in Wilson’s disease for hepatic, not neurologic, indications // Liver Transpl. 2000. Vol. 6. P. 662-664.
10. Bull P.C., Thomas G.R., Rommens J.M. et al. The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene // Nat. Genet. 1993. Vol. 5. P. 327-337.
11. Clayton R.J., Iber F.L., Ruebner B.H., McKusick V.A. Byler disease: fatal familial intrahepatic cholestasis in an Amish kindred // J. Pediatr. 1965. Vol. 67. P. 1025-1028.
12. Cochat P., Deloraine A., Rotily M. et al. Epidemiology of primary hyperoxaluria type 1. Nephrol. Dial. Transplant. 1995. Vol. 10, suppl. 8. P. 3-7.
13. Colombo C., Vajro P., Degiorgio D. et al. Clinical features and genotype-phenotype correlations in children with progressive familial intrahepatic cholestasis type 3 related to ABCB4 mutations // J. Pediatr. Gastroenterol. Nutr. 2011. Vol. 52. P. 73-83.
14. Cramer S.D., Ferree P., Lin K. et al. The gene encoding hydroxypyruvate reductase (GRHPR) is mutated in patients with primary hyper- oxaluria type II // Hum. Mol. Genet. 1999. Vol. 8, N 11. P. 2063-2069.
15. Cregeen G.R. Identification and expression of a cDNA for human hydroxypyruvate/glyoxylate reductase // Biochim. Biophys. Acta. 1999. Vol. 1446, N 3. P. 383-388.
16. Cunniff C., Carmack J.L., Kirby R.S., Fiser D.H. Contribution of heritable disorders to mortality in the pediatric intensive care unit // Pediatrics. 1995. Vol. 95. P. 678-81.
17. Danpure C.J, Rumsby G. Molecular aetiology of primary hyperoxaluria and its implications for clinical management // Expert Rev. Mol. Med. 2004. Vol. 6, N 1. P. 1-16.
18. Davit-Spraul A., Fabre M., Branchereau S. et al. ATP8B1 and ABCB11 analysis in 62 children with normal gamma-glutamyl transferase progressive familial Intrahepatic cholestasis (PFIC): phenotypic differences between PFIC1 and PFIC2 and natural history // Hepatology. 2010. Vol. 51. P. 1645-1655.
19. Dye D.E., Brameld K.G., Maxwell S. et. al. The impact of single gene and chromosomal disorders on hospital admissions of children and adolescents: a population-based study // Public Health Genomics. 2011. Vol. 14. P. 153-161.
20. Dye D.E., Brameld K.J., Maxwell S. et al. The impact of single gene and chromosomal disorders on hospital admissions in an adult population // J. Community Genet. 2011. Vol. 2, N 2. P. 81-90.
21. Eghtesad B., Nezakatgoo N., Geraci L.C. et al. Liver transplantation for Wilson’s disease: a singlecenter experience // Liver Transpl. Surg. 1999. Vol. 5. P. 467-474.
22. Ekstein J., Rubin B.Y., Anderson S.L. et al. Mutation frequencies for glycogen storage disease Ia in the Ashkenazi Jewish population // Am. J. Med. Genet A. 2004. Vol. 129. P. 162-164.
23. Emre S., Atillasoy E.O., Ozdemir S. et al. Orthotopic liver transplantation for Wilson’s disease: a singlecenter experience // Transplantation. 2001. Vol. 72. P. 1232-1236.
24. Fagiuoli S., Daina E., D’Antiga L. et al. Monogenic disease that can be cured by liver transplantation // J. Hepatol. 2013. Vol. 59. P. 595-612.
25. Fischer A., Cavazzana-Calvo M. Gene therapy of inherited diseases // Lancet. 2008. Vol. 371. P. 2044-2047.
26. Froissart R., Piraud M., Boudjemline A.M. et al. Glucose-6-phosphosphatase deficiency // Orphanet J. Rare Dis. 2011. Vol. 6. P. 27. doi:10.1186/1750-1172-6-27.
27. Frydman M. Genetic aspects of Wilson’s disease // J. Gastroenterol. Hepatol. 1990. Vol. 5. P. 483-490.
28. Guarino M., Stracciari A., D’Alessandro R., Pazzaglia P. No neurological improvement after liver transplantation for Wilson’s disease // Acta Neurol. Scand. 1995. Vol. 92. P. 405-408.
29. Harambat J., Fargue S., Baccetta J. et al. Primary hyperoxaluria // Int. J. Nephrol. 2011. Article ID: 864580.
30. Harper J.A., Yuan J.S., Tan J.B. et al. Notch signaling in development and disease // Clin. Genet. 2003. Vol. 64, N 6. P. 461-472.
31. Hiraiwa H., Pan C.J., LinB. et al. Inactivation of the glucose 6-phosphate transporter causes glycogen storage disease type 1b //J. Biol. Chem. 1999. Vol. 274. P. 5532-5536.
32. Hoppe B., Latta K. Primary hyperoxaluria: the German experience // Am. J. Nephrol. - 2005. Vol. 25, N 3. P. 276-281.
33. Hoppe B., Beck B., Milliner D. The primary hyperoxalurias//Kidney Int. 2009. Vol. 75, N 12. P. 1264-1271.
34. Hori T., Egawa H., Takada Y. et al. Liver disease in alpha-1 antitrypsin deficiency: current understanding and future therapy // COPD (Journal of Chronic Obstructive Pulmonary Disease). 2013. Vol. 10, suppl. 1. P. 35-43.
35. Illies F., Bonzel K., Wingen A. et al. Clearance and removal of oxalate in children on intensified dialysis for primary hyperoxaluria type 1 // Kidney Int. 2006. Vol. 70, N 9. P. 1642-1648.
36. Jamieson N.V. A 20-year experience of combined liver/kidney transplantation for primary hyperoxaluria (PH1): the European PH1 transplant registry experience 1984-2004 // Am. J. Nephrol. 2005. Vol. 25, N 3. P. 282-289.
37. Kamath B.M., Loomes K.M., Piccoli D.A. Medical Management of Alagille Syndrome // J. Pediatr. Gastroenterol. Nutr. 2010. Vol. 50, N 6. P. 580-586.
38. Kamath B.M., Bason L., Piccoli D.A. et al. Medical Genetics. Consequences of JAG1 mutations // J. Med. Genet. 2003. Vol. 40. P. 891-895.
39. Kassam N., Witt N., Kneteman N., Bain V.G. Liver transplantation for neuropsychiatric Wilson disease // Can. J. Gastroenterol. 1998. Vol. 12. P. 65-68.
40. Lei K.J., Shelly L.L., Pan C.J. et al. Mutations in the glucose- 6-phosphatase gene that cause glycogen storage disease type 1a // Science. - 1993. - Vol. 262. - P. 580-583.
41. Leumann N.K. Changing pattern of primary hyperoxaluria in Switzerland // Nephrol. Dial. Transplant. 1995. Vol. 10, N 12. P. 2224-2227.
42. Liu C., Aronow B.J., Jegga A.G. et al. Novel resequencing chip customized to diagnose mutations in patients with inherited syndromes of intrahepatic cholestasis // Gastroenterology. 2007. Vol. 132. P. 119-126.
43. Mistry J., Danpure C., Chalmers R. Hepatic D-glycerate dehydrogenase and glyoxylate reductase deficiency in primary hyperoxaluria type 2 // Biochem. Soc. Trans. 1988. Vol. 16, N 4. P. 626-627.
44. Monico C.G., Rossetti S., Belostotsky R. Primary hyperoxaluria type III gene HOGA1 (formerly DHDPSL) as a possible risk factor for idiopathic calcium oxalate urolithiasis // Clin. J. Am. Soc. Nephrol. 2011. Vol. 6, N 9. P. 2289-2295.
45. O’Malley M., Hutcheon R.G. Genetic disorders and congenital malformations in pediatric long-term care // J. Am. Med. Direct. Assoc. 2007. Vol. 8. P. 332-334.
46. Ozen H. Glycogen storage diseases: New perspectives // World J. Gastroenterol. 2007. Vol. 13, N 18. P. 2541-2553.
47. Petrukhin K., Fischer S.G., Pirastu M. et al. Mapping, cloning and genetic characterization of the region containing the Wilson disease gene // Nat. Genet. 1993. - Vol. 5. - P. 338-343.
48. Purdue P.E., Lumb M.J., Fox M. et al. Characterization and chromosomal mapping of a genomic clone encoding human alanine: glyoxylate aminotransferase // Genomics. 1991. Vol. 10, N 1. P. 34-42.
49. Rake J.P., Visser G., Labrune P. et al. Glycogen storage dis- ease type I: diagnosis, management, clinical course and outcome. Results of the European Study on Glycogen Storage Disease Type I (ESGSD I) // Eur. J. Pediatr. 2002. Vol. 161, suppl. 1. P. S20-S34.
50. Roberts E.A., Schilsky M.L. A practice guideline on Wilson disease // Hepatology. - 2003. Vol. 37, N 6. P. 1475-1492.
51. Schilsky M.L., Scheinberg I.H., Sternlieb I. Liver transplantation for Wilson’s disease: indications and outcome // Hepatology. 1994. Vol. 19. P. 583-587.
52. Schukfeh N., Metzelder M.L., Petersen C. et al. Normalization of serum bile acids after partial external biliary diversion indicates an excellent long-term outcome in children with progressive familial intrahepatic cholestasis // J. Pediatr. Surg. 2012. Vol. 47. P. 501-505.
53. Siebold L., Dick A.A., Thompson R. et al. Recurrent low gamma-glutamyl transpeptidase cholestasis following liver transplantation for bile salt export pump (BSEP) disease (post-transplant recurrent BSEP disease) // Liver Transpl. 2010. Vol. 16. P. 856-863.
54. Smithson S., Hall D., Trachtenberg B. et al. Treatment of cardiovascular complications of Alagille syndrome in clinical optimization for liver transplantation // Int. J. Cardiol. 2014. Vol. 176. P. 37-40.
55. Squires R.H., Ng V., Romero R. et al. Evaluation of the pediatric patient for liver transplantation: 2014 practice guideline by the American Association for the Study of Liver Diseases, American Society of Transplantation and the North American Society for Pediatric Gastroenterology // Hepatology. 2014. Vol. 60, N 1. P. 362-398.
56. Stevenson D.A, Carey J.C. Contribution of malformations and genetic disorders to mortality in a children’s hospital // Am. J. Med. Genet. A. 2004. Vol. 126A. P. 393-397.
57. TanziR.E.,PetrukhinK.,ChernovI.etal.TheWilsondisease gene is a copper transporting ATPase with homology to the Menkes disease gene // Nat. Genet. 1993. Vol. 5. P. 344-350.
58. van Woerden C.S., Groothoff J.W., Wanders R.J. et al. Primary hyperoxaluria type 1 in The Netherlands: prevalence and out- come // Nephrol. Dial. Transplant. 2003. Vol. 18, N 2. P. 273-279.
59. Verhulst P.M., van der Velden L.M., Oorschot V. et al. A flippase-independent function of ATP8B1, the protein affected in familial intrahepatic cholestasis type 1, is required for apical protein expression and microvillus formation in polarized epithelial cells // Hepatology. 2010. Vol. 51. P. 2049-2060.
60. Vermassen A., Boddaert J. Congenital agenesis of intrahepatic bile ducts // Maandschr. Kindergeneeskd. 1962. Vol. 30. P. 56-68.
61. von Gierke E. Hepato-nephromegalia glykogenica (Glyko- genspeicherkrankheit der Leber und Nieren) // Beitrage zur patho- logischen Anatomie und zur allgemeinen Pathologie, Jena. 1929. Bd 82. S. 497-513.
62. Walshe J.M. Wilson’s disease. New oral therapy // Lancet. 1956. Vol. I. P. 25-26.
63. Watson G.H., Miller V. Arterio-hepatic dysplasia. Familial pulmonary arterial stenosis with neonatal liver diseases // Arch. Dis. Child. 1973. Vol. 48. P. 459-466.
64. Watts R.W., Morgan S.H., Danpure C.J. et al. Combined hepatic and renal transplantation in primary hyperoxaluria type I: clinical report of nine cases // Am. J. Med. 1991. Vol. 90, N 2. P. 179-188.
65. Watts R.W., Veall N., Purkiss P. Oxalate dynamics and removal rates during haemodialysis and peritoneal dialysis in patients with primary hyperoxaluria and severe renal failure // Clin. Sci. (Lond.). 1984. Vol. 66, N 5. P. 591-597.
66. Wilson S.A.K. Progressive lenticular degeneration: a familial nervous disease associated with cirrhosis of the liver // Brain. 1912. Vol. 34. P. 295-507.
67. Yamaguchi Y., Heiny M.E., Gitlin J.D. Isolation and characterization of a human liver cDNA as a candidate gene for Wilson disease // Biochem. Biophys. Res. Commun. 1993. Vol. 197. P. 271-277.
68. Eramishantsev A.K., Got’e S.V, Skipenko O.G. et al. Clinical experience of liver transplantation in the Russian Scientific Center of Surgery named after Academician BV Petrovsky Academy of Medical Sciences. Rossiyskiy zhurnal gastroenterologii, gepatologii, koloproktologii [Russian Journal of Gastroenterology, Hepatology, Coloproctology]. 1995; Vol. 5, N 3, Suppl 1: 82. (in Russian)
69. Puzyrev V.P. Medical pathogenetics. Vavilovskiy zhurnal genetiki i selektsii [The Vavilov Journal of Genetics and Breeding]. 2014; Vol. 18, N 1: 7–21. (in Russian)
70. Filin A.V., Semenkov A.V., Koroteyeva N.A., Keligova A.Ya., Metelin A.V., Kim E.F., Dzhamanchin D.S., Khartukova N.E., Kamalov Yu.R., Kryzhanovskaya E.Yu., Khovrin V.A., Galyan T.N., Kaganov B.S., Kutyreva E.N., Zubovich A.I. Related liver fragment transplantation for type 1 glycogenosis: the first Russian experience. Transplantologiya [Тransplantology]. 2011; Vol. 2–3: 24–8. (in Russian)