Journal of Inherited Metabolic Disease

, Volume 37, Issue 3, pp 341–352 | Cite as

Natural course of Fabry disease and the effectiveness of enzyme replacement therapy: a systematic review and meta-analysis

Effectiveness of ERT in different disease stages
  • Saskia M. Rombach
  • Bouwien E. Smid
  • Gabor E. Linthorst
  • Marcel G. W. Dijkgraaf
  • Carla E. M. Hollak
Review

Abstract

Objective

Current available evidence on long-term effectiveness of enzyme replacement therapy (ERT) for Fabry disease is limited. More insight is needed whether ERT effectiveness differs in patients with and without baseline end-organ damage.

Design

Through a systematic review, untreated and ERT treated males and females with Fabry disease were compared for main clinical outcomes: renal function, left ventricular mass (LVmass), cerebral white matter lesions (WMLs) and end-organ complications. Through a meta-analysis ERT effectiveness was estimated in different disease stages.

Data extraction

Two reviewers assessed quality of the included studies according to guidelines for prognosis research. Data were synthesized using a random effects meta-analysis.

Results

Thirty-one studies were systematically reviewed while six studies were included in the meta-analysis. In patients with a GFR > 60 ml/min/1.73 m2, decline of renal function was similar for treated and untreated patients. Only ERT treated males with a GFR < 60 ml/min/1.73 m2 had a slower rate of decline in renal function, possibly attributable to anti-proteinuric therapy. Regardless of left ventricular hypertrophy (LVH) at baseline, LVmass remained stable or increased in males despite ERT, however at a slower rate compared to untreated male patients. In ERT treated females with LVH LVmass decreased, and remained stable in females without LVH. WMLs can not be prevented by ERT. Stroke, cardiac and end-stage renal complications develop, though the incidence of new complications seems to be reduced during ERT.

Conclusion

ERT is effective in reducing LVH, but has a limited effect on renal function. Improved treatment options are needed for Fabry disease.

Supplementary material

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References

  1. Alegra T, Vairo F, de Souza MV, Krug BC, Schwartz IV (2012) Enzyme replacement therapy for Fabry disease: a systematic review and meta-analysis. Genet Mol Biol 35:947–954PubMedCentralPubMedCrossRefGoogle Scholar
  2. Alfadhel M, Sirrs S (2011) Enzyme replacement therapy for Fabry disease: some answers but more questions. Ther Clin Risk Manag 7:69–82PubMedCentralPubMedGoogle Scholar
  3. Baehner F, Kampmann C, Whybra C, Miebach E, Wiethoff CM, Beck M (2003) Enzyme replacement therapy in heterozygous females with Fabry disease: results of a phase IIIB study. J Inherit Metab Dis 26:617–627PubMedCrossRefGoogle Scholar
  4. Banikazemi M, Bultas J, Waldek S et al (2007) Agalsidase-beta therapy for advanced Fabry disease: a randomized trial. Ann Intern Med 146:77–86PubMedCrossRefGoogle Scholar
  5. Beck M, Ricci R, Widmer U et al (2004) Fabry disease: overall effects of agalsidase alfa treatment. Eur J Clin Invest 34:838–844PubMedCrossRefGoogle Scholar
  6. Beer M, Weidemann F, Breunig F et al (2006) Impact of enzyme replacement therapy on cardiac morphology and function and late enhancement in Fabry’s cardiomyopathy. Am J Cardiol 97:1515–1518PubMedCrossRefGoogle Scholar
  7. Bierer G, Balfe D, Wilcox WR, Mosenifar Z (2006) Improvement in serial cardiopulmonary exercise testing following enzyme replacement therapy in Fabry disease. J Inherit Metab Dis 29:572–579PubMedCrossRefGoogle Scholar
  8. Borgwardt L, Feldt-Rasmussen U, Rasmussen A, Ballegaard M, Meldgaard LA (2013) Fabry disease in children: agalsidase-beta enzyme replacement therapy. Clin Genet 83:432–438PubMedCrossRefGoogle Scholar
  9. Brady RO, Gal AE, Bradley RM, Martensson E, Warshaw AL, Laster L (1967) Enzymatic defect in Fabry’s disease. Ceramidetrihexosidase deficiency. N Engl J Med 276:1163–1167PubMedCrossRefGoogle Scholar
  10. Branton MH, Schiffmann R, Sabnis SG et al (2002) Natural history of Fabry renal disease: influence of alpha-galactosidase A activity and genetic mutations on clinical course. Medicine (Baltimore) 81:122–138CrossRefGoogle Scholar
  11. Breunig F, Weidemann F, Strotmann J, Knoll A, Wanner C (2006) Clinical benefit of enzyme replacement therapy in Fabry disease. Kidney Int 69:1216–1221PubMedCrossRefGoogle Scholar
  12. Buechner S, Moretti M, Burlina AP et al (2008) Central nervous system involvement in Anderson-Fabry disease: a clinical and MRI retrospective study. J Neurol Neurosurg Psychiatry 79:1249–1254PubMedCrossRefGoogle Scholar
  13. Collin C, Briet M, Tran TC et al (2012) Long-term changes in arterial structure and function and left ventricular geometry after enzyme replacement therapy in patients affected with Fabry disease. Eur J Prev Cardiol 19:43–54PubMedCrossRefGoogle Scholar
  14. Crutchfield KE, Patronas NJ, Dambrosia JM et al (1998) Quantitative analysis of cerebral vasculopathy in patients with Fabry disease. Neurology 50:1746–1749PubMedCrossRefGoogle Scholar
  15. Deegan PB, Baehner AF, Barba Romero MA, Hughes DA, Kampmann C, Beck M (2006) Natural history of Fabry disease in females in the Fabry Outcome Survey. J Med Genet 43:347–352PubMedCentralPubMedCrossRefGoogle Scholar
  16. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188PubMedCrossRefGoogle Scholar
  17. Desnick RJ, Ioannou YA, Eng CM (2001) alpha-Galactosidase A deficiency: Fabry disease. In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds) The metabolic and molecular bases of inherited disease, vol 3, 8th edn., pp 3733–3774Google Scholar
  18. El Dib RP, Nascimento P, Pastores GM (2013) Enzyme replacement therapy for Anderson-Fabry disease. Cochrane Database Syst Rev 2, CD006663PubMedGoogle Scholar
  19. El Dib RP, Pastores GM (2010) Enzyme replacement therapy for Anderson-Fabry disease. Cochrane Database Syst Rev CD006663Google Scholar
  20. Elliott PM, Kindler H, Shah JS et al (2006) Coronary microvascular dysfunction in male patients with Anderson-Fabry disease and the effect of treatment with alpha galactosidase A. Heart 92:357–360PubMedCentralPubMedCrossRefGoogle Scholar
  21. Eng CM, Fletcher J, Wilcox WR et al (2007) Fabry disease: baseline medical characteristics of a cohort of 1765 males and females in the Fabry Registry. J Inherit Metab Dis 30:184–192PubMedCrossRefGoogle Scholar
  22. Eng CM, Guffon N, Wilcox WR et al (2001) Safety and efficacy of recombinant human alpha-galactosidase A–replacement therapy in Fabry’s disease. N Engl J Med 345:9–16PubMedCrossRefGoogle Scholar
  23. Engelen MA, Brand E, Baumeister TB et al (2012) Effects of enzyme replacement therapy in adult patients with Fabry disease on cardiac structure and function: a retrospective cohort study of the Fabry Munster Study (FaMuS) data. BMJ Open 2Google Scholar
  24. Eto Y, Ohashi T, Utsunomiya Y et al (2005) Enzyme replacement therapy in Japanese Fabry disease patients: the results of a phase 2 bridging study. J Inherit Metab Dis 28:575–583PubMedCrossRefGoogle Scholar
  25. Feriozzi S, Schwarting A, Sunder-Plassmann G, West M, Cybulla M (2009) Agalsidase alfa slows the decline in renal function in patients with Fabry disease. Am J Nephrol 29:353–361PubMedCrossRefGoogle Scholar
  26. Feriozzi S, Torras J, Cybulla M, Nicholls K, Sunder-Plassmann G, West M (2012) The effectiveness of long-term agalsidase alfa therapy in the treatment of Fabry nephropathy. Clin J Am Soc Nephrol 7:60–69PubMedCentralPubMedCrossRefGoogle Scholar
  27. Germain DP, Waldek S, Banikazemi M et al (2007) Sustained, long-term renal stabilization after 54 months of agalsidase beta therapy in patients with Fabry disease. J Am Soc Nephrol 18:1547–1557PubMedCrossRefGoogle Scholar
  28. Grewal RP, Barton NW (1992) Fabry’s disease presenting with stroke. Clin Neurol Neurosurg 94:177–179PubMedCrossRefGoogle Scholar
  29. Guffon N (2003) Clinical presentation in female patients with Fabry disease. J Med Genet 40:e38PubMedCentralPubMedCrossRefGoogle Scholar
  30. Gupta S, Ries M, Kotsopoulos S, Schiffmann R (2005) The relationship of vascular glycolipid storage to clinical manifestations of Fabry disease: a cross-sectional study of a large cohort of clinically affected heterozygous women. Medicine (Baltimore) 84:261–268CrossRefGoogle Scholar
  31. Hayden JA, Cote P, Bombardier C (2006) Evaluation of the quality of prognosis studies in systematic reviews. Ann Intern Med 144:427–437PubMedCrossRefGoogle Scholar
  32. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560PubMedCentralPubMedCrossRefGoogle Scholar
  33. Hollak CE, Aerts JM, Ayme S, Manuel J (2011) Limitations of drug registries to evaluate orphan medicinal products for the treatment of lysosomal storage disorders. Orphanet J Rare Dis 6:16PubMedCentralPubMedCrossRefGoogle Scholar
  34. Hughes DA, Barba Romero MA, Hollak CE, Giugliani R, Deegan PB (2011) Response of women with Fabry disease to enzyme replacement therapy: comparison with men, using data from FOS-the Fabry Outcome Survey. Mol Genet Metab 103(3):207-14. doi: 10.1016/j.ymgme.2011.03.022 Google Scholar
  35. Hughes DA, Elliott PM, Shah J et al (2008) Effects of enzyme replacement therapy on the cardiomyopathy of Anderson-Fabry disease: a randomised, double-blind, placebo-controlled clinical trial of agalsidase alfa. Heart 94:153–158PubMedCrossRefGoogle Scholar
  36. Imbriaco M, Pisani A, Spinelli L et al (2009) Effects of enzyme-replacement therapy in patients with Anderson-Fabry disease: a prospective long-term cardiac magnetic resonance imaging study. Heart 95:1103–1107PubMedCrossRefGoogle Scholar
  37. Jardim L, Vedolin L, Schwartz IV et al (2004) CNS involvement in Fabry disease: clinical and imaging studies before and after 12 months of enzyme replacement therapy. J Inherit Metab Dis 27:229–240PubMedCrossRefGoogle Scholar
  38. Jardim LB, Aesse F, Vedolin LM et al (2006) White matter lesions in Fabry disease before and after enzyme replacement therapy: a 2-year follow-up. Arq Neuropsiquiatr 64:711–717PubMedCrossRefGoogle Scholar
  39. Kalliokoski RJ, Kantola I, Kalliokoski KK et al (2006) The effect of 12-month enzyme replacement therapy on myocardial perfusion in patients with Fabry disease. J Inherit Metab Dis 29:112–118PubMedCrossRefGoogle Scholar
  40. Kampmann C, Linhart A, Baehner F et al (2008a) Onset and progression of the Anderson-Fabry disease related cardiomyopathy. Int J Cardiol 130:367–373PubMedCrossRefGoogle Scholar
  41. Kampmann C, Linhart A, Devereux RB et al (2009) Effect of agalsidase alfa replacement therapy on Fabry disease-related hypertrophic cardiomyopathy: a 12- to 36-month, retrospective, blinded echocardiographic pooled analysis. Clin Ther 31:1966–1976PubMedCrossRefGoogle Scholar
  42. Kampmann C, Wiethoff CM, Whybra C, Baehner FA, Mengel E, Beck M (2008b) Cardiac manifestations of Anderson-Fabry disease in children and adolescents. Acta Paediatr 97:463–469PubMedCrossRefGoogle Scholar
  43. Kint JA (1970) Fabry’s disease: alpha-galactosidase deficiency. Science 167:1268–1269PubMedCrossRefGoogle Scholar
  44. Kobayashi M, OhashiT, Sakuma M, Ida H, EtoY (2008) Clinical manifestations and natural history of Japanese heterozygous females with Fabry disease. J Inherit Metab Dis doi:10.1007/s10545-007-0740-6Google Scholar
  45. Koskenvuo JW, Hartiala JJ, Nuutila P et al (2008) Twenty-four-month alpha-galactosidase A replacement therapy in Fabry disease has only minimal effects on symptoms and cardiovascular parameters. J Inherit Metab Dis 31:432–441PubMedCrossRefGoogle Scholar
  46. Kovacevic-Preradovic T, Zuber M, Attenhofer Jost CH et al (2008) Anderson-Fabry disease: long-term echocardiographic follow-up under enzyme replacement therapy. Eur J Echocardiogr 9:729–735PubMedCrossRefGoogle Scholar
  47. Levey AS, Coresh J, Balk E et al (2003) National Kidney Foundation practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Ann Intern Med 139:137–147PubMedCrossRefGoogle Scholar
  48. Lidove O, West ML, Pintos-Morell G et al (2010) Effects of enzyme replacement therapy in Fabry disease–a comprehensive review of the medical literature. Genet Med 12:668–679PubMedCrossRefGoogle Scholar
  49. Lubanda JC, Anijalg E, Bzduch V, Thurberg BL, Benichou B, Tylki-Szymanska A (2009) Evaluation of a low dose, after a standard therapeutic dose, of agalsidase beta during enzyme replacement therapy in patients with Fabry disease. Genet Med 11:256–264PubMedCrossRefGoogle Scholar
  50. MacDermot KD, Holmes A, Miners AH (2001a) Anderson-Fabry disease: clinical manifestations and impact of disease in a cohort of 60 obligate carrier females. J Med Genet 38:769–775PubMedCentralPubMedCrossRefGoogle Scholar
  51. MacDermot KD, Holmes A, Miners AH (2001b) Anderson-Fabry disease: clinical manifestations and impact of disease in a cohort of 98 hemizygous males. J Med Genet 38:750–760PubMedCentralPubMedCrossRefGoogle Scholar
  52. Mehta A, Beck M, Elliott P et al (2009) Enzyme replacement therapy with agalsidase alfa in patients with Fabry’s disease: an analysis of registry data. Lancet 374:1986–1996PubMedCrossRefGoogle Scholar
  53. Mehta A, Ricci R, Widmer U et al (2004) Fabry disease defined: baseline clinical manifestations of 366 patients in the Fabry Outcome Survey. Eur J Clin Invest 34:236–242PubMedCrossRefGoogle Scholar
  54. Messalli G, Imbriaco M, Avitabile G et al (2012) Role of cardiac MRI in evaluating patients with Anderson-Fabry disease: assessing cardiac effects of long-term enzyme replacement therapy. Radiol Med 117:19–28PubMedCrossRefGoogle Scholar
  55. Mitsias P, Levine SR (1996) Cerebrovascular complications of Fabry’s disease. Ann Neurol 40:8–17PubMedCrossRefGoogle Scholar
  56. Moore DF, Altarescu G, Herscovitch P, Schiffmann R (2002) Enzyme replacement reverses abnormal cerebrovascular responses in Fabry disease. BMC Neurol 2:4PubMedCentralPubMedCrossRefGoogle Scholar
  57. Motwani M, Banypersad S, Woolfson P, Waldek S (2012) Enzyme replacement therapy improves cardiac features and severity of Fabry disease. Mol Genet Metab 107:197–202PubMedCrossRefGoogle Scholar
  58. Nakao S, Takenaka T, Maeda M et al (1995) An atypical variant of Fabry’s disease in men with left ventricular hypertrophy. N Engl J Med 333:288–293PubMedCrossRefGoogle Scholar
  59. Niemann M, Breunig F, Beer M et al (2010) The right ventricle in Fabry disease: natural history and impact of enzyme replacement therapy. Heart 96:1915–1919PubMedCrossRefGoogle Scholar
  60. Ortiz A, Cianciaruso B, Cizmarik M et al (2010) End-stage renal disease in patients with Fabry disease: natural history data from the Fabry Registry. Nephrol Dial Transplant 25:769–775PubMedCrossRefGoogle Scholar
  61. Patel MR, Cecchi F, Cizmarik M et al (2011) Cardiovascular events in patients with fabry disease natural history data from the fabry registry. J Am Coll Cardiol 57:1093–1099PubMedCrossRefGoogle Scholar
  62. Pisani A, Spinelli L, Sabbatini M et al (2005) Enzyme replacement therapy in Fabry disease patients undergoing dialysis: effects on quality of life and organ involvement. Am J Kidney Dis 46:120–127PubMedCrossRefGoogle Scholar
  63. Pisani A, Spinelli L, Visciano B et al (2013) Effects of switching from agalsidase Beta to agalsidase alfa in 10 patients with anderson-fabry disease. JIMD Rep 9:41–48PubMedCentralPubMedCrossRefGoogle Scholar
  64. Ramaswami U, Parini R, Kampmann C, Beck M (2011) Safety of agalsidase alfa in patients with Fabry disease under 7 years. Acta Paediatr 100:605–611PubMedCrossRefGoogle Scholar
  65. Ramaswami U, Parini R, Pintos-Morell G, Kalkum G, Kampmann C, Beck M (2012) Fabry disease in children and response to enzyme replacement therapy: results from the Fabry Outcome Survey. Clin Genet 81:485–490PubMedCrossRefGoogle Scholar
  66. Ramaswami U, Wendt S, Pintos-Morell G et al (2007) Enzyme replacement therapy with agalsidase alfa in children with Fabry disease. Acta Paediatr 96:122–127PubMedCrossRefGoogle Scholar
  67. Reisin RC, Romero C, Marchesoni C et al (2011) Brain MRI findings in patients with Fabry disease. J Neurol Sci 305:41–44PubMedCrossRefGoogle Scholar
  68. Ries M, Clarke JT, Whybra C et al (2006) Enzyme-replacement therapy with agalsidase alfa in children with Fabry disease. Pediatrics 118:924–932PubMedCrossRefGoogle Scholar
  69. Rombach SM, Aerts JM, Poorthuis BJ et al (2012) Long-term effect of antibodies against infused alpha-galactosidase A in Fabry disease on plasma and urinary (lyso)Gb3 reduction and treatment outcome. PLoS One 7:e47805PubMedCentralPubMedCrossRefGoogle Scholar
  70. Rombach SM, Smid BE, Bouwman MG, Linthorst GE, Dijkgraaf MG, Hollak CE (2013) Long term enzyme replacement therapy for Fabry disease: effectiveness on kidney, heart and brain. Orphanet J Rare Dis 8:47PubMedCentralPubMedCrossRefGoogle Scholar
  71. Schiffmann R (2009) Fabry disease. Pharmacol Ther 122:65–77PubMedCrossRefGoogle Scholar
  72. Schiffmann R, Askari H, Timmons M et al (2007) Weekly enzyme replacement therapy may slow decline of renal function in patients with Fabry disease who are on long-term biweekly dosing. J Am Soc Nephrol 18:1576–1583PubMedCentralPubMedCrossRefGoogle Scholar
  73. Schiffmann R, Kopp JB, Austin HA III et al (2001) Enzyme replacement therapy in Fabry disease: a randomized controlled trial. JAMA 285:2743–2749PubMedCrossRefGoogle Scholar
  74. Schiffmann R, Martin RA, Reimschisel T et al (2010) Four-year prospective clinical trial of agalsidase alfa in children with Fabry disease. J Pediatr 156(832–7):837Google Scholar
  75. Schiffmann R, Ries M, Timmons M, Flaherty JT, Brady RO (2006) Long-term therapy with agalsidase alfa for Fabry disease: safety and effects on renal function in a home infusion setting. Nephrol Dial Transplant 21:345–354PubMedCrossRefGoogle Scholar
  76. Schiffmann R, Warnock DG, Banikazemi M et al (2009) Fabry disease: progression of nephropathy, and prevalence of cardiac and cerebrovascular events before enzyme replacement therapy. Nephrol Dial Transplant 24:2102–2111PubMedCentralPubMedCrossRefGoogle Scholar
  77. Schwarting A, Dehout F, Feriozzi S, Beck M, Mehta A, Sunder-Plassmann G (2006) Enzyme replacement therapy and renal function in 201 patients with Fabry disease. Clin Nephrol 66:77–84PubMedGoogle Scholar
  78. Shah JS, Hughes DA, Sachdev B et al (2005a) Prevalence and clinical significance of cardiac arrhythmia in Anderson-Fabry disease. Am J Cardiol 96:842–846PubMedCrossRefGoogle Scholar
  79. Shah JS, Lee P, Hughes D et al (2005b) The natural history of left ventricular systolic function in Anderson-Fabry disease. Heart 91:533–534PubMedCentralPubMedCrossRefGoogle Scholar
  80. Sims K, Politei J, Banikazemi M, Lee P (2009) Stroke in Fabry disease frequently occurs before diagnosis and in the absence of other clinical events: natural history data from the Fabry Registry. Stroke 40:788–794PubMedCrossRefGoogle Scholar
  81. Smid BE, Rombach SM, Aerts JM et al (2011) Consequences of a global enzyme shortage of agalsidase beta in adult Dutch Fabry patients. Orphanet J Rare Dis 6:69PubMedCentralPubMedCrossRefGoogle Scholar
  82. Spinelli L, Pisani A, Sabbatini M et al (2004) Enzyme replacement therapy with agalsidase beta improves cardiac involvement in Fabry’s disease. Clin Genet 66:158–165PubMedCrossRefGoogle Scholar
  83. Tahir H, Jackson LL, Warnock DG (2007) Antiproteinuric therapy and fabry nephropathy: sustained reduction of proteinuria in patients receiving enzyme replacement therapy with agalsidase-beta. J Am Soc Nephrol 18:2609–2617PubMedCrossRefGoogle Scholar
  84. Takenaka T, Teraguchi H, Yoshida A et al (2008) Terminal stage cardiac findings in patients with cardiac Fabry disease: an electrocardiographic, echocardiographic, and autopsy study. J Cardiol 51:50–59PubMedCrossRefGoogle Scholar
  85. Tondel C, Bostad L, Larsen KK et al (2013) Agalsidase benefits renal histology in young patients with Fabry disease. J Am Soc Nephrol 24:137–148PubMedCrossRefGoogle Scholar
  86. Tsuboi K, Yamamoto H (2012) Clinical observation of patients with Fabry disease after switching from agalsidase beta (Fabrazyme) to agalsidase alfa (Replagal). Genet Med 14:779–786PubMedCentralCrossRefGoogle Scholar
  87. Vedder AC, Linthorst GE, Houge G et al (2007a) Treatment of Fabry disease: outcome of a comparative trial with agalsidase alfa or beta at a dose of 0.2 mg/kg. PLoS One 2:e598PubMedCentralPubMedCrossRefGoogle Scholar
  88. Vedder AC, Linthorst GE, van Breemen MJ et al (2007b) The Dutch Fabry cohort: diversity of clinical manifestations and Gb3 levels. J Inherit Metab Dis 30:68–78PubMedCrossRefGoogle Scholar
  89. Wanner C, Oliveira JP, Ortiz A et al (2010) Prognostic indicators of renal disease progression in adults with Fabry disease: natural history data from the Fabry registry. Clin J Am Soc Nephrol 5(12):2220-8. doi: 10.2215/CJN.04340510Google Scholar
  90. Warnock DG, Ortiz A, Mauer M et al (2011) Renal outcomes of agalsidase beta treatment for Fabry disease: role of proteinuria and timing of treatment initiation. Nephrol Dial Transplant 27(3):1042-9. doi: 10.1093/ndt/gfr420Google Scholar
  91. Warnock DG, Ortiz A, Mauer M et al (2012) Renal outcomes of agalsidase beta treatment for Fabry disease: role of proteinuria and timing of treatment initiation. Nephrol Dial Transplant 27:1042–1049PubMedCentralPubMedCrossRefGoogle Scholar
  92. Weidemann F, Breunig F, Beer M et al (2003) Improvement of cardiac function during enzyme replacement therapy in patients with Fabry disease: a prospective strain rate imaging study. Circulation 108:1299–1301PubMedCrossRefGoogle Scholar
  93. Weidemann F, Niemann M, Breunig F et al (2009) Long-term effects of enzyme replacement therapy on fabry cardiomyopathy: evidence for a better outcome with early treatment. Circulation 119:524–529PubMedCrossRefGoogle Scholar
  94. Weidemann F, Niemann M, Stork S et al (2013) Long-term outcome of enzyme-replacement therapy in advanced Fabry disease: evidence for disease progression towards serious complications. J Intern Med 274(4):331-41. doi: 10.1111/joim.12077 Google Scholar
  95. West M, Nicholls K, Mehta A et al (2009) Agalsidase alfa and kidney dysfunction in Fabry disease. J Am Soc Nephrol 20:1132–1139PubMedCentralPubMedCrossRefGoogle Scholar
  96. Wetzels JF, Kiemeney LA, Swinkels DW, Willems HL, den Heijer M (2007) Age- and gender-specific reference values of estimated GFR in Caucasians: the Nijmegen Biomedical Study. Kidney Int 72:632–637PubMedCrossRefGoogle Scholar
  97. Whybra C, Miebach E, Mengel E et al (2009) A 4-year study of the efficacy and tolerability of enzyme replacement therapy with agalsidase alfa in 36 women with Fabry disease. Genet Med 11:441–449PubMedCrossRefGoogle Scholar
  98. Wilcox WR, Banikazemi M, Guffon N et al (2004) Long-term safety and efficacy of enzyme replacement therapy for Fabry disease. Am J Hum Genet 75:65–74PubMedCentralPubMedCrossRefGoogle Scholar
  99. Wilcox WR, Oliveira JP, Hopkin RJ et al (2008) Females with Fabry disease frequently have major organ involvement: lessons from the Fabry Registry. Mol Genet Metab 93:112–128PubMedCrossRefGoogle Scholar
  100. Wraith JE, Tylki-Szymanska A et al (2008) Safety and efficacy of enzyme replacement therapy with agalsidase beta: an international, open-label study in pediatric patients with Fabry disease. J Pediatr 152(563–70):570Google Scholar
  101. Wuest W, Machann W, Breunig F et al (2011) Right ventricular involvement in patients with Fabry’s disease and the effect of enzyme replacement therapy. Rofo 183:1037–1042PubMedCrossRefGoogle Scholar
  102. Wyatt K, Henley W, Anderson L et al (2012) The effectiveness and cost-effectiveness of enzyme and substrate replacement therapies: a longitudinal cohort study of people with lysosomal storage disorders. Health Technol Assess 16:1–543PubMedGoogle Scholar

Copyright information

© SSIEM and Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Saskia M. Rombach
    • 1
  • Bouwien E. Smid
    • 1
  • Gabor E. Linthorst
    • 1
  • Marcel G. W. Dijkgraaf
    • 2
  • Carla E. M. Hollak
    • 1
    • 3
  1. 1.Department of Internal Medicine, Division of Endocrinology and MetabolismAcademic Medical CenterAmsterdamThe Netherlands
  2. 2.Clinical Research UnitAcademic Medical CenterAmsterdamThe Netherlands
  3. 3.Department of Internal Medicine/Endocrinology and MetabolismAcademic Medical CenterAmsterdamThe Netherlands

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