Therapeutic approaches to bone pathology in Gaucher disease: Past, present and future

Molecular Genetics and Metabolism

Volumn 104, Issue 4, 2011, Pages 438-447

  Goker Alpan, Ozlem ^a  

^a Lysosomal Disorders Research and Treatment Unit   (United States)

Author keywords

Bone; Enzyme replacement therapy; Gaucher disease; Glucocerebrosidase; Pathology; Treatment

Indexed keywords

ELIGLUSTAT; IMIGLUCERASE; MIGLUSTAT; TALIGLUCERASE ALFA; VELAGLUCERASE ALFA;

AVASCULAR NECROSIS; BLOOD VESSEL OCCLUSION; BONE CELL; BONE DISEASE; BONE MATRIX; BONE NECROSIS; BONE PAIN; CLINICAL FEATURE; DISEASE ACTIVITY; ENZYME REPLACEMENT; GAUCHER DISEASE; GENETIC HETEROGENEITY; HEMATOPOIESIS; HUMAN; LOOSE FECES; MEDICAL DECISION MAKING; OSTEOCLAST; OSTEOPENIA; PATIENT MONITORING; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; REVIEW; TREATMENT DURATION; TREMOR; UNSPECIFIED SIDE EFFECT;

BONE AND BONES; BONE DENSITY; BONE DISEASES; ENZYME REPLACEMENT THERAPY; GAUCHER DISEASE; GLUCOSYLCERAMIDASE; HUMANS;

EID: 82255179519     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2011.08.004     Document Type: Review

References (122)

1. Beutler E., Grabowski G.A. Gaucher disease. The Online Metabolic and Molecular Bases of Inherited Disease 2006, 3635-3668. The McGraw-Hill Companies, New York, NY. C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle, K. Vogelstein, Childs (Eds.).
2. Goker-Alpan O., Schiffmann R., Park J.K., Stubblefield B.K., Tayebi N., Sidransky E. Phenotypic continuum in neuronopathic Gaucher disease: an intermediate phenotype between type 2 and type 3. J. Pediatr. 2003, 143:273-276.
3. Lachmann R.H., Grant I.R., Halsall D., Cox T.M. Twin pairs showing discordance of phenotype in adult Gaucher's disease. QJM 2004, 97:199-204.
4. Amato D., Stachiw T., Clarke J.T., Rivard G.E. Gaucher disease: variability in phenotype among siblings. J. Inherit. Metab. Dis. 2004, 27:659-669.
5. Goker-Alpan O., Hruska K.S., Orvisky E., Kishnani P.S., Stubblefield B.K., Schiffmann R., Sidransky E. Divergent phenotypes in Gaucher disease implicate the role of modifiers. J. Med. Genet. 2005, 42:e37.
6. Conradi N.G., Kalimo H., Sourander P. Reactions of vessel walls and brain parenchyma to the accumulation of Gaucher cells in the Norrbottnian type (type III) of Gaucher disease. Acta Neuropathol. 1988, 75:385-390.
7. Wenstrup R.J., Roca-Espiau M., Weinreb N.J., Bembi B. Skeletal aspects of Gaucher disease: a review. Br. J. Radiol. 2002, 75(Suppl 1):A2-A12.
8. Beighton P., Goldblatt J., Sacks S. Bone involvement in Gaucher disease. Gaucher Disease: A Century of Delineation 1982, 107-129. Alan R. Liss, Inc., New York, NY. R. Desnick, S. Gatt, G. Grabowski (Eds.).
9. Weinreb N., Barranger J., Packman S., Prakash-Cheng A., Rosenbloom B., Sims K., Angell J., Skrinar A., Pastores G.M. Imiglucerase (Cerezyme) improves quality of life in patients with skeletal manifestations of Gaucher disease. Clin. Genet. 2007, 71:576-588.
10. Stowens D.W., Teitelbaum S.L., Kahn A.J., Barranger J.A. Skeletal complications of Gaucher disease. Medicine 1985, 64:310-322.
11. Grabowski G.A., Barton N.W., Pastores G., Dambrosia J.M., Banerjee T.K., McKee M.A., Parker C., Schiffmann R., Hill S.C., Brady R.O. Enzyme therapy in type 1 Gaucher disease: comparative efficacy of mannose-terminated glucocerebrosidase from natural and recombinant sources. Ann. Intern. Med. 1995, 122:33-39.
12. Elstein D., Cohn G.M., Wang N., Djordjevic M., Brutaru C., Zimran A. Early achievement and maintenance of the therapeutic goals using velaglucerase alfa in type 1 Gaucher disease. Blood Cells Mol. Dis. 2011, 46:119-123.
13. Aviezer D., Brill-Almon E., Shaaltiel Y., Hashmueli S., Bartfeld D., Mizrachi S., Liberman Y., Freeman A., Zimran A., Galun E. A plant-derived recombinant human glucocerebrosidase enzyme-a preclinical and phase I investigation. PLoS ONE 2009, 4:e4792.
14. Deegan P.B., Pavlova E., Tindall J., Stein P.E., Bearcroft P., Mehta A., Hughes D., Wraith J.E., Cox T.M. Osseous manifestations of adult Gaucher disease in the era of enzyme replacement therapy. Medicine 2011, 90:52-60.
15. Weinreb N.J., Charrow J., Andersson H.C., Kaplan P., Kolodny E.H., Mistry P., Pastores G., Rosenbloom B.E., Scott C.R., Wappner R.S., Zimran A. Effectiveness of enzyme replacement therapy in 1028 patients with type 1 Gaucher disease after 2 to 5years of treatment: a report from the Gaucher Registry. Am. J. Med. 2002, 113:112-119.
16. Pastores G.M., Weinreb N.J., Aerts H., Andria G., Cox T.M., Giralt M., Grabowski G.A., Mistry P.K., Tylki-Szymanska A. Therapeutic goals in the treatment of Gaucher disease. Semin. Hematol. 2004, 41:4-14.
17. Balwani M., Fuerstman L., Kornreich R., Edelmann L., Desnick R.J. Type 1 Gaucher disease: significant disease manifestations in "asymptomatic" homozygotes. Arch. Intern. Med. 2010, 170:1463-1469.
18. Mistry P.K., Deegan P., Vellodi A., Cole J.A., Yeh M., Weinreb N.J. Timing of initiation of enzyme replacement therapy after diagnosis of type 1 Gaucher disease: effect on incidence of avascular necrosis. Br. J. Haematol. 2009, 147:561-570.
19. Mistry P.K., Weinreb N.J., Kaplan P., Cole J.A., Gwosdow A.R., Hangartner T. Osteopenia in Gaucher disease develops early in life: response to imiglucerase enzyme therapy in children, adolescents and adults. Blood Cells Mol. Dis. 2011, 46:66-72.
20. Barthe C. Normal bone anatomy and physiology. Clin. J. Am. Soc. Nephrol. 2008, S131-S139.
21. Koide M., Kinugawa S., Takahashi N., Udagawa N. Osteoclastic bone resorption induced by innate immune responses. Periodontol. 2010, 2000(54):235-246.
22. Udagawa N., Takahashi N., Akatsu T., Tanaka H., Sasaki T., Nishihara T., Koga T., Martin T.J., Suda T. Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:7260-7264.
23. Boyce B.F., Yao Z., Xing L. Osteoclasts have multiple roles in bone in addition to bone resorption. Crit. Rev. Eukaryot. Gene Expr. 2009, 19:171-180.
24. Charrow J., Andersson H.C., Kaplan P., Kolodny E.H., Mistry P., Pastores G., Rosenbloom B.E., Scott C.R., Wappner R.S., Weinreb N.J., Zimran A. The Gaucher registry: demographics and disease characteristics of 1698 patients with Gaucher disease. Archives of Internal Medicine 2000, 160:2835-2843.
25. Stirnemann J., Boutten A., Vincent C., Mekinian A., Heraoui D., Fantin B., Fain O., Mentre F., Belmatoug N. Impact of imiglucerase on the serum glycosylated-ferritin level in Gaucher disease. Blood Cells Mol. Dis. 2011, 46:34-38.
26. Beutler E., Nguyen N.J., Henneberger M.W., Smolec J.M., McPherson R.A., West C., Gelbart T. Gaucher disease: gene frequencies in the Ashkenazi Jewish population. Am. J. Hum. Genet. 1993, 52:85-88.
27. DeMayo R.F., Haims A.H., McRae M.C., Yang R., Mistry P.K. Correlation of MRI-Based bone marrow burden score with genotype and spleen status in Gaucher's disease. AJR Am. J. Roentgenol. 2008, 191:115-123.
28. Taddei T.H., Kacena K.A., Yang M., Yang R., Malhotra A., Boxer M., Aleck K.A., Rennert G., Pastores G.M., Mistry P.K. The underrecognized progressive nature of N370S Gaucher disease and assessment of cancer risk in 403 patients. Am. J. Hematol. 2009, 84:208-214.
29. Pastores G.M., Wallenstein S., Desnick R.J., Luckey M.M. Bone density in Type 1 Gaucher disease. J. Bone Miner. Res. 1996, 11:1801-1807.
30. Elstein D., Itzchaki M., Mankin H.J. Skeletal involvement in Gaucher's disease. Bailliere's Clin. Haematol. 1997, 10:793-816.
31. Lebel E., Itzchaki M., Elstein D., Hadas-Halpern I., Abrahamov A., Zimran A. Skeletal manifestations in Gaucher disease: presentation and treatment. Isr. Med. Assoc. J. 1999, 1:267-271.
32. Pastores G.M., Patel M.J., Firooznia H. Bone and joint complications related to Gaucher disease. Curr. Rheumatol. Rep. 2000, 2:175-180.
33. Lutsky K.F., Tejwani N.C. Orthopaedic manifestations of Gaucher disease. Bull. NYU Hosp. Joint Dis. 2007, 65:37-42.
34. Weinreb N., Taylor J., Cox T., Yee J., vom Dahl S. A benchmark analysis of the achievement of therapeutic goals for type 1 Gaucher disease patients treated with imiglucerase. Am. J. Hematol. 2008, 83:890-895.
35. Zimran A., Morris E., Mengel E., Kaplan P., Belmatoug N., Hughes D.A., Malinova V., Heitner R., Sobreira E., Mrsic M., Granovsky-Grisaru S., Amato D., Vom Dahl S. The female Gaucher patient: the impact of enzyme replacement therapy around key reproductive events (menstruation, pregnancy and menopause). Blood Cells Mol. Dis. 2009, 43:264-288.
36. Granovsky-Grisaru S., Belmatoug N., Vom Dahl S., Mengel E., Morris E., Zimran A. The management of pregnancy in Gaucher disease. Eur. J. Obstet. Gynecol. Reprod. Biol. 2011, 156:3-8.
37. Elstein Y., Eisenberg V., Granovsky-Grisaru S., Rabinowitz R., Samueloff A., Zimran A., Elstein D. Pregnancies in Gaucher disease: a 5-year study. Am. J. Obstet. Gynecol. 2004, 190:435-441.
38. Bell R.S., Mankin H.J., Doppelt S.H. Osteomyelitis in Gaucher disease. J. Bone Joint Surg. Am. 1986, 68:1380-1388.
39. Itzchaki M., Lebel E., Dweck A., Patlas M., Hadas-Halpern I., Zimran A., Elstein D. Orthopedic considerations in Gaucher disease since the advent of enzyme replacement therapy. Acta Orthop. Scand. 2004, 75:641-653.
40. Rodrigue S.W., Rosenthal D.I., Barton N.W., Zurakowski D., Mankin H.J. Risk factors for osteonecrosis in patients with type 1 Gaucher's disease. Clin. Orthop. Relat. Res. 1999, 201-207.
41. Mistry P.K., Liu J., Yang M., Nottoli T., McGrath J., Jain D., Zhang K., Keutzer J., Chuang W.L., Mehal W.Z., Zhao H., Lin A., Mane S., Liu X., Peng Y.Z., Li J.H., Agrawal M., Zhu L.L., Blair H.C., Robinson L.J., Iqbal J., Sun L., Zaidi M. Glucocerebrosidase gene-deficient mouse recapitulates Gaucher disease displaying cellular and molecular dysregulation beyond the macrophage. Proc Natl Acad Sci U S A 2010, 107:19473-19478.
42. Javier R.M., Hachulla E., Rose C., Gressin V., Cherin P., Noel E., de Roux-Serratrice C., Dobbelaere D., Hartmann A., Jaussaud R., Clerson P., Grosbois B., Roux C. Vertebral fractures in Gaucher disease type I: data from the French "Observatoire" on Gaucher disease (FROG). Osteoporos. Int. 2011, 22:1255-1261.
43. Kaplan P., Andersson H.C., Kacena K.A., Yee J.D. The clinical and demographic characteristics of nonneuronopathic Gaucher disease in 887 children at diagnosis. Arch. Pediatr. Adolesc. Med. 2006, 160:603-608.
44. Kauli R., Zaizov R., Lazar L., Pertzelan A., Laron Z., Galatzer A., Phillip M., Yaniv Y., Cohen I.J. Delayed growth and puberty in patients with Gaucher disease type 1: natural history and effect of splenectomy and/or enzyme replacement therapy. Isr Med Assoc J 2000, 2:158-163.
45. Andersson H., Kaplan P., Kacena K., Yee J. Clinical Outcomes of Long-term (8Years) Enzyme Replacement Therapy in 884 Children with Type 1 Gaucher Disease [Abstract] 5th Symposium on Lysosomal Storage Disorders, Paris, France 2008, 30.
46. Bembi B., Ciana G., Mengel E., Terk M.R., Martini C., Wenstrup R.J. Bone complications in children with Gaucher disease. Br. J. Radiol. 2002, 75(Suppl. 1):A37-A44.
47. Hollak C.E., Corssmit E.P., Aerts J.M., Endert E., Sauerwein H.P., Romijn J.A., van Oers M.H. Differential effects of enzyme supplementation therapy on manifestations of type 1 Gaucher disease. Am. J. Med. 1997, 103:185-191.
48. Corssmit E.P., Hollak C.E., Endert E., van Oers M.H., Sauerwein H.P., Romijn J.A. Increased basal glucose production in type 1 Gaucher's disease. J. Clin. Endocrinol. Metab. 1995, 80:2653-2657.
49. Parisi M.S., Mastaglia S.R., Bagur A., Goldstein G., Zeni S.N., Oliveri B. Body composition and bone metabolism in young Gaucher disease type I patients treated with imiglucerase. Eur. J. Med. Res. 2008, 13:31-38.
50. Boven L.A., van Meurs M., Boot R.G., Mehta A., Boon L., Aerts J.M., Laman J.D. Gaucher cells demonstrate a distinct macrophage phenotype and resemble alternatively activated macrophages. Am. J. Clin. Pathol. 2004, 122:359-369.
51. Hollak C.E., van Weely S., van Oers M.H., Aerts J.M. Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. J. Clin. Investig. 1994, 93:1288-1292.
52. Boot R.G., Verhoek M., Langeveld M., Renkema G.H., Hollak C.E., Weening J.J., Donker-Koopman W.E., Groener J.E., Aerts J.M. CCL18: a urinary marker of Gaucher cell burden in Gaucher patients. J. Inherit. Metab. Dis. 2006, 29:564-571.
53. Aerts J.M., van Breemen M.J., Bussink A.P., Ghauharali K., Sprenger R., Boot R.G., Groener J.E., Hollak C.E., Maas M., Smit S., Hoefsloot H.C., Smilde A.K., Vissers J.P., de Jong S., Speijer D., de Koster C.G. Biomarkers for lysosomal storage disorders: identification and application as exemplified by chitotriosidase in Gaucher disease. Acta Paediatr. Suppl. 2008, 97:7-14.
54. Notelovitz M. Chapter 7: evaluating bone remodeling, osteoporosis: prevention 1997, Diagnosis and Management, PCI, Gainesville.
55. de Fost M., Vom Dahl S., Weverling G.J., Brill N., Brett S., Haussinger D., Hollak C.E. Increased incidence of cancer in adult Gaucher disease in Western Europe. Blood Cells Mol. Dis. 2006, 36:53-58.
56. Rosenbloom B.E., Weinreb N.J., Zimran A., Kacena K.A., Charrow J., Ward E. Gaucher disease and cancer incidence: a study from the Gaucher Registry. Blood 2005, 105:4569-4572.
57. Allen M.J., Myer B.J., Khokher A.M., Rushton N., Cox T.M. Pro-inflammatory cytokines and the pathogenesis of Gaucher's disease: increased release of interleukin-6 and interleukin-10. QJM 1997, 90:19-25.
58. Lichtenstein M., Zimran A., Horowitz M. Cytokine mRNA in Gaucher disease. Blood Cells Mol. Dis. 1997, 23:395-401.
59. Barak V., Acker M., Nisman B., Kalickman I., Abrahamov A., Zimran A., Yatziv S. Cytokines in Gaucher's disease. Eur. Cytokine Netw. 1999, 10:205-210.
60. Yao Z., Li P., Zhang Q., Schwarz E.M., Keng P., Arbini A., Boyce B.F., Xing L. Tumor necrosis factor-alpha increases circulating osteoclast precursor numbers by promoting their proliferation and differentiation in the bone marrow through up-regulation of c-Fms expression. J. Biol. Chem. 2006, 281:11846-11855.
61. van Dussen L., Lips P., Everts V.E., Bravenboer N., Jansen I.D., Groener J.E., Maas M., Blokland J.A., Aerts J.M., Hollak C.E. Markers of bone turnover in Gaucher disease: modeling the evolution of bone disease. J. Clin. Endocrinol. Metab. 2011, 96:2194-2205.
62. Tanaka Y., Nakayamada S., Okada Y. Osteoblasts and osteoclasts in bone remodeling and inflammation. Curr. Drug Targets Inflamm. Allergy 2005, 4:325-328.
63. Seibel M.J., Lang M., Geilenkeuser W.J. Interlaboratory variation of biochemical markers of bone turnover. Clin. Chem. 2001, 47:1443-1450.
64. Ciana G., Addobbati R., Tamaro G., Leopaldi A., Nevyjel M., Ronfani L., Vidoni L., Pittis M.G., Bembi B. Gaucher disease and bone: laboratory and skeletal mineral density variations during a long period of enzyme replacement therapy. J. Inherit. Metab. Dis. 2005, 28:723-732.
65. Campeau P.M., Rafei M., Boivin M.N., Sun Y., Grabowski G.A., Galipeau J. Characterization of Gaucher disease bone marrow mesenchymal stromal cells reveals an altered inflammatory secretome. Blood 2009, 114:3181-3190.
66. Andersson H.C., Charrow J., Kaplan P., Mistry P., Pastores G.M., Prakash-Cheng A., Rosenbloom B.E., Scott C.R., Wappner R.S., Weinreb N.J. Individualization of long-term enzyme replacement therapy for Gaucher disease. Genet. Med 2005, 7:105-110.
67. Vom Dahl S., Poll L., Di Rocco M., Ciana G., Denes C., Mariani G., Maas M. Evidence-based recommendations for monitoring bone disease and the response to enzyme replacement therapy in Gaucher patients. Curr. Med. Res. Opin. 2006, 22:1045-1064.
68. Cox T.M., Aerts J.M., Belmatoug N., Cappellini M.D., vom Dahl S., Goldblatt J., Grabowski G.A., Hollak C.E., Hwu P., Maas M., Martins A.M., Mistry P.K., Pastores G.M., Tylki-Szymanska A., Yee J., Weinreb N. Management of non-neuronopathic Gaucher disease with special reference to pregnancy, splenectomy, bisphosphonate therapy, use of biomarkers and bone disease monitoring. J. Inherit. Metab. Dis. 2008, 31:319-336.
69. Johnson L.A., Hoppel B.E., Gerard E.L., Miller S.P., Doppelt S.H., Zirzow G.C., Rosenthal D.I., Dambrosia J.M., Hill S.C., Brady R.O., et al. Quantitative chemical shift imaging of vertebral bone marrow in patients with Gaucher disease. Radiology 1992, 182:451-455.
70. Maas M., Hollak C.E., Akkerman E.M., Aerts J.M., Stoker J., Den Heeten G.J. Quantification of skeletal involvement in adults with type I Gaucher's disease: fat fraction measured by Dixon quantitative chemical shift imaging as a valid parameter. AJR Am J Roentgenol 2002, 179:961-965.
71. Hollak C., Maas M., Akkerman E., den Heeten A., Aerts H. Dixon quantitative chemical shift imaging is a sensitive tool for the evaluation of bone marrow responses to individualized doses of enzyme supplementation therapy in type 1 Gaucher disease. Blood Cells Mol. Dis. 2001, 27:1005-1012.
72. Maas M., van Kuijk C., Stoker J., Hollak C.E., Akkerman E.M., Aerts J.F., den Heeten G.J. Quantification of bone involvement in Gaucher disease: MR imaging bone marrow burden score as an alternative to Dixon quantitative chemical shift MR imaging-initial experience. Radiology 2003, 229:554-561.
73. Poll L.W., Willers R., Haussinger D., Modder U., Vom Dahl S. MRI Bone Marrow Findings in 63 Patients with Type I Gaucher Disease. Rofo 2010.
74. Mariani G., Filocamo M., Giona F., Villa G., Amendola A., Erba P., Buffoni F., Copello F., Pierini A., Minichilli F., Gatti R., Brady R.O. Severity of bone marrow involvement in patients with Gaucher's disease evaluated by scintigraphy with 99mTc-sestamibi. J. Nucl. Med. 2003, 44:1253-1262.
75. Mota R.M., Mankin H. Use of plain radiography to optimize skeletal outcomes in children with type 1 Gaucher disease in Brazil. J. Pediatr. Orthop. 2007, 27:347-350.
76. Maas M., Hangartner T., Mariani G., McHugh K., Moore S., Grabowski G.A., Kaplan P., Vellodi A., Yee J., Steinbach L. Recommendations for the assessment and monitoring of skeletal manifestations in children with Gaucher disease. Skeletal Radiol. 2008, 37:185-188.
77. Drelichman G., Ponce E., Basack N., Freigeiro D., Aversa L., Graciela E., Kohan R. Clinical consequences of interrupting enzyme replacement therapy in children with type 1 Gaucher disease. J. Pediatr. 2007, 151:197-201.
78. Rosenthal D.I., Doppelt S.H., Mankin H.J., Dambrosia J.M., Xavier R.J., McKusick K.A., Rosen B.R., Baker J., Niklason L.T., Hill S.C., et al. Enzyme replacement therapy for Gaucher disease: skeletal responses to macrophage-targeted glucocerebrosidase. Pediatrics 1995, 96:629-637.
79. Poll L.W., Maas M., Terk M.R., Roca-Espiau M., Bembi B., Ciana G., Weinreb N.J. Response of Gaucher bone disease to enzyme replacement therapy. Br. J. Radiol. 2002, 75(Suppl. 1):A25-A36.
80. Poll L.W., Koch J.A., Willers R., Aerts H., Scherer A., Haussinger D., Modder U., vom Dahl S. Correlation of bone marrow response with hematological, biochemical, and visceral responses to enzyme replacement therapy of nonneuronopathic (type 1) Gaucher disease in 30 adult patients. Blood Cells Mol. Dis. 2002, 28:209-220.
81. Vlieger E., Maas M., Akkerman E., Hollak C., Aerts J., den Heeten G. The application of the vertebra-disc ratio in a population of patients with Gaucher's disease. Proc. Intl. Soc. Magn. Reson. Med. 2000, 8:2131.
82. Robertson P.L., Maas M., Goldblatt J. Semiquantitative assessment of skeletal response to enzyme replacement therapy for Gaucher's disease using the bone marrow burden score. AJR Am J Roentgenol 2007, 188:1521-1528.
83. Poll L.W., Koch J.A., vom Dahl S., Willers R., Scherer A., Boerner D., Niederau C., Haussinger D., Modder U. Magnetic resonance imaging of bone marrow changes in Gaucher disease during enzyme replacement therapy: first German long-term results. Skeletal Radiol. 2001, 30:496-503.
84. Wenstrup R.J., Kacena K.A., Kaplan P., Pastores G.M., Prakash-Cheng A., Zimran A., Hangartner T.N. Effect of enzyme replacement therapy with imiglucerase on BMD in type 1 Gaucher disease. J. Bone Miner. Res. 2007, 22:119-126.
85. Sims K.B., Pastores G.M., Weinreb N.J., Barranger J., Rosenbloom B.E., Packman S., Kaplan P., Mankin H., Xavier R., Angell J., Fitzpatrick M.A., Rosenthal D. Improvement of bone disease by imiglucerase (Cerezyme) therapy in patients with skeletal manifestations of type 1 Gaucher disease: results of a 48-month longitudinal cohort study. Clin. Genet. 2008, 75:430-440.
86. Andersson H., Kaplan P., Kacena K., Yee J. Eight-year clinical outcomes of long-term enzyme replacement therapy for 884 children with Gaucher disease type 1. Pediatrics 2008, 122:1182-1190.
87. Schiffmann R., Mankin H., Dambrosia J.M., Xavier R.J., Kreps C., Hill S.C., Barton N.W., Rosenthal D.I. Decreased bone density in splenectomized Gaucher patients receiving enzyme replacement therapy. Blood Cells Mol. Dis. 2002, 28:288-296.
88. Lebel E., Dweck A., Foldes A.J., Golowa Y., Itzchaki M., Zimran A., Elstein D. Bone density changes with enzyme therapy for Gaucher disease. J. Bone Miner. Metab. 2004, 22:597-601.
89. Cohen I.J., Katz K., Kornreich L., Horev G., Frish A., Zaizov R. Low-dose high-frequency enzyme replacement therapy prevents fractures without complete suppression of painful bone crises in patients with severe juvenile onset type I Gaucher disease. Blood Cells Mol. Dis. 1998, 24:296-302.
90. Beutler E. Gaucher disease: new molecular approaches to diagnosis and treatment. Science 1992, 256:794-799.
91. Beutler E., Demina A., Laubscher K., Garver P., Gelbart T., Balicki D., Vaughan L. The clinical course of treated and untreated Gaucher disease. A study of 45 patients. Blood Cells Mol. Dis. 1995, 21:86-108.
92. Ida H., Rennert O.M., Kato S., Ueda T., Oishi K., Maekawa K., Eto Y. Severe skeletal complications in Japanese patients with type 1 Gaucher disease. J. Inherit. Metab. Dis. 1999, 22:63-73.
93. Terk M.R., Dardashti S., Liebman H.A. Bone marrow response in treated patients with Gaucher disease: evaluation by T1-weighted magnetic resonance images and correlation with reduction in liver and spleen volume. Skeletal Radiol. 2000, 29:563-571.
94. Pastores G.M., Sibille A.R., Grabowski G.A. Enzyme therapy in Gaucher disease type 1: dosage efficacy and adverse effects in 33 patients treated for 6 to 24months. Blood 1993, 82:408-416.
95. Elstein D., Hadas-Halpern I., Itzchaki M., Lahad A., Abrahamov A., Zimran A. Effect of low-dose enzyme replacement therapy on bones in Gaucher disease patients with severe skeletal involvement. Blood Cells Mol. Dis. 1996, 22:104-111. discussion 112-104.
96. Charrow J., Dulisse B., Grabowski G.A., Weinreb N.J. The effect of enzyme replacement therapy on bone crisis and bone pain in patients with type 1 Gaucher disease. Clin. Genet. 2007, 71:205-211.
97. de Fost M., Aerts J.M., Groener J.E., Maas M., Akkerman E.M., Wiersma M.G., Hollak C.E. Low frequency maintenance therapy with imiglucerase in adult type I Gaucher disease: a prospective randomized controlled trial. Haematologica 2007, 92:215-221.
98. Heitner R., Arndt S., Levin J.B. Imiglucerase low-dose therapy for paediatric Gaucher disease-a long-term cohort study. S. Afr. Med. J. = Suid-Afrikaanse Tydskrif vir Geneeskunde 2004, 94:647-651.
99. Hollak C.E., de Fost M., van Dussen L., Vom Dahl S., Aerts J.M. Enzyme therapy for the treatment of type 1 Gaucher disease: clinical outcomes and dose - response relationships. Expert. Opin. Pharmacother. 2009.
100. Kishnani P.S., DiRocco M., Kaplan P., Mehta A., Pastores G.M., Smith S.E., Puga A.C., Lemay R.M., Weinreb N.J. A randomized trial comparing the efficacy and safety of imiglucerase (Cerezyme) infusions every 4weeks versus every 2weeks in the maintenance therapy of adult patients with Gaucher disease type 1. Mol. Genet. Metab. 2009, 96:164-170.
101. Zimran A., Hadas-Halpern I., Zevin S., Levy-Lahad E., Abrahamov A. Low-dose high-frequency enzyme replacement therapy for very young children with severe Gaucher disease. Br. J. Haematol. 1993, 85:783-786.
102. Figueroa M.L., Rosenbloom B.E., Kay A.C., Garver P., Thurston D.W., Koziol J.A., Gelbart T., Beutler E. A less costly regimen of alglucerase to treat Gaucher's disease. N. Engl. J. Med. 1992, 327:1632-1636.
103. Wilson C., Spearing R., Teague L., Robertson P., Blacklock H. The outcome of clinical parameters in adults with severe Type I Gaucher disease using very low dose enzyme replacement therapy. Mol. Genet. Metab. 2007, 92:131-136.
104. Dweck A., Abrahamov A., Hadas-Halpern I., Bdolach-Avram T., Zimran A., Elstein D. Type I Gaucher disease in children with and without enzyme therapy. Pediatr. Hematol. Oncol. 2002, 19:389-397.
105. Zimran A., Abrahamov A., Elstein D. Children with type I Gaucher disease: growing into adulthood with and without enzyme therapy. Isr Med Assoc J 2000, 2:80-81.
106. Piran S., Roberts A., Patterson M.A., Amato D. The clinical course of untreated Gaucher disease in 22 patients over 10years: hematological and skeletal manifestations. Blood Cells Mol. Dis. 2009, 43:289-293.
107. Zimran A., Kay A., Gelbart T., Garver P., Thurston D., Saven A., Beutler E. Gaucher disease. Clinical, laboratory, radiologic, and genetic features of 53 patients. Medicine 1992, 71:337-353.
108. de Fost M., Hollak C.E., Groener J.E., Aerts J.M., Maas M., Poll L.W., Wiersma M.G., Haussinger D., Brett S., Brill N., vom Dahl S. Superior effects of high-dose enzyme replacement therapy in type 1 Gaucher disease on bone marrow involvement and chitotriosidase levels: a 2-center retrospective analysis. Blood 2006, 108:830-835.
109. de Fost M., van Noesel C.J., Aerts J.M., Maas M., Poll R.G., Hollak C.E. Persistent bone disease in adult type 1 Gaucher disease despite increasing doses of enzyme replacement therapy. Haematologica 2008, 93:1119-1120.
110. Sidransky E., Ginns E.I., Westman J.A., Ehmann W.C. Pathologic fractures may develop in Gaucher patients receiving enzyme replacement therapy. Am. J. Hematol. 1994, 47:247-249.
111. Brumshtein B., Salinas P., Peterson B., Chan V., Silman I., Sussman J.L., Savickas P.J., Robinson G.S., Futerman A.H. Characterization of gene-activated human acid-{beta}-glucosidase: crystal structure, glycan composition and internalization into macrophages. Glycobiology 2010, 20:24-32.
112. Shaaltiel Y., Bartfeld D., Hashmueli S., Baum G., Brill-Almon E., Galili G., Dym O., Boldin-Adamsky S.A., Silman I., Sussman J.L., Futerman A.H., Aviezer D. Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher's disease using a plant cell system. Plant Biotechnol. J. 2007, 5:579-590.
113. Van Patten S.M., Hughes H., Huff M.R., Piepenhagen P.A., Waire J., Qiu H., Ganesa C., Reczek D., Ward P.V., Kutzko J.P., Edmunds T. Effect of mannose chain length on targeting of glucocerebrosidase for enzyme replacement therapy of Gaucher disease. Glycobiology 2007, 17:467-478.
114. Elstein D., Foldes A.J., Zahrieh D., Cohn G.M., Djordjevic M., Brutaru C., Zimran A. Significant and continuous improvement in bone mineral density among type 1 Gaucher disease patients treated with velaglucerase alfa: 69-month experience, including dose reduction. Blood Cells Mol. Dis. 2011, 47:56-61.
115. Cox T., Lachmann R., Hollak C., Aerts J., van Weely S., Hrebicek M., Platt F., Butters T., Dwek R., Moyses C., Gow I., Elstein D., Zimran A. Novel oral treatment of Gaucher's disease with N-butyldeoxynojirimycin (OGT 918) to decrease substrate biosynthesis. Lancet 2000, 355:1481-1485.
116. Pastores G.M., Elstein D., Hrebicek M., Zimran A. Effect of miglustat on bone disease in adults with type 1 Gaucher disease: a pooled analysis of three multinational, open-label studies. Clin. Ther. 2007, 29:1645-1654.
117. Elstein D., Dweck A., Attias D., Hadas-Halpern I., Zevin S., Altarescu G., Aerts J.F., van Weely S., Zimran A. Oral maintenance clinical trial with miglustat for type I Gaucher disease: switch from or combination with intravenous enzyme replacement. Blood 2007, 110:2296-2301.
118. Hollak C.E., Hughes D., van Schaik I.N., Schwierin B., Bembi B. Miglustat (Zavesca(R)) in type 1 Gaucher disease: 5-year results of a post-authorisation safety surveillance programme. Pharmacoepidemiol. Drug Saf. 2009, 18:770-777.
119. Champion H., Ramaswami U., Imrie J., Lachmann R.H., Gallagher J., Cox T.M., Wraith J.E. Dietary modifications in patients receiving miglustat. J. Inherit. Metab. Dis. 2010.
120. Cox T.M. Eliglustat tartrate, an orally active glucocerebroside synthase inhibitor for the potential treatment of Gaucher disease and other lysosomal storage diseases. Curr. Opin. Investig. Drugs 2010, 11:1169-1181.
121. Lukina E., Watman N., Arreguin E.A., Banikazemi M., Dragosky M., Iastrebner M., Rosenbaum H., Phillips M., Pastores G.M., Rosenthal D.I., Kaper M., Singh T., Puga A.C., Bonate P.L., Peterschmitt M.J. A Phase 2 study of eliglustat tartrate (Genz-112638), an oral substrate reduction therapy for Gaucher disease type 1. Blood 2010, 116:893-899.
122. Lukina E., Watman N., Arreguin E.A., Dragosky M., Iastrebner M., Rosenbaum H., Phillips M., Pastores G.M., Kamath R.S., Rosenthal D.I., Kaper M., Singh T., Puga A.C., Peterschmitt M.J. Improvement in hematological, visceral, and skeletal manifestations of Gaucher disease type 1 with oral eliglustat tartrate (Genz-112638) treatment: 2-year results of a phase 2 study. Blood 2010, 116:4095-4098.