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Reviews in Endocrine and Metabolic Disorders

Published in:

Open Access 01-03-2018

Bone health in patients with inborn errors of metabolism

Published in: Reviews in Endocrine and Metabolic Disorders | Issue 1/2018

Abstract

Inborn errors of metabolism encompass a wide spectrum of disorders, frequently affecting bone. The most important metabolic disorders that primarily influence calcium or phosphate balance, resulting in skeletal pathology, are hypophosphatemic rickets and hypophosphatasia. Conditions involving bone marrow or affecting skeletal growth and development are mainly the lysosomal storage disorders, in particular the mucopolysaccharidoses. In these disorders skeletal abnormalities are often the presenting symptom and early recognition and intervention improves outcome in many of these diseases. Many disorders of intermediary metabolism may impact bone health as well, resulting in higher frequencies of osteopenia and osteoporosis. In these conditions factors contributing to the reduced bone mineralization can be the disorder itself, the strict dietary treatment, reduced physical activity or sunlight exposure and/or early ovarian failure. Awareness of these primary or secondary bone problems amongst physicians treating patients with inborn errors of metabolism is of importance for optimization bone health and recognition of skeletal complications.

Dussault PM, Lazzari AA. Epilepsy and osteoporosis risk. Curr Opin Endocrinol Diabetes Obes. 2017;24(6):395–401. https://doi.org/10.1097/MED.0000000000000366.CrossRefPubMed

Gattineni J. Inherited disorders of calcium and phosphate metabolism. Curr Opin Pediatr. 2014;26(2):215–22. https://doi.org/10.1097/MOP.0000000000000064.CrossRefPubMedPubMedCentral

Linglart A, Biosse-Duplan M. Hypophosphatasia. Curr Osteoporos Rep. 2016;14(3):95–105. https://doi.org/10.1007/s11914-016-0309-0.CrossRefPubMed

Fonta C, Salles JP. Neuromuscular features of hypophosphatasia. Arch Pediatr. 2017;24(5S2):5S85–5S8. https://doi.org/10.1016/S0929-693X(18)30021-6.CrossRefPubMed

Conti F, Ciullini L, Pugliese G. Hypophosphatasia: clinical manifestation and burden of disease in adult patients. Clin Cases Miner Bone Metab. 2017;14(2):230–4. https://doi.org/10.11138/ccmbm/2017.14.1.230.CrossRefPubMedPubMedCentral

Whyte MP, Mumm S, Deal C. Adult hypophosphatasia treated with teriparatide. J Clin Endocrinol Metab. 2007;92(4):1203–8. https://doi.org/10.1210/jc.2006-1902.CrossRefPubMed

Whyte MP, Greenberg CR, Salman NJ, Bober MB, McAlister WH, Wenkert D, et al. Enzyme-replacement therapy in life-threatening hypophosphatasia. N Engl J Med. 2012;366(10):904–13. https://doi.org/10.1056/NEJMoa1106173.CrossRefPubMed

Whyte MP, Madson KL, Phillips D, Reeves AL, McAlister WH, Yakimoski A, et al. Asfotase alfa therapy for children with hypophosphatasia. JCI Insight. 2016;1(9):e85971. https://doi.org/10.1172/jci.insight.85971.CrossRefPubMedPubMedCentral

Whyte MP, Rockman-Greenberg C, Ozono K, Riese R, Moseley S, Melian A, et al. Asfotase alfa treatment improves survival for perinatal and infantile Hypophosphatasia. J Clin Endocrinol Metab. 2016;101(1):334–42. https://doi.org/10.1210/jc.2015-3462.CrossRef

10.

Costain G, Moore AM, Munroe L, Williams A, Zlotnik Shaul R, Rockman-Greenberg C, et al. Enzyme replacement therapy in perinatal hypophosphatasia: case report of a negative outcome and lessons for clinical practice. Mol Genet Metab Rep. 2018;14:22–6. https://doi.org/10.1016/j.ymgmr.2017.10.006.CrossRefPubMed

11.

Ruppe MD. X-Linked Hypophosphatemia. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, Bean LJH, Stephens K et al., editors. GeneReviews((R)). Seattle (WA) 1993. Available from http://www.ncbi.nlm.nih.gov/books/NBK83985/ PubMedPMID:22319799. Accessed 1 June 2018.

12.

Quinlan C, Guegan K, Offiah A, Neill RO, Hiorns MP, Ellard S, et al. Growth in PHEX-associated X-linked hypophosphatemic rickets: the importance of early treatment. Pediatr Nephrol. 2012;27(4):581–8. https://doi.org/10.1007/s00467-011-2046-z.CrossRefPubMed

13.

Carpenter TO, Imel EA, Holm IA, de Beur JSM, Insogna KL. A clinician’s guide to X-linked hypophosphatemia. J Bone Miner Res. 2011;26(7):1381–8. https://doi.org/10.1002/jbmr.340.CrossRefPubMedPubMedCentral

14.

Rothenbuhler A, Esterle L, Gueorguieva I, Salles JP, Mignot B, Colle M, et al. Two-year recombinant human growth hormone (rhGH) treatment is more effective in pre-pubertal compared to pubertal short children with X-linked hypophosphatemic rickets (XLHR). Growth Hormon IGF Res. 2017;36:11–5. https://doi.org/10.1016/j.ghir.2017.08.001.CrossRef

15.

Carpenter TO, Imel EA, Ruppe MD, Weber TJ, Klausner MA, Wooddell MM, et al. Randomized trial of the anti-FGF23 antibody KRN23 in X-linked hypophosphatemia. J Clin Invest. 2014;124(4):1587–97. https://doi.org/10.1172/JCI72829.CrossRefPubMedPubMedCentral

16.

Strensiq EPAR: http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Public_assessment_report/human/003794/WC500194340.pdf.

17.

Mikosch P, Hughes D. An overview on bone manifestations in Gaucher disease. Wien Med Wochenschr. 2010;160(23–24):609–24. https://doi.org/10.1007/s10354-010-0841-y.CrossRefPubMed

18.

Schuchman EH, Wasserstein MP. Types a and B Niemann-pick disease. Pediatr Endocrinol Rev. 2016;13(Suppl 1):674–81.PubMed

19.

Wasserstein M, Godbold J, McGovern MM. Skeletal manifestations in pediatric and adult patients with Niemann pick disease type B. J Inherit Metab Dis. 2013;36(1):123–7. https://doi.org/10.1007/s10545-012-9503-0.CrossRefPubMed

20.

Wasserstein MP, Larkin AE, Glass RB, Schuchman EH, Desnick RJ, McGovern MM. Growth restriction in children with type B Niemann-pick disease. J Pediatr. 2003;142(4):424–8. https://doi.org/10.1067/mpd.2003.113.CrossRefPubMed

21.

Muenzer J. Overview of the mucopolysaccharidoses. Rheumatology (Oxford). 2011;50(Suppl 5):v4–12. https://doi.org/10.1093/rheumatology/ker394.CrossRef

22.

Clarke LA. The mucopolysaccharidoses: a success of molecular medicine. Expert Rev Mol Med. 2008;10:e1. https://doi.org/10.1017/S1462399408000550.CrossRefPubMed

23.

Palmucci S, Attina G, Lanza ML, Belfiore G, Cappello G, Foti PV, et al. Imaging findings of mucopolysaccharidoses: a pictorial review. Insights Imaging. 2013;4(4):443–59. https://doi.org/10.1007/s13244-013-0246-8.CrossRefPubMedPubMedCentral

24.

Beck M, Braun S, Coerdt W, Merz E, Young E, Sewell AC. Fetal presentation of Morquio disease type a. Prenat Diagn. 1992;12(12):1019–29.CrossRefPubMed

25.

Guarany NR, Schwartz IV, Guarany FC, Giugliani R. Functional capacity evaluation of patients with mucopolysaccharidosis. J Pediatr Rehabil Med. 2012;5(1):37–46. https://doi.org/10.3233/PRM-2012-0194.CrossRefPubMed

26.

Tylki-Szymanska A, Marucha J, Jurecka A, Syczewska M, Czartoryska B. Efficacy of recombinant human alpha-L-iduronidase (laronidase) on restricted range of motion of upper extremities in mucopolysaccharidosis type I patients. J Inherit Metab Dis. 2010;33(2):151–7. https://doi.org/10.1007/s10545-010-9059-9.CrossRefPubMed

27.

Tomatsu S, Yasuda E, Patel P, Ruhnke K, Shimada T, Mackenzie WG, et al. Morquio a syndrome: diagnosis and current and future therapies. Pediatr Endocrinol Rev. 2014;12(Suppl 1):141–51.PubMedPubMedCentral

28.

Oussoren E, Bessems J, Pollet V, van der Meijden JC, van der Giessen LJ, Plug I, et al. A long term follow-up study of the development of hip disease in Mucopolysaccharidosis type VI. Mol Genet Metab. 2017;121(3):241–51. https://doi.org/10.1016/j.ymgme.2017.05.008.CrossRefPubMed

29.

Langereis EJ, den Os MM, Breen C, Jones SA, Knaven OC, Mercer J, et al. Progression of hip dysplasia in Mucopolysaccharidosis type I hurler after successful hematopoietic stem cell transplantation. J Bone Joint Surg Am. 2016;98(5):386–95. https://doi.org/10.2106/JBJS.O.00601.CrossRefPubMed

30.

Brands MM, Gungor D, van den Hout JM, Karstens FP, Oussoren E, Plug I, et al. Pain: a prevalent feature in patients with mucopolysaccharidosis. Results of a cross-sectional national survey. J Inherit Metab Dis. 2015;38(2):323–31. https://doi.org/10.1007/s10545-014-9737-0.CrossRefPubMed

31.

Clarke LA, Hollak CE. The clinical spectrum and pathophysiology of skeletal complications in lysosomal storage disorders. Best Pract Res Clin Endocrinol Metab. 2015;29(2):219–35. https://doi.org/10.1016/j.beem.2014.08.010.CrossRefPubMed

32.

Oussoren E, Brands MM, Ruijter GJ, der Ploeg AT, Reuser AJ. Bone, joint and tooth development in mucopolysaccharidoses: relevance to therapeutic options. Biochim Biophys Acta. 2011;1812(11):1542–56. https://doi.org/10.1016/j.bbadis.2011.07.013.CrossRefPubMed

33.

Opoka-Winiarska V, Jurecka A, Emeryk A, Tylki-Szymanska A. Osteoimmunology in mucopolysaccharidoses type I, II, VI and VII. Immunological regulation of the osteoarticular system in the course of metabolic inflammation. Osteoarthr Cartil. 2013;21(12):1813–23. https://doi.org/10.1016/j.joca.2013.08.001.CrossRefPubMed

34.

Tomatsu S, Almeciga-Diaz CJ, Montano AM, Yabe H, Tanaka A, Dung VC, et al. Therapies for the bone in mucopolysaccharidoses. Mol Genet Metab. 2015;114(2):94–109. https://doi.org/10.1016/j.ymgme.2014.12.001.CrossRefPubMed

35.

Muenzer J. Early initiation of enzyme replacement therapy for the mucopolysaccharidoses. Mol Genet Metab. 2014;111(2):63–72. https://doi.org/10.1016/j.ymgme.2013.11.015.CrossRefPubMed

36.

van der Linden MH, Kruyt MC, Sakkers RJ, de Koning TJ, Oner FC, Castelein RM. Orthopaedic management of Hurler's disease after hematopoietic stem cell transplantation: a systematic review. J Inherit Metab Dis. 2011;34(3):657–69. https://doi.org/10.1007/s10545-011-9304-x.CrossRefPubMedPubMedCentral

37.

Hennermann JB, Gokce S, Solyom A, Mengel E, Schuchman EH, Simonaro CM. Treatment with pentosan polysulphate in patients with MPS I: results from an open label, randomized, monocentric phase II study. J Inherit Metab Dis. 2016;39(6):831–7. https://doi.org/10.1007/s10545-016-9974-5.CrossRefPubMed

38.

Spranger J, Gehler J, Cantz M. The radiographic features of mannosidosis. Radiology. 1976;119(2):401–7. https://doi.org/10.1148/119.2.401.CrossRefPubMed

39.

Beck M, Olsen KJ, Wraith JE, Zeman J, Michalski JC, Saftig P, et al. Natural history of alpha mannosidosis a longitudinal study. Orphanet J Rare Dis. 2013;8:88. https://doi.org/10.1186/1750-1172-8-88.CrossRefPubMedPubMedCentral

40.

Gerards AH, Winia WP, Westerga J, Dijkmans BA, van Soesbergen RM. Destructive joint disease in alpha-mannosidosis. A case report and review of the literature. Clin Rheumatol. 2004;23(1):40–2. https://doi.org/10.1007/s10067-003-0770-x.CrossRefPubMed

41.

Malm D, Riise Stensland HM, Edvardsen O, Nilssen O. The natural course and complications of alpha-mannosidosis--a retrospective and descriptive study. J Inherit Metab Dis. 2014;37(1):79–82. https://doi.org/10.1007/s10545-013-9622-2.CrossRefPubMed

42.

Grewal SS, Shapiro EG, Krivit W, Charnas L, Lockman LA, Delaney KA, et al. Effective treatment of alpha-mannosidosis by allogeneic hematopoietic stem cell transplantation. J Pediatr. 2004;144(5):569–73. https://doi.org/10.1016/j.jpeds.2004.01.025.CrossRefPubMed

43.

Yesilipek AM, Akcan M, Karasu G, Uygun V, Kupesiz A, Hazar V. Successful unrelated bone marrow transplantation in two siblings with alpha-mannosidosis. Pediatr Transplant. 2012;16(7):779–82. https://doi.org/10.1111/j.1399-3046.2012.01763.x.CrossRefPubMed

44.

Bedilu R, Nummy KA, Cooper A, Wevers R, Smeitink J, Kleijer WJ, et al. Variable clinical presentation of lysosomal beta-mannosidosis in patients with null mutations. Mol Genet Metab. 2002;77(4):282–90.

45.

Gelb BD, Shi GP, Chapman HA, Desnick RJ. Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science. 1996;273(5279):1236–8.CrossRefPubMed

46.

Lamy M, Maroteaux P. Pycnodysostosis. Rev Esp Pediatr. 1965;21(124):433–7.PubMed

47.

Xue Y, Cai T, Shi S, Wang W, Zhang Y, Mao T, et al. Clinical and animal research findings in pycnodysostosis and gene mutations of cathepsin K from 1996 to 2011. Orphanet J Rare Dis. 2011;6:20. https://doi.org/10.1186/1750-1172-6-20.CrossRefPubMedPubMedCentral

48.

Arman A, Bereket A, Coker A, Kiper PO, Guran T, Ozkan B, et al. Cathepsin K analysis in a pycnodysostosis cohort: demographic, genotypic and phenotypic features. Orphanet J Rare Dis. 2014;9:60. https://doi.org/10.1186/1750-1172-9-60.CrossRefPubMedPubMedCentral

49.

Aghili H, Tabatabaei SMA, Goldani MM. Clinical and radiographic features of Pycnodysostosis with emphasis on Dentofacial problems. Case Rep Dent. 2017;2017:4352485. https://doi.org/10.1155/2017/4352485.CrossRefPubMedPubMedCentral

50.

Testani E, Scarano E, Leoni C, Dittoni S, Losurdo A, Colicchio S, et al. Upper airway surgery of obstructive sleep apnea in pycnodysostosis: case report and literature review. Am J Med Genet A. 2014;164A(8):2029–35. https://doi.org/10.1002/ajmg.a.36557.CrossRef

51.

Introne WJ, Gahl WA. Alkaptonuria. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, Bean LJH, Stephens K et al., editors. GeneReviews((R)). Seattle (WA) 1993. Available from http://www.ncbi.nlm.nih.gov/books/NBK1454/ PubMed PMID: 20301627. Accessed 1 June 2018.

52.

Ranganath LR, Cox TF. Natural history of alkaptonuria revisited: analyses based on scoring systems. J Inherit Metab Dis. 2011;34(6):1141–51. https://doi.org/10.1007/s10545-011-9374-9.CrossRefPubMed

53.

Arnoux JB, Le Quan Sang KH, Brassier A, Grisel C, Servais A, Wippf J, et al. Old treatments for new insights and strategies: proposed management in adults and children with alkaptonuria. J Inherit Metab Dis. 2015;38(5):791–6. https://doi.org/10.1007/s10545-015-9844-6.CrossRefPubMed

54.

Ranganath LR, Milan AM, Hughes AT, Dutton JJ, Fitzgerald R, Briggs MC, et al. Suitability of Nitisinone in Alkaptonuria 1 (SONIA 1): an international, multicentre, randomised, open-label, no-treatment controlled, parallel-group, dose-response study to investigate the effect of once daily nitisinone on 24-h urinary homogentisic acid excretion in patients with alkaptonuria after 4 weeks of treatment. Ann Rheum Dis. 2016;75(2):362–7. https://doi.org/10.1136/annrheumdis-2014-206033.CrossRefPubMed

55.

Coelho AI, Rubio-Gozalbo ME, Vicente JB, Rivera I. Sweet and sour: an update on classic galactosemia. J Inherit Metab Dis. 2017;40(3):325–42. https://doi.org/10.1007/s10545-017-0029-3.CrossRefPubMedPubMedCentral

56.

van Erven B, Welling L, van Calcar SC, Doulgeraki A, Eyskens F, Gribben J, et al. Bone health in classic Galactosemia: systematic review and Meta-analysis. JIMD Rep. 2017;35:87–96. https://doi.org/10.1007/8904_2016_28.CrossRefPubMed

57.

Batey LA, Welt CK, Rohr F, Wessel A, Anastasoaie V, Feldman HA, et al. Skeletal health in adult patients with classic galactosemia. Osteoporos Int. 2013;24(2):501–9. https://doi.org/10.1007/s00198-012-1983-0.CrossRefPubMed

58.

Waisbren SE, Potter NL, Gordon CM, Green RC, Greenstein P, Gubbels CS, et al. The adult galactosemic phenotype. J Inherit Metab Dis. 2012;35(2):279–86. https://doi.org/10.1007/s10545-011-9372-y.CrossRefPubMedPubMedCentral

59.

Panis B, Vermeer C, van Kroonenburgh M, Nieman FHM, Menheere P, Spaapen LJ, et al. Effect of calcium, vitamins K1 and D3 on bone in galactosemia. Bone. 2006;39(5):1123–9. https://doi.org/10.1016/j.bone.2006.05.002.CrossRefPubMed

60.

Fridovich-Keil JL, Gubbels CS, Spencer JB, Sanders RD, Land JA, Rubio-Gozalbo E. Ovarian function in girls and women with GALT-deficiency galactosemia. J Inherit Metab Dis. 2011;34(2):357–66. https://doi.org/10.1007/s10545-010-9221-4.CrossRefPubMed

61.

Levasseur R. Bone tissue and hyperhomocysteinemia. Joint Bone Spine. 2009;76(3):234–40. https://doi.org/10.1016/j.jbspin.2008.11.002.CrossRefPubMed

62.

Mudd SH, Skovby F, Levy HL, Pettigrew KD, Wilcken B, Pyeritz RE, et al. The natural history of homocystinuria due to cystathionine beta-synthase deficiency. Am J Hum Genet. 1985;37(1):1–31.

63.

Weber DR, Coughlin C, Brodsky JL, Lindstrom K, Ficicioglu C, Kaplan P, et al. Low bone mineral density is a common finding in patients with homocystinuria. Mol Genet Metab. 2016;117(3):351–4. https://doi.org/10.1016/j.ymgme.2015.12.003.CrossRefPubMed

64.

Morris AA, Kozich V, Santra S, Andria G, Ben-Omran TI, Chakrapani AB, et al. Guidelines for the diagnosis and management of cystathionine beta-synthase deficiency. J Inherit Metab Dis. 2017;40(1):49–74. https://doi.org/10.1007/s10545-016-9979-0.CrossRefPubMed

65.

Lim JS, Lee DH. Changes in bone mineral density and body composition of children with well-controlled homocystinuria caused by CBS deficiency. Osteoporos Int. 2013;24(9):2535–8. https://doi.org/10.1007/s00198-013-2351-4.CrossRefPubMed

66.

Yap S, Naughten E. Homocystinuria due to cystathionine beta-synthase deficiency in Ireland: 25 years' experience of a newborn screened and treated population with reference to clinical outcome and biochemical control. J Inherit Metab Dis. 1998;21(7):738–47.CrossRefPubMed

67.

Mundy HR, Williams JE, Lee PJ, Fewtrell MS. Reduction in bone mineral density in glycogenosis type III may be due to a mixed muscle and bone deficit. J Inherit Metab Dis. 2008;31(3):418–23. https://doi.org/10.1007/s10545-008-0830-0.CrossRefPubMed

68.

van den Berg LE, Zandbergen AA, van Capelle CI, de Vries JM, Hop WC, van den Hout JM, et al. Low bone mass in Pompe disease: muscular strength as a predictor of bone mineral density. Bone. 2010;47(3):643–9. https://doi.org/10.1016/j.bone.2010.06.021.CrossRefPubMed

69.

Bertoldo F, Zappini F, Brigo M, Moggio M, Lucchini V, Angelini C, et al. Prevalence of asymptomatic vertebral fractures in late-onset Pompe disease. J Clin Endocrinol Metab. 2015;100(2):401–6. https://doi.org/10.1210/jc.2014-2763.CrossRef

70.

Lee PJ, Patel JS, Fewtrell M, Leonard JV, Bishop NJ. Bone mineralisation in type 1 glycogen storage disease. Eur J Pediatr. 1995;154(6):483–7.CrossRefPubMed

71.

Schwahn B, Rauch F, Wendel U, Schonau E. Low bone mass in glycogen storage disease type 1 is associated with reduced muscle force and poor metabolic control. J Pediatr. 2002;141(3):350–6. https://doi.org/10.1067/mpd.2002.126456.CrossRefPubMed

72.

Rake JP, Visser G, Huismans D, Huitema S, van der Veer E, Piers DA, et al. Bone mineral density in children, adolescents and adults with glycogen storage disease type Ia: a cross-sectional and longitudinal study. J Inherit Metab Dis. 2003;26(4):371–84.CrossRefPubMed

73.

Rodriguez-Gomez I, Santalla A, Diez-Bermejo J, Munguia-Izquierdo D, Alegre LM, Nogales-Gadea G, et al. A new condition in McArdle disease: poor bone health-benefits of an active lifestyle. Med Sci Sports Exerc. 2018;50(1):3–10. https://doi.org/10.1249/MSS.0000000000001414.CrossRefPubMed

74.

Melis D, Pivonello R, Cozzolino M, Della Casa R, Balivo F, Del Puente A, et al. Impaired bone metabolism in glycogen storage disease type 1 is associated with poor metabolic control in type 1a and with granulocyte colony-stimulating factor therapy in type 1b. Horm Res Paediatr. 2014;81(1):55–62. https://doi.org/10.1159/000351022.CrossRefPubMed

75.

Wong EM, Lehman A, Acott P, Gillis J, Metzger DL, Sirrs S. Hypogonadotropic hypogonadism in males with glycogen storage disease type 1. JIMD Rep. 2017;36:79–84. https://doi.org/10.1007/8904_2016_38.CrossRefPubMedPubMedCentral

76.

Minarich LA, Kirpich A, Fiske LM, Weinstein DA. Bone mineral density in glycogen storage disease type Ia and Ib. Genet Med. 2012;14:737–41. https://doi.org/10.1038/gim.2012.36.CrossRef

77.

Al Hafid N, Christodoulou J. Phenylketonuria: a review of current and future treatments. Transl Pediatr. 2015;4(4):304–17. https://doi.org/10.3978/j.issn.2224-4336.2015.10.07.CrossRefPubMedPubMedCentral

78.

Demirdas S, Coakley KE, Bisschop PH, Hollak CE, Bosch AM, Singh RH. Bone health in phenylketonuria: a systematic review and meta-analysis. Orphanet J Rare Dis. 2015;10:17. https://doi.org/10.1186/s13023-015-0232-y.CrossRefPubMedPubMedCentral

79.

Hansen KE, Ney D. A systematic review of bone mineral density and fractures in phenylketonuria. J Inherit Metab Dis. 2014;37(6):875–80. https://doi.org/10.1007/s10545-014-9735-2.CrossRefPubMedPubMedCentral

80.

Demirdas S, van Spronsen FJ, Hollak CEM, van der Lee JH, Bisschop PH, Vaz FM, et al. Micronutrients, essential fatty acids and bone health in phenylketonuria. Ann Nutr Metab. 2017;70(2):111–21. https://doi.org/10.1159/000465529.CrossRefPubMed

81.

Touati G, Valayannopoulos V, Mention K, de Lonlay P, Jouvet P, Depondt E, et al. Methylmalonic and propionic acidurias: management without or with a few supplements of specific amino acid mixture. J Inherit Metab Dis. 2006;29(2–3):288–98. https://doi.org/10.1007/s10545-006-0351-7.CrossRefPubMed

82.

Martin-Hernandez E, Lee PJ, Micciche A, Grunewald S, Lachmann RH. Long-term needs of adult patients with organic acidaemias: outcome and prognostic factors. J Inherit Metab Dis. 2009;32(4):523–33. https://doi.org/10.1007/s10545-009-1191-12.CrossRefPubMed

83.

Wilcox G, Strauss BJ, Francis DE, Upton H, Boneh A. Body composition in young adults with inborn errors of protein metabolism--a pilot study. J Inherit Metab Dis. 2005;28(5):613–26. https://doi.org/10.1007/s10545-005-0036-7.CrossRefPubMed

84.

Simell O, Perheentupa J, Rapola J, Visakorpi JK, Eskelin LE. Lysinuric protein intolerance. Am J Med. 1975;59(2):229–40.CrossRefPubMed

85.

Posey JE, Burrage LC, Miller MJ, Liu P, Hardison MT, Elsea SH, et al. Lysinuric protein intolerance presenting with multiple fractures. Mol Genet Metab Rep. 2014;1:176–83. https://doi.org/10.1016/j.ymgmr.2014.03.004.CrossRefPubMedPubMedCentral

86.

Carpenter TO, Levy HL, Holtrop ME, Shih VE, Anast CS. Lysinuric protein intolerance presenting as childhood osteoporosis. Clinical and skeletal response to citrulline therapy. N Engl J Med. 1985;312(5):290–4. https://doi.org/10.1056/NEJM198501313120506.CrossRefPubMed

87.

Parto K, Penttinen R, Paronen I, Pelliniemi L, Simell O. Osteoporosis in lysinuric protein intolerance. J Inherit Metab Dis. 1993;16(2):441–50.CrossRefPubMed

88.

Jennings A, MacGregor A, Spector T, Cassidy A. Amino acid intakes are associated with bone mineral density and prevalence of low bone mass in women: evidence from discordant monozygotic twins. J Bone Miner Res. 2016;31(2):326–35. https://doi.org/10.1002/jbmr.2703.CrossRefPubMed

89.

Sebastio G, Sperandeo MP, Andria G. Lysinuric protein intolerance: reviewing concepts on a multisystem disease. Am J Med Genet C: Semin Med Genet. 2011;157C(1):54–62. https://doi.org/10.1002/ajmg.c.30287.CrossRef

90.

Gomez L, Garcia-Cazorla A, Gutierrez A, Artuch R, Varea V, Martin J, et al. Treatment of severe osteoporosis with alendronate in a patient with lysinuric protein intolerance. J Inherit Metab Dis. 2006;29(5):687. https://doi.org/10.1007/s10545-006-0236-9.CrossRefPubMed

91.

Biewenga M, Matawlie RHS, Friesema ECH, Koole-Lesuis H, Langeveld M, Wilson JHP, et al. Osteoporosis in patients with erythropoietic protoporphyria. Br J Dermatol. 2017;177(6):1693–8. https://doi.org/10.1111/bjd.15893.CrossRefPubMed

92.

Allo G, del Carmen G-AM, Mendez M, De Salamanca RE, Martinez G, Hawkins F. Bone mineral density and vitamin D levels in erythropoietic protoporphyria. Endocrine. 2013;44(3):803–7. https://doi.org/10.1007/s12020-013-9934-x.CrossRefPubMed

93.

Weiss KH, Van de Moortele M, Gotthardt DN, Pfeiffenberger J, Seessle J, Ullrich E, et al. Bone demineralisation in a large cohort of Wilson disease patients. J Inherit Metab Dis. 2015;38(5):949–56. https://doi.org/10.1007/s10545-015-9815-y.CrossRefPubMed

94.

Quemeneur AS, Trocello JM, Ea HK, Ostertag A, Leyendecker A, Duclos-Vallee JC, et al. Bone status and fractures in 85 adults with Wilson's disease. Osteoporos Int. 2014;25(11):2573–80. https://doi.org/10.1007/s00198-014-2806-2.CrossRefPubMed

95.

Golding DN, Walshe JM. Arthropathy of Wilson's disease. Study of clinical and radiological features in 32 patients. Ann Rheum Dis. 1977;36(2):99–111.CrossRefPubMedPubMedCentral

96.

Quemeneur AS, Trocello JM, Ea HK, Woimant F, Liote F. Miscellaneous non-inflammatory musculoskeletal conditions. Musculoskeletal conditions associated with Wilson's disease. Best Pract Res Clin Rheumatol. 2011;25(5):627–36. https://doi.org/10.1016/j.berh.2011.10.021.CrossRefPubMed

97.

van Karnebeek CDM, Wortmann SB, Tarailo-Graovac M, Langeveld M, Ferreira CR, van de Kamp JM, et al. The role of the clinician in the multi-omics era: are you ready? J Inherit Metab Dis. 2018;41(3):571–82. https://doi.org/10.1007/s10545-017-0128-1.CrossRefPubMedPubMedCentral

98.

Williams N, Challoumas D, Ketteridge D, Cundy PJ, Eastwood DM. The mucopolysaccharidoses: advances in medical care lead to challenges in orthopaedic surgical care. Bone Joint J. 2017;99-B(9):1132–9. https://doi.org/10.1302/0301-620X.99B9.BJJ-2017-0487.CrossRefPubMed

99.

de Ruijter J, Maas M, Janssen A, Wijburg FA. High prevalence of femoral head necrosis in Mucopolysaccharidosis type III (Sanfilippo disease): a national, observational, cross-sectional study. Mol Genet Metab. 2013;109(1):49–53. https://doi.org/10.1016/j.ymgme.2013.03.004.CrossRefPubMed

100.

Cimaz R, Vijay S, Haase C, Coppa GV, Bruni S, Wraith E, et al. Attenuated type I mucopolysaccharidosis in the differential diagnosis of juvenile idiopathic arthritis: a series of 13 patients with Scheie syndrome. Clin Exp Rheumatol. 2006;24(2):196–202.

Title: Bone health in patients with inborn errors of metabolism
Publication date: 01-03-2018
Published in: Reviews in Endocrine and Metabolic Disorders / Issue 1/2018
Print ISSN: 1389-9155
Electronic ISSN: 1573-2606
DOI: https://doi.org/10.1007/s11154-018-9460-5

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