Osteoporosis of genetic origin: a literature review
Keywords:
osteoporosis, children, genes, metabolism, fracturesAbstract
Numerous cases of genetic (primary) osteoporosis are reported in the literature, thanks to the in-depth investigation of suspicious scenarios, where a child or young adult presents with bone fragility. Thorough diagnostic work up is required in order to exclude more frequent, treatable, secondary causes of osteoporosis (e.g. leukaemia or Crohn’s disease). When first line investigations exclude secondary osteoporosis and in the presence of specific clinical clues (e.g. blue sclerae, joint laxity) or of a suspicious family history of early onset osteoporosis, a genetic work up should be undertaken. There are many new genes implicated in the pathogenesis of primary osteoporosis, playing different roles in bone formation and/or resorption, depending on the metabolic bone path involved. The greater understanding of the complexity of bone metabolism opens new research roads for new, gene-specific treatments. Herein, the latest literature data on the osteoporosis of genetic origin are being presented. Emphasis is also given on the importance of lateral thinking, when it comes to children and young adults whose fracture history is remarkable and cannot be attributed solely to injury. Finally, the importance of not missing significant chronic disorders leading to osteoporosis is also highlighted.
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References
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2. Lewiecki EM, Gordon CM, Baim S et al. International society for clinical densitometry 2007 adult and pediatric official positions. Bone 2008; 43(6):1115–1121.
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6. Kralick AE, Zemel BS. Evolutionary perspectives on the developing skeleton and implications for lifelong health. Front Endocrinol (Lausanne). 2020; 11:99
7. Mäkitie O, Zillikens MC. Early-onset osteoporosis. Calc Tissue Int 2022; 110:546–561
8. Mortier GR, Cohn DH, Cormier-Daire V et al. Nosology and classification of genetic skeletal disorders: 2019 revision. Am J Med Genet A 2019; 179(12): 2393–419
9. van Dijk FS, Semler O, Etich J et al. Interaction between KDELR2 and HSP47 as a key determinant in osteogenesis imperfecta caused by bi-allelic variants in KDELR2. Am J Hum Genet 2020; 107(5):989-999
10. Marini JC, Forlino A, Bachinger HP et al. Osteogenesis imperfecta. Nature Rev Dis Primers 2017; 3: 17052
11. Forlino A, Marini JC. Osteogenesis imperfecta. Lancet 2016; 387(10028):1657–71
12. Folkestad L, Hald JD, Ersbøll AK et al. Fracture rates and fracture sites in patients with osteogenesis imperfecta: a nationwide register-based cohort study. J Bone Miner Res 2017; 32(1):125–34
13. El-Gazzar A, Högler W. Mechanisms of Bone Fragility: From Osteogenesis Imperfecta to Secondary Osteoporosis. Int J Mol Sci 2021; 22: 625
14. Warman, M.L, Cormier-Daire, V, Hall, C et al. Nosology and classification of genetic skeletal disorders: 2010 revision. Am J Med Genet A 2011; 155A: 943–968.
15. Roschger P, Jain A, Kol M et al. Osteoporosis and skeletal dysplasia caused by pathogenic variants in SGMS2. JCI Insight 2019; 4(7):e126180
16. Robinson ME, Bardai G, Veilleux LN et al. Musculoskeletal phenotype in two unrelated individuals with a recurrent nonsense variant in SGMS2. Bone 2020; 134:115261
17. Van Dijk FS, Zillikens MC, Micha D et al. PLS3 mutations in X-linked osteoporosis with fractures. N Engl J Med 2013; 369(16):1529–36
18. Laine CM, Wessman M, Toiviainen-Salo S et al. A novel splice mutation in PLS3 causes X-linked early onset low-turnover osteoporosis. J Bone Miner Res 2015;30(3):510–8
19. Makitie RE, Niinimaki T, Suo-Palosaari M et al.PLS3 mutations cause severe age and sex-related spinal pathology. Front Endocrinol (Lausanne) 2020; 23(11):393
20. Tanaka-Kamioka K, Kamioka H, Ris H et al. Osteocyte shape is dependent on actin filaments and osteocyte processes are unique actin-rich projections. J Bone Miner Res 1998; 13(10):1555–1568.
21. Makitie RE, Kampe A, Costantini A et al. Biomarkers in WNT1 and PLS3 osteoporosis: altered concentrations of DKK1 and FGF23. J Bone Miner Res 2020;35: 901–12
22. Westendorf JJ, Kahler RA, Schroeder TM. Wnt signaling in osteoblasts and bone diseases. Gene 2004; 341:19–39
23. Nampoothiri S, Guillemyn B, Elcioglu N et al. Ptosis as a unique hallmark for autosomal recessive WNT1-associated osteogenesis imperfecta. Am J Med Genet A 2019; 179(6):908–914.
24. Makitie RE, Haanpaa M, Valta H et al. Skeletal characteristics of WNT1 osteoporosis in children and young adults. J Bone Miner Res 2016; 31(9):1734–1742
25. Laine CM, Joeng KS, Campeau PM et al. WNT1 mutations in early-onset osteoporosis and osteogenesis imperfecta. N Engl J Med 2013;368(19):1809–16
26. Makitie RE, Kampe A, Costantini A et al. Biomarkers in WNT1 and PLS3 osteoporosis:altered concentrations of DKK1 and FGF23. J Bone Miner Res 2020; 35(5):901–912.
27. Sturznickel J, Rolvien T, Delsmann A et al. Clinical phenotype and relevance of LRP5 and LRP6 variants in patients with early-onset osteoporosis (EOOP). J Bone Miner Res 2021; 36(2):271–282
28. Hartikka H, Makitie O, Mannikko M et al. Heterozygous mutations in the LDL receptor related protein 5 (LRP5) gene are associated with primary osteoporosis in children. J Bone Miner Res 2005; 20 (5):783–9
29. Gong Y, Slee RB, Fukai N et al. Osteoporosis-Pseudoglioma Syndrome Collaborative Group. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 2001; 107(4):513–23
30. Campos-Obando N, Oei L, Hoefsloot LH et al. Osteoporotic vertebral fractures during pregnancy: be aware of a potential underlying genetic cause. J Clin Endocrinol Metab 2014; 99(4):1107–1111.
31. Saarinen A, Saukkonen T, Kivela Tet al. Low density lipoprotein receptor-related protein 5 (LRP5) mutations and osteoporosis, impaired glucose metabolism and hypercholesterolaemia. Clin Endocrinol (Oxf) 2010; 72(4):481–488
32. Foer D, Zhu M, Cardone RL et al. Impact of gain-of-function mutations in the low-density lipoprotein receptor-related protein 5 (LRP5) on glucose and lipid homeostasis. Osteoporos Int 2017; 28(6):2011–2017
33. Hilton MJ, Tu X, Wu X et al. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat Med 2008; 14: 306–314
34. Narumi Y, Min BJ, Shimizu K et al. Clinical consequences in truncating mutations in exon 34 of NOTCH2: Report of six patients with Hajdu-Cheney syndrome and a patient with serpentine fibula polycystic kidney syndrome. Am J Med Genet A 2013; 161A: 518–526
35. Sakka S, Gafni R.I, Davies J.H et al. Bone Structural Characteristics and Response to Bisphosphonate Treatment in Children With Hajdu-Cheney Syndrome. J Clin Endocrinol Metab 2017; 102: 4163–4172
36. Van Hul W, Boudin E, Vanhoenacker FM et al. Camurati-Engelmann Disease. Calcif Tissue Int 2019; 104: 554–560
37. Verstraeten A, Alaerts M, Van Laer L et al. Marfan Syndrome and Related Disorders: 25 Years of Gene Discovery. Hum Mutat 2016; 37: 524–531
38. Tan EW, Offoha RU, Oswald GL et al. Increased fracture risk and low bone mineral density in patients with Loeys-Dietz syndrome. Am J Med Genet A 2013; 161A:1910–1914.
39. Grafe I, Yang T, Alexander S et al. Excessive transforming growth factor-beta signaling is a common mechanism in osteogenesis imperfecta. Nat Med 2014; 20: 670–675
40. Manousaki D, Kampe A, Forgetta V et al. Increased burden of common risk alleles in children with a significant fracture history. J Bone Miner Res 2020; 35(5):875–882
41. Fahed AC, Wang M, Homburger JR et al. Polygenic background modifies penetrance of monogenic variants for tier 1 genomic conditions. Nat Commun 2020; 11(1):3635
42. Kyoung-Tae K , Young-Seok L, Inbo H. The Role of Epigenomics in Osteoporosis and Osteoporotic Vertebral Fracture. Int J Mol Sci 2020; 21: 9455
43. Rocha-Braz MGM, Franca MM, Fernandes AM et al.Comprehensive genetic analysis of 128 candidate genes in a cohort with idiopathic,severe, or familial osteoporosis. J Endocr Soc 2020; 4(12):148
44. Ciancia S , van Rijn RR, Högler W et al. Osteoporosis in children and adolescents: when to suspect and how to diagnose it. Eur J Ped 2022; 181:2549–2561
45. Costantini A, Mäkitie RE, Hartmann MA et al. Early-Onset Osteoporosis: Rare Monogenic Forms Elucidate the Complexity of Disease Pathogenesis Beyond Type I Collagen. JBMR 2022; 37(9):1623–1641.
46. Makitie RE, Niinimaki T, Nieminen MT et al. Impaired WNT signaling and the spine-heterozygous WNT1 mutation causes severe age-related spinal pathology. Bone 2017;101:3-9.
47. Faqeih E, Shaheen R, Alkuraya FS. WNT1 mutation with recessive osteogenesis imperfecta and profound neurological phenotype. J Med Genet 2013; 50(7):491-492
48. Pomeranz ES. Child Abuse and Conditions That Mimic It. Pediatr Clin North Am 2018; 65(6):1135-1150
49. Pandya NK, Baldwin K, Kamath AF et al. Unexplained fractures: child abuse or bone disease? A systematic review. Clin Orthop Relat Res 2011;469(3):805-12
50. van Rijn RR, Sieswerda-Hoogendoorn T. Educational paper: imaging child abuse: the bare bones. Eur J Pediatr 2012; 171(2):215-24
51. Xuan J, Yu Y, Qing T et al.Next-generation sequencing in the clinic: promises and challenges. Cancer Lett 2013;340(2):284-295
52. Peris P, Monegal A, Martinez MA et al. Bone mineral density evolution in young premenopausal women with idiopathic osteoporosis. Clin Rheumatol 2007; 26(6):958–961
53. Islam MZ, Shamim AA, Viljakainen HT et al. Effect of vitamin D, calcium and multiple micronutrient supplementation on vitamin D and bone status in Bangladeshi premenopausal garment factory workers with hypovitaminosis D: a double-blinded, randomised, placebo-controlled 1-year intervention. Br J Nutr 2010; 104(2):241–247
54. Mayranpaa MK, Viljakainen HT, Toiviainen-Salo S et al. Impaired bone health and asymptomatic vertebral compressions in fracture-prone children: a case-control study. J Bone Miner Res 2012; 27(6):1413–1424
55. Kobayashi T, Nakamura Y, Suzuki T et al. Efficacy and Safety of Denosumab Therapy for Osteogenesis Imperfecta Patients with Osteoporosis—Case Series. J Clin Med 2018;7(12):479
56. Sokal A, Elefant E, Leturcq T et al. Pregnancy and newborn outcomes after exposure to bisphosphonates: a case control study. Osteoporos Int 2019; 30(1):221–229
57. Langdahl BL. Osteoporosis in premenopausal women. Curr Opin Rheumatol 2017; 29(4):410–415
58. Sabir AH, Cole T. The evolving therapeutic landscape of genetic skeletal disorders. Orphanet J Rare Dis 2019; 14:300
59. Uday S, Gaston C.L, Rogers L et al. Osteonecrosis of the Jaw and Rebound Hypercalcemia in Young People Treated With Denosumab for Giant Cell Tumor of Bone. J Clin Endocrinol Metab 2018; 103: 596–603
60. Tsourdi E, Zillikens MC, Meier C et al. Fracture risk and management of discontinuation of denosumab therapy: a systematic review and position statement by ECTS. J Clin Endocrinol Metab 2020;26:756
61. Raulston S.Treatment of OI with PTH and Zoledronic acid 2018. https://ukctg.nihr.ac.uk/trials,trial number ISRCTN15313991
62. Van Bezooijen R.L, ten Dijke P., Papapoulos, S.E. et al. SOST/sclerostin, an osteocyte-derived negative regulator of bone formation. Cytokine Growth Factor Rev 2005; 16: 319–327
63. Tauer J.T, Robinson M.E, Rauch F. Osteogenesis Imperfecta: New Perspectives From Clinical and Translational Research. JBMR Plus 2019; 3: e10174
64. Gaudio A, Fiore V, Rapisarda R et al. Sclerostin is a possible candidate marker of arterial stiffness: Results from a cohort study in Catania. Mol Med Rep 2017; 15: 3420–3424.
65. Glorieux FH, Devogelaer JP, Durigova M et al. BPS804 anti-sclerostin antibody in adults with moderate osteogenesis imperfecta: results of a randomized phase 2a trial. J Bone Miner Res 2017; 32(7):1496–504
66. Wu M, Chen G, Li YP. TGF-β and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Res 2016;4:16009
67. Grafe I, Yang T, Alexander S et al. Excessive transforming growth factor-β signaling is a common mechanism in osteogenesis imperfecta. Nat Med 2014;20(6):670
68. Multicenter study to evaluate safety of fresolimumab treatment in adults with moderate to severe OI 2019 https://www. rarediseasesnetwork.org/cms/bbd/studies/7706
69. Mo C, Ke, J, Zhao D et al. Role of the renin-angiotensin-aldosterone system in bone metabolism. J Bone Miner Metab 2020; 38: 772–779
70. Ayyavoo A, Derraik JG, Cutfield WS et al. Elimination of pain and improvement of exercise capacity in Camurati-Engelmann disease with losartan. J Clin Endocrinol Metab 2014; 99: 3978–3982.
71. Yang Y, Yujiao W, Fang W et al. The roles of miRNA, lncRNA and circRNA in the development of osteoporosis. Biol Res 2020; 53:40
72. Gallo A; Tandon M, Alevizos I et al. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS ONE 2012; 7: e30679
73. Zhou Q, Li M, Wang X et al. X. Immune-related MicroRNAs are Abundant in Breast Milk Exosomes. Int J Biol Sci 2011; 8: 118–123
74. Le Blanc K, Gotherstrom C, Ringden O, et al. Fetal mesenchymal stem-cell engraftment in bone after in uterotransplantation in a patient with severe osteogenesis imperfecta. Transplantation 2005;79(11):1607–14
75. Crouzin-Frankel J. The savior cells? Science 2016; 352(6283):284–7
76. Chevrel G, Cimaz R. Osteogenesis imperfecta: new treatment options. Curr Rheumatol Rep 2006;8(6):474–92. 77. Shapiro JR, Rowe DW. Genetic approach to treatment of osteogenesis imperfecta in Osteogenesis imperfecta. 1st ed. London: Elsevier Science and Technology; 2013
2. Lewiecki EM, Gordon CM, Baim S et al. International society for clinical densitometry 2007 adult and pediatric official positions. Bone 2008; 43(6):1115–1121.
3. Makras P., Anastasilakis AD, Antypas G et al. The 2018 Guidelines for the diagnosis and treatment of osteoporosis in Greece. Arch Osteopor 2019;14:39
4. Ferrari S, Bianchi ML, Eisman JA et al.IOF Committee of Scientific Advisors Working Group on Osteoporosis Pathophysiology. Osteoporosis in young adults: pathophysiology, diagnosis, and management. Osteoporos Int 2012; 23(12):2735–48.
5. Hernandez CJ, Beaupre GS, Carter DR. A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporos Int. 2003;14(10):843–7.
6. Kralick AE, Zemel BS. Evolutionary perspectives on the developing skeleton and implications for lifelong health. Front Endocrinol (Lausanne). 2020; 11:99
7. Mäkitie O, Zillikens MC. Early-onset osteoporosis. Calc Tissue Int 2022; 110:546–561
8. Mortier GR, Cohn DH, Cormier-Daire V et al. Nosology and classification of genetic skeletal disorders: 2019 revision. Am J Med Genet A 2019; 179(12): 2393–419
9. van Dijk FS, Semler O, Etich J et al. Interaction between KDELR2 and HSP47 as a key determinant in osteogenesis imperfecta caused by bi-allelic variants in KDELR2. Am J Hum Genet 2020; 107(5):989-999
10. Marini JC, Forlino A, Bachinger HP et al. Osteogenesis imperfecta. Nature Rev Dis Primers 2017; 3: 17052
11. Forlino A, Marini JC. Osteogenesis imperfecta. Lancet 2016; 387(10028):1657–71
12. Folkestad L, Hald JD, Ersbøll AK et al. Fracture rates and fracture sites in patients with osteogenesis imperfecta: a nationwide register-based cohort study. J Bone Miner Res 2017; 32(1):125–34
13. El-Gazzar A, Högler W. Mechanisms of Bone Fragility: From Osteogenesis Imperfecta to Secondary Osteoporosis. Int J Mol Sci 2021; 22: 625
14. Warman, M.L, Cormier-Daire, V, Hall, C et al. Nosology and classification of genetic skeletal disorders: 2010 revision. Am J Med Genet A 2011; 155A: 943–968.
15. Roschger P, Jain A, Kol M et al. Osteoporosis and skeletal dysplasia caused by pathogenic variants in SGMS2. JCI Insight 2019; 4(7):e126180
16. Robinson ME, Bardai G, Veilleux LN et al. Musculoskeletal phenotype in two unrelated individuals with a recurrent nonsense variant in SGMS2. Bone 2020; 134:115261
17. Van Dijk FS, Zillikens MC, Micha D et al. PLS3 mutations in X-linked osteoporosis with fractures. N Engl J Med 2013; 369(16):1529–36
18. Laine CM, Wessman M, Toiviainen-Salo S et al. A novel splice mutation in PLS3 causes X-linked early onset low-turnover osteoporosis. J Bone Miner Res 2015;30(3):510–8
19. Makitie RE, Niinimaki T, Suo-Palosaari M et al.PLS3 mutations cause severe age and sex-related spinal pathology. Front Endocrinol (Lausanne) 2020; 23(11):393
20. Tanaka-Kamioka K, Kamioka H, Ris H et al. Osteocyte shape is dependent on actin filaments and osteocyte processes are unique actin-rich projections. J Bone Miner Res 1998; 13(10):1555–1568.
21. Makitie RE, Kampe A, Costantini A et al. Biomarkers in WNT1 and PLS3 osteoporosis: altered concentrations of DKK1 and FGF23. J Bone Miner Res 2020;35: 901–12
22. Westendorf JJ, Kahler RA, Schroeder TM. Wnt signaling in osteoblasts and bone diseases. Gene 2004; 341:19–39
23. Nampoothiri S, Guillemyn B, Elcioglu N et al. Ptosis as a unique hallmark for autosomal recessive WNT1-associated osteogenesis imperfecta. Am J Med Genet A 2019; 179(6):908–914.
24. Makitie RE, Haanpaa M, Valta H et al. Skeletal characteristics of WNT1 osteoporosis in children and young adults. J Bone Miner Res 2016; 31(9):1734–1742
25. Laine CM, Joeng KS, Campeau PM et al. WNT1 mutations in early-onset osteoporosis and osteogenesis imperfecta. N Engl J Med 2013;368(19):1809–16
26. Makitie RE, Kampe A, Costantini A et al. Biomarkers in WNT1 and PLS3 osteoporosis:altered concentrations of DKK1 and FGF23. J Bone Miner Res 2020; 35(5):901–912.
27. Sturznickel J, Rolvien T, Delsmann A et al. Clinical phenotype and relevance of LRP5 and LRP6 variants in patients with early-onset osteoporosis (EOOP). J Bone Miner Res 2021; 36(2):271–282
28. Hartikka H, Makitie O, Mannikko M et al. Heterozygous mutations in the LDL receptor related protein 5 (LRP5) gene are associated with primary osteoporosis in children. J Bone Miner Res 2005; 20 (5):783–9
29. Gong Y, Slee RB, Fukai N et al. Osteoporosis-Pseudoglioma Syndrome Collaborative Group. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 2001; 107(4):513–23
30. Campos-Obando N, Oei L, Hoefsloot LH et al. Osteoporotic vertebral fractures during pregnancy: be aware of a potential underlying genetic cause. J Clin Endocrinol Metab 2014; 99(4):1107–1111.
31. Saarinen A, Saukkonen T, Kivela Tet al. Low density lipoprotein receptor-related protein 5 (LRP5) mutations and osteoporosis, impaired glucose metabolism and hypercholesterolaemia. Clin Endocrinol (Oxf) 2010; 72(4):481–488
32. Foer D, Zhu M, Cardone RL et al. Impact of gain-of-function mutations in the low-density lipoprotein receptor-related protein 5 (LRP5) on glucose and lipid homeostasis. Osteoporos Int 2017; 28(6):2011–2017
33. Hilton MJ, Tu X, Wu X et al. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat Med 2008; 14: 306–314
34. Narumi Y, Min BJ, Shimizu K et al. Clinical consequences in truncating mutations in exon 34 of NOTCH2: Report of six patients with Hajdu-Cheney syndrome and a patient with serpentine fibula polycystic kidney syndrome. Am J Med Genet A 2013; 161A: 518–526
35. Sakka S, Gafni R.I, Davies J.H et al. Bone Structural Characteristics and Response to Bisphosphonate Treatment in Children With Hajdu-Cheney Syndrome. J Clin Endocrinol Metab 2017; 102: 4163–4172
36. Van Hul W, Boudin E, Vanhoenacker FM et al. Camurati-Engelmann Disease. Calcif Tissue Int 2019; 104: 554–560
37. Verstraeten A, Alaerts M, Van Laer L et al. Marfan Syndrome and Related Disorders: 25 Years of Gene Discovery. Hum Mutat 2016; 37: 524–531
38. Tan EW, Offoha RU, Oswald GL et al. Increased fracture risk and low bone mineral density in patients with Loeys-Dietz syndrome. Am J Med Genet A 2013; 161A:1910–1914.
39. Grafe I, Yang T, Alexander S et al. Excessive transforming growth factor-beta signaling is a common mechanism in osteogenesis imperfecta. Nat Med 2014; 20: 670–675
40. Manousaki D, Kampe A, Forgetta V et al. Increased burden of common risk alleles in children with a significant fracture history. J Bone Miner Res 2020; 35(5):875–882
41. Fahed AC, Wang M, Homburger JR et al. Polygenic background modifies penetrance of monogenic variants for tier 1 genomic conditions. Nat Commun 2020; 11(1):3635
42. Kyoung-Tae K , Young-Seok L, Inbo H. The Role of Epigenomics in Osteoporosis and Osteoporotic Vertebral Fracture. Int J Mol Sci 2020; 21: 9455
43. Rocha-Braz MGM, Franca MM, Fernandes AM et al.Comprehensive genetic analysis of 128 candidate genes in a cohort with idiopathic,severe, or familial osteoporosis. J Endocr Soc 2020; 4(12):148
44. Ciancia S , van Rijn RR, Högler W et al. Osteoporosis in children and adolescents: when to suspect and how to diagnose it. Eur J Ped 2022; 181:2549–2561
45. Costantini A, Mäkitie RE, Hartmann MA et al. Early-Onset Osteoporosis: Rare Monogenic Forms Elucidate the Complexity of Disease Pathogenesis Beyond Type I Collagen. JBMR 2022; 37(9):1623–1641.
46. Makitie RE, Niinimaki T, Nieminen MT et al. Impaired WNT signaling and the spine-heterozygous WNT1 mutation causes severe age-related spinal pathology. Bone 2017;101:3-9.
47. Faqeih E, Shaheen R, Alkuraya FS. WNT1 mutation with recessive osteogenesis imperfecta and profound neurological phenotype. J Med Genet 2013; 50(7):491-492
48. Pomeranz ES. Child Abuse and Conditions That Mimic It. Pediatr Clin North Am 2018; 65(6):1135-1150
49. Pandya NK, Baldwin K, Kamath AF et al. Unexplained fractures: child abuse or bone disease? A systematic review. Clin Orthop Relat Res 2011;469(3):805-12
50. van Rijn RR, Sieswerda-Hoogendoorn T. Educational paper: imaging child abuse: the bare bones. Eur J Pediatr 2012; 171(2):215-24
51. Xuan J, Yu Y, Qing T et al.Next-generation sequencing in the clinic: promises and challenges. Cancer Lett 2013;340(2):284-295
52. Peris P, Monegal A, Martinez MA et al. Bone mineral density evolution in young premenopausal women with idiopathic osteoporosis. Clin Rheumatol 2007; 26(6):958–961
53. Islam MZ, Shamim AA, Viljakainen HT et al. Effect of vitamin D, calcium and multiple micronutrient supplementation on vitamin D and bone status in Bangladeshi premenopausal garment factory workers with hypovitaminosis D: a double-blinded, randomised, placebo-controlled 1-year intervention. Br J Nutr 2010; 104(2):241–247
54. Mayranpaa MK, Viljakainen HT, Toiviainen-Salo S et al. Impaired bone health and asymptomatic vertebral compressions in fracture-prone children: a case-control study. J Bone Miner Res 2012; 27(6):1413–1424
55. Kobayashi T, Nakamura Y, Suzuki T et al. Efficacy and Safety of Denosumab Therapy for Osteogenesis Imperfecta Patients with Osteoporosis—Case Series. J Clin Med 2018;7(12):479
56. Sokal A, Elefant E, Leturcq T et al. Pregnancy and newborn outcomes after exposure to bisphosphonates: a case control study. Osteoporos Int 2019; 30(1):221–229
57. Langdahl BL. Osteoporosis in premenopausal women. Curr Opin Rheumatol 2017; 29(4):410–415
58. Sabir AH, Cole T. The evolving therapeutic landscape of genetic skeletal disorders. Orphanet J Rare Dis 2019; 14:300
59. Uday S, Gaston C.L, Rogers L et al. Osteonecrosis of the Jaw and Rebound Hypercalcemia in Young People Treated With Denosumab for Giant Cell Tumor of Bone. J Clin Endocrinol Metab 2018; 103: 596–603
60. Tsourdi E, Zillikens MC, Meier C et al. Fracture risk and management of discontinuation of denosumab therapy: a systematic review and position statement by ECTS. J Clin Endocrinol Metab 2020;26:756
61. Raulston S.Treatment of OI with PTH and Zoledronic acid 2018. https://ukctg.nihr.ac.uk/trials,trial number ISRCTN15313991
62. Van Bezooijen R.L, ten Dijke P., Papapoulos, S.E. et al. SOST/sclerostin, an osteocyte-derived negative regulator of bone formation. Cytokine Growth Factor Rev 2005; 16: 319–327
63. Tauer J.T, Robinson M.E, Rauch F. Osteogenesis Imperfecta: New Perspectives From Clinical and Translational Research. JBMR Plus 2019; 3: e10174
64. Gaudio A, Fiore V, Rapisarda R et al. Sclerostin is a possible candidate marker of arterial stiffness: Results from a cohort study in Catania. Mol Med Rep 2017; 15: 3420–3424.
65. Glorieux FH, Devogelaer JP, Durigova M et al. BPS804 anti-sclerostin antibody in adults with moderate osteogenesis imperfecta: results of a randomized phase 2a trial. J Bone Miner Res 2017; 32(7):1496–504
66. Wu M, Chen G, Li YP. TGF-β and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Res 2016;4:16009
67. Grafe I, Yang T, Alexander S et al. Excessive transforming growth factor-β signaling is a common mechanism in osteogenesis imperfecta. Nat Med 2014;20(6):670
68. Multicenter study to evaluate safety of fresolimumab treatment in adults with moderate to severe OI 2019 https://www. rarediseasesnetwork.org/cms/bbd/studies/7706
69. Mo C, Ke, J, Zhao D et al. Role of the renin-angiotensin-aldosterone system in bone metabolism. J Bone Miner Metab 2020; 38: 772–779
70. Ayyavoo A, Derraik JG, Cutfield WS et al. Elimination of pain and improvement of exercise capacity in Camurati-Engelmann disease with losartan. J Clin Endocrinol Metab 2014; 99: 3978–3982.
71. Yang Y, Yujiao W, Fang W et al. The roles of miRNA, lncRNA and circRNA in the development of osteoporosis. Biol Res 2020; 53:40
72. Gallo A; Tandon M, Alevizos I et al. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS ONE 2012; 7: e30679
73. Zhou Q, Li M, Wang X et al. X. Immune-related MicroRNAs are Abundant in Breast Milk Exosomes. Int J Biol Sci 2011; 8: 118–123
74. Le Blanc K, Gotherstrom C, Ringden O, et al. Fetal mesenchymal stem-cell engraftment in bone after in uterotransplantation in a patient with severe osteogenesis imperfecta. Transplantation 2005;79(11):1607–14
75. Crouzin-Frankel J. The savior cells? Science 2016; 352(6283):284–7
76. Chevrel G, Cimaz R. Osteogenesis imperfecta: new treatment options. Curr Rheumatol Rep 2006;8(6):474–92. 77. Shapiro JR, Rowe DW. Genetic approach to treatment of osteogenesis imperfecta in Osteogenesis imperfecta. 1st ed. London: Elsevier Science and Technology; 2013
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