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Complicated Muscle-Bone Interactions in Children with Cerebral Palsy

  • Muscle and Bone (L. Bonewald and M. Hamrick, Section Editors)
  • Published:
Current Osteoporosis Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

The goal of this review is to highlight the deficits in muscle and bone in children with cerebral palsy (CP), discuss the muscle-bone relationship in the CP population, and identify muscle-based intervention strategies that may stimulate an improvement in their bone development.

Recent Findings

The latest research suggests that muscle and bone are both severely underdeveloped and weak in children with CP, even in ambulatory children with mild forms of the disorder. The small and low-performing muscles and limited participation in physical activity are likely the major contributors to the poor bone development in children with CP. However, the muscle-bone relationship may be complicated by other factors, such as a high degree of fat and collagen infiltration of muscle, atypical muscle activation, and muscle spasticity. Muscle-based interventions, such as resistance training, vibration, and nutritional supplementation, have the potential to improve bone development in children with CP, especially if they are initiated before puberty.

Summary

Studies are needed to identify the muscle-related factors with the greatest influence on bone development in children with CP. Identifying treatment strategies that capitalize on the relationship between muscle and bone, while also improving balance, coordination, and physical activity participation, is an important step toward increasing bone strength and minimizing fractures in children with CP.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006;84(3):475–82.

    CAS  PubMed  Google Scholar 

  2. DeFronzo RA, Gunnarsson R, Bjorkman O, Olsson M, Wahren J. Effects of insulin on peripheral and splanchnic glucose metabolism in noninsulin-dependent (type II) diabetes mellitus. J Clin Invest. 1985;76(1):149–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Civitelli R, Ziambaras K. Calcium and phosphate homeostasis: concerted interplay of new regulators. J Endocrinol Investig. 2011;34(7 Suppl):3–7.

    CAS  Google Scholar 

  4. Kirby RS, Wingate MS, Van Naarden BK, Doernberg NS, Arneson CL, Benedict RE, et al. Prevalence and functioning of children with cerebral palsy in four areas of the United States in 2006: a report from the autism and developmental disabilities monitoring network. Res Dev Disabil. 2011;32(2):462–9.

    PubMed  Google Scholar 

  5. Graham HK, Rosenbaum P, Paneth N, Dan B, Lin JP, Damiano DL, et al. Cerebral palsy. Nat Rev Dis Primers. 2016;2.

  6. Himmelmann K, Horber V, De La Cruz J, Horridge K, Mejaski-Bosnjak V, Hollody K, et al. MRI classification system (MRICS) for children with cerebral palsy: development, reliability, and recommendations. Dev Med Child Neurol. 2017;59(1):57–64.

    PubMed  Google Scholar 

  7. Moreno-De-Luca A, Ledbetter DH, Martin CL. Genetic insights into the causes and classification of the cerebral palsies. Lancet Neurol. 2012;11(3):283–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Schaefer GB. Genetics considerations in cerebral palsy. Semin Pediatr Neurol. 2008;15(1):21–6.

    PubMed  Google Scholar 

  9. MacLennan AH, Thompson SC, Gecz J. Cerebral palsy: causes, pathways, and the role of genetic variants. Am J Obstet Gynecol. 2015;213(6):779–88.

    PubMed  Google Scholar 

  10. Wood E, Rosenbaum P. The gross motor function classification system for cerebral palsy: a study of reliability and stability over time. Dev Med Child Neurol. 2000;42(5):292–6.

    CAS  PubMed  Google Scholar 

  11. Elder GCB, Kirk J, Stewart G, Cook K, Weir D, Marshall A, et al. Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol. 2003;45(8):542–50.

    PubMed  Google Scholar 

  12. Stackhouse SK, Binder-Macleod SA, Lee SCK. Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve. 2005;31(5):594–601.

    PubMed  PubMed Central  Google Scholar 

  13. Wiley ME, Damiano DL. Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol. 1998;40(2):100–7.

    CAS  PubMed  Google Scholar 

  14. Damiano DL, Martellotta TL, Quinlivan JM, Abel MF. Deficits in eccentric versus concentric torque in children with spastic cerebral palsy. Med Sci Sports Exerc. 2001;33(1):117–22.

    CAS  PubMed  Google Scholar 

  15. Davids JR, Oeffinger DJ, Bagley AM, Sison-Williamson M, Gorton G. Relationship of strength, weight, age, and function in ambulatory children with cerebral palsy. J Pediatr Orthop. 2015;35(5):523–9.

    PubMed  Google Scholar 

  16. Moreau NG, Holthaus K, Marlow N. Differential adaptations of muscle architecture to high-velocity versus traditional strength training in cerebral palsy. Neurorehabil Neural Repair. 2013;27(4):325–34.

    PubMed  Google Scholar 

  17. Moreau NG, Falvo MJ, Damiano DL. Rapid force generation is impaired in cerebral palsy and is related to decreased muscle size and functional mobility. Gait Posture. 2012;35(1):154–8.

    PubMed  Google Scholar 

  18. Fry NR, Gough M, McNee AE, Shortland AP. Changes in the volume and length of the medial gastrocnemius after surgical recession in children with spastic diplegic cerebral palsy. J Pediatr Orthop. 2007;27(7):769–74.

    PubMed  Google Scholar 

  19. Malaiya R, McNee AE, Fry NR, Eve LC, Gough M, Shortland AP. The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy. J Electromyogr Kinesiol. 2007;17(6):657–63.

    PubMed  Google Scholar 

  20. Johnson DL, Miller F, Subramanian P, Modlesky CM. Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr. 2009;154(5):715–20.

    PubMed  Google Scholar 

  21. Modlesky CM, Cavaiola ML, Smith JJ, Rowe DA, Johnson DL, Miller F. A DXA-based mathematical model predicts midthigh muscle mass from magnetic resonance imaging in typically developing children but not in those with quadriplegic cerebral palsy. J Nutr. 2010;140(12):2260–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. • Whitney DG, Singh H, Miller F, Barbe MF, Slade JM, Pohlig RT, et al. Cortical bone deficit and fat infiltration of bone marrow and skeletal muscle in ambulatory children with mild spastic cerebral palsy. Bone. 2017;94:90–7 This study showed that the defict in bone architecture previously shown in nonambulatory children with severe CP is also present in ambulatory children with mild CP. The study also showed an infiltration of fat within the muscle and bone marrow of children wth CP.

    PubMed  Google Scholar 

  23. Noble JJ, Charles-Edwards GD, Keevil SF, Lewis AP, Gough M, Shortland AP. Intramuscular fat in ambulant young adults with bilateral spastic cerebral palsy. BMC Musculoskelet Disord. 2014;15(1):236.

    PubMed  PubMed Central  Google Scholar 

  24. Booth CM, Cortina-Borja MJ, Theologis TN. Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol. 2001;43(5):314–20.

    CAS  PubMed  Google Scholar 

  25. Brouwer B, Wheeldon RK, Stradiotto-Parker N, Allum J. Reflex excitability and isometric force production in cerebral palsy: the effect of serial casting. Dev Med Child Neurol. 1998;40(3):168–75.

    CAS  PubMed  Google Scholar 

  26. Barber L, Hastings-Ison T, Baker R, Barrett R, Lichtwark G. Medial gastrocnemius muscle volume and fascicle length in children aged 2 to 5 years with cerebral palsy. Dev Med Child Neurol. 2011;53(6):543–8.

    PubMed  Google Scholar 

  27. Kruse A, Schranz C, Tilp M, Svehlik M. Muscle and tendon morphology alterations in children and adolescents with mild forms of spastic cerebral palsy. BMC Pediatr. 2018;18(1):156.

    PubMed  PubMed Central  Google Scholar 

  28. Lampe R, Grassl S, Mitternacht J, Gerdesmeyer L, Gradinger R. MRT-measurements of muscle volumes of the lower extremities of youths with spastic hemiplegia caused by cerebral palsy. Brain Dev. 2006;28(8):500–6.

    PubMed  Google Scholar 

  29. Riad J, Modlesky CM, Gutierrez-Farewik EM, Brostrom E. Are muscle volume differences related to concentric muscle work during walking in spastic hemiplegic cerebral palsy? Clin Orthop Relat Res. 2012;470(5):1278–85.

    PubMed  Google Scholar 

  30. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture of the medial gastrocnemius in children with spastic diplegia. Dev Med Child Neurol. 2002;44(3):158–63.

    PubMed  Google Scholar 

  31. Shortland AP, Fry NR, Eve LC, Gough M. Changes to medial gastrocnemius architecture after surgical intervention in spastic diplegia. Dev Med Child Neurol. 2004;46(10):667–73.

    PubMed  Google Scholar 

  32. Hamrick MW, McGee-Lawrence ME, Frechette DM. Fatty infiltration of skeletal muscle: mechanisms and comparisons with bone marrow adiposity. Front Endocrinol (Lausanne). 2016;7:69.

    Google Scholar 

  33. Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr. 2000;71(4):885–92.

    CAS  PubMed  Google Scholar 

  34. Miljkovic I, Kuipers AL, Cauley JA, Prasad T, Lee CG, Ensrud KE, et al. Greater skeletal muscle fat infiltration is associated with higher all-cause and cardiovascular mortality in older men. J Gerontol A Biol Sci Med Sci. 2015;70(9):1133–40.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB, et al. Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study. J Bone Miner Res. 2010;25(3):513–9.

    PubMed  Google Scholar 

  36. Marciniak C, Li X, Zhou P. An examination of motor unit number index in adults with cerebral palsy. J Electromyogr Kinesiol. 2015;25(3):444–50.

    PubMed  Google Scholar 

  37. Mockford M, Caulton JM. The pathophysiological basis of weakness in children with cerebral palsy. Pediatr Phys Ther. 2010;22(2):222–33.

    PubMed  Google Scholar 

  38. Theroux MC, Akins RE, Barone C, Boyce B, Miller F, Dabney KW. Neuromuscular junctions in cerebral palsy: presence of extrajunctional acetylcholine receptors. Anesthesiology. 2002;96(2):330–5.

    CAS  PubMed  Google Scholar 

  39. Novak I. Evidence-based diagnosis, health care, and rehabilitation for children with cerebral palsy. J Child Neurol. 2014;29(8):1141–56.

    PubMed  Google Scholar 

  40. Ross SA, Engsberg JR. Relationships between spasticity, strength, gait, and the GMFM-66 in persons with spastic diplegia cerebral palsy. Arch Phys Med Rehabil. 2007;88(9):1114–20.

    PubMed  Google Scholar 

  41. Morrell DS, Pearson JM, Sauser DD. Progressive bone and joint abnormalities of the spine and lower extremities in cerebral palsy. Radiographics. 2002;22(2):257–68.

    PubMed  Google Scholar 

  42. Smith LR, Chambers HG, Lieber RL. Reduced satellite cell population may lead to contractures in children with cerebral palsy. Dev Med Child Neurol. 2013;55(3):264–70.

    PubMed  Google Scholar 

  43. Smith LR, Lee KS, Ward SR, Chambers HG, Lieber RL. Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length. J Physiol. 2011;589(10):2625–39.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Presedo A, Dabney KW, Miller F. Fractures in patients with cerebral palsy. J Pediatr Orthop. 2007;27(2):147–53.

    PubMed  Google Scholar 

  45. Worlock P, Stower M. Fracture patterns in Nottingham children. J Pediatr Orthop. 1986;6(6):656–60.

    CAS  PubMed  Google Scholar 

  46. Binkley T, Johnson J, Vogel L, Kecskemethy H, Henderson R, Specker B. Bone measurements by peripheral quantitative computed tomography (pQCT) in children with cerebral palsy. J Pediatr. 2005;147(6):791–6.

    PubMed  Google Scholar 

  47. Modlesky CM, Kanoff SA, Johnson DL, Subramanian P, Miller F. Evaluation of the femoral midshaft in children with cerebral palsy using magnetic resonance imaging. Osteoporos Int. 2009;20(4):609–15.

    CAS  PubMed  Google Scholar 

  48. Modlesky CM, Subramanian P, Miller F. Underdeveloped trabecular bone microarchitecture is detected in children with cerebral palsy using high-resolution magnetic resonance imaging. Osteoporos Int. 2008;19(2):169–76.

    CAS  PubMed  Google Scholar 

  49. Modlesky CM, Whitney DG, Singh H, Barbe MF, Kirby JT, Miller F. Underdevelopment of trabecular bone microarchitecture in the distal femur of nonambulatory children with cerebral palsy becomes more pronounced with distance from the growth plate. Osteoporos Int. 2015;26(2):505–12.

    CAS  PubMed  Google Scholar 

  50. Henderson RC, Lark RK, Gurka MJ, Worley G, Fung EB, Conaway M, et al. Bone density and metabolism in children and adolescents with moderate to severe cerebral palsy. Pediatrics. 2002;110(1).

    PubMed  Google Scholar 

  51. Shaw NJ, White CP, Fraser WD, Rosenbloom L. Osteopenia in cerebral palsy. Arch Dis Child. 1994;71(3):235–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Krick J, MurphyMiller P, Zeger S, Wright E. Pattern of growth in children with cerebral palsy. J Am Diet Assoc. 1996;96(7):680–5.

    CAS  PubMed  Google Scholar 

  53. Luu YK, Capilla E, Rosen CJ, Gilsanz V, Pessin JE, Judex S, et al. Mechanical stimulation of mesenchymal stem cell proliferation and differentiation promotes osteogenesis while preventing dietary-induced obesity. J Bone Miner Res. 2009;24(1):50–61.

    CAS  PubMed  Google Scholar 

  54. Rantalainen T, Nikander R, Heinonen A, Cervinka T, Sievanen H, Daly RM. Differential effects of exercise on tibial shaft marrow density in young female athletes. J Clin Endocrinol Metab. 2013;98(5):2037–44.

    CAS  PubMed  Google Scholar 

  55. Meunier P, Aaron J, Edouard C, Vignon G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res. 1971;80:147–54.

    CAS  PubMed  Google Scholar 

  56. Minaire P, Edouard C, Arlot M, Meunier PJ. Marrow changes in paraplegic patients. Calcif Tissue Int. 1984;36(3):338–40.

    CAS  PubMed  Google Scholar 

  57. Martin RB, Zissimos SL. Relationships between marrow fat and bone turnover in ovariectomized and intact rats. Bone. 1991;12(2):123–31.

    CAS  PubMed  Google Scholar 

  58. Jilka RL, Weinstein RS, Takahashi K, Parfitt AM, Manolagas SC. Linkage of decreased bone mass with impaired osteoblastogenesis in a murine model of accelerated senescence. J Clin Invest. 1996;97(7):1732–40.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Beresford JN, Bennett JH, Devlin C, Leboy PS, Owen ME. Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci. 1992;102(Pt 2):341–51.

    CAS  PubMed  Google Scholar 

  60. Di Iorgi N, Mo AO, Grimm K, Wren TA, Dorey F, Gilsanz V. Bone acquisition in healthy young females is reciprocally related to marrow adiposity. J Clin Endocrinol Metab. 2010;95(6):2977–82.

    PubMed  PubMed Central  Google Scholar 

  61. Wren TA, Chung SA, Dorey FJ, Bluml S, Adams GB, Gilsanz V. Bone marrow fat is inversely related to cortical bone in young and old subjects. J Clin Endocrinol Metab. 2011;96(3):782–6.

    CAS  PubMed  Google Scholar 

  62. Shen W, Velasquez G, Chen J, Jin Y, Heymsfield SB, Gallagher D, et al. Comparison of the relationship between bone marrow adipose tissue and volumetric bone mineral density in children and adults. J Clin Densitom. 2014;17(1):163–9.

    PubMed  Google Scholar 

  63. Huovinen V, Saunavaara V, Kiviranta R, Tarkia M, Honka H, Stark C, et al. Vertebral bone marrow glucose uptake is inversely associated with bone marrow fat in diabetic and healthy pigs: [(18)F]FDG-PET and MRI study. Bone. 2014;61:33–8.

    CAS  PubMed  Google Scholar 

  64. Slade JM, Coe LM, Meyer RA, McCabe LR. Human bone marrow adiposity is linked with serum lipid levels not T1-diabetes. J Diabetes Complicat. 2012;26(1):1–9.

    PubMed  Google Scholar 

  65. Baum T, Yap SP, Karampinos DC, Nardo L, Kuo D, Burghardt AJ, et al. Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine bone mineral density, and blood biomarkers in women with type 2 diabetes mellitus? J Magn Reson Imaging. 2012;35(1):117–24.

    PubMed  Google Scholar 

  66. Sharir A, Stern T, Rot C, Shahar R, Zelzer E. Muscle force regulates bone shaping for optimal load-bearing capacity during embryogenesis. Development. 2011;138(15):3247–59.

    CAS  PubMed  Google Scholar 

  67. Braun T, Gautel M. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev Mol Cell Biol. 2011;12(6):349–61.

    CAS  PubMed  Google Scholar 

  68. Bajaj D, Allerton BM, Kirby JT, Miller F, Rowe DA, Pohlig RT, et al. Muscle volume is related to trabecular and cortical bone architecture in typically developing children. Bone. 2015;81:217–27.

    PubMed  PubMed Central  Google Scholar 

  69. Leonard MB, Elmi A, Mostoufi-Moab S, Shults J, Burnham JM, Thayu M, et al. Effects of sex, race, and puberty on cortical bone and the functional muscle bone unit in children, adolescents, and young adults. J Clin Endocrinol Metab. 2010;95(4):1681–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Wolff J. Das gesetz der transformation der knochen. A Hirshwald. 1892;1:1–152.

    Google Scholar 

  71. Frost HM. Bone “mass” and the “mechanostat”: a proposal. Anat Rec. 1987;219:1–9.

    CAS  PubMed  Google Scholar 

  72. Robling AG. Is bone’s response to mechanical signals dominated by muscle forces? Med Sci Sports Exerc. 2009;41(11):2044–9.

    PubMed  PubMed Central  Google Scholar 

  73. O’Connor JA, Lanyon LE. The influence of strain rate on adaptive bone remodelling. J Biomech. 1982;15:767–81.

    PubMed  Google Scholar 

  74. Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg. 1984;66-A(3):397–402.

    Google Scholar 

  75. Otter MW, Cochran GV. Comments on ‘fluid movement in bone: theoretical and empirical’ [letter; comment]. J Biomech. 1992;25(12):1495.

    CAS  PubMed  Google Scholar 

  76. Nashner LM, Shumway-Cook A, Marin O. Stance posture control in select groups of children with cerebral palsy: deficits in sensory organization and muscular coordination. Exp Brain Res. 1983;49(3):393–409.

    CAS  PubMed  Google Scholar 

  77. Donker SF, Ledebt A, Roerdink M, Savelsbergh GJ, Beek PJ. Children with cerebral palsy exhibit greater and more regular postural sway than typically developing children. Exp Brain Res. 2008;184(3):363–70.

    PubMed  Google Scholar 

  78. Roncesvalles MN, Woollacott MW, Burtner PA. Neural factors underlying reduced postural adaptability in children with cerebral palsy. Neuroreport. 2002;13(18):2407–10.

    CAS  PubMed  Google Scholar 

  79. Woollacott MH, Shumway-Cook A. Postural dysfunction during standing and walking in children with cerebral palsy: what are the underlying problems and what new therapies might improve balance? Neural Plast. 2005;12(2–3):211–9 discussion 63-72.

    PubMed  PubMed Central  Google Scholar 

  80. Bjornson KF, Belza B, Kartin D, Logsdon R, McLaughlin JF. Ambulatory physical activity performance in youth with cerebral palsy and youth who are developing typically. Phys Ther. 2007;87(3):248–57.

    PubMed  PubMed Central  Google Scholar 

  81. Bjornson KF, Zhou C, Stevenson R, Christakis D, Song K. Walking activity patterns in youth with cerebral palsy and youth developing typically. Disabil Rehabil. 2014;36(15):1279–84.

    PubMed  Google Scholar 

  82. • Noble JJ, Fry N, Lewis AP, Charles-Edwards GD, Keevil SF, Gough M, et al. Bone strength is related to muscle volume in ambulant individuals with bilateral spastic cerebral palsy. Bone. 2014;66:251–5 This study showed an inconsistent relatonship between muscle and bone in individuals with CP. There was a significant positive relationship between the bone properties of the femur and the surrounding thigh musculature, but a nonsignficant relationship between bone properties of the tibia and the surrounding leg musculature.

    PubMed  Google Scholar 

  83. Ziv I, Blackburn N, Rang M, Koreska J. Muscle growth in normal and spastic mice. Dev Med Child Neurol. 1984;26(1):94–9.

    CAS  PubMed  Google Scholar 

  84. Kim W, Lee SJ, Yoon YK, Shin YK, Cho SR, Rhee Y. Adults with spastic cerebral palsy have lower bone mass than those with dyskinetic cerebral palsy. Bone. 2015;71:89–93.

    PubMed  Google Scholar 

  85. Hamrick MW. Increased bone mineral density in the femora of GDF8 knockout mice. Anat Rec A Discov Mol Cell Evol Biol. 2003;272a(1):388–91.

    CAS  Google Scholar 

  86. Gopal S, Majumder S, Batchelor AG, Knight SL, De Boer P, Smith RM. Fix and flap: the radical orthopaedic and plastic treatment of severe open fractures of the tibia. J Bone Joint Surg (Br). 2000;82(7):959–66.

    CAS  Google Scholar 

  87. Harry LE, Sandison A, Paleolog EM, Hansen U, Pearse MF, Nanchahal J. Comparison of the healing of open tibial fractures covered with either muscle or fasciocutaneous tissue in a murine model. J Orthop Res. 2008;26(9):1238–44.

    PubMed  Google Scholar 

  88. Zacks SI, Sheff MF. Periosteal and metaplastic bone formation in mouse minced muscle regeneration. Lab Investig. 1982;46(4):405–12.

    CAS  PubMed  Google Scholar 

  89. Duda GN, Taylor WR, Winkler T, Matziolis G, Heller MO, Haas NP, et al. Biomechanical, microvascular, and cellular factors promote muscle and bone regeneration. Exerc Sport Sci Rev. 2008;36(2):64–70.

    PubMed  Google Scholar 

  90. Landry PS, Marino AA, Sadasivan KK, Albright JA. Effect of soft-tissue trauma on the early periosteal response of bone to injury. J Trauma. 2000;48(3):479–83.

    CAS  PubMed  Google Scholar 

  91. Xian LL, Wu XW, Pang LJ, Lou M, Rosen CJ, Qiu T, et al. Matrix IGF-1 maintains bone mass by activation of mTOR in mesenchymal stem cells. Nat Med. 2012;18(7):1095.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Ashpole NM, Herron JC, Mitschelen MC, Farley JA, Logan S, Yan H, et al. IGF-1 regulates vertebral bone aging through sex-specific and time-dependent mechanisms. J Bone Miner Res. 2016;31(2):443–54.

    CAS  PubMed  Google Scholar 

  93. Liang K, Pun S, Wronski TJ. Bone anabolic effects of basic fibroblast growth factor in ovariectomized rats. Endocrinology. 1999;140(12):5780–8.

    CAS  PubMed  Google Scholar 

  94. Fei YR, Xiao LP, Doetschman T, Coffin DJ, Hurley MM. Fibroblast growth factor 2 stimulation of osteoblast differentiation and bone formation is mediated by modulation of the Wnt signaling pathway. J Biol Chem. 2011;286(47):40575–83.

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Hamrick MW. A role for Myokines in muscle-bone interactions. Exerc Sport Sci Rev. 2011;39(1):43–7.

    PubMed  PubMed Central  Google Scholar 

  96. Colaianni G, Mongelli T, Colucci S, Cinti S, Grano M. Crosstalk between muscle and bone via the muscle-Myokine Irisin. Curr Osteoporos Rep. 2016;14(4):132–7.

    CAS  PubMed  Google Scholar 

  97. Bettis T, Kim BJ, Hamrick MW. Impact of muscle atrophy on bone metabolism and bone strength: implications for muscle-bone crosstalk with aging and disuse. Osteoporos Int. 2018;29(8):1713–20.

    CAS  PubMed  Google Scholar 

  98. Rahemi H, Nigam N, Wakeling JM. The effect of intramuscular fat on skeletal muscle mechanics: implications for the elderly and obese. J R Soc Interface. 2015;12(109).

    PubMed Central  Google Scholar 

  99. Rivas DA, McDonald DJ, Rice NP, Haran PH, Dolnikowski GG, Fielding RA. Diminished anabolic signaling response to insulin induced by intramuscular lipid accumulation is associated with inflammation in aging but not obesity. Am J Phys Regul Integr Comp Phys. 2016;310(7):R561–9.

    Google Scholar 

  100. Manske SL, Boyd SK, Zernicke RF. Muscle changes can account for bone loss after botulinum toxin injection. Calcif Tissue Int. 2010;87(6):541–9.

    CAS  PubMed  Google Scholar 

  101. Manske SL, Boyd SK, Zernicke RF. Muscle and bone follow similar temporal patterns of recovery from muscle-induced disuse due to botulinum toxin injection. Bone. 2010;46(1):24–31.

    CAS  PubMed  Google Scholar 

  102. Warner SE, Sanford DA, Becker BA, Bain SD, Srinivasan S, Gross TS. Botox induced muscle paralysis rapidly degrades bone. Bone. 2006;38(2):257–64.

    CAS  PubMed  Google Scholar 

  103. Williams SA, Reid S, Elliott C, Shipman P, Valentine J. Muscle volume alterations in spastic muscles immediately following botulinum toxin type-a treatment in children with cerebral palsy. Dev Med Child Neurol. 2013;55(9):813–20.

    PubMed  Google Scholar 

  104. Damiano DL. Activity, activity, activity: rethinking our physical therapy approach to cerebral palsy. Phys Ther. 2006;86(11):1534–40.

    PubMed  Google Scholar 

  105. Lee M, Ko Y, Shin MMS, Lee W. The effects of progressive functional training on lower limb muscle architecture and motor function in children with spastic cerebral palsy. J Phys Ther Sci. 2015;27(5):1581–4.

    PubMed  PubMed Central  Google Scholar 

  106. Gillett JG, Boyd RN, Carty CP, Barber LA. The impact of strength training on skeletal muscle morphology and architecture in children and adolescents with spastic cerebral palsy: a systematic review. Res Dev Disabil. 2016;56:183–96.

    PubMed  Google Scholar 

  107. Lee BK, Chon SC. Effect of whole body vibration training on mobility in children with cerebral palsy: a randomized controlled experimenter-blinded study. Clin Rehabil. 2013;27(7):599–607.

    PubMed  Google Scholar 

  108. Wren TAL, Lee DC, Hara R, Rethlefsen SA, Kay RM, Dorey FJ, et al. Effect of high-frequency, low-magnitude vibration on bone and muscle in children with cerebral palsy. J Pediatr Orthop. 2010;30(7):732–8.

    PubMed  PubMed Central  Google Scholar 

  109. Reyes ML, Hernandez M, Holmgren LJ, Sanhueza E, Escobar RG. High-frequency, low-intensity vibrations increase bone mass and muscle strength in upper limbs, improving autonomy in disabled children. J Bone Miner Res. 2011;26(8):1759–66.

    PubMed  Google Scholar 

  110. Singh H, Whitney DG, Knight CA, Miller F, Manal K, Kolm P, et al. Site-specific transmission of a floor-based, high-frequency, low-magnitude vibration stimulus in children with spastic cerebral palsy. Arch Phys Med Rehabil. 2016;97(2):218–23.

    PubMed  Google Scholar 

  111. El-Shamy SM. Effect of whole-body vibration on muscle strength and balance in diplegic cerebral palsy: a randomized controlled trial. Am J Phys Med Rehabil. 2014;93(2):114–21.

    PubMed  Google Scholar 

  112. Stallings VA, Charney EB, Davies JC, Cronk CE. Nutritional status and growth of children with diplegic or hemiplegic cerebral palsy. Dev Med Child Neurol. 1993;35(11):997–1006.

    CAS  PubMed  Google Scholar 

  113. Stallings VA, Cronk CE, Zemel BS, Charney EB. Body composition in children with spastic quadriplegic cerebral palsy. J Pediatr. 1995;126(5 Pt 1):833–9.

    CAS  PubMed  Google Scholar 

  114. Stevenson RD, Hayes RP, Cater LV, Blackman JA. Clinical correlates of linear growth in children with cerebral palsy. Dev Med Child Neurol. 1994;36(2):135–42.

    CAS  PubMed  Google Scholar 

  115. Verschuren O, Smorenburg ARP, Luiking Y, Bell K, Barber L, Peterson MD. Determinants of muscle preservation in individuals with cerebral palsy across the lifespan: a narrative review of the literature. J Cachexia Sarcopenia Muscle. 2018;9(3):453–64.

    PubMed  PubMed Central  Google Scholar 

  116. Modlesky CM, Slade JM, Bickel CS, Meyer RA, Dudley GA. Deteriorated geometric structure and strength of the mid-femur in men with complete spinal cord injury. Bone. 2005;36:331–9.

    PubMed  Google Scholar 

  117. Pang MY, Ashe MC, Eng JJ. Tibial bone geometry in chronic stroke patients: influence of sex, cardiovascular health, and muscle mass. J Bone Miner Res. 2008;23(7):1023–30.

    PubMed  PubMed Central  Google Scholar 

  118. DeVivo MJ. Epidemiology of traumatic spinal cord injury: trends and future implications. Spinal Cord. 2012;50(5):365–72.

    CAS  PubMed  Google Scholar 

  119. Feigin VL, Lawes CMM, Bennett DA, Anderson CS. Stroke epidemiology: a review of population-based studies of incidence, prevalence, and case-fatality in the late 20th century. Lancet Neurol. 2003;2(1):43–53.

    PubMed  Google Scholar 

  120. Kannus P, Haapasalo H, Sankelo M, Sievanen H, Pasanen M, Heinonen A, et al. Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players. Ann Intern Med. 1995;123:27–31.

    CAS  PubMed  Google Scholar 

  121. Fuchs RK, Bauer JJ, Snow CM. Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. J Bone Miner Res. 2001;16(1):148–56.

    CAS  PubMed  Google Scholar 

  122. Petit MA, McKay HA, MacKelvie KJ, Heinonen A, Khan KM, Beck TJ. A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study. J Bone Miner Res. 2002;17(3):363–72.

    CAS  PubMed  Google Scholar 

  123. Modlesky CM, Lewis RD. Does exercise during growth have a long-term effect on bone health? Exerc Sport Sci Rev. 2002;30(4):171–6.

    PubMed  Google Scholar 

  124. Gunter K, Baxter-Jones AD, Mirwald RL, Almstedt H, Fuchs RK, Durski S, et al. Impact exercise increases BMC during growth: an 8-year longitudinal study. J Bone Miner Res. 2008;23(7):986–93.

    PubMed  Google Scholar 

  125. Nelson ME, Fiatarone MA, Morganti CM, Trice I, Greenberg RA, Evans WJ. Effect of high-intensity strength training on multiple risk factors for osteoporotic fractures. JAMA. 1994;272:1909–14.

    CAS  PubMed  Google Scholar 

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Funding

The authors received funding from the Eunice Kennedy Shriver National Institute of Child Health and Human Development, HD090126.

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Modlesky, C.M., Zhang, C. Complicated Muscle-Bone Interactions in Children with Cerebral Palsy. Curr Osteoporos Rep 18, 47–56 (2020). https://doi.org/10.1007/s11914-020-00561-y

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