Cortical bone deficit and fat infiltration of bone marrow and skeletal muscle in ambulatory children with mild spastic cerebral palsy
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Introduction Nonambulatory children with severe cerebral palsy (CP) have underdeveloped bone architecture, low bone strength and a high degree of fat infiltration in the lower extremity musculature. The present study aims to determine if such a profile exists in ambulatory children with mild CP and if excess fat infiltration extends into the bone marrow.Materials and methods Ambulatory children with mild spastic CP and typically developing children (4 to 11years; 12/group) were compared. Magnetic resonance imaging was used to estimate cortical bone, bone marrow and total bone volume and width, bone strength [i.e., section modulus (Z) and polar moment of inertia (J)], and bone marrow fat concentration in the midtibia, and muscle volume, intermuscular, subfascial, and subcutaneous adipose tissue (AT) volume and intramuscular fat concentration in the midleg. Accelerometer-based activity monitors worn on the ankle were used to assess physical activity.Results There were no group differences in age, height, body mass, body mass percentile, BMI, BMI percentile or tibia length, but children with CP had lower height percentile (19th vs. 50th percentile) and total physical activity counts (44%) than controls (both p<0.05). Children with CP also had lower cortical bone volume (30%), cortical bone width in the posterior (16%) and medial (32%) portions of the shaft, total bone width in the medial-lateral direction (15%), Z in the medial-lateral direction (34%), J (39%) and muscle volume (39%), and higher bone marrow fat concentration (82.1±1.8% vs. 80.5±1.9%), subfascial AT volume (3.3 fold) and intramuscular fat concentration (25.0±8.0% vs. 16.1±3.3%) than controls (all p<0.05). When tibia length was statistically controlled, all group differences in bone architecture, bone strength, muscle volume and fat infiltration estimates, except posterior cortical bone width, were still present (all p<0.05). Furthermore, a higher intermuscular AT volume in children with CP compared to controls emerged (p<0.05).Conclusions Ambulatory children with mild spastic CP exhibit an underdeveloped bone architecture and low bone strength in the midtibia and a greater infiltration of fat in the bone marrow and surrounding musculature compared to typically developing children. Whether the deficit in the musculoskeletal system of children with CP is associated with higher chronic disease risk and whether the deficit can be mitigated requires further investigation.
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Individuals with cerebral palsy have low levels of physical activity regardless of their level of motor impairment.
“Specifically, individuals with CP have low levels of physical activity regardless of the level of motor impairment.7”
From Mental Health Disorders and Physical Risk Factors in Children with Cerebral Palsy: A Cross-Sectional Study (2019) · cites this paper as [7]
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Cites
CDC growth charts: United States.
Kuczmarski, R. J., Ogden, C. L., Grummer‐Strawn, L. M., Flegal, K. M., Guo, S. S., Wei, R. X., Mei, Z., Curtin, L. R., Roche, A. F., & Johnson, C. L. (2000) · PubMed · Cited by 5,298 · see citing works
Mitsiopoulos, N., Baumgartner, R. N., Heymsfield, S. B., Lyons, W., Gallagher, D., & Ross, R. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.85.1.115 · Cited by 1,522 · see citing works
Cowin, S. C. (2001) · CRC Press eBooks · doi:10.1201/b14263 · Cited by 1,456 · see citing works
Osteoporosis and the Replacement of Cell Populations of the Marrow by Adipose Tissue
Meunier, P. J., Aaron, J., Edouard, C. M., & VlGNON, G. (1971) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-197110000-00021 · Cited by 779 · see citing works
Goodpaster, B. H., Thaete, F. L., & Kelley, D. E. (2000) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.4.885 · Cited by 707 · cited 3× · see citing works
“It has been established that elevated AT surrounding muscle and fat within muscle are associated with a disturbance of euglycemic conditions [12] and insulin resistance [16], as well as promoting a pro-inflammatory Whitney et al.”
BackgroundWood, E. P., & Rosenbaum, P. (2000) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162200000529 · Cited by 659 · see citing works
Prediction of activity energy expenditure using accelerometers in children.
Puyau, M. R., Adolph, A. L., Vohra, F. A., Zakeri, I., & Butte, N. F. (2004) · PubMed · Cited by 472 · see citing works
Low Magnitude Mechanical Loading Is Osteogenic in Children With Disabling Conditions
Ward, K. A., Alsop, C. W., Caulton, J. M., Rubin, C. T., Adams, J. E., & Zulf Mughal, M. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040129 · Cited by 432 · see citing works
Bone Density and Metabolism in Children and Adolescents With Moderate to Severe Cerebral Palsy
Henderson, R. C., Lark, R. K., Gurka, M. J., Worley, G., Fung, E. B., Conaway, M. R., Stallings, V. A., & Stevenson, R. D. (2002) · PEDIATRICS · doi:10.1542/peds.110.1.e5 · Cited by 381 · see citing works
ActiGraph and Actical Physical Activity Monitors
John, D., & Freedson, P. S. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3182399f5e · Cited by 353 · see citing works
Eser, P., Frotzler, A., Zehnder, Y., Wick, L., Knecht, H., Denoth, J., & Schießl, H. (2004) · Bone · doi:10.1016/j.bone.2004.01.001 · Cited by 324 · see citing works
David, V., Martin, A., Lafage‐Proust, M., Malaval, L., Peyroche, S., Jones, D. B., Vico, L., & Guignandon, A. (2007) · Endocrinology · doi:10.1210/en.2006-1704 · Cited by 321 · see citing works
Invited Review Carbohydrate And Lipid Metabolism In Chronic Spinal Cord Injury
Bauman, W. A., & Spungen, A. M. (2001) · Journal of Spinal Cord Medicine · doi:10.1080/10790268.2001.11753584 · Cited by 273 · see citing works
Contributing factors to muscle weakness in children with cerebral palsy
Elder, G. C. B., Kirk, J., Stewart, G., et al. (2003) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162203000999 · Cited by 239 · see citing works
Intramuscular fat and glucose tolerance after spinal cord injury – a cross-sectional study
Elder, C. P., Apple, D. F., Bickel, C. S., Meyer, R. A., & Dudley, G. A. (2004) · Spinal Cord · doi:10.1038/sj.sc.3101652 · Cited by 233 · see citing works
Contributing factors to muscle weakness in children with cerebral palsy
Elder, G. C. B., BSc, G. S., Cook, K., et al. (2003) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2003.tb00954.x · Cited by 233 · see citing works
Baum, T. H., Yap, S. P., Karampinos, D. C., Nardo, L., Kuo, D. Z., Burghardt, A. J., Masharani, U. B., Schwartz, A. V., Li, X., & Link, T. M. (2011) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.22757 · Cited by 227 · see citing works
Henderson, R. C., Lark, R. K., Kecskemethy, H. H., et al. (2002) · The Journal of Pediatrics · doi:10.1067/mpd.2002.128207 · Cited by 222 · see citing works
Gait function and decline in adults with cerebral palsy: a systematic review
Morgan, P., & McGinley, J. (2014) · Disability and Rehabilitation · doi:10.3109/09638288.2013.775359 · Cited by 209 · see citing works
Causes of excess mortality in cerebral palsy
Strauss, D., Cable, W., & Shavelle, R. (1999) · Developmental Medicine & Child Neurology · doi:10.1017/s001216229900122x · Cited by 202 · see citing works
Intramuscular fat and inflammation differ in older adults: The impact of frailty and inactivity
Addison, O. R., Drummond, M. J., LaStayo, P. C., Dibble, L. E., Wende, A. R., McClain, D. A., & Marcus, R. L. (2014) · The journal of nutrition health & aging · doi:10.1007/s12603-014-0019-1 · Cited by 181 · see citing works
Whole Bone Mechanics and Bone Quality
Cole, J. H., & van der Meulen, M. C. H. (2011) · Clinical Orthopaedics and Related Research · doi:10.1007/s11999-011-1784-3 · Cited by 168 · see citing works
John Suckling, A., Sigmundsson, T., Greenwood, K., & Bullmore, E. T. (1999) · Magnetic Resonance Imaging · doi:10.1016/s0730-725x(99)00055-7 · Cited by 152 · see citing works
Age, gender, and skeletal variation in bone marrow composition: A preliminary study at 3.0Tesla
Liney, G. P., Bernard, C. P., Manton, D. J., Turnbull, L. W., & Langton, C. M. (2007) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.21072 · Cited by 148 · see citing works
Trudel, G., Payne, M. W. C., Mädler, B., Ramachandran, N., Lecompte, M., Wade, C. E., Biolo, G., Blanc, S., Hughson, R. L., Bear, L. A., et al. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91530.2008 · Cited by 134 · see citing works
Comparison of fat quantification methods: A phantom study at 3.0T
Bernard, C. P., Liney, G. P., Manton, D. J., Turnbull, L. W., & Langton, C. M. (2007) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.21201 · Cited by 129 · see citing works
Fractures in Patients With Cerebral Palsy
Presedo, A., DABNEY, K. W., & Miller, F. (2007) · Journal of Pediatric Orthopaedics · doi:10.1097/bpo.0b013e3180317403 · Cited by 128 · see citing works
Self-citationMarrow changes in paraplegic patients
MINAIRE, P. M., Edouard, C. M., ARLOT, M. E., & Meunier, P. J. (1984) · Calcified Tissue International · doi:10.1007/bf02405340 · Cited by 121 · see citing works
Adipose Tissue Infiltration of Skeletal Muscle in Children with Cerebral Palsy
Johnson, D. L., Miller, F., Subramanian, P., & Modlesky, C. M. (2008) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2008.10.046 · Cited by 119 · see citing works
Self-citationBone Marrow Fat Is Inversely Related to Cortical Bone in Young and Old Subjects
Wren, T. A. L., Chung, S. A., Dorey, F. J., Blüml, S., Adams, G. B., & Gilsanz, V. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1922 · Cited by 102 · see citing works
Effect of High-frequency, Low-magnitude Vibration on Bone and Muscle in Children With Cerebral Palsy
Wren, T. A. L., Lee, D. C., Hara, R., Rethlefsen, S. A., Kay, R. M., Dorey, F. J., & Gilsanz, V. (2010) · Journal of Pediatric Orthopaedics · doi:10.1097/bpo.0b013e3181efbabc · Cited by 100 · see citing works
Binkley, T. L., Johnson, J. B., Vogel, L., et al. (2005) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2005.07.014 · Cited by 98 · see citing works
Human bone marrow adiposity is linked with serum lipid levels not T1-diabetes
Slade, J. M., Coe, L. M., Meyer, R. A., & McCabe, L. R. (2012) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2011.11.001 · Cited by 83 · see citing works
Self-citationBone Acquisition in Healthy Young Females Is Reciprocally Related to Marrow Adiposity
Iorgi, N. D., Mo, A. O., Grimm, K. E., et al. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2336 · Cited by 81 · see citing works
Fractures in Patients with Cerebral Palsy
McIVOR, W. C., & Samilson, R. L. (1966) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-196648050-00003 · Cited by 78 · see citing works
Intramuscular fat in ambulant young adults with bilateral spastic cerebral palsy
Noble, J. J., Charles‐Edwards, G., Keevil, S., Lewis, A. P., Gough, M., & Shortland, A. P. (2014) · BMC Musculoskeletal Disorders · doi:10.1186/1471-2474-15-236 · Cited by 77 · see citing works
Secondary muscle pathology and metabolic dysregulation in adults with cerebral palsy
Peterson, M. D., Gordon, P. M., Hurvitz, E. A., & Burant, C. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00338.2012 · Cited by 73 · see citing works
Experimental Techniques for Bone Mechanics
Cowin, S. C. (2001) · CRC Press eBooks · doi:10.1201/b14263-12 · Cited by 72 · see citing works
Modlesky, C. M., Subramanian, P., & Miller, F. (2007) · Osteoporosis International · doi:10.1007/s00198-007-0433-x · Cited by 71 · see citing works
Self-citationModlesky, C. M., Slade, J. M., Bickel, C. S., Meyer, R. A., & Dudley, G. A. (2005) · Bone · doi:10.1016/j.bone.2004.10.012 · Cited by 67 · see citing works
Self-citationDifferential Effects of Exercise on Tibial Shaft Marrow Density in Young Female Athletes
Rantalainen, T., Nikander, R., Heinonen, A. O., Cervinka, T., Sievänen, H. T., & Daly, R. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3748 · Cited by 66 · see citing works
Premenopausal women with idiopathic low-trauma fractures and/or low bone mineral density
Cohen, A., Recker, R. R., Lappe, J. M., Dempster, D. W., Cremers, S., McMahon, D. J., Stein, E. M., Fleischer, J. B., Rosen, C. J., Rogers, H., et al. (2011) · Osteoporosis International · doi:10.1007/s00198-011-1560-y · Cited by 59 · see citing works
Evaluation of the femoral midshaft in children with cerebral palsy using magnetic resonance imaging
Modlesky, C. M., Kanoff, S. A., Johnson, D. L., Subramanian, P., & Miller, F. (2008) · Osteoporosis International · doi:10.1007/s00198-008-0718-8 · Cited by 58 · see citing works
Self-citationWoodhead, H. J., Kemp, A., Blimkie, C. J. R., BRIODY, J. N., Duncan, C. S., Thompson, M., LAM, A. H., Howman-Giles, R., & Cowell, C. T. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.12.2251 · Cited by 53 · see citing works
Modlesky, C. M., Whitney, D. G., Singh, H., Barbe, M. F., Kirby, J. T., & Miller, F. (2014) · Osteoporosis International · doi:10.1007/s00198-014-2873-4 · Cited by 43 · see citing works
Self-citationGorgey, A. S., Poarch, H. J., Adler, R. A., Khalil, R. E., & Gater, D. R. (2013) · PM&R · doi:10.1016/j.pmrj.2013.05.006 · Cited by 35 · see citing works
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- [20]Tanner J Growth and Adolescence 2 Oxford Blackwell Scientific Publications 1962
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Fragala, M. S., Cadore, E. L., Dorgo, S., Izquierdo, M., Kraemer, W. J., Peterson, M. D., & Ryan, E. D. (2019) · Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000003230 · Cited by 1,290 · see citing works
Whitney, D. G., Warschausky, S. A., & Peterson, M. D. (2019) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.14083 · Cited by 106 · see citing works
Self-citationPrevalence of Mental Health Disorders Among Adults With Cerebral Palsy: A Cross-sectional Analysis
Whitney, D. G., Warschausky, S. A., Ng, S., Hurvitz, E. A., Kamdar, N. S., & Peterson, M. D. (2019) · Annals of Internal Medicine · doi:10.7326/m18-3420 · Cited by 93 · see citing works
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- Authors
- Whitney, D. G., Singh, H., Miller, F., Barbe, M. F., Slade, J. M., Pohlig, R. T., & Modlesky, C. M.
- Affiliations
- University of Delaware (US)
- Alfred I. duPont Hospital for Children (US)
- Temple University (US)
- Michigan State University (US)
- Corresponding author
- Modlesky, Christopher M.
- ORCID
- Venue
- Bone
- Publisher
- Elsevier BV
- Published
- 2017-01
- Volume
- 94
- Pages
- 90-97
- ISSN
- 1873-2763 (ISSN-L)
- 8756-3282
- PMC
- PMC5912954
- OpenAlex
- W2530376686
- Cited by
- 108
- References
- 46
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 14 · 2023: 14 · 2022: 13 · 2021: 12 · 2020: 18 · 2019: 15 · 2018: 13 · 2017: 2
- FWCI
- 8.88
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Bone (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (HD071397)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Cerebral Palsy and Movement Disorders
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Neurology › Botulinum Toxin and Related Neurological Disorders
- Keywords
- spastic cerebral palsy, ambulatory children, intramuscular fat, tibia, bone strength, section modulus, polar moment of inertia, muscle volume, physical activity, bone structure, body fat distribution, bone mineral area, bone mineral density
- MeSH terms
- Cortical Bone, Adipose Tissue, Biomechanical Phenomena, Bone Marrow, Cerebral Palsy, Child, Child, Preschool, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Tibia, Case-Control Studies, Walking, Muscle, Skeletal, Adiposity
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