Abstract
Introduction
The deleterious influence of increased mechanical forces on capital femoral epiphysis development is well established; however, the growth of the physis in the absence of such forces remains unclear. The hips of non-ambulatory cerebral palsy (CP) patients provide a weight-restricted (partial weightbearing) model which can elucidate the influence of decreased mechanical forces on the development of physis morphology, including features related to development of slipped capital femoral epiphysis (SCFE). Here we used 3D image analysis to compare the physis morphology of children with non-ambulatory CP, as a model for abnormal hip loading, with age-matched native hips.
Materials and methods
CT images of 98 non-ambulatory CP hips (8–15 years) and 80 age-matched native control hips were used to measure height, width, and length of the tubercle, depth, width, and length of the metaphyseal fossa, and cupping height across different epiphyseal regions. The impact of age on morphology was assessed using Pearson correlations. Mixed linear model was used to compare the quantified morphological features between partial weightbearing hips and full weightbearing controls.
Results
In partial weightbearing hips, tubercle height and length along with fossa depth and length significantly decreased with age, while peripheral cupping height increased with age (r > 0.2, P < 0.04). Compared to normally loaded (full weightbearing) hips and across all age groups, partially weightbearing hips’ epiphyseal tubercle height and length were smaller (P < .05), metaphyseal fossa depth was larger (P < .01), and posterior, inferior, and anterior peripheral cupping heights were smaller (P < .01).
Conclusions
Smaller epiphyseal tubercle and peripheral cupping with greater metaphyseal fossa size in partial weightbearing hips suggests that the growing capital femoral epiphysis requires mechanical stimulus to adequately develop epiphyseal stabilizers. Deposit low prevalence and relevance of SCFE in CP, these findings highlight both the role of normal joint loading in proper physis development and how chronic abnormal loading may contribute to various pathomorphological changes of the proximal femur (i.e., capital femoral epiphysis).
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All data for this study are presented in the figures and in the body of the manuscript.
References
Millis MB, Novais EN (2011) In situ fixation for slipped capital femoral epiphysis: perspectives in 2011. J Bone Joint Surg Am 93(Suppl 2):46–51
Fraitzl CR et al (2007) Radiological evidence of femoroacetabular impingement in mild slipped capital femoral epiphysis: a mean follow-up of 14.4 years after pinning in situ. J Bone Joint Surg Br 89(12):1592–1596
Lehmann CL et al (2006) The epidemiology of slipped capital femoral epiphysis: an update. J Pediatr Orthop 26(3):286–290
Zhang C et al (2015) Femoroacetabular impingement and osteoarthritis of the hip. Can Fam Physician 61(12):1055–1060
Bedi A, Kelly BT (2013) Femoroacetabular impingement. J Bone Joint Surg Am 95(1):82–92
Benson EC et al (2008) A new look at the incidence of slipped capital femoral epiphysis in new Mexico. J Pediatr Orthop 28(5):529–533
Murray AW, Wilson NI (2008) Changing incidence of slipped capital femoral epiphysis: a relationship with obesity? J Bone Joint Surg Br 90(1):92–94
Beck, M., et al., Hip morphology influences the pattern of damage to the acetabular cartilage: femoroacetabular impingement as a cause of early osteoarthritis of the hip. 2005. p. 1012–8.
Novais EN, Millis MB (2012) Slipped capital femoral epiphysis: prevalence, pathogenesis, and natural history. Clin Orthop Relat Res 470(12):3432–3438
Novais EN et al (2018) Body mass index affects proximal femoral but not acetabular morphology in adolescents without hip pathology. J Bone Joint Surg Am 100(1):66–74
Agricola R et al (2012) The development of Cam-type deformity in adolescent and young male soccer players. Am J Sports Med 40(5):1099–1106
Manoff EM, Banffy MB, Winell JJ (2005) Relationship between Body Mass Index and slipped capital femoral epiphysis. J Pediatr Orthop 25(6):744–746
Siebenrock KA et al (2013) Growth plate alteration precedes cam-type deformity in elite basketball players. Clin Orthop Relat Res 471(4):1084–1091
Siebenrock KA et al (2013) Prevalence of cam-type deformity and hip pain in elite ice hockey players before and after the end of growth. Am J Sports Med 41(10):2308–2313
Murgier J et al (2014) The frequency of sequelae of slipped upper femoral epiphysis in cam-type femoroacetabular impingement. Bone Joint J 96-B(6):724–729
Ziebarth K et al (2013) Slipped capital femoral epiphysis: relevant pathophysiological findings with open surgery. Clin Orthop Relat Res 471(7):2156–2162
Goodman DA et al (1997) Subclinical slipped capital femoral epiphysis. Relationship to osteoarthrosis of the hip. J Bone Joint Surg Am 79(10):1489–1497
Roels P et al (2014) Mechanical factors explain development of cam-type deformity. Osteoarthritis Cartilage 22(12):2074–2082
Albers CE et al (2015) Twelve percent of hips with a primary cam deformity exhibit a slip-like morphology resembling sequelae of slipped capital femoral epiphysis. Clin Orthop Relat Res 473(4):1212–1223
Liu RW et al (2013) An anatomic study of the epiphyseal tubercle and its importance in the pathogenesis of slipped capital femoral epiphysis. J Bone Joint Surg Am 95(6):e341–e348
Tayton K (2007) Does the upper femoral epiphysis slip or rotate? J Bone Joint Surg Br 89(10):1402–1406
Tayton K (2009) The epiphyseal tubercle in adolescent hips. Acta Orthop 80(4):416–419
Jonasson PS et al (2014) Strength of the porcine proximal femoral epiphyseal plate: the effect of different loading directions and the role of the perichondrial fibrocartilaginous complex and epiphyseal tubercle - an experimental biomechanical study. J Exp Orthop 1(1):4
Agricola R et al (2014) A cam deformity is gradually acquired during skeletal maturation in adolescent and young male soccer players: a prospective study with minimum 2-year follow-up. Am J Sports Med 42(4):798–806
Palmer A et al (2018) Physical activity during adolescence and the development of cam morphology: a cross-sectional cohort study of 210 individuals. Br J Sports Med 52(9):601–610
Hosseinzadeh S et al (2020) The metaphyseal fossa surrounding the epiphyseal tubercle is larger in hips with moderate and severe slipped capital femoral epiphysis than normal hips. J Child Orthop 14(3):184–189
Novais EN et al (2018) Age- and sex-specific morphologic variations of capital femoral epiphysis growth in children and adolescents without hip disorders. Orthop J Sports Med 6(6):2325967118781579
Hosseinzadeh, S., et al., Age- and sex-specific morphologic changes in the metaphyseal fossa adjacent to epiphyseal tubercle in children and adolescents without hip disorders. J Orthop Res, 2020.
Novais EN et al (2018) Age- and gender-specific variations of the epiphyseal tilt and epiphyseal angle in adolescents without hip pathology. J Child Orthop 12(2):152–159
Kim HT, Wenger DR (1997) Location of acetabular deficiency and associated hip dislocation in neuromuscular hip dysplasia: three-dimensional computed tomographic analysis. J Pediatric Orthop 17(2):143–151
Bosmans L et al (2014) Hip contact force in presence of aberrant bone geometry during normal and pathological gait. J Orthop Res 32(11):1406–1415
Brunner R, Picard C, Robb J (1997) Morphology of the acetabulum in hip dislocations caused by cerebral palsy. J Pediatr Orthopaed B 6(3):207–211
Gose S et al (2009) Morphometric analysis of acetabular dysplasia in cerebral palsy: three-dimensional CT study. J Pediatr Orthopaed 29(8):896–902
Chung CY et al (2006) Morphometric analysis of acetabular dysplasia in cerebral palsy. J Bone Jt Surg Br 88-B(2):243–247
Inai T et al (2018) Effect of hip joint angle at seat-off on hip joint contact force during sit-to-stand movement: a computer simulation study. Biomed Eng Online 17(1):177
Pin TW (2007) Effectiveness of static weight-bearing exercises in children with cerebral palsy. Pediatr Phys Ther 19(1):62–73
Kecskemethy HH et al (2008) Quantifying weight bearing while in passive standers and a comparison of standers. Dev Med Child Neurol 50(7):520–523
Van Houcke J et al (2017) Computer-based estimation of the hip joint reaction force and hip flexion angle in three different sitting configurations. Appl Ergon 63:99–105
Kiapour AM et al (2019) Relative contribution of epiphyseal tubercle and peripheral cupping to capital femoral epiphysis stability during daily activities. J Orthop Res
Novais EN et al (2019) Smaller epiphyseal tubercle and larger peripheral cupping in slipped capital femoral epiphysis compared with healthy hips: A 3-Dimensional Computed Tomography Study. J Bone Joint Surg Am
Carter DR, Wong M (2003) Modelling cartilage mechanobiology. Philos Trans R Soc Lond B Biol Sci 358(1437):1461–1471
Stevens SS, Beaupre GS, Carter DR (1999) Computer model of endochondral growth and ossification in long bones: biological and mechanobiological influences. J Orthop Res 17(5):646–653
Rodriguez JI et al (1992) Morphological changes in long bone development in fetal akinesia deformation sequence: an experimental study in curarized rat fetuses. Teratology 45(2):213–221
Gomez C et al (2007) Absence of mechanical loading in utero influences bone mass and architecture but not innervation in Myod-Myf5-deficient mice. J Anat 210(3):259–271
Sharir A et al (2011) Muscle force regulates bone shaping for optimal load-bearing capacity during embryogenesis. Development 138(15):3247–3259
Nhamoucha Y et al (2018) Slipped capital femoral epiphysis in a patient with cerebral palsy due to seizure. Pan Afr Med J 31:89
Kardashian G, Strongwater AM (2010) Slipped capital femoral epiphysis in a cerebral palsy patient: a case report. J Pediatr Orthop B 19(5):428–430
Perry DC et al (2018) Childhood obesity and slipped capital femoral epiphysis. Pediatrics 142(5)
Wylie JD, Novais EN (2019) Evolving understanding of and treatment approaches to slipped capital femoral epiphysis. Curr Rev Musculoskelet Med 12(2):213–219
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Children’s Hospital Orthopaedic Surgery Foundation (AMK) and Boston Children’s Hospital Faculty Council (AMK).
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Study concept and design was done by AMK, ENN, BS, SH, AE). Data collection and analysis was done by CFM, KE, AE, SH, and AMK). Interpretation of the findings was done by CFM, AE, SH, BS, ENN and AMK. First draft of the manuscript was developed by CFM, SH, and AMK. All co-authors contributed to the reviewing and finalizing the manuscript.
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This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Institutional Review Board of Boston Children’s Hospital (IRB-P00015233).
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Mitchell, C., Emami, K., Emami, A. et al. Effects of joint loading on the development of capital femoral epiphysis morphology. Arch Orthop Trauma Surg 143, 5457–5466 (2023). https://doi.org/10.1007/s00402-023-04795-0
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DOI: https://doi.org/10.1007/s00402-023-04795-0