Physiologic and Pathologic Development of the Infantile and Adolescent Hip Joint: Descriptive and Functional Aspects

Abstract

The basic law of mechanobiology states that the external form and internal architecture of the skeleton and joints follow the functional stimuli that act upon them. Radiographs and magnetic resonance imaging reflect the loading history of the growing child, enabling an experienced radiologist to analyze the clinical functioning of patients by interpreting imaging studies. Concerning the hip joint, the physes of the coxal femoral end, the coxal femoral epiphysis with its epiphyseal growth plate, as well as the apophysis of the greater trochanter with its trochanteric growth plate, are the essential organ structures subject to internal forces. They determine the definitive geometric shape of the proximal femur. Indirectly they influence the appearance of the acetabulum and the centration of the hip joint.

Keywords

hip development - proximal femur - hip joint - mechanobiology - functional anatomy

• References

• 1 Frost HM, Schönau E. The “muscle-bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab 2000; 13 (06) 571-590
• 2 Leucht Ph, Kim JB, Helms JA. Cellular and molecular foundation for fracture healing in children. Eur J Trauma 2005; 2: 90-104
• 3 Villemure I, Stokes IAF. Growth plate mechanics and mechanobiology. A survey of present understanding. J Biomech 2009; 42 (12) 1793-1803
• 4 Mackie EJ, Tatarczuch L, Mirams M. The skeleton: a multi-functional complex organ: the growth plate chondrocyte and endochondral ossification. J Endocrinol 2011; 211 (02) 109-121
• 5 Brian JM, Choi DH, Moore MM. The primary physis. Semin Musculoskelet Radiol 2018; 22 (01) 95-103
• 6 Siffert RS. Patterns of deformity of the developing hip. Clin Orthop Relat Res 1981; (160) 14-29
• 7 Ogden JA. Development and growth of the hip. In Katz JF, Siffert RS. , eds. Management of Hip Disorders in Children. Philadelphia, PA: JB Lippincott; 1983
• 8 Serrat MA, Reno PL, McCollum MA, Meindl RS, Lovejoy CO. Variation in mammalian proximal femoral development: comparative analysis of two distinct ossification patterns. J Anat 2007; 210 (03) 249-258
• 9 Putz R, Milz S. Macroscopic and functional anatomy of the apophyseal plate [in German]. Orthopade 2016; 45 (03) 199-205
• 10 Jouve JL, Glard Y, Garron E. , et al. Anatomical study of the proximal femur in the fetus. J Pediatr Orthop B 2005; 14 (02) 105-110
• 11 Bonneau N, Simonis C, Seringe R, Tardieu C. Study of femoral torsion during prenatal growth: interpretations associated with the effects of intrauterine pressure. Am J Phys Anthropol 2011; 145 (03) 438-445
• 12 Tönnis D. Normal values of the hip joint for the evaluation of X-rays in children and adults. Clin Orthop Relat Res 1976; (119) 39-47
• 13 Wientroub S, Tardiman R, Green I, Salama R, Weissman SL. The development of the normal infantile hip as expressed by radiological measurements. Int Orthop 1981; 4 (04) 239-241
• 14 Scoles PV, Boyd A, Jones PK. Roentgenographic parameters of the normal infant hip. J Pediatr Orthop 1987; 7 (06) 656-663
• 15 Than P, Sillinger T, Kránicz J, Bellyei A. Radiographic parameters of the hip joint from birth to adolescence. Pediatr Radiol 2004; 34 (03) 237-244
• 16 Birkenmaier C, Jorysz G, Jansson V, Heimkes B. Normal development of the hip: a geometrical analysis based on planimetric radiography. J Pediatr Orthop B 2010; 19 (01) 1-8
• 17 Graf R. Guide to Sonography of the Infant Hip. Stuttgart, Germany: Thieme; 1986
• 18 Wegener V, Jorysz G, Arnoldi A. , et al. Normal radiological unossified hip joint space and femoral head size development during growth in 675 children and adolescents. Clin Anat 2017; 30 (02) 267-275
• 19 Heimkes B, Posel P, Plitz W, Jansson V. Forces acting on the juvenile hip joint in the one-legged stance. J Pediatr Orthop 1993; 13 (04) 431-436
• 20 Heimkes B, Posel P, Plitz W, Zimmer M. Age-related force distribution at the proximal end of the femur in normally growing children [in German]. Z Orthop Ihre Grenzgeb 1997; 135 (01) 17-23
• 21 Wolff J. Das Gesetz der Transformation der Knochen. Berlin, Germany: A.Hischwald; 1892
• 22 Roux W. Gesammelte Abhandlungen über Entwicklungsmechanik der Organismen. Bd II. Leipzig, Germany: Wilhelm Engelmann; 1895
• 23 Pauwels F. Biomechanics of the Normal and Diseased Hip: Theoretical Foundation, Technique and Results of Treatment: An Atlas. Berlin, Germany: Springer; 1976
• 24 Miller F, Slomczykowski M, Cope R, Lipton GE. Computer modeling of the pathomechanics of spastic hip dislocation in children. J Pediatr Orthop 1999; 19 (04) 486-492
• 25 Ribble TG, Santare MH, Miller F. Stresses in the growth plate of the developing proximal femur. J Appl Biomech 2001; 17: 129-141
• 26 Carter DR, Beaupré GS. Skeletal Function and Form. Mechanobiology of Skeletal Development, Aging, and Regeneration. New York, NY: Cambridge University Press; 2001
• 27 Fetto J, Leali A, Moroz A. Evolution of the Koch model of the biomechanics of the hip: clinical perspective. J Orthop Sci 2002; 7 (06) 724-730
• 28 Shefelbine SJ, Carter DR. Mechanobiological predictions of femoral anteversion in cerebral palsy. Ann Biomed Eng 2004; 32 (02) 297-305
• 29 Lenaerts G, Bartels W, Gelaude F. , et al. Subject-specific hip geometry and hip joint centre location affects calculated contact forces at the hip during gait. J Biomech 2009; 42 (09) 1246-1251
• 30 Carriero A, Zavatsky A, Stebbins J. , et al. Influence of altered gait patterns on the hip joint contact forces. Comput Methods Biomech Biomed Engin 2014; 17 (04) 352-359
• 31 Yadav P, Shefelbine SJ, Pontén E, Gutierrez-Farewik EM. Influence of muscle groups' activation on proximal femoral growth tendency. Biomech Model Mechanobiol 2017; 16 (06) 1869-1883
• 32 Chan EF, Farnsworth CL, Klisch SM, Hosalkar HS, Sah RL. 3-dimensional metrics of proximal femoral shape deformities in Legg-Calvé-Perthes disease and slipped capital femoral epiphysis. J Orthop Res 2018; 36 (05) 1526-1535
• 33 Pinheiro MDS, Dobson C, Clarke NM, Fagan M. The potential role of variations in juvenile hip geometry on the development of Legg-Calvé-Perthes disease: a biomechanical investigation. Comput Methods Biomech Biomed Engin 2018; 21 (02) 194-200
• 34 Tardieu C. Development of the human hind limb and its importance for the evolution of bipedalism. Evol Anthropol 2010; 19: 174-186
• 35 Bonneau N, Baylac M, Gagey O, Tardieu C. Functional integrative analysis of the human hip joint: the three-dimensional orientation of the acetabulum and its relation with the orientation of the femoral neck. J Hum Evol 2014; 69: 55-69
• 36. Ruff C, Holt B, Trinkaus E. Who's afraid of the big bad Wolff?: “Wolff's law” and bone functional adaptation. Am J Phys Anthropol 2006; 129 (04) 484-498
• 37 Heimkes B. The great apophyses: Functional strain and relevance [in German]. Orthopade 2016; 45 (03) 206-212
• 38 Lovejoy CO. The natural history of human gait and posture. Part 2. Hip and thigh. Gait Posture 2005; 21 (01) 113-124
• 39 Holliday TW, Hutchinson VT, Morrow MMB, Livesay GA. Geometric morphometric analyses of hominid proximal femora: taxonomic and phylogenetic considerations. Homo 2010; 61 (01) 3-15
• 40 Anderson M, Messner MB, Green WT. Distribution of lengths of the normal femur and tibia in children from one to eighteen years of age. J Bone Joint Surg Am 1964; 46: 1197-1202
• 41 Long Y, Leslie WD, Luo Y. Study of DXA-derived lateral-medial cortical bone thickness in assessing hip fracture risk. Bone Rep 2015; 2: 44-51
• 42 Duncan JS, Schofield G, Duncan EK. Step count recommendations for children based on body fat. Prev Med 2007; 44 (01) 42-44
• 43 Laurson KR, Eisenmann JC, Welk GJ, Wickel EE, Gentile DA, Walsh DA. Evaluation of youth pedometer-determined physical activity guidelines using receiver operator characteristic curves. Prev Med 2008; 46 (05) 419-424
• 44 Dollman J, Olds TS, Esterman A, Kupke T. Pedometer step guidelines in relation to weight status among 5- to 16-year-old Australians. Pediatr Exerc Sci 2010; 22 (02) 288-300
• 45 Bergmann G, Graichen F, Rohlmann A. Hip joint loading during walking and running, measured in two patients. J Biomech 1993; 26 (08) 969-990
• 46 Correa TA, Crossley KM, Kim HJ, Pandy MG. Contributions of individual muscles to hip joint contact force in normal walking. J Biomech 2010; 43 (08) 1618-1622
• 47 Skuban TP, Vogel T, Baur-Melnyk A, Jansson V, Heimkes B. Function-orientated structural analysis of the proximal human femur. Cells Tissues Organs 2009; 190 (05) 247-255
• 48 Sallam A, Ziegler CM, Jansson V, Heimkes B. The underused hip in ipsilaterally orthotics-dependent children. J Child Orthop 2015; 9 (04) 255-262
• 49 Steinbrueck A, Hocke S, Heimkes B. Apophyseolysis of the greater trochanter through excessive sports: a case report. Am J Sports Med 2011; 39 (01) 195-198
• 50 Oskoui M, Coutinho F, Dykeman J, Jetté N, Pringsheim T. An update on the prevalence of cerebral palsy: a systematic review and meta-analysis. Dev Med Child Neurol 2013; 55 (06) 509-519
• 51 Robin J, Graham HK, Selber P, Dobson F, Smith K, Baker R. Proximal femoral geometry in cerebral palsy: a population-based cross-sectional study. J Bone Joint Surg Br 2008; 90 (10) 1372-1379
• 52 Larnert P, Risto O, Hägglund G, Wagner P. Hip displacement in relation to age and gross motor function in children with cerebral palsy. J Child Orthop 2014; 8 (02) 129-134
• 53 Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997; 39 (04) 214-223
• 54 El-Sobky TA, Fayyad TA, Kotb AM, Kaldas B. Bony reconstruction of hip in cerebral palsy children Gross Motor Function Classification System levels III to V: a systematic review. J Pediatr Orthop B 2018; 27 (03) 221-230
• 55 Heimkes B, Stotz S, Heid T. Pathogenesis and prevention of spastic hip dislocation [in German]. Z Orthop Ihre Grenzgeb 1992; 130 (05) 413-418
• 56 Heimkes B, Martignoni K, Utzschneider S, Stotz S. Soft tissue release of the spastic hip by psoas-rectus transfer and adductor tenotomy for long-term functional improvement and prevention of hip dislocation. J Pediatr Orthop B 2011; 20 (04) 212-221
• 57 Mockford M, Caulton JM. The pathophysiological basis of weakness in children with cerebral palsy. Pediatr Phys Ther 2010; 22 (02) 222-233
• 58 Reimers J. The stability of the hip in children. A radiological study of the results of muscle surgery in cerebral palsy. Acta Orthop Scand Suppl 1980; 184: 1-100
• 59 Langenskiöld A, Salenius P. Epiphyseodesis of the greater trochanter. Acta Orthop Scand 1967; 38 (02) 199-219
• 60 Schneidmueller D, Carstens C, Thomsen M. Surgical treatment of overgrowth of the greater trochanter in children and adolescents. J Pediatr Orthop 2006; 26 (04) 486-490
• 61 Günther CMJ, Komm M, Jansson V, Heimkes B. Midterm results after subtrochanteric end-to-side valgization osteotomy in severe infantile coxa vara. J Pediatr Orthop 2013; 33 (04) 353-360
• 62 Heimkes B, Komm M, Melcher C. Subtrochanteric end-to-side valgus osteotomy for severe infantile coxa vara [in German]. Oper Orthop Traumatol 2009; 21 (01) 97-111
• 63 Eilert RE, Hill K, Bach J. Greater trochanteric transfer for the treatment of coxa brevis. Clin Orthop Relat Res 2005; (434) 92-101
• 64 Hefti F, Morscher E. The femoral neck lengthening osteotomy. Orthop Traumatol 1993; 2 (03) 144-151
• 65 Viernstein K, Rosemeyer B, Henning A. Eine Möglichkeit zur operativen Therapie der primären Protrusio acetabuli. Arch Orthop Traumatol 1970; 67: 291-302
• 66 Leunig M, Nho SJ, Turchetto L, Ganz R. Protrusio acetabuli: new insights and experience with joint preservation. Clin Orthop Relat Res 2009; 467 (09) 2241-2250
• 67 Heimkes B, Schmidutz F, Rösner J, Frimberger V, Weber P. Modified Salter innominate osteotomy in adults [in German]. Oper Orthop Traumatol 2018; 30 (06) 457-468
• 68 Stem ES, O'Connor MI, Kransdorf MJ, Crook J. Computed tomography analysis of acetabular anteversion and abduction. Skeletal Radiol 2006; 35 (06) 385-389
• 69 Werner CML, Ramseier LE, Ruckstuhl T. , et al. Normal values of Wiberg's lateral center-edge angle and Lequesne's acetabular index—a coxometric update. Skeletal Radiol 2012; 41 (10) 1273-1278
• 70 Crockarell Jr JR, Trousdale RT, Guyton JL. The anterior centre-edge angle. A cadaver study. J Bone Joint Surg Br 2000; 82 (04) 532-534
• 71 Siebenrock KA, Wahab KHA, Werlen S, Kalhor M, Leunig M, Ganz R. Abnormal extension of the femoral head epiphysis as a cause of cam impingement. Clin Orthop Relat Res 2004; (418) 54-60
• 72 Lütken P. Bone-bridge formation between the greater trochanter and the femoral head: a normal variation of the pattern of the ossification in the upper end of the femur in adolescence. Acta Orthop Scand 1961; 31: 209-215
• 73 Struijs PAA, Oostra RJ, van Rijn RR, Besselaar PP. Abnormal growth of the proximal femur due to apophyseal-epiphyseal coalescence resulting in coxa valga—a report of two cases in adolescents. Acta Orthop 2011; 82 (04) 507-509
• 74 Murray RO, Duncan C. Athletic activity in adolescence as an etiological factor in degenerative hip disease. J Bone Joint Surg Br 1971; 53 (03) 406-419
• 75 Agricola R, Heijboer M, Ginai AZ. , et al. A cam deformity is gradually acquired during skeletal maturation in adolescent and young male soccer players. Am J Sports Med 2014; 4: 798-806
• 76 Klit J, Gosvig K, Magnussen E. , et al. Cam deformity and hip degeneration are common after fixation of a slipped capital femoral epiphysis. Acta Orthop 2014; 85 (06) 585-591
• 77 Loder RT. Controversies in slipped capital femoral epiphysis. Orthop Clin North Am 2006; 37 (02) 211-221 , vii