Study of femoral torsion during prenatal growth: Interpretations associated with the effects of intrauterine pressure

American Journal of Physical Anthropology

Volumn 145, Issue 3, 2011, Pages 438-445

  Bonneau, Noémie ^a   Simonis, Caroline ^a   Seringe, Raphaël ^b   Tardieu, Christine ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b HÔPITAL SAINT VINCENT DE PAUL   (France)

Author keywords

biomechanics; epigenetic; Homo sapiens; proximal femur

Indexed keywords

ARTICLE; BIOMECHANICS; BIRTH; BONE REMODELING; COMPARATIVE STUDY; EPIGENETICS; FEMUR; FETUS; FETUS DEVELOPMENT; GENETICS; HUMAN; INTRAUTERINE PRESSURE; LEG; PELVIS; PLASTICITY; PRENATAL GROWTH; PRENATAL PERIOD; SKELETON; TORSION; UTERUS;

BIOMECHANICS; EPIGENESIS, GENETIC; FEMALE; FEMUR; FETAL DEVELOPMENT; HUMANS; INFANT, NEWBORN; LINEAR MODELS; MALE; PREGNANCY; PRESSURE; SKELETON; TORSION, MECHANICAL; UTERUS;

EID: 79959310253     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.21521     Document Type: Article

References (88)

1. Abitbol MM,. 1987. Evolution of the lumbosacral angle. Am J Phys Anthropol 72: 361-372. (Pubitemid 17037268)
2. Abitbol MM,. 1993. Growth of the fetus in the abdominal cavity. Am J Phys Anthropol 91: 367-378. (Pubitemid 23180386)
3. Adalian P,. 2002. Nouvelle formule de détermination de l'âge d'un ftus. C R Biol 325: 261-269.
4. Altmann F,. 1924. Untersuchungen über die torsio femoris. Zeit Anat Entwick 75: 82-126.
5. Amtman E,. 1979. Biomechanical interpretation of form and structure of bones: role of genetics and function in growth and remodelling. In:, Morbeck ME, Preuschoft H, Gomberg N, editors. Environment, behaviour and morphology: dynamic interactions in primates. New York: Gustav Fischer. p 347-401.
6. Arkin AL, Katz JF,. 1956. The effects of pressure on epiphyseal growth: the mechanism of plasticity of growing bone. J Bone Joint Surg Am 38: 1056-1076.
7. Benson-Martin J, Zammaretti P, Bilic G, Schweizer T, Portmann-Lanz B, Burkhardt T, Zimmermenn R, Ochsenbein-Kölble N,. 2006. The Young's modulus of fetal preterm and term amniotic membranes. Eur J Obstet Gynecol Reprod Biol 128: 103-107. (Pubitemid 44311334)
8. Carter DR, Beaupré GS,. 2001. Skeletal function and form: mechanobiology of skeletal development, aging and regeneration. Cambridge: Cambridge University Press.
9. Carter DR, Orr TE,. 1992. Skeletal development and bone functional adaptation. J Bone Miner Res 7: S389-S395. (Pubitemid 23020197)
10. Carter DR, van der Meulen MCH, Beaupré GS,. 1996. Mechanical factors in bone growth and development. Bone 18: 5S-10S. (Pubitemid 26047537)
11. Carter DR, Wong M,. 1988. Mechanical stresses and endochondral ossification in the chondroepiphysis. J Orthop Res 6: 148-154. (Pubitemid 18010244)
12. Chamay A, Tschantz P,. 1972. Mechanical influence in bone remodelling. Experimental research on Wolff's law. J Biomech 5: 173-180.
13. Clavert JM,. 1987. Développement de la hanche embryonnaire et foetale. In: La hanche pédiatrique actualité. Paris: Masson Ed. p 1-7.
14. Cowgill LW,. 2010. The ontogeny of Holocene and late Pleistocene human postcranial strength. Am J Phys Anthropol 141: 16-37.
15. Cowgill LW, Hager LD,. 2007. Variation in the development of postcranial robusticity: an example from Çatalhöyük, Turkey. Int J Osteoarchaeol 17: 235-252.
16. Crane L,. 1959. Femoral torsion and its relation to toeing-in and toeing-out. J Bone Joint Surg Am 41: 421-428.
17. de Vries JIP, Visser GHA, Prechtl HFR,. 1982. The emergence of fetal behaviour. I. Qualitative aspects. Early Hum Dev 7: 301-322. (Pubitemid 13188242)
18. de Vries JIP, Visser GHA, Prechtl HFR,. 1984. Fetal mobility in the first half of pregnancy. In:, Prechtl HFR, editor. Continuity of neural functions from prenatal from postnatal life. Cambridge: Cambridge University Press. p 46-64.
19. Dunlap K, Shands AR, Hollister LC, Gaul JS, Streit HA,. 1953. A new method for determination of torsion of the femur. JBone Joint Surg 35: 289-311.
20. Dunn PM,. 1999. John Braxton Hicks (1823-97) and painless uterine contractions. Arch Dis Child Fetal Neonatal Ed 81: F157-F158.
21. Frost HM,. 1982. Mechanical determinants of bone modelling. Metab Bone Dis 4: 217-229.
22. Frost HM,. 2004. A 2003 update of bone physiology and Wolff's law for clinicians. Angle Orthod 74: 3-15. (Pubitemid 38968834)
23. Gomez C, David V, Peet NM, Vico L, Chenu C, Malaval L, Skerry TM,. 2007. Absence of mechanical loading in utero influences bone mass and architecture but not innervation in Myod-Myf5-deficient mice. J Anat 210: 259-271. (Pubitemid 46344563)
24. Guilhard-Costa AM, Droullé P, Larroche JC,. 1991. Growth velocity of the biparietal diameter, abdominal diameter and femur length in the fetal period. Early Hum Dev 27: 93-102.
25. Hadlock FP, Harrist RB, Deter RL, Park SK,. 1982. Fetal femur length as a predictor of menstrual age: sonographically measured. Am J Roentgenol 138: 875-878. (Pubitemid 12117584)
26. Hall BK,. 1972. Immobilization and cartilage transformation into bone in the embryonic chick. Anat Rec 173: 391-404.
27. Hall BK, Herring SW,. 1990. Paralysis and growth of the musculoskeletal system in the embryonic chick. J Morphol 206: 45-56. (Pubitemid 20343412)
28. Heimkes B, Posel P, Plitz W, Jansson V,. 1993. Forces acting on the juvenile hip joint in the one-legged stance. J Pediatr Orthop 13: 431-436. (Pubitemid 23174649)
29. Henderson JH, Carter DR,. 2002. Mechanical induction in limb morphogenesis: the role of growth-generated strains and pressures. Bone 31: 645-653. (Pubitemid 36092086)
30. Hicks JB,. 1871. On the contractions of the uterus throughout pregnancy: their physiological effects and their value in the diagnosis of pregnancy. Trans Obstet Soc Lond 13: 216-231.
31. Hieber AD, Corcino D, Motosue J, Sandberg LB, Roos PJ, Yeh Yu S, Csiszar K, Kagan HM, Boyd CD, Bryant-Greenwood GD,. 1997. Detection of elastin in the human fetal membranes: proposed molecular basis for elasticity. Placenta 18: 301-312. (Pubitemid 27214234)
32. Ingber BE,. 1998. Cellular basis of mechanotransduction. Biol Bull 194: 323-327.
33. Jabareen M, Mallik AS, Bilic G, Zisch AH, Mazza E,. 2009. Relation between mechanical properties and microstructure of human fetal membranes: an attempt towards a quantitative analysis. Eur J Obstet Gynecol Reprod Biol 144: S134-S141.
34. Jouve JL, Glard Y, Garron E, Piercecchi MD, Dutour O, Tardieu C, Bollini G,. 2005. Anatomical study of proximal femur in the foetus. J Pediatr Orthop B 14: 105-110. (Pubitemid 40328212)
35. Kember NF, Sissons HA,. 1976. Quantitative histology of the human growth plate. J Bone Joint Surg Br 58: 426-435.
36. Kingsley PC, Olmsted KL,. 1948. A study to determine the angle of anteversion of the neck of the femur. J Bone Joint Surg Am 30: 745-751.
37. Kiss MZ, Hobson MA, Varghese T, Harter J, Kliewer MA, Hartenbach EM, Zagzebski JA,. 2006. Frequency-dependent complex modulus of the uterus: preliminary results. Phys Med Biol 51: 3683-3695. (Pubitemid 44131358)
38. Le Damany P,. 1903. Les torsions osseuses: leur rôle dans la transformation des membres. J Anat Physiol 39: 126-165,313-337,426-450,534-545.
39. Le Damany P,. 1905. L'adaptation de l'homme à la station debout. J Anat Physiol 41: 133-170.
40. Le Damany P,. 1906. Les torsions osseuses où se font-elles? note complétementaires. J Anat Physiol 42: 293-296.
41. Liebermann DE, Devlin MJ, Pearson M,. 2001. Articular area responses to mechanical loading: effects of exercise, age and skeletal location. Am J Phys Anthropol 116: 266-277. (Pubitemid 33104496)
42. Lovejoy CO,. 2005. The natural history of human gait and posture, Part 2: hip and thigh. Gait Posture 21: 113-124. (Pubitemid 41569258)
43. Lovejoy CO, Cohn MJ, White TD,. 1999. Morphological analysis of the mammalian postcranium: a development perspective. Proc Natl Acad Sci USA 96: 13247-13252.
44. Macchiarelli R, Bondioli L, Galichon V, Tobias PV,. 1999. Hip bone trabecular architecture shows uniquely distinctive locomotor behaviour in South African australopithecines. J Hum Evol 36: 211-232. (Pubitemid 29181983)
45. Martin RB,. 2000. Toward a unifying theory of bone remodelling. Bone 26: 1-6.
46. Mikulicz J,. 1878. Über die individuellen Formdifferenzen am femur und an der Tibia des Menschen. Arch Anat Physiol 1: S351-S404.
47. Morland MS,. 1980. Morphological effects of torsion applied to growing bone. J Bone Joint Surg Br 62: 230-237.
48. Nuzzo S, Meneghini C, Braillon P, Bouvier R, Mobilio S, Peyrin F,. 2003. Microarchitectural and physical changes during fetal growth in human vertebral bone. J Bone Miner Res 18: 760-768. (Pubitemid 36903246)
49. Pearson OM, Lieberman DE,. 2004. The aging of Wolff's "law": ontogeny and responses to mechanical loading in cortical bone. Yearb Phys Anthropol 47: 68-99.
50. Peyrin F, Boivin G, Braillon P,. 2005. Bone microarchitecture in human fetuses. Clin Cases Miner Bone Metab 2: 150-157. (Pubitemid 41681054)
51. Pitsillides AA,. 2006. Early effects of embryonic movement: 'a shot out of the dark.' J Anat 208: 417-431.
52. Pous JG, Dimeglio A, Baldet P, Bonnel F,. 1980. Cartilage de conjugaison et croissance. Notions fondamentales en orthopédie. Paris: Doin Ed.
53. Preuschoff H, Hayama S, Günther MM,. 1988. Curvature of the lumbar spine as a consequence of mechanical necessities in Japanese macaques trained for bipedalism. Folia Primatol 50: 42-58.
54. R Development Core Team. 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL.
55. Rigaud A, Bonjean P, Buchet C, Rideau Y,. 1965. Tibial torsion and femoral torsion. Arch Anat Pathol 13: 111-113.
56. Roberts WH,. 1962. Femoral torsion in normal human development and as related to dysplasia. Anat Rec 143: 369-375.
57. Rodíguez JI, Garía-Alix A, Palacios J, Paniagua R,. 1988b. Changes in the long bones due to fetal immobility caused by neuromuscular disease. A radiographic and histological study. J Bone Joint Surg Am 70: 1052-1060.
58. Rodríguez JI, Palacios J, Garía-Alix A, Pastor I, Paniagua R,. 1988a. Effects of immobilization on fetal bone development. A morphometric study in newborns with congenital diseases with intrauterine onset. Calcif Tissue Int 43: 335-339. (Pubitemid 19006479)
59. Roodenburg PJ, Wladimiroff JW, van Es A, Prechtl HFR,. 1991. Classification and quantitative aspects of fetal movements during the second half of normal pregnancy. Early Hum Dev 25: 19-35.
60. Ruff C,. 2003a. Ontogenetic adaptation to bipedalism: age changes in femoral to humeral length and strength proportions in humans, with a comparison to baboons. J Hum Evol 45: 317-349. (Pubitemid 37388385)
61. Ruff C,. 2003b. Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 33: 317-329. (Pubitemid 37103248)
62. Ruff C, Holt B, Trinkaus E,. 2006. Who's afraid of big bad Wolff?: "Wolff's law" and bone functional adaptation. Am J Phys Anthropol 129: 484-498.
63. Ruff CB, Walker A, Trinkaus E,. 1994. Postcranial robusticity in Homo. III. Ontogeny. Am J Phys Anthropol 93: 35-54. (Pubitemid 24020097)
64. Ruimerman R, Hilbers P, van Rietbergen B, Huiskes R,. 2005. A theoretical framework for strain-related trabecular bone maintenance and adaptation. J Biomech 38: 931-941. (Pubitemid 40248478)
65. Ryan TM, Krovitz GE,. 2006. Trabecular bone ontogeny in the human proximal femur. J Hum Evol 51: 591-602. (Pubitemid 44688976)
66. Salle BL, Rauch F, Travers R, Bouvier R, Glorieux FH,. 2002. Human fetal bone development: histomorphometric evaluation of the proximal femoral metaphysic. Bone 30: 823-828. (Pubitemid 34616008)
67. Seringe R,. 1998. Dysplasie et luxation congénitale de la hanche. In: Encyclopédie Médico-Chirurgicale. Paris: Elsevier.
68. Seringe R, Cressaty J, Girard B, Francoual C,. 1981. L'examen orthopédique de 1500 nouveau-nés en maternité. Chir Pédiat 22: 365-387. (Pubitemid 12178460)
69. Seringe R, Kharrat K,. 1982. Dysplasie et luxation congénitale de la hanche. Anatomie pathologique chez le nouveau-né et le nourrisson. Rev Chir Orthop Reparatrice Appar Mot 68: 145-160. (Pubitemid 12121947)
70. Shands AR, Steele MK,. 1958. Torsion of the femur: a follow-up report on the use of the Dunlap method for its determination. J Bone Joint Surg Am 40: 803-816.
71. Shefelbine S, Tardieu C, Carter DR,. 2001. Mechanobiology in the evolution and development of the human bicondylar angle. Am J Phys Anthrop Suppl 36: 136-145.
72. Skedros JG, Hunt KJ, Bloebaum RD,. 2004. Relationships of loading history and structural and material characteristics of bone: development of the mule deer calcaneus. J Morphol 259: 281-307. (Pubitemid 38319058)
73. Skuban TP, Vogel T, Baur-Melnyk A, Jansson V, Heimkes B,. 2009. Function-orientation structural analysis of the proximal human femur. Cells Tissues Organs 190: 247-255.
74. Staheli LT, Corbett M, Wyss C, King H,. 1985. Lower-extremity rotational problems in children. Normal values to guide management. J Bone Joint Surg Am 67: 38-47.
75. Staheli LT, Duncan WR, Schaefer E,. 1968. Growth alteration in the hemiplegic child. A study of femoral anteversion, neck-shaft angle, hip rotation, C.E. angle, limb length and circumference in 50 hemiplegic children. Clin Orthop 60: 205-212.
76. Sumner DR, Andriacchi TP,. 1996. Adaptation to differential loading: comparison of growth-related changes in cross-sectional properties of the human femur and humerus. Bone 19: 121-126. (Pubitemid 26283225)
77. Tardieu C, Glard Y, Garron E, Boulay C, Jouve JL, Dutour O, Boetsch G, Bollini G,. 2006. Relationship between formation of the femoral bicondylar angle and trochlear shape: independence of diaphyseal and epiphyseal growth. Am J Phys Anthrop 130: 491-500. (Pubitemid 44099967)
78. Tardieu C, Trinkaus E,. 1994. Early ontogeny of the human femoral bicondylar angle. Am J Phys Anthrop 95: 183-195. (Pubitemid 24299027)
79. Tayton E,. 2007. Femoral anteversion. A necessary angle or an evolutionary vestige? J Bone Joint Surg Br 89: 1283-1288.
80. Thame M, Osmond C, Bennett F, Wilks R, Forrester T,. 2004. Fetal growth is directly related to maternal anthropometry and placental volume. Eur J Clin Nutr 58: 894-900. (Pubitemid 38923188)
81. Thiebeaugeorges O, Pineau JC, Guihard-Costa AM,. 2006. Optimal growth standards in fetuses: to each biometric variable its fitting model. Fetal Diagn Ther 21: 396-399.
82. Upadhyay SS, Burwell RG, Moulton A, Small PG, Wallace WA,. 1990. Femoral anteversion in healthy children. Application of a new method using ultrasound. J Anat 169: 49-61. (Pubitemid 20136600)
83. Van der Meulen MCH, Huiskes R,. 2002. Why mechanobiology? A survey article. J Biomech 35: 401-414. (Pubitemid 34273633)
84. Volpato V, Viola TB, Nakatsukasa M, Bondiolo L, Macchiarelli R,. 2008. Textural characteristics of iliac-femoral trabecular pattern in a bipedally trained Japanese macaque. Primates 49: 16-25.
85. von Lanz T, Mayet A,. 1953. Die gelenkorper des menschlichen hufgelenkes in der progredienten phase iherer unwegigen ausformung. Z Anat 117: 317-345.
86. Waddington CH,. 1942. Canalization of development and the inheritance of acquired characters. Nature 150: 563-565.
87. Watanabe RS,. 1974. Embryology of the human hip. Rev Chir Orthop Reparatrice Appar Mot 98: 8-26.
88. Wolff J,. 1892. Das gresetz der transformation der knochen. Berlin: Hirschwald.