Ontogenetic changes in femoral cross-sectional geometry during childhood locomotor development.

OBJECTIVES The femur is a major weight-bearing bone that is variably loaded throughout growth as children transition through locomotory states prior to the attainment of a mature bipedal gait. Here, we document ontogenetic trends in femoral cross-sectional geometry (CSG) and explore how changes in loading regime may impact the structural arrangement of cortical bone along the length of the developing diaphysis. MATERIALS AND METHODS Micro-CT scans of 110 immature femora were generated from a documented archaeological sample ranging in age from birth to 8.5 years old. CSG properties indicative of relative bone strength and bending rigidity were analyzed from cross-sections extracted at 35%, 50% and 65% of total intermetaphyseal length. RESULTS Infants experience a marked redistribution of cortical bone between birth and 7 months facilitating a more advantageous mechanical structure for early load bearing behaviors as bone is displaced further from the section centroid. Early walkers are characterized by a mediolaterally reinforced cross-section that becomes more circular as gait continues to develop. DISCUSSION During ontogeny the femur undergoes distinct morphological phases, which correspond with changes in loading regime. This study illustrates the importance of loading conditions in shaping immature bone morphology. Nonmechanical factors such as changes in hormonal environmental can also impact on this dynamic.

[1]  Ann Hallemans,et al.  Changes in 3D joint dynamics during the first 5 months after the onset of independent walking: a longitudinal follow-up study. , 2006, Gait & posture.

[2]  V. Muggeo.  Estimating regression models with unknown break‐points , 2003, Statistics in medicine.

[3]  T. Andriacchi,et al.  Adaptation to differential loading: comparison of growth-related changes in cross-sectional properties of the human femur and humerus. , 1996, Bone.

[4]  A. Tardón,et al.  Circulating 25-Hydroxyvitamin D3 in Pregnancy and Infant Neuropsychological Development , 2012, Pediatrics.

[5]  B. Vereijken,et al.  Early independent walking: a longitudinal study of load perturbation effects. , 2009, Developmental psychobiology.

[6]  W. Hayes,et al.  Cross-sectional geometry of Pecos Pueblo femora and tibiae--a biomechanical investigation: I. Method and general patterns of variation. , 1983, American journal of physical anthropology.

[7]  C. Tardieu,et al.  Evolution of the angle of obliquity of the femoral diaphysis during growth — correlations , 1997, Surgical and Radiologic Anatomy.

[8]  Robert E Black,et al.  Iron and zinc supplementation promote motor development and exploratory behavior among Bangladeshi infants. , 2004, The American journal of clinical nutrition.

[9]  S. Black,et al.  Development of the fetal ilium – challenging concepts of bipedality , 2009, Journal of anatomy.

[10]  Karen E Adolph,et al.  Baby carriage: infants walking with loads. , 2007, Child development.

[11]  Eckhard Schoenau,et al.  The Developing Bone: Slave or Master of Its Cells and Molecules? , 2001, Pediatric Research.

[12]  E. Thelen,et al.  The relationship between physical growth and a newborn reflex , 1984 .

[13]  C. Ruff.  Biomechanical Analyses of Archaeological Human Skeletons , 2007 .

[14]  Libby W Cowgill,et al.  Biomechanical implications of the onset of walking. , 2018, Journal of human evolution.

[15]  R. Rizzoli,et al.  Peak Bone Mass and Its Regulation , 2012 .

[16]  Blandine Bril,et al.  Posture and independent locomotion in early childhood: Learning to walk or learning dynamic postural control? , 1993 .

[17]  D. Strait,et al.  Finite element analysis of a femur to deconstruct the paradox of bone curvature. , 2014, Journal of theoretical biology.

[18]  K. Robson Brown,et al.  Early Trabecular Development in Human Vertebrae: Overproduction, Constructive Regression, and Refinement , 2015, Front. Endocrinol..

[19]  R. Ketcham,et al.  Patterns in ontogeny of human trabecular bone from SunWatch Village in the Prehistoric Ohio Valley: general features of microarchitectural change. , 2009, American journal of physical anthropology.

[20]  M. Onis.  WHO Motor Development Study: Windows of achievement for six gross motor development milestones , 2006, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[21]  E. Seeman,et al.  Skeletal Growth in Males , 2010 .

[22]  M. Brickley,et al.  Chapter 2 – The Study of Metabolic Bone Disease in Bioarchaeology , 2008 .

[23]  Cara Ocobock,et al.  Waddling and toddling: the biomechanical effects of an immature gait. , 2010, American journal of physical anthropology.

[24]  J. Stock,et al.  Which measures of diaphyseal robusticity are robust? A comparison of external methods of quantifying the strength of long bone diaphyses to cross-sectional geometric properties. , 2007, American journal of physical anthropology.

[25]  M. Jaffe,et al.  The Motor Development of Fat Babies , 1982, Clinical pediatrics.

[26]  M L Mendelsohn,et al.  THE ANALYSIS OF CELL IMAGES * , 1966, Annals of the New York Academy of Sciences.

[27]  M. McGraw.  Neuromuscular development of the human infant as exemplified in the achievement of erect locomotion , 1940 .

[28]  Beatrix Vereijken,et al.  What changes in infant walking and why. , 2003, Child development.

[29]  G. Krovitz,et al.  Trabecular bone ontogeny in the human proximal femur. , 2006, Journal of human evolution.

[30]  Christopher Ruff,et al.  Ontogenetic adaptation to bipedalism: age changes in femoral to humeral length and strength proportions in humans, with a comparison to baboons. , 2003, Journal of human evolution.

[31]  B. Hopkins,et al.  Maternal handling and motor development: an intracultural study. , 1988, Genetic, social, and general psychology monographs.

[32]  L. Shapiro,et al.  Developments in development: What have we learned from primate locomotor ontogeny? , 2018, American journal of physical anthropology.

[33]  M. Djuric,et al.  Region-dependent patterns of trabecular bone growth in the human proximal femur: A study of 3D bone microarchitecture from early postnatal to late childhood period. , 2017, American journal of physical anthropology.

[34]  C. Tardieu,et al.  Evolution of the angle of obliquity of the femoral diaphysis during growth - Correlations , 1997, Surgical and Radiologic Anatomy.

[35]  F. Rauch,et al.  Changes in Bone Density During Childhood and Adolescence: An Approach Based on Bone's Biological Organization , 2001, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[36]  S. Mays,et al.  Dry-bone manifestations of rickets in infancy and early childhood , 1998 .

[37]  V. Sládek,et al.  Effect of deriving periosteal and endosteal contours from microCT scans on computation of cross‐sectional properties in non‐adults: the femur , 2018, Journal of anatomy.

[38]  Timothy M. Ryan,et al.  An ontogenetic framework linking locomotion and trabecular bone architecture with applications for reconstructing hominin life history. , 2015, Journal of human evolution.

[39]  M. G. Belcastro,et al.  Trabecular Analysis of the Distal Radial Metaphysis during the Acquisition of Crawling and Bipedal Walking in Childhood: A Preliminary Study , 2019, Bulletins et Mémoires de la Société d'Anthropologie de Paris.

[40]  J. Golding,et al.  Does the Supine Sleeping Position Have Any Adverse Effects on the Child? II. Development in the First 18 Months , 1998, Pediatrics.

[41]  Ann Hallemans,et al.  Mechanical energy in toddler gait A trade-off between economy and stability? , 2004, Journal of Experimental Biology.

[42]  H. Forssberg.  Ontogeny of human locomotor control I. Infant stepping, supported locomotion and transition to independent locomotion , 2004, Experimental Brain Research.

[43]  D. Lieberman,et al.  Articular area responses to mechanical loading: effects of exercise, age, and skeletal location. , 2001, American journal of physical anthropology.

[44]  Amy S. Joh,et al.  Motor development: How infants get into the act , 2006 .

[45]  E. Thelen,et al.  Newborn stepping: An explanation for a "disappearing" reflex. , 1982 .

[46]  Lois Bly,et al.  Motor Skills Acquisition in the First Year: An Illustrated Guide to Normal Development , 1994 .

[47]  P. Aerts,et al.  Pressure Distribution Patterns under the Feet of New Walkers: The First Two Months of Independent Walking , 2003, Foot & ankle international.

[48]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[49]  J. Clement,et al.  Ontogenetic Patterning of Cortical Bone Microstructure and Geometry at the Human Mid‐Shaft Femur , 2009, Anatomical record.

[50]  D. Sutherland,et al.  The Development of Mature Gait , 1997 .

[51]  K. Adolph,et al.  Learning to crawl. , 1998, Child development.

[52]  H. Sigmundsson,et al.  Exploring Task-Specific Independent Standing in 3- to 5-Month-Old Infants , 2017, Front. Psychol..

[53]  L. Adair,et al.  Infant overweight is associated with delayed motor development. , 2010, The Journal of pediatrics.

[54]  R. Ives.  Insights into Health , Life and Death in Victorian London ’ s East End , 2015 .

[55]  H. Goldman,et al.  Birth is but our death begun: a bioarchaeological assessment of skeletal emaciation in immature human skeletons in the context of environmental, social, and subsistence transition. , 2014, American journal of physical anthropology.

[56]  Anthony C. Jones,et al.  Construction of the Femoral Neck During Growth Determines Its Strength in Old Age , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[57]  C. Shaw,et al.  Development of Cortical Bone Geometry in the Human Femoral and Tibial Diaphysis , 2013, Anatomical record.

[58]  M. Djuric,et al.  Morphological characteristics of the developing proximal femur: a biomechanical perspective. , 2012, Srpski arhiv za celokupno lekarstvo.

[59]  N. Kaciroti,et al.  Motor development in 9-month-old infants in relation to cultural differences and iron status. , 2011, Developmental psychobiology.

[60]  J. Stock,et al.  Baby steps towards linking calcaneal trabecular bone ontogeny and the development of bipedal human gait , 2019, Journal of anatomy.

[61]  Ann Hallemans,et al.  Changes in foot-function parameters during the first 5 months after the onset of independent walking: a longitudinal follow-up study. , 2006, Gait & posture.

[62]  E. Gibson,et al.  Going Somewhere: An Ecological and Experimental Approach to Development of Mobility , 1989 .

[63]  C. Super.  Environmental Effects on Motor Development: the Case of ‘African Infant Precocity’ , 1976, Developmental medicine and child neurology.

[64]  D. Lieberman,et al.  Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs , 2003, Journal of Experimental Biology.

[65]  S. Mays,et al.  The Bioarchaeology of Metabolic Bone Disease , 2020 .

[66]  O. Pearson,et al.  The importance of accounting for the area of the medullary cavity in cross-sectional geometry: A test based on the femoral midshaft. , 2010, American journal of physical anthropology.

[67]  J. Jensen,et al.  Ontogenetic changes in foot strike pattern and calcaneal loading during walking in young children. , 2018, Gait & posture.

[68]  R Huiskes,et al.  On the modelling of long bones in structural analyses. , 1982, Journal of biomechanics.

[69]  R. Moon,et al.  Effects of Sleep Position on Infant Motor Development , 1998, Pediatrics.

[70]  S. Mays,et al.  Skeletal manifestations of rickets in infants and young children in a historic population from England. , 2006, American journal of physical anthropology.

[71]  E Trinkaus,et al.  Early ontogeny of the human femoral bicondylar angle. , 1994, American journal of physical anthropology.

[72]  C. Kovacs.  Calcium, phosphorus, and bone metabolism in the fetus and newborn. , 2015, Early human development.

[73]  A. W. Trettien.  Creeping and Walking , 1900 .

[74]  E. Thelen,et al.  Hidden skills: a dynamic systems analysis of treadmill stepping during the first year. , 1991, Monographs of the Society for Research in Child Development.

[75]  Jesse M. Lingeman,et al.  Go naked: diapers affect infant walking. , 2012, Developmental science.

[76]  Christopher Ruff,et al.  Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. , 2003, Bone.

[77]  J. Gosman,et al.  Skeletal biology over the life span: a view from the surfaces. , 2011, American journal of physical anthropology.

[78]  F. Lacquaniti,et al.  Development of pendulum mechanism and kinematic coordination from the first unsupported steps in toddlers , 2004, Journal of Experimental Biology.