The goal of this research is to study trabecular bone microarchitecture during growth and development, producing new quantitative and structural knowledge about the development and remodeling of normal trabecular structure as demonstrated in a subadult archaeological skeletal sample from the Late Prehistoric Ohio Valley. Cancellous bone microarchitecture has a predictable relationship to functional and external loading patterns applied throughout ontogeny and maturity. This factor makes it potentially attractive for the bioarchaeological study of long-term loading history reflecting physical activity and human behavior combined with growth and development. Relatively little research has been directed toward the structure of and variation in trabecular bone during ontogeny, creating a deficiency in the foundation upon which trabecular bone adaptation can be used bioarchaeological inferences. This research project tests hypotheses characterizing the temporal sequence and variation in trabecular bone volume fraction and degree of anisotropy as a reflection of growth and development, as associated with the timing and acquisition of normal functional activities (crawling, initial bipedal gait, and independent physical activities), and as associated with changing body mass.

    The Late Prehistoric archaeological site SunWatch (33-My-57) is a Fort Ancient village on the floodplain of the Great Miami River in Dayton, Ohio. Excavations have demonstrated a circular, organized, agricultural settlement characterized by a central plaza with a central post complex and concentric rings of burials, storage/trash pits, and wattle and daub, thatch-roofed houses.  A skeletal sample of 40 subadult proximal tibiae has been selected from 109 subadult skeletons based on preservation, absence of pathological conditions, and dental developmental stages. Four age groupings are used (0.0 –24 years). Analysis consists of nondestructive microCT scanning of the proximal metaphyseal tibia demonstrating the microarchitectural trabecular structure; quantitative 3-D structural analyses using finite element modeling will develop structural parameters (bone volume fraction BV/TV and degree of anisotropy DA). The expectations of this study are to provide quantitative morphological and scan-image data on sequential ontogenetic changes in human trabecular bone structure in a single archaeological skeletal sample from the Late Prehistoric Ohio Valley, highlighting the dynamic relationships between growth/development, general functional activities, and trabecular distribution/architecture.

    Initial data consist of proof-of-method test scans performed on two subadult tibial samples of differing ages from an Ohio Late Prehistoric population. The proximal tibiae were scanned with the HRXCT scanner at the CT/UT (University of Texas at Austin) facility and structural analysis (Quant3D) performed; distinct differences in BV/TV and DA are observed. The results are demonstrated in figures 1-4: Figures 1 and 2- (sample 409, 4 y/o), thin relatively densely-packed trabeculae (higher BV/TV = 0.45) and two planar orientation (low DA) the strongest being closer to superior- inferior; Figures 3 and 4- (sample 401, 8 y/o), thicker, but relatively less dense (lower BV/TV= 0.24), more aligned trabeculae in a predominantly anterior-posterior orientation (higher DA). These scans indicate that age-related changes in trabecular bone volume and anisotropy from subadult archaeological remains can be demonstrated by the proposed methodology and that a temporal sequence of ontogenetic trabecular morphological change, based on scan data, can be quantified.

 

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Figure 1: Scan slice just distal to proximal epiphyseal plate.
 

 

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Figure 2: Quant3D representing multi-planar trabecular orientation.

 

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Figure 3: Scan slice just distal to proximal epiphyseal plate.

 

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Figure 4: Quant3D representing anisotropic anterior-posterior aligned trabeculae.
 

    This study represents a natural experiment of human ontogeny, mechanical loading, and trabecular bone. The intellectual merit centers on the potential of using recent advances in mechanobiological modeling, non-invasive micro-imaging techniques, and finite element computational methodologies to advance understanding of socially structured human behavior, environmental influences, and skeletal response during ontogeny in ancient subadult populations. While this study is focused on the problem of ontogenetic changes in trabecular bone, the applicability of the project design can form the foundation for expanded comparative studies in physical anthropology, skeletal biology, growth and development, and bioarchaeology.

    Cancellous bone analysis is situated within the broad framework of research in musculoskeletal biology with society-wide implications in the areas of skeletal adaptation in varying genetic and environmental settings, serious public health conditions (osteoarthritis and osteoporosis), and skeletal regenerative and implant investigations. This study enhances the infrastructure of research by incorporating recent technological and methodological advances, fostering a multidisciplinary approach towards understanding skeletal biology, and augmenting relevance to biocultural studies of ancient and recent populations.

Related References

Abel TJ, Koralewski JM, and DeMuth GB (2000) Cemetery Ridge: An Early Village Site Located in Sandusky County, Ohio. In RA Genheimer (ed.): Cultures Before Contact. Columbus: Ohio Archaeological Council, pp. 384- 403.

Armelagos G, Mielke J, Owen K, and Van Gerven D (1972) Bone Growth and Development in Prehistoric Populations from Sudanese Nubia. Journal of Human Evolution 1:89-119.

Atkinson P (1967) Variation in Trabecular Structure of Vertebrae with Age. Calcified Tissue Research 1:24-32.

Bass S (2000) The Prepubertal Years: A Uniquely Opportune Stage of Growth When the Skeleton is Most Responsive to Exercise? Sports Medicine 30:73-78.

Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, and Seeman E (1999) The Differing Tempo of Growth in Bone size, Mass, and Density in Girls is Region-Specific. Journal of Clinical Investigation 104:795- 804.

Bass S, Saxon L, Daly RM, et al (2002) The Effect of Mechanical Loading on the Size and Shape of Bone in Pre-, Peri-, and Postpubetal Girls: A Study in Tennis Players. Journal of Bone and Mineral Research 17:2274- 2280.

Beaupre' G, Orr T, and Carter D (1990) An Approach for Time-Dependent Bone Modeling and Remodeling-Theoretical Development. Journal of Orthopaedic Research 8:651-661.

Beaupre G, Stevens SS, and Carter D (2000) Mechanobiology in the Development, Maintenance, and Degeneration of Articular Cartilage. Journal of Rehabilitation Research and Development 37:145-152.

Bertram J, and Swartz S (1991) The "Law of Bone Transformation": A Case of Crying Wolff? Biological Review 66.

Biewener AA, Fazzalari NL, Konieczynski DD, and Baudinette RV (1996) Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse. Bone 19:1-8.

Brandt K, Doherty M, and Lohmander L, eds. (2003) Osteoarthritis Second Edition. Oxford: Oxford University Press.

Bridges PS, Blitz JH, and Solano MC (2000) Changes in Long Bone Diaphyseal Strength with Horticultural Intensification in West-Central Illinois. American Journal of Physical Anthropology 112:217-238.

Burr D, Milgrom C, Fyhrie M, et al (1996) In Vivo Measurement of Human Tibial Strains During Vigorous Activity. Bone 18:405-410.

Burr D, Robling A, and Turner C (2002) Effects of Biomechanical Stress on Bones in Animals. Bone 30:781-786.

Carskadden J, and Morton J (2000) Fort Ancient in the Central Muskingum Valley of Eastern Ohio: A View from the Philo II Site. In RA Genheimer (ed.): Cultures Before Contact. Columbus: Ohio Archaeological Council, pp. 158-193.

Carter D, and Beaupre G (2001) Skeletal Function and Form: Mechanobiology of Skeletal Development, Aging, and Regeneration. Cambridge: Cambridge University Press.

Church F, and Nass Jr J (2002) Central Ohio Valley During the Late Prehistoric Period. In J Hart and C Rieth (eds.): Northeast Subsistence-Settlement Change: AD 700-1300. Albany: SUNY, pp. 11-42.

Ding M, Odgaard A, Danielson CD, and Hvid I (2002) Mutual associations among microstructural, physical and mechanical properties of human cancellous bone. Journal of Bone and Joint Surgery 84-B:900-907.

Ding M, Odgaard A, and Hvid I (2003) Changes in the Three-Dimensional Microstructure of Human Tibial Cancellous Bone in Early Osteoarthritis. Journal of Bone and Joint Surgery 85-B:906-912.

Dunn M (1988) Burials- The Human Factor. In J Heilman, M Lileas and C Turnbow (eds.): A History of 17 Years of Excavation and Reconstruction- A Chronicle of 12th Century Human Values and the Built Environment. Dayton: Dayton Museum of Natural History, pp. 299-313.

Duppe H, Cooper C, Gardsell P, and Johnell O (1997) The Relationship Between Childhood Growth, Bone Mass, and Muscle Strength in Male and Female Adolescents. Calcified Tissue International 60:405- 409.

Eveleth P, and Tanner J (1990) Worldwide Variation in Human Growth. Cambridge: Cambridge University Press.

Fajardo RJ, et al (2005) Allometry of Anthropoid Femoral Neck Trabecular Architecture using 3D microCT. American Journal of Physical Anthropology Supplement 40:101.

Fajardo RJ, and Muller R (2001) Three-Dimensional analysis of nonhuman primate trabecular architecture using micro-computed tomography. American Journal of Physical Anthropology 115:327-336.

Fajardo RJ, Ryan TM, and Kappelman J (2002) Assessing the accuracy of high-resolution X-ray computed tomography of primate trabecular bone by comparisons with histological sections. American Journal of Physical Anthropology 118:1-10.

Feldkamp L, Goldstein S, Parfitt A, et al (1989) The Direct Examination of Three Dimensional Bone Architecture in vitro by Computed Tomography. Journal of Bone and Mineral Research 4:3-11.

Forwood M, Baxter-Jones A, Beck T, et al (2006) Physical Activity and Strength of the Femoral Neck During the Adolescent Growth Spurt: A Longitudinal Analysis. Bone 38:576-583.

Forwood M, and Burr D (1993) Physical Activity and Bone Mass: Exercises in Futility? Bone and Mineral 21:89-112.

Freeman M, and Pinskerova V (2005) The Movement of the Normal Tibio-Femoral Joint. Journal of Biomechanics 38:197-208.

Frost H (1987) Bone "mass" and the "mechanostat: A Proposal. Anatomical Record 219:1-9.

Frost HM (1998) Perspectives: A Proposed General Model of the "Mechanostat" (Suggestions from a New Skeletal-Biological Paradigm). Anatomical Record 244:139-147.

Garn S (1980) Human Growth. Annual Review of Anthropology 9:275-292.

Genheimer RA, ed. (2000) Cultures Before Contact: The Late Prehistory of Ohio and Surrounding Regions. Columbus: Ohio Archaeological Council.

Goldstein S, Mathews L, Kuhn J, and Hollister S (1991) Trabecular Bone Remodeling: An Experimental Model. Journal of Biomechanics 24S:135-150.

Huiskes R, Rulmerman R, van Lenthe G, and Jannsen J (2000) Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405:704-706.

Jacobs C (2000) The Mechanobiology of Cancellous Bone Structural Adaptation. Journal of Rehabilitation Research and Development 37:1-16.

Jacobs C, Simo JC, Beaupre G, and Carter D (1997) Adaptive Bone Remodeling Incorporating Simultaneous Density and Anisotropy Considerations. Journal of Biomechanics 30:603-613.

Janz K, Burns T, Levy S, and al e (2004) Everyday Activity Predicts Bone Geometry in Children: The Iowa Bone Development Study. Medicine and Science in Sports and Exercise 36:1124-1131.

Johnston F, and Zimmer L (1989) Assessment of Growth and Age in the Immature Skeleton. In M Iscan and K Kennedy (eds.): Reconstruction of Life From the Skeleton. New York: Alan R. Liss, pp. 11-21.

Ketcham R, and Ryan TM (2004) Quantification and Visualization of Anisotropy in Trabecular Bone. Journal of Microscopy 213:158-171.

Kneissel M, Roschager P, Steiner W, et al (1997) Cancellous Bone Structure in the Growing and Aging Lumbar Spine in a Historic Nubian Population. Calcified Tissue International 61:95-100.

Kontulainen S, MacDonald H, Khan K, and McKay H (2005) Examining Bone Surfaces Across Puberty. Journal of Bone and Mineral Research 20:1202-1207.

Korstjens C, Geraets W, Ginkel F, et al (1995) Longitudinal Analysis of Radiographic Trabecular Pattern by Image Processing. Bone 17:527-532.

Kothari M, Keaveny TM, Lin JC, Newitt DC, Genant HK, and Majumdar S (1998) Impact of Spatial Resolution on the Prediction of Trabecular Architecture Parameters. Bone 22:437-443.

Lanyon L (1982) Mechanical Function and Bone Remodeling. In G Sumner-Smith (ed.): Bone in Clinical Orthopaedics. Philadelphia: Saunders, pp. 273-304.

Larsen CS (1995) Biological Changes in Human Populations with Agriculture. Annual Review of Anthropology 24:185-213.

Larsen CS (1997) Bioarchaeology: Interpreting Behavior from the Human Skeleton. Cambridge: Cambridge University Press.

Layton M, Goldstein S, Goulet R, et al (1988) Examination of Subchondral Bone Architecture in Experimental Osteoarthritis by Microscopic Computed Axial Tomography. Arthritis and Rheumatism 31:1400-5.

Lieberman DE, Devlin MJ, and Pearson OM (2001) Articular Area Responses to Mechanical Loading: Effects of Exercise, Age, and Skeletal Location. American Journal of Physical Anthropology 116:266-277.

Lloyd T, Beck T, Lin H, et al (2002) Modifiable Determinants of Bone Status in Young Women. Bone 30:416-421.

MacKelvie K, Petit M, Khan K, Beck T, and McKay H (2004) Bone Mass and Structure are Enhanced Following a 2-Year Randomized Controlled Trial of Exercise in Prepubertal Boys. Bone 34:755-764.

MacLatchy l, and Muller R (2002) A Comparison of the Femoral Head and Neck Trabecular Architecture of Galago and Perodicticus Using Micro-Computed Tomography. Journal of Human Evolution 43:89-105.

Martin R, Burr D, and Sharkey N (1998) Skeletal Tissue Mechanics. New York: Springer.

Muller R, Hildebrand T, and Ruegsegger P (1994) Non-invasive Bone Biopsy: a New Method to Analyze and Display the Three-Dimensional Structure of Trabecular Bone. Physics in Medicine and Biology 39:145-164.

Muller R, and Ruegsegger P (1995) Three-Dimensional Finite Element Modelling of Non-invasively Assessed Trabecular Bone Structures. Medical Engineering and Physics 17:126-133.

Nafei A, Danielson C, Linde F, and Hvid I (2000a) Properties of Growing Trabecular Ovine Bone. Journal of Bone and Joint Surgery 82-B:910-920.

Nafei A, Kabel J, Odgaard A, Linde F, and Hvid I (2000b) Properties of Growing Trabecular Ovine Bone. Part II: Architectural and Mechanical Properties. Journal of Bone and Joint Surgery [Br] 82-B:921-927.

Odgaard A (1997) Three-Dimensional Methods for Quantification of Cancellous Bone Architecture. Bone:315-328.

Parfitt A, et al (1987) Bone Histomorphometry: Standardization of Nomenclature, Symbols, and Units. Journal of Bone and Mineral Research 2:595-610.

Pearson OM (2000) Activity, Climate, And Postcranial Robusticity. Current Anthropology 41:569-607.

Pearson OM, and Lieberman DE (2004) The Aging of Wolff's "Law": Ontogeny and Responses to Mechanical Loading in Cortical Bone. Yearbook of Physical Anthropology 47:63-99.

Pollack D, and Henderson AG (2000) Insights into Fort Ancient Culture Change: A View from South of the Ohio River. In RA Genheimer (ed.): Cultures Before Contact. Columbus: Ohio Archaeological Council, pp. 194-227.

Pontzer H, Lieberman DE, Momin E, Devlin MJ, and al e (2006) Trabecular Bone in the Bird Knee Responds with High Sensitivity to Changes in Load Orientation. Journal of Experimental Biology 209:57-65.

Rafferty K, and Ruff C (1994) Articular Structure and Function in Hylobates, Colobus, and Papio. American Journal of Physical Anthropology 94:395-408.

Redmond BG (2000) Reviewing the Late Prehistory of Ohio. In RA Genheimer (ed.): Cultures Before Contact. Columbus: Ohio Archaeological Council, pp. 426-437.

Richman B (2004) Trabecular Bone Structure in Human and Chimpanzee Knee Joints. American Journal of Physical Anthropology 123:167.

Roesler H (1987) The History of Some Fundamental Concepts in Bone Biomechanics. Journal of Biomechanics 20:1025-1034.

Rubin CT, Turner A, Mallinckrodt C, et al (2002) Mechanical Strain, Induced Noninvasively in the High Frequency Domain, Is Anabolic to Cancellous Bone, But Not Cortical Bone. Bone 30:445-452.

Ruegsegger P, Koller B, and Muller R (1996) A Microtomographic System for the Nondestructive Evaluation of Bone Architecture. Calcified Tissue International 58:24-29.

Ruff C, Holt B, and Trinkaus E (2006) Who's Afraid of the Big Bad Wolff?: "Wolff's Law" and Bone Functional Adaptation. American Journal of Physical Anthropology 000 (published online):NA.

Ruff C, Walker A, and Trinkaus E (1994) Postcranial Robusticity in Homo. III. Ontogeny. American Journal of Physical Anthropology 93.

Ruff CB (2000) Body Size, Body Shape, and Long Bone Strength in Modern Humans. Journal of Human Evolution 38:269-290.

Ruff CB (2003) Growth in Strength, Body Size, and Muscle Size in a Juvenile Longitudinal Sample. Bone 33:317-329.

Ruff CB (2006) Body Size Prediction from Juvenile Skeletal Remains, with Application to KNM-WT 15000. submitted for publication.

Ruimerman R, Hilbers P, van Rietbergen B, and Huiskes R (2005) A Theoretical Framework for Strain-Related Trabecular Bone Maintenance and Adaptation. Journal of Biomechanics 38:931-941.

Ryan T, and van Rietbergen B (2005) Mechanical Significance of Femoral Head Trabecular Bone Structure in Loris and Galago Evaluated Using Micromechanical Finite Element Models. American Journal of Physical Anthropology 1261:82-96.

Ryan TM, and Ketcham R (2000a) The Three-Dimensional Structure of Trabecular Bone in the Femoral Head of Strepsirrhine Primates. Journal of Human Evolution 43:1-63.

Ryan TM, and Ketcham R (2000b) Femoral Head Trabecular Bone Structure in Two Omomyid Primates. Journal of Human Evolution 43:241-63.

Ryan TM, and Krovitz GE (2005) Ontogeny of Three-Dimension Trabecular Bone Architecture in the Human Proximal Femur. American Journal of Physical Anthropology Supplement 40:180-181.

Ryan TM, and van Rietbergen B (2005) Mechanical Significance of Femoral Head Trabecular Bone Structure in Loris and Galago Evaluated Using Micromechanical Finite Element Models. American Journal of Physical Anthropology 121:82-96.

Saunders S (2000) Subadult Skeletons and Growth-Related Studies. In M Katzenberg and S Saunders (eds.): Biological Anthropology of the Human Skeleton. New York: Wiley-Liss.

Saunders S, and Hoppa R (1993) Growth Deficit in Survivors and Non-survivors: Biological Mortality Bias in Subadult Skeletal Samples. Yearbook of Physical Anthropology 36:127-151.

Sciulli P, and Oberly J (2002) Native Americans in Eastern North America: The Southern Great Lakes and Upper Ohio Valley. In R Steckel and J Rose (eds.): The Backbone of History: Health and Nutrition in the Western Hemisphere. Cambridge: Cambridge University Press, pp. 440-480.

Skedros J, Hunt K, and Bloebaum R (2004) Relationships of Loading History and Structural and Material Characteristics of Bone: Development of the Mule Deer Calcaneus. Journal of Morphology 259:281-307.

Smith BD (1989) Origins of Agriculture in Eastern North America. Science 246:1566-1571.

Sone T, Imai Y, Joo Y, et al (2006) Side-to-Side Differences in Cortical Bone Mineral Density of Tibiae in Young Male Athletes. Bone 38:708-13.

Spoor F, Wood B, and Zonneveld F (1994) Implications of Early Hominid Labyrinthine Morphology for the Evolution of Human Locomotion. Nature 369:645-648.

Steckel R, and Rose J, eds. (2002) The Backbone of History: Health and Nutrition in the Western Hemisphere. Cambridge: Cambridge University Press.

Sundberg M, Gardsell P, Johnell O, Karlsson MK, et al (2001) Peripubertal Moderate Exercise Increases Bone Mass in Boys but Not in Girls: A Population-Based Intervention Study. Osteoporosis International 12:230-238.

Sundberg M, Gardsell P, Johnell O, Karlsson MK, et al (2002) Physical Activity Increases Bone Size in Prepubertal Boys and Bone Mass in Prepubertal Girls: A Combined Cross-Sectional and 3-Year Longitudinal Study. Calcified Tissue International 71:406- 415.

Tanck E, Hannink G, Ruimerman R, Buma P, et al (2006) Cortical Bone Development Under the Growth Plate is Regulated by Mechanical Load Transfer. Journal of Anatomy 208:73-79.

Tanck E, Homminga J, Van Lenthe G, and Huiskes R (2001) Increase in Bone Volume Fraction Precedes Architectural Adaptation in Growing Bone. Bone 28:650-654.

Tardieu C, Glard Y, Garron E, et al (2006) Relationship between Formation of the Femoral Bicondylar Angle and Trochlear Shape: Independence of Diaphyseal and Epiphyseal Growth. American Journal of Physical Anthropology 130:491-500.

Tatarek B, and Sciulli P (2000) Comparison of Population Structure in Ohio's Late Archaic and Late Prehistoric Periods. American Journal of Physical Anthropology 112:363-376.

Turner C, and Robling A (2003) Designing Exercise Regimens to Increase Bone Strength. Exercise and Sport Scientific Review 31.

Uchiyama T, Tanizawa T, Muramatsu H, Endo N, Takahashi HE, and Hara T (1999) Three-Dimensional microstructural analysis of human trabecular bone in relation to its mechanical properties. Bone 25:487-491.

Ulrich D, van Rietbergen B, Laib A, and Ruegsegger P (1999) The Ability of Three-Dimensional Structural Indices to Reflect Mechanical Aspects of Trabecular Bone. Bone 25:55-60.

Uusi-Rasi, Sievanen H, and Heinonen A (2006) Long-Term Recreational Gymnastics Provides a Clear Benefit in Age-Related Functional Decline and Bone Loss. A Prospective 6-Year Study. Osteoporosis International 17:1154-1164.

Valdimarsson O, Alborg H, Duppe H, et al (2005) Reduced Training is Associated With Increased Loss of BMD. Journal of Bone and Mineral Research 20:906-12.

van der Meulen M, Beaupre G, and Carter D (1993) Mechanobiologic Influences in Long Bone Cross-Sectional Growth. Bone 14:635-642.

van der Meulen M, and Huiskes R (2002) Why Mechanobiology? A Survey Article. Journal of Biomechanics 35:401-414.

van Rietbergen B, Odgaard A, Kabel J, and Huiskes R (1998) Relationships Between Bone Morphology and Bone Elastic Properties can be Accurately Quantified using High-Resolution Computer Reconstructions. Journal of Orthopaedic Research 16:23-28.

van Rietbergen B, Weinans H, Huiskes R, and Odgaard A (1995) A New Method to Determine Trabecular Bone Elastic Properties and Loading Using Micromechanical Finite-Element Models. Journal of Biomechanics 28:69-81.

Wolff J (1892) The Law of Bone Remodeling. (Translation by P. Maquet and R. Furlong). Berlin: Springer-Verlag.

Wong M, and Carter D (1990) A Theoretical Model of Endochondral Ossification and Bone Architectural Construction in Long Bone Ontogeny. Anatomy and Embryology 181:523-532.

You L, Cowin S, Schaffer M, and Weinbaum S (2001) A Model for Strain Amplification in the Actin Cytoskeleton of Osteocytes due to Fluid Drag on Pericellular Matrix. Journal of Biomechanics 34:1375-1386.

Zysset PK (2003) A Review of Morphology- Elastic Relationships in Human Trabecular Bone: Theories and Experiments. Journal of Biomechanics 36:1469-1485.

 

 


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