Recent advancements in the analysis of bone microstructure: New dimensions in forensic anthropology

Abstract Bone is a mechanically active, three-dimensionally (3D) complex, and dynamic tissue that changes in structure over the human lifespan. Bone tissue exists and remodels in 3D and changes over time, introducing a fourth dimension. The products of the remodelling process, secondary and fragmentary osteons, have been studied substantially using traditional two-dimensional (2D) techniques. As a result, much has been learned regarding the biological information encrypted in the histomorphology of bone, yielding a wealth of information relating to skeletal structure and function. Three-dimensional imaging modalities, however, hold the potential to provide a much more comprehensive understanding of bone microarchitecture. The visualization and analysis of bone using high-resolution 3D imaging will improve current understandings of bone biology and have numerous applications in both biological anthropology and biomedicine. Through recent technological advancements, we can hone current anthropological applications of the analysis of bone microstructure and accelerate research into the third and fourth dimensional realms. This review will explore the methodological approaches used historically by anthropologists to assess cortical bone microstructure, spanning from histology to current ex vivo imaging modalities, discuss the growing capabilities of in vivo imaging, and conclude with an introduction of novel non-histological modalities for investigating bone quality.

[1]  D. Hans,et al.  Quantitative Ultrasound of the Tibia Depends on Both Cortical Density and Thickness , 2001, Osteoporosis International.

[2]  S. Sacco,et al.  Maternal Consumption of Hesperidin and Naringin Flavanones Exerts Transient Effects to Tibia Bone Structure in Female CD-1 Offspring , 2017, Nutrients.

[3]  Frost Hm Treatment of osteoporoses by manipulation of coherent bone cell populations. , 1979 .

[4]  Andrei L. Turinsky,et al.  Effect of Voxel Size on 3D Micro-CT Analysis of Cortical Bone Porosity , 2007, Calcified Tissue International.

[5]  D. Cooper,et al.  Modalities for Visualization of Cortical Bone Remodeling: The Past, Present, and Future , 2015, Front. Endocrinol..

[6]  G Lowet,et al.  Assessment of the strength of the proximal femur in vitro: relationship with ultrasonic measurements of the calcaneus. , 1997, Bone.

[7]  I. J. Singh,et al.  Estimation of age at death in human males from quantitative histology of bone fragments. , 1970, American journal of physical anthropology.

[8]  J. Currey The many adaptations of bone. , 2003, Journal of biomechanics.

[9]  H. Frost Treatment of osteoporoses by manipulation of coherent bone cell populations. , 1979, Clinical orthopaedics and related research.

[10]  D. Thompson,et al.  The core technique in the determination of age at death of skeletons. , 1979, Journal of forensic sciences.

[11]  Z. Zadik,et al.  Pediatric reference curves for multi-site quantitative ultrasound and its modulators , 2003, Osteoporosis International.

[12]  R. Paine,et al.  Brief communication: histological age estimation using rib and clavicle. , 1992, American journal of physical anthropology.

[13]  R. Fajardo,et al.  Assessing the accuracy of high-resolution X-ray computed tomography of primate trabecular bone by comparisons with histological sections. , 2002, American journal of physical anthropology.

[14]  S. Sacco,et al.  Nutritional Programming of Bone Structure in Male Offspring by Maternal Consumption of Citrus Flavanones , 2017, Calcified Tissue International.

[15]  J G Clement,et al.  The relationship between porosity and specific surface in human cortical bone is subject specific. , 2015, Bone.

[16]  M. Daudon,et al.  Diffraction techniques and vibrational spectroscopy opportunities to characterise bones , 2009, Osteoporosis International.

[17]  L. Claes,et al.  Prediction of fracture load at different skeletal sites by geometric properties of the cortical shell , 1996, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[18]  D B Burr,et al.  Errors in bone remodeling: toward a unified theory of metabolic bone disease. , 1989, The American journal of anatomy.

[19]  Françoise Peyrin,et al.  Spatial distribution of tissue level properties in a human femoral cortical bone. , 2012, Journal of biomechanics.

[20]  H Weinans,et al.  Detecting and tracking local changes in the tibiae of individual rats: a novel method to analyse longitudinal in vivo micro-CT data. , 2004, Bone.

[21]  D. Cooper,et al.  Technological Developments in the Analysis of Cortical Bone Histology: The Third Dimension and Its Potential in Anthropology , 2011 .

[22]  T S Smith,et al.  Three‐dimensional microimaging (MRμI and μCT), finite element modeling, and rapid prototyping provide unique insights into bone architecture in osteoporosis , 2001, The Anatomical record.

[23]  R Huiskes,et al.  Osteocyte density and histomorphometric parameters in cancellous bone of the proximal femur in five mammalian species , 1996, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[24]  Frost Hm Metastases to bone and hypercalcemia. , 1973 .

[25]  Thomas A. Einhorn,et al.  Perspectives: Ultrasound assessment of bone , 1993 .

[26]  S. F. Ahmed,et al.  Quantitative ultrasound assessment of bone in preterm and term neonates , 2005, Archives of Disease in Childhood - Fetal and Neonatal Edition.

[27]  F. Terlizzi,et al.  Assessment of Skeletal Development in Preterm and Term Infants by Quantitative Ultrasound , 2005, Pediatric Research.

[28]  S. Joshi,et al.  Disorders of calcium, phosphorus and magnesium metabolism. , 2008, The Journal of the Association of Physicians of India.

[29]  M. Bouxsein,et al.  Prediction of the strength of the elderly proximal femur by bone mineral density and quantitative ultrasound measurements of the heel and tibia. , 1999, Bone.

[30]  Eve Donnelly,et al.  Methods for Assessing Bone Quality: A Review , 2011, Clinical orthopaedics and related research.

[31]  C. Njeh,et al.  Does Combining the Results from Multiple Bone Sites Measured by a New Quantitative Ultrasound Device Improve Discrimination of Hip Fracture? , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[32]  R. Miiller,et al.  Three-dimensional finite element modelling of non-invasively assessed trabecular bone structures , 1995 .

[33]  Michael D Morris,et al.  Raman Assessment of Bone Quality , 2011, Clinical orthopaedics and related research.

[34]  Sabine Bensamoun,et al.  Three-dimensional characterization of cortical bone microstructure by microcomputed tomography: validation with ultrasonic and microscopic measurements , 2007, Journal of orthopaedic science : official journal of the Japanese Orthopaedic Association.

[35]  R. Madsen,et al.  Population-specific histological age-estimating method: a model for known African-American and European-American skeletal remains. , 2002, Journal of forensic sciences.

[36]  G. Buonocore,et al.  Feasibility of quantitative ultrasound measurements on the humerus of newborn infants for the assessment of the skeletal status , 2004, Osteoporosis International.

[37]  Y. Yeni,et al.  The influence of bone morphology on fracture toughness of the human femur and tibia. , 1997, Bone.

[38]  A. Burstein,et al.  The elastic and ultimate properties of compact bone tissue. , 1975, Journal of biomechanics.

[39]  C. M. Langton,et al.  The role of ultrasound in the assessment of osteoporosis: A review , 2005, Osteoporosis International.

[40]  D. Ubelaker,et al.  Differences in osteon banding between human and nonhuman bone. , 2001, Journal of forensic sciences.

[41]  A. Eliakim,et al.  Bone turnover markers and bone strength during the first weeks of life in very low birth weight premature infants , 2004, Journal of perinatal medicine.

[42]  P. Lips,et al.  Bone Histomorphometric and Biochemical Marker Results of a 2‐Year Placebo‐Controlled Trial of Raloxifene in Postmenopausal Women , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[43]  G. Breart,et al.  Ultrasonographic heel measurements to predict hip fracture in elderly women: the EPIDOS prospective study , 1996, The Lancet.

[44]  P. Laugier,et al.  A determination of the minimum sizes of representative volume elements for the prediction of cortical bone elastic properties , 2011, Biomechanics and modeling in mechanobiology.

[45]  L. Wright,et al.  The Use of Transmission Ultrasonics to Assess Bone Status in the Human Newborn , 1987, Pediatric Research.

[46]  M. Bouxsein,et al.  Tibial ultrasound velocity measured in situ predicts the material properties of tibial cortical bone. , 1997, Bone.

[47]  H. Gundersen Stereology of arbitrary particles * , 1986, Journal of microscopy.

[48]  H. McDevitt,et al.  Changes in Quantitative Ultrasound in Infants Born at Less than 32 Weeks’ Gestation Over the First 2 Years of Life: Influence of Clinical and Biochemical Changes , 2007, Calcified Tissue International.

[49]  D. Fyhrie,et al.  Histomorphometric assessment of Haversian canal and osteocyte lacunae in different-sized osteons in human rib. , 2003, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[50]  Anke Schnapper,et al.  The architecture of growing compact bone in the dog: visualization by 3D-reconstruction of histological sections. , 2002, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[51]  D B Burr,et al.  Targeted and nontargeted remodeling. , 2002, Bone.

[52]  S. Gehlert,et al.  Effects of field size when using Kerley's histological method for determination of age at death. , 1982, American journal of physical anthropology.

[53]  H. Frost Tetracycline bone labeling in anatomy. , 1968, American journal of physical anthropology.

[54]  Fran Adar,et al.  Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. , 2004, Bone.

[55]  C. Rimnac,et al.  A physical, chemical, and mechanical study of lumbar vertebrae from normal, ovariectomized, and nandrolone decanoate-treated cynomolgus monkeys (Macaca fascicularis). , 2000, Bone.

[56]  M Schultz,et al.  Diagnostic value of micro-CT in comparison with histology in the qualitative assessment of historical human postcranial bone pathologies. , 2007, Homo : internationale Zeitschrift fur die vergleichende Forschung am Menschen.

[57]  John G. Clement,et al.  Femoral osteocyte lacunar density, volume and morphology in women across the lifespan. , 2013, Journal of structural biology.

[58]  O. Yılmaz,et al.  Changes in quantitative ultrasound in preterm and term infants during the first year of life. , 2011, European journal of radiology.

[59]  D. Cooper,et al.  Occurrence of osteon banding in adult human cortical bone. , 2017, American journal of physical anthropology.

[60]  S. Sacco,et al.  Repeated irradiation from micro-computed tomography scanning at 2, 4 and 6 months of age does not induce damage to tibial bone microstructure in male and female CD-1 mice. , 2017, BoneKEy reports.

[61]  E. Trimmer,et al.  OSTEOPOROSIS , 1965, The Lancet.

[62]  H K Genant,et al.  A new method for quantitative ultrasound measurements at multiple skeletal sites: first results of precision and fracture discrimination. , 2000, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[63]  H. McDevitt,et al.  Longitudinal changes in bone health as assessed by the speed of sound in very low birth weight preterm infants. , 2006, The Journal of pediatrics.

[64]  A. Boskey,et al.  Bone Fragility and Collagen Cross‐Links , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[65]  J. Hert,et al.  Osteon orientation of the diaphysis of the long bones in man. , 1994, Bone.

[66]  K. Jepsen,et al.  Understanding bone strength: size isn't everything. , 2001, Bone.

[67]  D. Ubelaker,et al.  Differentiating Human from Nonhuman Bone Microstructure , 2011 .

[68]  S. Majumdar,et al.  High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. , 2010, Journal of Clinical Endocrinology and Metabolism.

[69]  E. Kerley,et al.  The microscopic determination of age in human bone. , 1965, American journal of physical anthropology.

[70]  D. C. Sterio The unbiased estimation of number and sizes of arbitrary particles using the disector , 1984, Journal of microscopy.

[71]  S. Goldstein,et al.  The direct examination of three‐dimensional bone architecture in vitro by computed tomography , 1989, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[72]  T. Gursoy,et al.  Bone Speed of Sound Curves of Twin and Singleton Neonates , 2008, Journal of pediatric endocrinology & metabolism : JPEM.

[73]  P W Thompson,et al.  Quantitative ultrasound (QUS) of the heel predicts wrist and osteoporosis-related fractures in women age 45-75 years. , 1998, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[74]  Victoria M. Dominguez,et al.  Bone Histology as an Integrated Tool in the Process of Human Identification , 2018 .

[75]  M. Weiss,et al.  Discrimination of Proximal Hip Fracture by Quantitative Ultrasound Measurement at the Radius , 2000, Osteoporosis International.

[76]  N. Tappen Three-dimensional studies on resorption spaces and developing osteons. , 1977, The American journal of anatomy.

[77]  S. Stout The use of bone histomorphometry in skeletal identification: the case of Francisco Pizarro. , 1986, Journal of forensic sciences.

[78]  J. Davis,et al.  Predicting vertebral deformity using bone densitometry at various skeletal sites and calcaneus ultrasound. , 1995, Bone.

[79]  J. Cauley,et al.  Broadband ultrasound attenuation predicts fractures strongly and independently of densitometry in older women. A prospective study. Study of Osteoporotic Fractures Research Group. , 1997, Archives of Internal Medicine.

[80]  M. Mughal,et al.  Relationship of tibial speed of sound and lower limb length to nutrient intake in preterm infants , 2007, Archives of Disease in Childhood Fetal and Neonatal Edition.

[81]  I. Pratt,et al.  Evaluating differential nuclear DNA yield rates and osteocyte numbers among human bone tissue types: A synchrotron radiation micro-CT approach. , 2017, Forensic science international. Genetics.

[82]  Andrew G Peele,et al.  Variation in osteocyte lacunar morphology and density in the human femur--a synchrotron radiation micro-CT study. , 2013, Bone.

[83]  H K Genant,et al.  Assessment of bone status using speed of sound at multiple anatomical sites. , 2001, Ultrasound in medicine & biology.

[84]  J. Jowsey Studies of Haversian systems in man and some animals. , 1966, Journal of anatomy.

[85]  Alon Eliakim,et al.  Early physical activity intervention prevents decrease of bone strength in very low birth weight infants. , 2003, Pediatrics.

[86]  T. Ryan,et al.  The three-dimensional structure of trabecular bone in the femoral head of strepsirrhine primates. , 2002, Journal of human evolution.

[87]  R. Martin,et al.  Is all cortical bone remodeling initiated by microdamage? , 2002, Bone.

[88]  M. Mughal,et al.  Tibial Speed of Sound in Term and Preterm Infants , 2004, Neonatology.

[89]  R Stern,et al.  Measurement of the velocity of ultrasound in human cortical bone in vivo. Estimation of its potential value in the diagnosis of osteoporosis and metabolic bone disease. , 1981, Radiology.

[90]  W. Koo,et al.  Quantitative bone US measurements in neonates and their mothers , 2008, Pediatric Radiology.

[91]  E. Bossy,et al.  In vivo performance evaluation of bi-directional ultrasonic axial transmission for cortical bone assessment. , 2009, Ultrasound in medicine & biology.

[92]  Rei-Cheng Yang,et al.  Bone status and associated factors measured by quantitative ultrasound in preterm and full-term newborn infants. , 2012, Early human development.

[93]  D. Cooper,et al.  Normal variation in cortical osteocyte lacunar parameters in healthy young males , 2014, Journal of anatomy.

[94]  H. Frost Tetracycline-based histological analysis of bone remodeling , 2005, Calcified Tissue Research.

[95]  M F Ericksen,et al.  Histologic estimation of age at death using the anterior cortex of the femur. , 1991, American journal of physical anthropology.

[96]  D. Rao,et al.  Reduced Iliac Cancellous Osteocyte Density in Patients With Osteoporotic Vertebral Fracture , 2003, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[97]  T. Link,et al.  Quantitative ultrasound in the assessment of skeletal status , 2009, European Radiology.

[98]  David B. Burr,et al.  Skeletal Tissue Mechanics , 1998, Springer New York.

[99]  D. Nemet,et al.  Quantitative ultrasound measurements of bone speed of sound in premature infants , 2001, European Journal of Pediatrics.

[100]  J. Ahlqvist,et al.  A modification of Kerley's method for the microscopic determination of age in human bone. , 1969, Journal of forensic sciences.

[101]  C H Turner,et al.  Basic biomechanical measurements of bone: a tutorial. , 1993, Bone.

[102]  D. Ubelaker,et al.  A comparison of two methods for the microscopic determination of age at death. , 1977, American journal of physical anthropology.

[103]  Árbara,et al.  Three-dimensional characterization of cortical bone microstructure by microcomputed tomography : validation with ultrasonic and microscopic measurements , 2007 .

[104]  L. Bachrach,et al.  Comparison of calcaneus ultrasound and dual X-ray absorptiometry in children at risk of osteopenia. , 2003, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[105]  G. Lipowsky,et al.  Ultrasound for the assessment of bone quality in preterm and term infants , 2012, Journal of Perinatology.

[106]  F. Mimouni,et al.  Bone Ultrasound Velocity of Infants Born Small for Gestational Age , 2005, Journal of pediatric endocrinology & metabolism : JPEM.

[107]  G. Moro,et al.  Quantitative ultrasound for the assessment of osteopenia in preterm infants. , 2003, European journal of endocrinology.

[108]  S. D. Stout,et al.  Computer-Assisted 3D Reconstruction of Serial Sections of Cortical Bone to Determine the 3D Structure of Osteons , 1999, Calcified Tissue International.

[109]  D. Rao,et al.  Relationships between osteocyte density and bone formation rate in human cancellous bone. , 2002, Bone.

[110]  D. Vashishth,et al.  Sexual dimorphism and age dependence of osteocyte lacunar density for human vertebral cancellous bone. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[111]  H. Frost Metabolism of bone. , 1973, The New England journal of medicine.

[112]  T. Fuerst,et al.  Quantitative ultrasound bone measurement , 1997, European Radiology.

[113]  M. Bouxsein,et al.  Bone quality: where do we go from here? , 2003, Osteoporosis International.

[114]  M. Popovtzer,et al.  Quantitative ultrasound of the tibia: a novel approach for assessment of bone status. , 1995, Bone.

[115]  R. Amprino A contribution to the functional meaning of the substitution of primary by secondary bone tissue. , 1948, Acta anatomica.

[116]  Steven K Boyd,et al.  Radiation effects on bone architecture in mice and rats resulting from in vivo micro-computed tomography scanning. , 2008, Medical engineering & physics.

[117]  J. Cohen,et al.  The three-dimensional anatomy of haversian systems. , 1958, The Journal of bone and joint surgery. American volume.

[118]  T. Ashmeade,et al.  The Use of Quantitative Ultrasound in Assessing Bone Status in Newborn Preterm Infants , 2003, Journal of Perinatology.

[119]  H. Macdonald,et al.  Changes in trabecular and cortical bone microarchitecture at peripheral sites associated with 18 months of teriparatide therapy in postmenopausal women with osteoporosis , 2010, Osteoporosis International.

[120]  D. Nemet,et al.  Body composition and its components in preterm and term newborns: A cross‐sectional, multimodal investigation , 2010, American journal of human biology : the official journal of the Human Biology Council.

[121]  Brief communication: cortical remodeling data are affected by sampling location. , 1995, American journal of physical anthropology.

[122]  T. Ryan,et al.  Femoral head trabecular bone structure in two omomyid primates. , 2002, Journal of human evolution.

[123]  G. Baroncelli Quantitative bone analysis in children: current methods and recommendations. , 2006, The Journal of pediatrics.

[124]  S. Pfeiffer Cortical bone age estimates from historically known adults. , 1992, Zeitschrift fur Morphologie und Anthropologie.

[125]  E. Özek,et al.  Quantitative ultrasound and biochemical parameters for the assessment of osteopenia in preterm infants , 2007, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[126]  S. Boonen,et al.  The bone quality framework: determinants of bone strength and their interrelationships, and implications for osteoporosis management. , 2005, Clinical therapeutics.

[127]  H. Genant,et al.  Image-Based Assessment of Spinal Trabecular Bone Structure from High-Resolution CT Images , 1998, Osteoporosis International.

[128]  David B. Burr,et al.  Bone Morphology and Organization , 2014 .

[129]  F. Mimouni,et al.  Bone Ultrasound Velocity Curves of Newly Born Term and Preterm Infants , 2003, Journal of pediatric endocrinology & metabolism : JPEM.

[130]  R. Paine,et al.  Histological age estimation using rib and clavicle , 1992 .

[131]  P. Ross,et al.  Prediction of Fracture Risk by Radiographic Absorptiometry and Quantitative Ultrasound: A Prospective Study , 1998, Calcified Tissue International.

[132]  F. Vasciaveo,et al.  Vascular channels and resorption cavities in the long bone cortex. The bovine bone. , 1961, Acta anatomica.

[133]  A. Robling,et al.  Histomorphometry of Human Cortical Bone: Applications to Age Estimation , 2007 .

[134]  A. Boskey,et al.  Fourier transform infrared imaging of femoral neck bone: Reduced heterogeneity of mineral‐to‐matrix and carbonate‐to‐phosphate and more variable crystallinity in treatment‐naive fracture cases compared with fracture‐free controls , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[135]  P. Fiala,et al.  Spatial organization of the haversian bone in man. , 1996, Journal of biomechanics.