Skip to main content

Advertisement

SpringerLink
Log in

Cortical Histomorphometry of the Human Humerus During Ontogeny

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

Modeling and remodeling are two key determinants of human skeletal growth though little is known about the histomorphometry of cortical bone during ontogeny. In this study, we examined the density and geometric properties of primary and secondary osteons (osteon area and diameter, vascular canal area and diameter) in subperiosteal cortical bone from the human humerus (n = 84) between birth and age 18 years. Sections were removed from the anterior midshaft aspect of humeri from skeletons. Age-at-death was reconstructed using standard osteological techniques. Analyses revealed significant correlation between the histomorphometric variables and age. Higher densities of primary osteons occurred between infancy and 7 years of age but were almost completely replaced by secondary osteons after 14 years of age. The geometry of primary osteons was less clearly related to age. Secondary osteons were visible after 2 years of age and reached their greatest densities in the oldest individuals. Osteon size was positively but weakly influenced by age. Our data imply that modeling and remodeling are age-dependent processes that vary markedly from birth to adulthood in the human humerus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Goldman HM, McFarlin SC, Cooper DML et al (2009) Ontogenetic patterning of cortical bone microstructure and geometry at the human mid-shaft femur. Anat Rec 292:48–64. doi:10.1002/ar.20778

    Article  CAS  Google Scholar 

  2. Maggiano IS, Maggiano CM, Tiesler VG et al (2015) Drifting diaphyses: Asymmetry in diametric growth and adaption along the humeral and femoral length. Anat Rec 298:1689–1699. doi:10.1002/ar.23201

    Article  Google Scholar 

  3. Cambra-Moo O, Nacarino Meneses C, Rodríguez Barbero MÁ et al (2014) An approach to the histomorphological and histochemical variations of the humerus cortical bone through human ontogeny. J Anat 224:634–646. doi:10.1111/joa.12172

    Article  PubMed  PubMed Central  Google Scholar 

  4. Maggiano CM (2012) Histomorphometry of humeral primary bone: evaluating the endosteal lamellar pocket as an indicator of modeling drift in archaeological and modern skeletal samples. PhD Dissertation

  5. Maggiano CM, Maggiano IS, Tiesler VG et al (2016) Methods and theory in bone modeling drift: comparing spatial analyses of primary bone distributions in the human humerus. J Anat 228:190–202. doi:10.1111/joa.12383

    Article  PubMed  Google Scholar 

  6. Rauch F, Travers R, Glorieux FH (2007) Intracortical remodeling during human bone development-A histomorphometric study. Bone 40:274–280. doi:10.1016/j.bone.2006.09.012

    Article  PubMed  Google Scholar 

  7. Eleazer CD, Jankauskas R (2016) Mechanical and metabolic interactions in cortical bone development. Am J Phys Anthropol 160:317–333. doi:10.1002/ajpa.22967

    Article  PubMed  Google Scholar 

  8. Kerley ER (1965) The microscopic determination of age in human bone. Am J Phys Anthr 23:149–163

    Article  CAS  Google Scholar 

  9. Streeter M (2010) A four-stage method of age at death estimation for use in the subadult rib cortex. J Forensic Sci 55:1019–1024. doi:10.1111/j.1556-4029.2010.01396.x

    Article  PubMed  Google Scholar 

  10. Martin RB, Burr DB, Sharkey NA, Fyhrie DP (2015) Skeletal tissue mechanics. Springer, Berlin

  11. Ogden JA (2006) Skeletal injury in the child. Springer, Berlin

  12. Maggiano CM (2011) Making the mold: a microstructural perspective on bone Modeling during growth and mechanical adaption. In: Crowder C, Stout SD (eds) Bone histology: An anthropological perspective. CRC Press, Boca Raton, p 45–90

    Chapter  Google Scholar 

  13. Currey JD (2002) Bones: structure and mechanics. Princeton University Press, Princeton

  14. Robling AG, Castillo AB, Turner CH (2006) Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 8:455–498. doi:10.1146/annurev.bioeng.8.061505.095721

    Article  CAS  PubMed  Google Scholar 

  15. De Margerie E, Robin J-P, Verrier D et al (2004) Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus). J Exp Biol 207:869–879. doi:10.1242/jeb.00841

    Article  PubMed  Google Scholar 

  16. Cubo J, Legendre P, De Ricqlès A et al (2008) Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes. Evol Dev 10:217–227. doi:10.1111/j.1525-142X.2008.00229.x

    Article  PubMed  Google Scholar 

  17. Cambra-Moo O, Nacarino-Meneses C, Díaz-Güemes I et al (2015) Multidisciplinary characterization of the long-bone cortex growth patterns through sheep’s ontogeny. J Struct Biol 191:1–9. doi:10.1016/j.jsb.2015.06.013

    Article  PubMed  Google Scholar 

  18. Starck JM, Chinsamy A (2002) Bone microstructure and developmental plasticity in birds and other dinosaurs. J Morphol 254:232–246. doi:10.1002/jmor.10029

    Article  PubMed  Google Scholar 

  19. Lieberman DE, Devlin MJ, Pearson OM (2001) Articular area responses to mechanical loading: effects of exercise, age, and skeletal location. Am J Phys Anthropol 116:266–277. doi:10.1002/ajpa.1123

    Article  CAS  PubMed  Google Scholar 

  20. Burr DB (2002) Targeted and nontargeted remodeling. Bone 30:2–4. doi:10.1016/S8756-3282(01)00619-6

    Article  CAS  PubMed  Google Scholar 

  21. van Oers RF, Ruimerman R, Tanck E et al (2008) A unified theory for osteonal and hemi-osteonal remodelling. Bone 42(2):250–259

    Article  PubMed  Google Scholar 

  22. Britz HM, Thomas CDL, Clement JG, Cooper DML (2009) The relation of femoral osteon geometry to age, sex, height and weight. Bone 45:77–83. doi:10.1016/j.bone.2009.03.654

    Article  PubMed  Google Scholar 

  23. Stout S, Crowder C (2011) Bone remodeling, histomorphology, and histomorphometry. In: Crowder C, Stout S (eds) Bone histology: an anthropological perspective. CRC Press, Boca Raton, p 23–44

    Chapter  Google Scholar 

  24. Frost HM (1987) Secondary osteon populations: An algorithm for determining mean bone tissue age. Am J Phys Anthropol 30:221–238. doi:10.1002/ajpa.1330300512

    Article  Google Scholar 

  25. Caccia G, Magli F, Tagi VM et al (2016) Histological determination of the human origin from dry bone: a cautionary note for subadults. Int J Leg Med 130:299–307. doi:10.1007/s00414-015-1271-6

    Article  Google Scholar 

  26. Paine RR, Brenton BP (2006) Dietary health does affect histological age assessment: An evaluation of the Stout and Paine (1992) age estimation equation using secondary osteons from the rib. J Forensic Sci 51:489–492. doi:10.1111/j.1556-4029.2006.00118.x

    Article  PubMed  Google Scholar 

  27. Storm T, Steiniche T, Thamsborg G, Melsen F (1993) Changes in bone histomorphometry after long-term treatment with intermittent, cyclic etidronate for postmenopausal osteoporosis. J Bone Miner Res 8:199–208. doi:10.1002/jbmr.5650080211

    Article  CAS  PubMed  Google Scholar 

  28. Duncombe J, Batterly N (1785) The history and antiquities of the three archiepiscopal hospitals and other charitable foundations at and near Canterbury. Bibliotheca Topographica Britannica No XXX. London

  29. Mays S, Elders J, Humphrey L, White W, Marshall P (2013) Science and the Dead: a guidelines for the destructive sampling of archaeological human remains for scientific analysis. Advisory panel on the archaeology of burials in England. English Heritage

  30. Miszkiewicz JJ, Mahoney P (2016) Ancient human bone microstructure in Medieval England: comparisons between two socio-economic groups. Anat Rec 299:42–59. doi:10.1002/ar.23285

    Article  Google Scholar 

  31. Moorrees CF, Fanning E a, Hunt EE (1963) Age variation of formation stages for ten permanent teeth. J Dent Res 42:1490–1502. doi:10.1177/00220345630420062701

    Article  CAS  PubMed  Google Scholar 

  32. Al Qahtani SJ, Hector MP, Liversidge HM (2010) Brief communication: The London atlas of human tooth development and eruption. Am J Phys Anthropol 142:481–490. doi:10.1002/ajpa.21258

    Article  CAS  Google Scholar 

  33. Scheuer L, Black S (2000) Development and ageing of the juvenile skeleton. In: Cox M, Mays S (eds) Hum Osteol Archaeol Forensic Sci. Greenwich Medical Media Ltd, London, pp 9–21

    Google Scholar 

  34. Crowder C, Stout S (2011) Bone histology: an anthropological perspective. CRC Press, Boca Raton

    Google Scholar 

  35. Villa C, Lynnerup N (2010) Technical note: A stereological analysis of the cross-sectional variability of the femoral osteon population. Am J Phys Anthropol 142:491–496. doi:10.1002/ajpa.21269

    Article  PubMed  Google Scholar 

  36. Pfeiffer S (1998) Variability in osteon size in recent human populations. Am J Phys Anthropol 106:219–227

    Article  CAS  PubMed  Google Scholar 

  37. Goulding A (2007) Risk factors for fractures in normally active children and adolescents. In: Daly R, P°etit M (eds) Optimizing bone mass and strength; the role of physical activity and nutrition during growth. Med Sport Sci, vol 51. Karger, Basel, p 102–120. doi:10.1159/000103007

    Chapter  Google Scholar 

  38. Carter DR, Spengler DM (1978) Mechanical properties and composition of cortical bone. Clin Orthop Relat Res 135:192–217

    Google Scholar 

  39. Baxter-Jones AD, Faulkner RA, Forwood MR et al (2011) Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res 26(8):1729–1739

    Article  PubMed  Google Scholar 

  40. Schnitzler CM, Mesquita JM (2013) Cortical porosity in children is determined by age-dependent osteonal morphology. Bone 55:476–486. doi:10.1016/j.bone.2013.03.021

    Article  PubMed  Google Scholar 

  41. Skedros JG, Knight AN, Clark GC et al (2013) Scaling of Haversian canal surface area to secondary osteon bone volume in ribs and limb bones. Am J Phys Anthropol 151(2):230–244

    Article  PubMed  Google Scholar 

  42. Pfeiffer S, Crowder C, Harrington L, Brown M (2006) Secondary osteon and Haversian canal dimensions as behavioral indicators. Am J Phys Anthropol 131:460–468. doi:10.1002/ajpa.20454

    Article  PubMed  Google Scholar 

  43. Skedros JG, Mason MW, Bloebaum RD (1994) Differences in osteonal micromorphology between tensile and compressive cortices of a bending skeletal system: Indications of potential strain- specific differences in bone microstructure. Anat Rec 239:405–413. doi:10.1002/ar.1092390407

    Article  CAS  PubMed  Google Scholar 

  44. Robling AG, Stout SD (1999) Morphology of the drifting osteon. Cells Tissues Organs 164:192–204. doi:10.1159/000016659

    Article  CAS  PubMed  Google Scholar 

  45. Sedlin ED, Frost HM, Villanueva AR (1963) Variations in cross-section area of rib cortex with age. J Gerontol 18:9–13

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Human Osteology Lab, Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury, CT2 7NR, UK

    Rosie Pitfield & Patrick Mahoney

  2. Skeletal Biology and Forensic Anthropology Research Group, School of Archaeology and Anthropology, The Australian National University, Canberra, 2601, Australia

    Justyna J. Miszkiewicz

Authors
  1. Rosie Pitfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Justyna J. Miszkiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrick Mahoney
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosie Pitfield.

Ethics declarations

Conflict of interest

Rosie Pitfield, Patrick Mahonaey, and Justyna, J. Miszkiewicz declare that they have no conflict of interest.

Ethical Approval

No permits were required for the present study as the skeletal samples are archaeological, and pre-date the Human Tissue Act. All sampling followed appropriate codes of ethics for research conducted on human skeletons from an archaeological context.

Informed Consent

This article does not contain information from any living human participants.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pitfield, R., Miszkiewicz, J.J. & Mahoney, P. Cortical Histomorphometry of the Human Humerus During Ontogeny. Calcif Tissue Int 101, 148–158 (2017). https://doi.org/10.1007/s00223-017-0268-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-017-0268-1

Keywords

Search

Navigation