Inter-population variation of histomorphometric variables used in the estimation of age-at-death

Abstract

Population variation of several microscopic structures used in age-at-death estimation was assessed for three different population samples. The aim of the study was to determine if the need exists for population-specific standards when dealing with individuals of African and European origin. A total sample 223 bone sections from the anterior cortex of the femur (n = 99 black South Africans, n = 94 white South Africans and n = 30 Danish individuals) were analysed using a stereological protocol. Variables assessed included the average number of osteons per grid area (OPD), osteon size and Haversian canal size. ANCOVA was employed for assessment of statistically significant differences. The results indicated that OPD differed significantly between the three groups, but that osteon size was similar for all individuals. Haversian canal size showed unpredictable changes with age and high levels of variation, making it unsuitable to use for age estimation as a single factor. As there are conflicting opinions in the literature on whether to use population-specific equations for the estimation of age-at-death or not, this paper provided additional insight into the use of specific variables and its related variation between groups.

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References

  1. 1.

    Thompson DD (1979) The core technique in the determination of age at death of skeletons. J Forensic Sci 24:902–915

    CAS  PubMed  Google Scholar 

  2. 2.

    Ericksen MF, Stix AI (1991) Histologic examination of age of the first African Baptist church adults. Am J Phys Anthropol 85:247–252

    CAS  PubMed  Google Scholar 

  3. 3.

    Stout SD, Paine RR (1992) Histological age estimation using rib and clavicle. Am J Phys Anthropol 87:111–115

    CAS  PubMed  Google Scholar 

  4. 4.

    Eriksen EF, Axelrod DW, Melsen F (1994) Bone Histomorphometry. Raven Press, New York

    Google Scholar 

  5. 5.

    Crowder C, Heinrich J, Dominquez V (2009) Histological age estimation. In: Blau S, Ubelaker D (eds) Handbook of forensic anthropology and archaeology. Left Coast Press, Walnut Creek, CA, pp 222–235

    Google Scholar 

  6. 6.

    Maat GJR, Maes A, Aarents J, Nagelkerke NJD (2006) Histological age prediction from the femur in a contemporary Dutch sample: a decrease of nonremodeled bone in the anterior cortex. J Forensic Sci 51:230–237

    PubMed  Google Scholar 

  7. 7.

    Villa C, Lynnerup N (2009) A stereological analysis of the cross-sectional variability of the femoral osteon population. Am J Phys Anthropol 142:491–496

    Google Scholar 

  8. 8.

    Lynneryp N, Frohlich B, Thomsen JL (2006) Assessment of age at death by microscopy: unbiased quantification of secondary osteons in femoral cross sections. Forensic Sci Int 159S:S100–S103

    Google Scholar 

  9. 9.

    Keough N (2007) Estimation of age at death from the microscopic structure of the femur. MSc Dissertation, University of Pretoria

  10. 10.

    Bryant RJ, Wastney ME, Martin RR et al (2003) Racial differences in bone turnover and calcium metabolism in adolescent females. J Clin Endocrinol Metab 88:1043–1047

    CAS  PubMed  Google Scholar 

  11. 11.

    Wetzsteon RJ, Hughes JM, Kaufman BC, Vazquez G, Stoffregen TA, Stovitz SD, Petit MA (2009) Ethnic differences in bone geometry and strength are apparent in childhood. Bone 44:970–975

    CAS  PubMed  Google Scholar 

  12. 12.

    Pollock NK, Laing EM, Taylor RG, Baile CA, Hamrick MW, Hall DB, Lewis RD (2011) Comparisons of trabecular and cortical bone in late adolescent black and white females. J Bone Miner Metab 29:44–53

    PubMed  Google Scholar 

  13. 13.

    Nelson DA, Jacobsen G, Barondess DA, Parfitt AM (1995) Ethnic differences in regional bone density, hip axis length, and lifestyle variables among health black and white men. J Bone Miner Res 10:782–787

    CAS  PubMed  Google Scholar 

  14. 14.

    Aloia JF, Vaswani A, Ma R, Flaster E (1997) Comparison of body composition in black and white premenopausal women. J Lab Clin Med 129:294–299

    CAS  PubMed  Google Scholar 

  15. 15.

    Gilsanz V, Roe TF, Mora S, Costin G, Goodman WG (1991) Changes in vertebral bone density in black and white girls during childhood and puberty. N Engl J Med 325:1597–1600

    CAS  PubMed  Google Scholar 

  16. 16.

    Hochberg MC (2007) Racial differences in bone strength. Trans Am Clin Climatol Assoc 118:305–315

    PubMed  PubMed Central  Google Scholar 

  17. 17.

    Cohn SH, Abesamis C, Zanzi I et al (1977) Body elemental composition: comparison between black and white adults. Am J Phys 232:E419–E422

    CAS  Google Scholar 

  18. 18.

    Wang M, Bachrach L, Loan V et al (2005) The relative contributions of lean tissue mass and fat mass to bone density in young women. Bone 37:474–481

    CAS  PubMed  Google Scholar 

  19. 19.

    Weinstein R, Bell N (1988) Diminished rates of bone formation in normal black adults. N Engl J Med 319:1698–1701

    CAS  PubMed  Google Scholar 

  20. 20.

    Kleerekoper M, Nelson DA, Peterons EL et al (1994) Reference data for bone mass, calciotropic hormones and biochemical markers of bone remodelling in older (55-75) postmenopausal white and black women. J Bone Miner Res 9:1267–1276

    CAS  PubMed  Google Scholar 

  21. 21.

    Schnitzler CM, Pettifor JM, Mesquita JM et al (1990) Histomorphometry of the iliac crest bone in 346 normal black and white south African adults. Bone Miner 10:18–199

    Google Scholar 

  22. 22.

    Schnitzler CM, Mesquita JM (2006) Cortical bone histomorphometry of the iliac crest in normal black and white south African adults. Calcif Tissue Int 79:373–382

    CAS  PubMed  Google Scholar 

  23. 23.

    Mikhail MB, Vaswani AN, Aloia JF (1996) Racial differences in femoral dimensions and their relationship to hip fracture. Osteoporos Int 6:22–24

    CAS  PubMed  Google Scholar 

  24. 24.

    Braun M, Palacios C, Wigertz K, Jackman LA, Bryant RJ, McCabe LD, Martin BR, McCabe GP, Peacock M, Weaver CM (2007) Racial differences in skeletal calcium retention in adolescent girls with varied controlled calcium intakes. Am J Clin Nutr 85:1657–1663

    CAS  PubMed  Google Scholar 

  25. 25.

    Heaney RP (2002) Ethnicity, bone status and the calcium requirement. Nutr Res 22:153–178

    CAS  Google Scholar 

  26. 26.

    Aloia JF, Talwar SA, Pollack S, Yeh J (2005) A randomized controlled trial of vitamin D3 supplementation in African American women. Arch Intern Med 165:1618–1623

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Aloia JF (2008) African Americans, 25-hydroxyvitamin D and osteoporosis: a paradox. Am J Clin Nutr 88(suppl):545–550

    Google Scholar 

  28. 28.

    Fleet JC, Harris SS, Wood RJ, Dawson-Hughes B (1995) The BsmI vitamin D receptor restriction fragment length polymorphism (BB) predicts low bone density in premenopausal black and white women. J Bone Miner Res 10:985–990

    CAS  PubMed  Google Scholar 

  29. 29.

    Peacock M, Turner CH, Econs MJ, Foroud T (2002) Genetics of osteoporosis. Endocr Rev 23:303–326

    CAS  PubMed  Google Scholar 

  30. 30.

    Daniels ED, Pettifor JM, Schnitzler CM, Russell SW, Patel DN (1995) Ethnic differences in bone density in female south African nurses. J Bone Miner Res 10:359–367

    CAS  PubMed  Google Scholar 

  31. 31.

    Qiu S, Rao DS, Palnitkar S, Parfitt AM (2006) Differences in osteocyte and lacunar density between black and white American women. Bone 38:130–135

    PubMed  Google Scholar 

  32. 32.

    Williams DR (1999) Race, socioeconomic status and health: the added effects of racism and discrimination. Ann N Y Acad Sci 896:173–188

    CAS  PubMed  Google Scholar 

  33. 33.

    Steyn M, Meiring JJ, Nienaber WC (1997) Forensic anthropology in South Africa: a profile of cases from 1993 to 1995 at the Department of Anatomy, University of Pretoria. S Afr J Ethnol 20:23–26

    Google Scholar 

  34. 34.

    Mundy GR (1999) Bone remodelling. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism. Lippencott. Williams and Wilkins, Philadelphia, pp 30–38

    Google Scholar 

  35. 35.

    Kohrt WM, Bloomfield SA, Little KD et al (2004) Physical activity and bone health. Am Coll Sports Med:1985–1996

  36. 36.

    Lanyon LE, Rubin CT, Baust G (1986) Modulation of bone loss during calcium insufficiency by controlled dynamic loading. Calcif Tissue Int 38:209–216

    CAS  PubMed  Google Scholar 

  37. 37.

    Palacios C (2006) The role of nutrients in bone health, from a to Z. Crit Rev Food Sci Nutr 46:621–628

    CAS  PubMed  Google Scholar 

  38. 38.

    Cashman KD (2007) Diet, nutrition and bone health. J Nutr 137:2507S–2512S

    CAS  PubMed  Google Scholar 

  39. 39.

    Ullits LR, Ejlskov L, Mortensen RN, Hansen SM, Kræmer SRJ, Vardinghus-Nielsen H, Fonager K, Bøggild H, Torp-Pedersen C, Overgaard C (2015) Socioeconomic inequality and mortality – a regional Danish cohort study. BMC Public Health 15:490

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Smith AM, Baghurst KI (1992) Public health implications of dietary differences between social status and occupational category groups. J Epidemiol Community Health 46:409–416

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Smith GD, Brunner E (1997) Socio-economic differentials in health: the role of nutrition. Proc Nutr Soc 56:75–90

    CAS  PubMed  Google Scholar 

  42. 42.

    Mackenbach JP, Kunst AE, Cavelaar AEJM et al (1997) Socioeconomic inequalities in morbidity and mortality in western Europe. Lancet 349:1655–1659

    CAS  PubMed  Google Scholar 

  43. 43.

    Groth MV, Fagt S, Brøndsted L (2001) Original communication: social determinants of dietary habits in Denmark. Eur J Clin Nutr 55:959–966

    CAS  PubMed  Google Scholar 

  44. 44.

    Keough N, L’Abbé EN, Steyn M (2009) The evaluation of age-related histomorphometric variables in a cadaver sample of lower socioeconomic status: implications for estimation of age at death. Forensic Sci Int 191:114.e1–114.e6

    CAS  Google Scholar 

  45. 45.

    Botha D, Bhagwandin A, Lynnerup N, Steyn M (2018) The use of stereological methods in the histomorphometric assessment of bone for age-at-death estimation. Forensic Sci Int 290:353.e1–353.e7

    CAS  Google Scholar 

  46. 46.

    L’Abbé EN, Loots M, Meiring JH (2005) The Pretoria bone collection: a modern south African skeletal sample. HOMO – J Comp Hum Biol 56:197–205

    Google Scholar 

  47. 47.

    Maat GJR, Van den Bos RPM, Aarents MJ (2002) Manual for the Preparation of Ground Sections for theMicroscopy of Bone Tissue. Published by Barge’s Anthropologica Nr. 7. Leiden University Medical Centre, Leiden

  48. 48.

    Howard CV, Reed MG (2010) Unbiased stereology, 2nd edn. QTP Publications, Liverpool

    Google Scholar 

  49. 49.

    Huitema BE (2011) The analysis of covariance and alternatives. Wiley, Hobokon

    Google Scholar 

  50. 50.

    Cho H, Stout SD, Madsen RW, Streeter MA (2002) Population-specific histological age-estimating method: a model for known African-American and European-American skeletal remains. J Forensic Sci 47:12–18

    PubMed  Google Scholar 

  51. 51.

    Lynnerup N, Thomsen JL, Frohlich B (1998) Intra- and inter-observer variation in histological criteria use in age at death determination based on femoral cortical bone. Forensic Sci Int 91:219–230

    CAS  PubMed  Google Scholar 

  52. 52.

    Pfeiffer S, Heinrich J, Beresheim A, Alblas M (2016) Cortical bone histomorphometry of known-age skeletons from the Kirsten collection, Stellenbosch University, South Africa. Am J Phys Anthropol 160:137–147

    PubMed  PubMed Central  Google Scholar 

  53. 53.

    Kim J-N, Lee J-Y, Shin K-J, Gil YC, Koh KS, Song WC (2015) Haversian system of compact bone and comparison between endosteal and periosteal sides using three-dimensional reconstruction in rat. Anat Cell Biol 48:258–261

    PubMed  PubMed Central  Google Scholar 

  54. 54.

    Pratte DG, Pfeiffer S (1999) Histological age estimation of a cadaveral sample of diverse origins. Can Soc Forensic Sci J 32:155–167

    Google Scholar 

  55. 55.

    Berenson AB, Rahman M, Wilkinson G (2009) Racial differences in the correlates of bone mineral content/density and age at peak among reproductive-aged women. Osteoporos Int 20:1439–1449

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Hui SL, Perkins AJ, Harezlak J, Peacock M, McClintock CL, Johnston CC Jr (2010) Velocities of bone mineral accrual in black and white American children. J Bone Miner Res 25:1527–1535

    PubMed  PubMed Central  Google Scholar 

  57. 57.

    Ettinger B, Sidney S, Cummings SR et al (1997) Racial differences in bone density between young adult black and white subjects persist after adjustment for anthropometric, lifestyle and biochemical differences. J Clin Endocrinol Metab 82:429–434

    CAS  PubMed  Google Scholar 

  58. 58.

    Wilkin LD, Jackson MC, Sims TD, Haddock BL (2010) Racial/ethnic differences in bone mineral density of young adults. Int J Exerc Sci 3:197–205

    PubMed  PubMed Central  Google Scholar 

  59. 59.

    Perry HM III, Horowitz M, Morley JE et al (1996) Ageing and bone metabolism in African American and Caucasian women. J Clin Endocrinol Metab 81:1108–1117

    CAS  PubMed  Google Scholar 

  60. 60.

    Armas LA, Dowell S, Akhter M et al (2007) Ultraviolet-B radiation increases serum 25-hydroxyvitamin D levels: the effect of UVB dose and skin color. J Am Acad Dermatol 57:588–593

    PubMed  Google Scholar 

  61. 61.

    Gloth FM 3rd, Alam W, Hollis B (1999) Vitamin D vs broad spectrum phototherapy in the treatment of seasonal affective disorder. J Nutr Health Aging 3:5–7

    PubMed  Google Scholar 

  62. 62.

    Harris SS, Eccleshall TR, Gross C et al (1997) The vitamin D receptor start codon polymorphism (FokI) and bone mineral density in premenopausal American black and white women. J Bone Miner Res 12:1043–1048

    CAS  PubMed  Google Scholar 

  63. 63.

    Aloia JF, Vaswani A, Ma R, Flaster E (1996) Body composition in normal black women: the four-compartment model. J Clin Endocrinol Metab 81:2363–2369

    CAS  PubMed  Google Scholar 

  64. 64.

    Shaffer JR, Kammerer CM, Reich D, McDonald G, Patterson N, Goodpaster B, Bauer DC, Li J, Newman AB, Cauley JA, Harris TB, Tylavsky F, Ferrell RE, Zmuda JM, for the Health ABC study (2007) Genetic markers for ancestry are correlated with body composition traits in older African Americans. Osteoporos Int 18:733–741

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank the curators of the collections for granting permission to access the bone samples, Prof. Ripamonti for the use of the Bone Research Laboratory (WITS), Prof. Manger for the use of the stereology system and Dr. Bhagwandin for technical assistance in producing the images for analysis.

Funding

Funding for this project was provided by the NRF.

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Correspondence to D. Botha.

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Botha, D., Lynnerup, N. & Steyn, M. Inter-population variation of histomorphometric variables used in the estimation of age-at-death. Int J Legal Med 134, 709–719 (2020). https://doi.org/10.1007/s00414-019-02048-7

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Keywords

  • Femur
  • Stereology
  • OPD
  • Osteon size
  • Haversian canal size