Advertisement

Socio-economic Determinants of Bone Health from Past to Present

  • Justyna J. MiszkiewiczEmail author
  • Karen M. Cooke
Review Article

Abstract

Increasing epidemiology evidence amounts for social determinants of bone health underlying musculo-skeletal conditions such as osteoporosis. Amongst different facets influencing skeletal health, socio-economic status (SES) has been identified as a critical factor determining one’s access to resources, health care, education, nutrition, and physical activity. Recent conceptual and epigenetic studies assessing SES links with DNA methylation offer further support for the adverse effects of social disadvantage in early life on bone quantity and quality in adulthood. However, this evidence for socially patterned risks in bone fragility is not restricted to the contemporary society. Data exist for ancient human skeletal samples deriving from SES stratified cemeteries that also reflect bone changes consistent with lifestyles specific to social standing. Similarly to modern data, the conclusion drawn from the ancient times has been for a negative effect of low SES on bone growth and maintenance. Some contradictory results, mirroring previously reported inconsistencies in epidemiological studies, have also been reported showing that high SES can equally result in poor bone health. It becomes clear that ancient perspectives can offer a further line of support into these ongoing epidemiological and epigenetic research efforts. Taken together, a holistic approach to clinical understanding and practice of bone health is recommended, building upon ancient and modern findings to target living groups who are most at risk of developing low bone mass and compromised bone micro-architecture.

Keywords

Socio-economic status Osteoporosis Inequality Inequity DNA methylation Bone loss Histomorphometry Lifestyle Epigenetics Social epidemiology Bioarchaeology Biological anthropology 

Abbreviations

aDNA

Ancient DNA

BMD

Bone mineral density

CT

Computed tomography

DISH

Diffuse idiopathic skeletal hyperostosis

DXA

Dual-energy X-ray absorptiometry

DNAm

DNA methylation

DOHaD

Developmental Origins of Health and Disease

GWAS

Genome-wide association study

LEH

Linear enamel hypoplasia

MES

Minimum effective strain

miRNA

Micro-RNA

PTH

Parathyroid hormone

RANKL

Receptor activator of nuclear factor kappa-Β ligand

SDoH

Social Determinants of Health

SES

Socio-economic status

SFI

Skeletal frailty index

Notes

Acknowledgements

The authors would like to thank Dr. Patrick Mahoney for facilitating access to samples at the Human Osteology Laboratory at the University of Kent (UK)—image in Fig. 1 represents a sample processed by JJM during her PhD studentship there. We also thank Prof Matthew Allen and Prof Jose Riancho for inviting us to write this review, and two anonymous reviewers whose comments greatly improved our article. The completion of this article was possible thanks to OSP 2019 funds from the Australian National University (to JJM) and the Australian Government Research Training Program (RTP) Scholarship (to KMC).

Compliance with Ethical Standards

This article does not feature data from living humans, human autopsies, or animals. We include an image of medieval human femur bone histology sample from an anthropological collection curated at the University of Kent, Canterbury, UK. The collection pre-dates the Human Tissue Act and was studied following the 2008 British Association for Biological Anthropology and Osteoarchaeology (BABAO) Code of Ethics, 2010 BABAO Code of Practice, 2012 American Anthropological Association Code of Ethics, and 2003 Code of Ethics of the American Association of Physical Anthropologists.

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with living human participants or animals performed by any of the authors.

Informed Consent

Not applicable.

References

  1. 1.
    Burr DB, Allen MR. Basic and applied bone biology. San Diego: Academic Press; 2019.Google Scholar
  2. 2.
    Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng. 2006;8:455–98.  https://doi.org/10.1146/annurev.bioeng.8.061505.095721.CrossRefPubMedGoogle Scholar
  3. 3.
    Kenkre JS, Bassett JH. The bone remodelling cycle. Ann Clin Biochem. 2018;55(3):308–27.  https://doi.org/10.1177/0004563218759371.CrossRefPubMedGoogle Scholar
  4. 4.
    Florencio-Silva R, Sasso GR, Sasso-Cerri E, Simões MJ, Cerri PS. Biology of bone tissue: structure, function, and factors that influence bone cells. Biomed Res Int. 2015;2015:1–17.  https://doi.org/10.1155/2015/421746.CrossRefGoogle Scholar
  5. 5.
    Frenkel B, Hong A, Baniwal SK, Coetzee GA, Ohlsson C, Khalid O, et al. Regulation of adult bone turnover by sex steroids. J Cell Physiol. 2010;224(2):305–10.  https://doi.org/10.1002/jcp.22159.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Cwikel J, Fried AV. The social epidemiology of falls among community-dwelling elderly: guidelines for prevention. Disabil Rehabil. 1992;14(3):113–21.CrossRefPubMedGoogle Scholar
  7. 7.
    Moradzadeh R, Nadrian H, Golboni F, Kazemi-Galougahi MH, Moghimi N. Economic inequalities amongst women with osteoporosis-related fractures: an application of concentration index decomposition. Health Promot Perspect. 2016;6(4):190–5.  https://doi.org/10.15171/hpp.2016.31.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Syddall HE, Evandrou M, Dennison EM, Cooper C, Sayer AA. Social inequalities in osteoporosis and fracture among community-dwelling older men and women: findings from the Hertfordshire Cohort Study. Arch Osteoporos. 2012;7(1-2):37–48.  https://doi.org/10.1007/s11657-012-0069-0.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Brennan SL, Holloway KL, Williams LJ, Kotowicz MA, Bucki-Smith G, Moloney DJ, et al. The social gradient of fractures at any skeletal site in men and women: data from the Geelong Osteoporosis Study Fracture Grid. Osteoporos Int. 2015;26(4):1351–9.  https://doi.org/10.1007/s00198-014-3004-y.CrossRefPubMedGoogle Scholar
  10. 10.
    Brennan SL, Henry MJ, Nicholson GC, Kotowicz MA, Pasco JA. Socioeconomic status, obesity and lifestyle in men: the Geelong Osteoporosis Study. J Men's Health. 2010;7(1):31–41.  https://doi.org/10.1016/j.jomh.2009.10.004.CrossRefGoogle Scholar
  11. 11.
    Brennan-Olsen SL, Williams LJ, Holloway KL, Hosking SM, Stuart AL, Dobbins AG, et al. Small area-level socioeconomic status and all-cause mortality within 10 years in a population-based cohort of women: data from the Geelong Osteoporosis Study. Prev Med Rep. 2015;2:505–11.  https://doi.org/10.1016/j.pmedr.2015.05.011.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Quah C, Boulton C, Moran C. The influence of socioeconomic status on the incidence, outcome and mortality of fractures of the hip. J Bone Joint Surg Br. 2011;93(6):801–5.  https://doi.org/10.1302/0301-620X.93B6.24936.CrossRefPubMedGoogle Scholar
  13. 13.
    Brennan SL, Leslie WD, Lix LM. Associations between adverse social position and bone mineral density in women aged 50 years or older: data from the Manitoba Bone Density Program. Osteoporos Int. 2013;24(9):2405–12.  https://doi.org/10.1007/s00198-013-2311-z.CrossRefPubMedGoogle Scholar
  14. 14.
    Navarro MD, Saavedra P, Jódar E, Gómez de Tejada MJ, Mirallave A, Sosa M. Osteoporosis and metabolic syndrome according to socio-economic status, contribution of PTH, vitamin D and body weight: the Canarian Osteoporosis Poverty Study (COPS). Clin Endocrinol. 2013;78(5):681–6.  https://doi.org/10.1111/cen.12051.CrossRefGoogle Scholar
  15. 15.
    Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res. 2007;22(3):465–75.  https://doi.org/10.1359/jbmr.061113.CrossRefPubMedGoogle Scholar
  16. 16.
    Hernlund E, Svedbom A, Ivergård M, Compston J, Cooper C, Stenmark J, et al. Osteoporosis in the European Union: medical management, epidemiology and economic burden. Arch Osteoporos. 2013;8(1-2):136.  https://doi.org/10.1007/s11657-013-0136-1.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Mohd-Tahir NA, Li SC. Economic burden of osteoporosis-related hip fracture in Asia: a systematic review. Osteoporos Int. 2017;28(7):2035–44.  https://doi.org/10.1007/s00198-017-3985-4.CrossRefPubMedGoogle Scholar
  18. 18.
    Riggs BL, Melton LJ III. The prevention and treatment of osteoporosis. N Engl J Med. 1992;327(9):620–7.  https://doi.org/10.1056/NEJM199208273270908.CrossRefPubMedGoogle Scholar
  19. 19.
    Bougioukli S, Κollia P, Koromila T, Varitimidis S, Hantes M, Karachalios T, et al. Failure in diagnosis and under-treatment of osteoporosis in elderly patients with fragility fractures. J Bone Miner Metab. 2019;37(2):327–35.  https://doi.org/10.1007/s00774-018-0923-2.CrossRefPubMedGoogle Scholar
  20. 20.
    Siris ES, Modi A, Tang J, Gandhi S, Sen S. Substantial under-treatment among women diagnosed with osteoporosis in a US managed-care population: a retrospective analysis. Curr Med Res Opin. 2014;30(1):123–30.  https://doi.org/10.1185/03007995.2013.851074.CrossRefPubMedGoogle Scholar
  21. 21.
    Feldstein AC, Nichols G, Orwoll E, Elmer PJ, Smith DH, Herson M, et al. The near absence of osteoporosis treatment in older men with fractures. Osteoporos Int. 2005;16(8):953–62.  https://doi.org/10.1007/s00198-005-1950-0.CrossRefPubMedGoogle Scholar
  22. 22.
    Brennan-Olsen SL, Page RS, Berk M, Riancho JA, Leslie WD, Wilson SG, et al. DNA methylation and the social gradient of osteoporotic fracture: a conceptual model. Bone. 2016;84:204–12.  https://doi.org/10.1016/j.bone.2015.12.015.CrossRefPubMedGoogle Scholar
  23. 23.
    Riancho JA, Brennan-Olsen SL. The epigenome at the crossroad between social factors, inflammation, and osteoporosis risk. Clinic Rev Bone Miner Metab. 2017;15(2):59–68.  https://doi.org/10.1007/s12018-017-9229-5.CrossRefGoogle Scholar
  24. 24.
    Bocheva G, Boyadjieva N. Epigenetic regulation of fetal bone development and placental transfer of nutrients: progress for osteoporosis. Interdiscip Toxicol. 2011;4(4):167–72.  https://doi.org/10.2478/v10102-011-0026-6.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Agarwal SC, Stout SD. Bone loss and osteoporosis: an anthropological perspective. New York: Springer US; 2003.  https://doi.org/10.1007/978-1-4419-8891-1.CrossRefGoogle Scholar
  26. 26.
    Miszkiewicz JJ, Mahoney P. Ancient human bone microstructure in medieval England: comparisons between two socio-economic groups. Anat Rec. 2016;299(1):42–59.  https://doi.org/10.1002/ar.23285.CrossRefGoogle Scholar
  27. 27.
    Robb J, Bigazzi R, Lazzarini L, Scarsini C, Sonego F. Social “status” and biological “status”: a comparison of grave goods and skeletal indicators from Pontecagnano. Am J Phys Anthropol. 2001;115(3):213–22.  https://doi.org/10.1002/ajpa.1076.CrossRefPubMedGoogle Scholar
  28. 28.
    Agarwal SC. Bone morphologies and histories: life course approaches in bioarchaeology. Am J Phys Anthropol. 2016;159(Suppl 61):S130–49.  https://doi.org/10.1002/ajpa.22905.CrossRefPubMedGoogle Scholar
  29. 29.
    Vercellotti G, Stout SD, Boano R, Sciulli PW. Intrapopulation variation in stature and body proportions: social status and sex differences in an Italian medieval population (Trino Vercellese, VC). Am J Phys Anthropol. 2011;145(2):203–14.  https://doi.org/10.1002/ajpa.21486.CrossRefPubMedGoogle Scholar
  30. 30.
    Agarwal SC, Grynpas MD. Bone quantity and quality in past populations. Anat Rec. 1996;246(4):423–32.  https://doi.org/10.1002/(SICI)1097-0185(199612)246:4<423::AID-AR1>3.0.CO;2-W.CrossRefPubMedGoogle Scholar
  31. 31.
    Miszkiewicz JJ, Brennan-Olsen S, Riancho JA. Bone Health: a reflection of the Social Mosaic. Singapore: Springer Nature Medicine; 2019 In press.  https://doi.org/10.1007/978-981-13-7256-8.CrossRefGoogle Scholar
  32. 32.
    Dahlgren G, Whitehead M. Policies and strategies to promote social equity and health. World Health Organisation: Copenhagen; 1992.Google Scholar
  33. 33.
    Toulouse C, Kodadek M. Continuous access to medication and health outcomes in uninsured adults with type 2 diabetes. J Am Assoc Nurse Pract. 2016;28(6):327–34.  https://doi.org/10.1002/2327-6924.12326.CrossRefPubMedGoogle Scholar
  34. 34.
    Bowen EA, Walton QL. Disparities and the social determinants of mental health and addictions: opportunities for a multifaceted social work response. Health Soc Work. 2015;40(3):e59–65.  https://doi.org/10.1093/hsw/hlv034.CrossRefGoogle Scholar
  35. 35.
    Lee DR, Santo EC, Lo JC, Weintraub ML, Patton M, Gordon NP. Understanding functional and social risk characteristics of frail older adults: a cross-sectional survey study. BMC Fam Pract. 2018;19(1):170.  https://doi.org/10.1186/s12875-018-0851-1.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007;261(5):412–7.  https://doi.org/10.1111/j.1365-2796.2007.01809.x.CrossRefPubMedGoogle Scholar
  37. 37.
    Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;1(8489):1077–81.  https://doi.org/10.1016/S0140-6736(86)91340-1.CrossRefPubMedGoogle Scholar
  38. 38.
    Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577–80.  https://doi.org/10.1016/s0140-6736(89)90710-1.CrossRefPubMedGoogle Scholar
  39. 39.
    Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993;341(8850):938–41.  https://doi.org/10.1016/0140-6736(93)91224-a.CrossRefPubMedGoogle Scholar
  40. 40.
    Wadhwa PD, Buss C, Entringer S, Swanson JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009;27(5):358–68.  https://doi.org/10.1055/s-0029-1237424.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Armitage JA, Poston L, Taylor PD. Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity. Front Horm Res. 2008;36:73–84.  https://doi.org/10.1159/0000115355.CrossRefPubMedGoogle Scholar
  42. 42.
    Tuovinen S, Räikkönen K, Pesonen AK, Lahti M, Heinonen K, Wahlbeck K, et al. Hypertensive disorders in pregnancy and risk of severe mental disorders in the offspring in adulthood: the Helsinki Birth Cohort Study. J Psychiatr Res. 2012;46(3):303–10.  https://doi.org/10.1016/j.jpsychires.2011.11.015.CrossRefPubMedGoogle Scholar
  43. 43.
    Walker CL, Ho SM. Developmental reprogramming of cancer susceptibility. Nat Rev Cancer. 2012;12(7):479–86.  https://doi.org/10.1038/nrc3220.CrossRefPubMedGoogle Scholar
  44. 44.
    Inadera H. Developmental origins of obesity and type 2 diabetes: molecular aspects and role of chemicals. Environ Health Prev Med. 2013;18(3):185–97.  https://doi.org/10.1007/s12199-013-0328-8.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Wood CL, Wood AM, Harker C, Embleton ND. Bone mineral density and osteoporosis after preterm birth: the role of early life factors and nutrition. Int J Endocrinol. 2013;2013:902513–7.  https://doi.org/10.1155/2013/902513.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Wood CL, Stenson C, Embleton N. The developmental origins of osteoporosis. Curr Genomics. 2015;16(6):411–8.  https://doi.org/10.2174/1389202916666150817202217.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Dennison EM, Syddall HE, Sayer AA, Gilbody HJ, Cooper C. Birth weight and weight at 1 year are independent determinants of bone mass in the seventh decade: the Hertfordshire cohort study. Pediatr Res. 2005;57(4):582–6.  https://doi.org/10.1203/01.PDR.0000155754.67821.CA.CrossRefPubMedGoogle Scholar
  48. 48.
    Hanson M, Cooper C. DOHaD: the concept, its implications and applications. In: Harvey NC, Cooper C, editors. Osteoporosis: a lifecourse epidemiology approach to skeletal Health. Boca Raton: CRC Press; 2018. p. 21–31.  https://doi.org/10.1201/9781351234627.CrossRefGoogle Scholar
  49. 49.
    Harvey NC, Cooper C. Osteoporosis: a lifecourse epidemiology approach to skeletal Health. Boca Raton: CRC Press. 2018.  https://doi.org/10.1201/9781351234627.
  50. 50.
    Brennan SL, Pasco JA, Urquhart DM, Oldenburg B, Wang Y, Wluka AE. Association between socioeconomic status and bone mineral density in adults: a systematic review. Osteoporos Int. 2011;22(2):517–27.  https://doi.org/10.1007/s00198-010-1261-y.CrossRefPubMedGoogle Scholar
  51. 51.
    Valimaki MJ, Karkkainen M, Lamberg-Allardt C, Laitinen K, Alhava E, Heikkinen J, et al. Exercise, smoking, and calcium intake during adolescence and early adulthood as determinants of peak bone mass. Cardiovascular Risk in Young Finns Study Group. BMJ. 1994;309(6949):230–5.  https://doi.org/10.1136/bmj.309.6949.230.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Suen LK. Occupation and risk of hip fracture. J Public Health Med. 1998;20(4):428–33.CrossRefPubMedGoogle Scholar
  53. 53.
    Johnson NA, Jeffery J, Stirling E, Thompson J, Dias JJ. Effects of deprivation, ethnicity, gender and age on distal radius fracture incidence and surgical intervention rate. Bone. 2019;121:1–8.  https://doi.org/10.1016/j.bone.2018.12.018.CrossRefPubMedGoogle Scholar
  54. 54.
    Farahmand BY, Persson PG, Michaëlsson K, Baron JA, Parker MG, Ljunghall S, et al. Socioeconomic status, marital status and hip fracture risk: a population-based case–control study. Osteoporos Int. 2000;11(9):803–8.  https://doi.org/10.1007/s001980070060.CrossRefPubMedGoogle Scholar
  55. 55.
    Varenna M, Binelli L, Zucchi F, Ghiringhelli D, Gallazzi M, Sinigaglia L. Prevalence of osteoporosis by educational level in a cohort of postmenopausal women. Osteoporos Int. 1999;9(3):236–41.  https://doi.org/10.1007/s001980050143.CrossRefPubMedGoogle Scholar
  56. 56.
    Brennan-Olsen SL, Hyde NK, Duckham RL, Zengin A, Talevski J, Green D, et al. Bone quality in socially and ethnically diverse groups: downstream and upstream determinants across the life course. In: Miszkiewicz JJ, Brennan-Olsen SL, Riancho JA, editors. Bone health: a reflection of the social mosaic. Singapore: Springer Medicine; 2019 In press. p. 51–66.  https://doi.org/10.1007/978-981-13-7256-8.CrossRefGoogle Scholar
  57. 57.
    Brennan-Olsen SL, Zengin A, Duckham RL, Hosking SM, Talevski J, Hyde NK. Differences in fracture risk between countries, within countries and between social and ethnic groups. In: Miszkiewicz JJ, Brennan-Olsen SL, Riancho JA, editors. Bone health: a reflection of the social mosaic. Singapore: Springer Medicine; 2019 In press. p. 67–82.  https://doi.org/10.1007/978-981-13-7256-8.CrossRefGoogle Scholar
  58. 58.
    Fields J, Trivedi NJ, Horton E, Mechanick JI. Vitamin D in the Persian Gulf: integrative physiology and socioeconomic factors. Curr Osteoporos Rep. 2011;9(4):243–50.  https://doi.org/10.1007/s11914-011-0071-2.CrossRefPubMedGoogle Scholar
  59. 59.
    Vatanparast H, Nisbet C, Gushulak B. Vitamin D insufficiency and bone mineral status in a population of newcomer children in Canada. Nutrients. 2013;5(5):1561–72.  https://doi.org/10.3390/nu5051561.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Hochberg Z, Hochberg I. Evolutionary perspective in rickets and vitamin D. Front Endocrinol (Lausanne). 2019;10:306.  https://doi.org/10.3389/fendo.2019.00306.CrossRefGoogle Scholar
  61. 61.
    Mendes MM, Darling AL, Hart KH, Morse S, Murphy RJ, Lanham-New SA. Impact of high latitude, urban living and ethnicity on 25-hydroxyvitamin D status: a need for multidisciplinary action? J Steroid Biochem Mol Biol. 2019;188:95–102.  https://doi.org/10.1016/j.jsbmb.2018.12.012.CrossRefPubMedGoogle Scholar
  62. 62.
    Letarouilly JG, Broux O, Clabaut A. New insights into the epigenetics of osteoporosis. Genomics. 2018.  https://doi.org/10.1016/j.ygeno.2018.05.001.
  63. 63.
    Riancho JA. Epigenetics of osteoporosis: critical analysis of epigenetic epidemiology studies. Curr Genomics. 2015;16(6):405–10.  https://doi.org/10.2174/1389202916666150817213250.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell. 2007;128(4):635–8.  https://doi.org/10.1016/j.cell.2007.02.006.CrossRefPubMedGoogle Scholar
  65. 65.
    Hollstein M, Alexandrov LB, Wild CP, Ardin M, Zavadil J. Base changes in tumour DNA have the power to reveal the causes and evolution of cancer. Oncogene. 2017;36(2):158–67.  https://doi.org/10.1038/onc.2016.192.CrossRefPubMedGoogle Scholar
  66. 66.
    Zhang T, Cooper S, Brockdorff N. The interplay of histone modifications–writers that read. EMBO Rep. 2015;16(11):1467–81.  https://doi.org/10.15252/embr.201540945.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Marchese FP, Huarte M. Long non-coding RNAs and chromatin modifiers: their place in the epigenetic code. Epigenetics. 2014;9(1):21–6.  https://doi.org/10.4161/epi.27472.CrossRefPubMedGoogle Scholar
  68. 68.
    Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science. 2001;293(5532):1068–70.  https://doi.org/10.1126/science.1063852.CrossRefPubMedGoogle Scholar
  69. 69.
    Gordon JA, Montecino MA, Aqeilan RI, Stein JL, Stein GS, Lian JB. Epigenetic pathways regulating bone homeostasis: potential targeting for intervention of skeletal disorders. Curr Osteoporos Rep. 2014;12(4):496–506.  https://doi.org/10.1007/s11914-014-0240-1.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Westendorf JJ. Histone deacetylases in control of skeletogenesis. J Cell Biochem. 2007;102(2):332–40.  https://doi.org/10.1002/jcb.21486.CrossRefPubMedGoogle Scholar
  71. 71.
    Yang S, Duan X. Epigenetics, bone remodeling and osteoporosis. Curr Stem Cell Res Ther. 2018;13(2).  https://doi.org/10.2174/1574888X11666161221125656.
  72. 72.
    Santurtún A, del Real A, Riancho JA. Postnatal social factors, the epigenome and the skeleton. In: Miszkiewicz JJ, Brennan-Olsen SL, Riancho JA, editors. Bone health: a reflection of the social mosaic. Singapore: Springer Medicine; 2019 In press. p. 145–70.  https://doi.org/10.1007/978-981-13-7256-8.CrossRefGoogle Scholar
  73. 73.
    Stringhini S, Polidoro S, Sacerdote C, Kelly RS, Van Veldhoven K, Agnoli C, et al. Life-course socioeconomic status and DNA methylation of genes regulating inflammation. Int J Epidemiol. 2015;44(4):1320–30.  https://doi.org/10.1093/ije/dyv060.CrossRefPubMedGoogle Scholar
  74. 74.
    Velupillai YN, Packard CJ, Batty GD, Bezlyak V, Burns H, Cavanagh J, et al. Psychological, social and biological determinants of ill health (pSoBid): study protocol of a population-based study. BMC Public Health. 2008;8:–126.  https://doi.org/10.1186/1471-2458-8-126.
  75. 75.
    McGuinness D, McGlynn LM, Johnson PC, MacIntyre A, Batty GD, Burns H, et al. Socio-economic status is associated with epigenetic differences in the pSoBid cohort. Int J Epidemiol. 2012;41(1):151–60.  https://doi.org/10.1093/ije/dyr215.CrossRefPubMedGoogle Scholar
  76. 76.
    Stanitz E, Juhasz K, Gombos K, Gőcze K, Toth C, Kiss I. Alteration of miRNA expression correlates with lifestyle, social and environmental determinants in esophageal carcinoma. Anticancer Res. 2015;35(2):1091–7.PubMedGoogle Scholar
  77. 77.
    Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci. 2008;105(44):17046–9.  https://doi.org/10.1073/pnas.0806560105.CrossRefPubMedGoogle Scholar
  78. 78.
    Schulz LC. The Dutch Hunger Winter and the developmental origins of health and disease. Proc Natl Acad Sci. 2010;107(39):16757–8.  https://doi.org/10.1073/pnas.1012911107.CrossRefPubMedGoogle Scholar
  79. 79.
    Tobi EW, Slieker RC, Stein AD, Suchiman HE, Slagboom PE, Van Zwet EW, et al. Early gestation as the critical time-window for changes in the prenatal environment to affect the adult human blood methylome. Int J Epidemiol. 2015;44(4):1211–23.  https://doi.org/10.1093/ije/dyv043.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Jintaridth P, Tungtrongchitr R, Preutthipan S, Mutirangura A. Hypomethylation of Alu elements in post-menopausal women with osteoporosis. PLoS One. 2013;8(8):e70386.  https://doi.org/10.1371/journal.pone.0070386.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Delgado-Calle J, Fernández AF, Sainz J, Zarrabeitia MT, Sañudo C, García-Renedo R, et al. Genome-wide profiling of bone reveals differentially methylated regions in osteoporosis and osteoarthritis. Arthritis Rheum. 2013;65(1):197–205.  https://doi.org/10.1002/art.37753.CrossRefPubMedGoogle Scholar
  82. 82.
    Needham BL, Smith JA, Zhao W, Wang X, Mukherjee B, Kardia SL, et al. Life course socioeconomic status and DNA methylation in genes related to stress reactivity and inflammation: the multi-ethnic study of atherosclerosis. Epigenetics. 2015;10(10):958–69.  https://doi.org/10.1080/15592294.2015.1085139.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    McDade TW, Ryan C, Jones MJ, MacIsaac JL, Morin AM, Meyer JM, et al. Social and physical environments early in development predict DNA methylation of inflammatory genes in young adulthood. Proc Natl Acad Sci. 2017;114(29):7611–6.  https://doi.org/10.1073/pnas.1620661114.CrossRefPubMedGoogle Scholar
  84. 84.
    Appleton AA, Armstrong DA, Lesseur C, Lee J, Padbury JF, Lester BM, et al. Patterning in placental 11-B hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity. PLoS One. 2013;8(9):e74691.  https://doi.org/10.1371/journal.pone.0074691.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Borghol N, Suderman M, McArdle W, Racine A, Hallett M, Pembrey M, et al. Associations with early-life socio-economic position in adult DNA methylation. Int J Epidemiol. 2012;41(1):62–74.  https://doi.org/10.1093/ije/dyr147.CrossRefPubMedGoogle Scholar
  86. 86.
    Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE, et al. Factors underlying variable DNA methylation in a human community cohort. Proc Natl Acad Sci. 2012;109(Suppl 2):17253–60.  https://doi.org/10.1073/pnas.1121249109.CrossRefPubMedGoogle Scholar
  87. 87.
    McDade TW, Ryan CP, Jones MJ, Hoke MK, Borja J, Miller GE, et al. Genome-wide analysis of DNA methylation in relation to socioeconomic status during development and early adulthood. Am J Phys Anthropol. 2019;169(1):3–11.  https://doi.org/10.1002/ajpa.23800.CrossRefPubMedGoogle Scholar
  88. 88.
    Dahly DL, Gordon-Larsen P, Popkin BM, Kaufman JS, Adair LS. Associations between multiple indicators of socioeconomic status and obesity in young adult Filipinos vary by gender, urbanicity, and indicator used. J Nutr. 2010;140(2):366–70.  https://doi.org/10.3945/jn.109.114207.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Jiang R, Jones MJ, Chen E, Neumann SM, Fraser HB, Miller GE, et al. Discordance of DNA methylation variance between two accessible human tissues. Sci Rep. 2015;5(1):8257.  https://doi.org/10.1038/srep08257.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Kanis JA. Diagnosis and clinical aspects of osteoporosis. In: Ferrari SL, Roux C, editors. Pocket reference to osteoporosis. Switzerland: Springer Nature; 2019. p. 11–20.  https://doi.org/10.1007/978-3-319-26757-9.CrossRefGoogle Scholar
  91. 91.
    Crowder C, Stout S. Bone histology: an anthropological perspective. Boca Raton: CRC Press; 2011.Google Scholar
  92. 92.
    Katzenberg MA, Grauer AL. Biological anthropology of the human skeleton. Hoboken: John Wiley & Sons; 2018.CrossRefGoogle Scholar
  93. 93.
    Agarwal SC, Glencross BA. Social bioarchaeology. Hoboken: John Wiley & Sons; 2011.CrossRefGoogle Scholar
  94. 94.
    Cucina A, Tiesler V. Dental caries and antemortem tooth loss in the Northern Peten area, Mexico: a biocultural perspective on social status differences among the Classic Maya. Am J Phys Anthropol. 2003;122(1):1–10.  https://doi.org/10.1002/ajpa.10267.CrossRefPubMedGoogle Scholar
  95. 95.
    Nakayama N. The relationship between linear enamel hypoplasia and social status in 18th to 19th century Edo. Japan Int J Ostearchaeol. 2016;26(6):1034–44.  https://doi.org/10.1002/oa.2515.CrossRefGoogle Scholar
  96. 96.
    Kinaston RL, Buckley HR, Gray A. Diet and social status on Taumako, a Polynesian outlier in the Southeastern Solomon Islands. Am J Phys Anthropol. 2013;151(4):589–603.  https://doi.org/10.1002/ajpa.22314.CrossRefPubMedGoogle Scholar
  97. 97.
    Quintelier K, Ervynck A, Müldner G, Van Neer W, Richards MP, Fuller BT. Isotopic examination of links between diet, social differentiation, and DISH at the post-medieval Carmelite Friary of Aalst. Belgium Am J Phys Anthropol. 2014;153(2):203–13.  https://doi.org/10.1002/ajpa.22420.CrossRefPubMedGoogle Scholar
  98. 98.
    Newman SL, Gowland RL. Dedicated followers of fashion? Bioarchaeological perspectives on socio-economic status, inequality, and health in urban children from the industrial revolution (18th–19th C). England Int J Osteoarchaeol. 2017;27(2):217–29.  https://doi.org/10.1002/oa.2531.CrossRefPubMedGoogle Scholar
  99. 99.
    Roberts C. Health and welfare in medieval England: the human skeletal remains contextualized. In: Gilchrist R, editor. Reflections: 50 years of medieval archaeology, 1957-2007. No. 30: 50 Years of Medieval Archaeology 1957–2007: Routledge; 2018.Google Scholar
  100. 100.
    Arthur JW. Pottery use-alteration as an indicator of socioeconomic status: an ethnoarchaeological study of the Gamo of Ethiopia. J Archaeol Method Th. 2002;9(4):331–55.  https://doi.org/10.1023/A:1021309616231.CrossRefGoogle Scholar
  101. 101.
    Roberts CA, Manchester K. The archaeology of disease. New York: Cornell University Press; 2007.Google Scholar
  102. 102.
    Miszkiewicz JJ, Stewart TJ, Deter CA, Fahy G, Mahoney P. Skeletal health in medieval societies: insights from bone collagen stable isotopes and dental histology. In: Miszkiewicz JJ, Brennan-Olsen SL, Riancho JA, editors. Bone health: a reflection of the social mosaic. Singapore: Springer Medicine; 2019 In Press. p. 15–32.  https://doi.org/10.1007/978-981-13-7256-8.CrossRefGoogle Scholar
  103. 103.
    Walker M, Street E, Pitfield R, Miszkiewicz JJ, Brennan-Olsen S, Mahoney P. Ancient human bone microstructure case studies from medieval England. In: Miszkiewicz JJ, Brennan-Olsen SL, Riancho JA, editors. Bone health: a reflection of the social mosaic. Singapore: Springer Medicine; 2019 In Press. p. 33–50.  https://doi.org/10.1007/978-981-13-7256-8.CrossRefGoogle Scholar
  104. 104.
    Miszkiewicz JJ. The effect of English Medieval socio-economic status inequality on bone health – what lessons are there to be learnt for the living? In: Miszkiewicz JJ, Brennan-Olsen SL, Riancho JA, editors. Bone health: a reflection of the social mosaic. Singapore: Springer Medicine; 2019 In Press. p. 1–14.  https://doi.org/10.1007/978-981-13-7256-8.CrossRefGoogle Scholar
  105. 105.
    Miszkiewicz JJ. Linear enamel hypoplasia and age-at-death at medieval (11th-16th centuries) St. Gregory’s priory and cemetery, Canterbury, UK. Int J Osteoarchaeol. 1994;25(1):79–87.  https://doi.org/10.1002/oa.2265.CrossRefGoogle Scholar
  106. 106.
    Dyer C. Making a living in the middle ages: the people of Britain 850–1520. Yale University Press; 2002.Google Scholar
  107. 107.
    Dyer C. Everyday life in medieval England. London: Hambledon and London Publishers; 2000.Google Scholar
  108. 108.
    Bennett JM, Hollister CW. Medieval Europe: a short history. New York: McGraw-Hill; 2006.Google Scholar
  109. 109.
    Bridbury AR. The black death. Econ Hist Rev. 1973;26(4):577–92.  https://doi.org/10.1111/j.1468-0289.1973.tb01955.x.CrossRefPubMedGoogle Scholar
  110. 110.
    Dyer C. Standards of living in the Later Middle Ages: social change in England, 1200–1520. Cambridge: University Press; 1989.CrossRefGoogle Scholar
  111. 111.
    Biddick K. Medieval English peasants and market involvement. J Econ Hist. 1985;45(4):823–31.  https://doi.org/10.1017/S0022050700035117.CrossRefGoogle Scholar
  112. 112.
    Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Looker A, Marcus R, et al. Peak bone mass. Osteoporos Int. 2000;11(12):985–1009.  https://doi.org/10.1007/s001980070020.CrossRefPubMedGoogle Scholar
  113. 113.
    Frost HM. A determinant of bone architecture. The minimum effective strain. Clin Orthop Relat Res. 1983;175:286–92.Google Scholar
  114. 114.
    Curate F, Lopes C, Cunha E. A 14th–17th century osteoporotic hip fracture from the Santa Clara-a-Velha Convent in Coimbra (Portugal). Int J Osteoarchaeol. 2010;20(5):591–6.  https://doi.org/10.1002/oa.1076.CrossRefGoogle Scholar
  115. 115.
    Mays S, Turner-Walker G, Syversen U. Osteoporosis in a population from medieval Norway. Am J Phys Anthropol. 2006;131(3):343–51.  https://doi.org/10.1002/ajpa.20445.CrossRefPubMedGoogle Scholar
  116. 116.
    Borrè A, Boano R, Di Stefano M, Castiglione A, Ciccone G, Isaia GC, et al. X-ray, CT and DXA study of bone loss on medieval remains from North-West Italy. Radiol Med. 2015;120(7):674–82.  https://doi.org/10.1007/s11547-015-0507-3.CrossRefPubMedGoogle Scholar
  117. 117.
    Mays SA. Age-dependent cortical bone loss in a medieval population. Int J Osteoarchaeol. 1996;6(2):144–54.  https://doi.org/10.1002/(SICI)1099-1212(199603)6:2<144::AID-OA261>3.0.CO;2-G.CrossRefGoogle Scholar
  118. 118.
    Marklein KE, Crews DE. Frail or hale: skeletal frailty indices in Medieval London skeletons. PLoS One. 2017;12(5):e0176025.  https://doi.org/10.1371/journal.pone.0176025.CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Rogers J, Waldron T. DISH and the monastic way of life. Int J Osteoarchaeol. 2001;11(5):357–65.  https://doi.org/10.1002/oa.574.CrossRefGoogle Scholar
  120. 120.
    Jankauskas R. The incidence of diffuse idiopathic skeletal hyperostosis and social status correlations in Lithuanian skeletal materials. Int J Osteoarchaeol. 2003;13(5):289–93.  https://doi.org/10.1002/oa.697.CrossRefGoogle Scholar
  121. 121.
    Reale B, Marchi D, Borgognini Tarli SM. A case of diffuse idiopathic skeletal hyperostosis (DISH) from a medieval necropolis in southern Italy. Int J Osteoarchaeol. 1999;9(5):369–73.  https://doi.org/10.1002/(SICI)1099-1212(199909/10)9:5<369::AID-OA486>3.0.CO;2-9.CrossRefGoogle Scholar
  122. 122.
    Weiss NM, Vercellotti G, Boano R, Girotti M, Stout SD. Body size and social status in medieval Alba (Cuneo), Italy. Am J Phys Anthropol. 2019;168(3):595–605.  https://doi.org/10.1002/ajpa.23776.CrossRefPubMedGoogle Scholar
  123. 123.
    Rewekant A. Do environmental disturbances of an individual's growth and development influence the later bone involution processes? A study of two mediaeval populations. Int J Osteoarchaeol. 2001;11(6):433–43.  https://doi.org/10.1002/oa.584.CrossRefGoogle Scholar
  124. 124.
    Dequeker J, Ortner DJ, Stix AI, Cheng XG, Brys P, Boonen S. Hip fracture and osteoporosis in a XIIth dynasty female skeleton from Lisht, upper Egypt. J Bone Miner Res. 1997;12(6):881–8.  https://doi.org/10.1359/jbmr.1997.12.6.881.CrossRefPubMedGoogle Scholar
  125. 125.
    Mays SA. Age-related cortical bone loss in women from a 3rd–4th century AD population from England. Am J Phys Anthropol. 2006;129(4):518–28.  https://doi.org/10.1002/ajpa.20365.CrossRefPubMedGoogle Scholar
  126. 126.
    Pillai S, Littlejohn G. Metabolic factors in diffuse idiopathic skeletal hyperostosis–a review of clinical data. Open Rheumatol J. 2014;8(1):116–28.  https://doi.org/10.2174/1874312901408010116.CrossRefPubMedPubMedCentralGoogle Scholar
  127. 127.
    Hosking SM, Brennan-Olsen SL, Beauchamp A, Buchbinder R, Williams LJ, Pasco JA. Health literacy in a population-based sample of Australian women: a cross-sectional profile of the Geelong Osteoporosis Study. BMC Public Health. 2018;18(1):876.  https://doi.org/10.1186/s12889-018-5751-8.CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Thayer ZM, Non AL. Anthropology meets epigenetics: current and future directions. Am Anthropol. 2015;117(4):722–35.  https://doi.org/10.1111/aman.12351.CrossRefGoogle Scholar
  129. 129.
    Gokhman D, Meshorer E, Carmel L. Epigenetics: it's getting old. Past meets future in paleoepigenetics. Trends Ecol Evol. 2016;31(4):290–300.  https://doi.org/10.1016/j.tree.2016.01.010.CrossRefPubMedGoogle Scholar
  130. 130.
    Llamas B, Holland ML, Chen K, Cropley JE, Cooper A, Suter CM. High-resolution analysis of cytosine methylation in ancient DNA. PLoS One. 2012;7(1):e302e26.  https://doi.org/10.1371/journal.pone.0030226.CrossRefGoogle Scholar
  131. 131.
    Slatkin M, Racimo F. Ancient DNA and human history. Proc Natl Acad Sci U S A. 2016;113(23):6380–7.  https://doi.org/10.1073/pnas.1524306113.CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    Donoghue HD, Spigelman M, O'grady J, Szikossy I, Pap I, Lee OY, et al. Ancient DNA analysis–an established technique in charting the evolution of tuberculosis and leprosy. Tuberculosis (Edinb). 2015;95(Suppl 1):S140–4.  https://doi.org/10.1016/j.tube.2015.02.020.CrossRefGoogle Scholar
  133. 133.
    Lorentzon M. Treating osteoporosis to prevent fractures: current concepts and future developments. J Intern Med. 2019;285(4):381–94.  https://doi.org/10.1111/joim.12873.CrossRefPubMedGoogle Scholar
  134. 134.
    Kendler DL, Bauer DC, Davison KS, Dian L, Hanley DA, Harris ST, et al. Vertebral fractures: clinical importance and management. Am J Med. 2016;129(2):221.e1–10.  https://doi.org/10.1016/j.amjmed.2015.09.020.CrossRefGoogle Scholar
  135. 135.
    Golob AL, Laya MB. Osteoporosis: screening, prevention, and management. Med Clin North Am. 2015;99(3):587–606.  https://doi.org/10.1016/j.mcna.2015.01.010.CrossRefPubMedGoogle Scholar
  136. 136.
    Hannan MT, Felson DT, Dawson-Hughes B, Tucker KL, Cupples LA, Wilson PW, et al. Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res. 2000;15(4):710–20.  https://doi.org/10.1359/jbmr.2000.15.4.710.CrossRefPubMedGoogle Scholar
  137. 137.
    Kai MC, Anderson M, Lau E. Exercise interventions: defusing the world’s osteoporosis time bomb. Bull World Health Organ. 2003;81(11):827–30.PubMedGoogle Scholar
  138. 138.
    Prentice A. Diet, nutrition and the prevention of osteoporosis. Proc Nutr Soc. 2006;65(4):348–60.CrossRefPubMedPubMedCentralGoogle Scholar
  139. 139.
    Cusano NE. Skeletal effects of smoking. Curr Osteoporos Rep. 2015;13(5):302–9.  https://doi.org/10.1007/s11914-015-0278-8.CrossRefPubMedGoogle Scholar
  140. 140.
    Cheraghi Z, Doosti-Irani A, Almasi A, Baigi V, Mansournia N, Etminan M, et al. The effect of alcohol on osteoporosis; a systematic review and meta-analysis. Drug Alcohol Depend. 2019;197:197–202.  https://doi.org/10.1016/j.drugalcdep.2019.01.025.CrossRefPubMedGoogle Scholar
  141. 141.
    Ralston SH, Uitterlinden AG. Genetics of osteoporosis. Endocr Rev. 2010;31(5):629–62.  https://doi.org/10.1210/er.2009-0044.CrossRefPubMedGoogle Scholar
  142. 142.
    Kinkopf KM, Agarwal SC, Goodson C, Candilio F, Coppa A, Rubini M. The role of social status in spinal degenerative joint disease outcomes: evidence from Medieval Villamagna, Italy (800–1450 AD). Am J Phys Anthropol. 2019;168:126.Google Scholar
  143. 143.
    Beauchesne P, Trombley T, Agarwal SC, Kinkopf K, Goodson C, Candilio F, et al. Timing is everything: implementing a life course perspective to investigate developmental origins of health and disease in a medieval Italian skeletal sample. Am J Phys Anthropol. 2019;168:14.Google Scholar
  144. 144.
    Gillespie LD, Robertson MC, Gillespie WJ, Sherrington C, Gates S, Clemson LM, et al. Interventions for preventing falls in older people living in the community. Cochrane Database Syst Rev. 2012;9:CD007146.  https://doi.org/10.1002/14651858.CD007146.pub3.CrossRefGoogle Scholar
  145. 145.
    Law MR, Wald NJ, Meade TW. Strategies for prevention of osteoporosis and hip fracture. BMJ. 1991;303(6800):453–9.  https://doi.org/10.1136/bmj.303.6800.453.CrossRefPubMedPubMedCentralGoogle Scholar
  146. 146.
    Bonura F. Prevention, screening, and management of osteoporosis: an overview of the current strategies. Postgrad Med. 2009;121(4):5–17.  https://doi.org/10.1089/jwh.2013.4611.CrossRefPubMedGoogle Scholar
  147. 147.
    Ponzano M, Rodrigues IB, Giangregorio LM. Physical activity for fall and fracture prevention. Curr Treatm Opt Rheumatol. 2018;4(3):268–78.  https://doi.org/10.1007/s40674-018-0103-5.CrossRefGoogle Scholar
  148. 148.
    Kanis JA, Cooper C, Rizzoli R, Reginster JY, ESCEO IOF. Executive summary of European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Calcif Tissue Int. 2019;104(3):235–8.  https://doi.org/10.1007/s00198-018-4704-5.CrossRefPubMedPubMedCentralGoogle Scholar
  149. 149.
    Khashayar P, Taheri E, Adib G, Zakraoui L, Larijani B. Osteoporosis strategic plan for the Middle East and North Africa region. Arch Osteoporos. 2019;14(1):20.  https://doi.org/10.1007/s11657-019-0567-4.CrossRefPubMedGoogle Scholar
  150. 150.
    Chandran M. Fracture liaison services in South East Asia: notes from a large public hospital in Singapore. In: Seibel MJ, Mitchell PJ, editors. Secondary fracture pevention: An international perspective. Elsevier Academic Press; 2019. p. 123–132.  https://doi.org/10.1016/B978-0-12-813136-7.00008-9

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Skeletal Biology and Forensic Anthropology Research Group, School of Archaeology and AnthropologyAustralian National UniversityCanberraAustralia
  2. 2.Skeletal Biology Research Centre, School of Anthropology and ConservationUniversity of KentCanterburyUK

Personalised recommendations