Advertisement

International Journal of Legal Medicine

, Volume 133, Issue 4, pp 1225–1239 | Cite as

Diabetic bone lesions: a study on 38 known modern skeletons and the implications for forensic scenarios

  • Lucie Biehler-GomezEmail author
  • Elisa Castoldi
  • Elisa Baldini
  • Annalisa Cappella
  • Cristina Cattaneo
Original Article

Abstract

Diabetes mellitus is a condition with severe and life-threatening complications and epidemic proportions worldwide. The study of diabetes on bones can provide crucial information to the forensic practice, the archeological field and medical research. In this paper, the authors report and discuss the lesions observed on the skeletons of 38 individuals (plus 11 negative control samples) of the CAL Milano Cemetery Skeletal Collection with known diabetes. As a result, different types of lesions were highlighted in the feet: periosteal new bone formation, lysis of tuft, lytic lesions, evidence of trauma, osteomyelitis, and osteochondritis dissecans. In 50% of the skeletons of the study sample, lesions were located on bones of the first ray of the foot. Vascular calcifications were also collected and considered. None of these lesions is pathognomonic of diabetes and each implies a broad differential diagnosis that can be confronted with the upper and axial lesions. However, they are coherent with the disease development and complications. This study is the first to document skeletons with known diabetes from an identified collection and discuss their diagnostic potential.

Keywords

Forensic anthropology Bone pathology Diabetes Dry bone Biological profile 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Zimmet P, Alberti KGMM, Shaw J (2001) Global and societal implications of the diabetes epidemic. Nature 414:782–787CrossRefGoogle Scholar
  2. 2.
    Evans JMM, Newton RW, Ruta DA, MacDonald TM, Morris AD (2000) Socio-economic status, obesity and prevalence of type 1 and type 2 diabetes mellitus. Diabet Med 17:478–480.  https://doi.org/10.1046/j.1464-5491.2000.00309.x CrossRefGoogle Scholar
  3. 3.
    Mathers CD, Loncar D (2006) Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3:e442.  https://doi.org/10.1371/journal.pmed.0030442 CrossRefGoogle Scholar
  4. 4.
    Biehler-Gomez L, Cappella A, Castoldi E, Martrille L, Cattaneo C (2018) Survival of atherosclerotic calcifications in skeletonized material: forensic and pathological implications. J Forensic Sci 63:386–394.  https://doi.org/10.1111/1556-4029.13592 CrossRefGoogle Scholar
  5. 5.
    Castoldi E, Cappella A, Gibelli D, Sforza C, Cattaneo C (2017) The difficult task of diagnosing prostate cancer metastases on dry bone. J Forensic Sci 63:672–682.  https://doi.org/10.1111/1556-4029.13617 CrossRefGoogle Scholar
  6. 6.
    Cattaneo C, Mazzarelli D, Cappella A, Castoldi E, Mattia M, Poppa P, de Angelis D, Vitello A, Biehler-Gomez L (2018) A modern documented Italian identified skeletal collection of 2127 skeletons: the CAL Milano Cemetery Skeletal Collection. Forensic Sci Int 287:219.e1–219.e5.  https://doi.org/10.1016/j.forsciint.2018.03.041 CrossRefGoogle Scholar
  7. 7.
    Schwartz AV (2003) Diabetes mellitus: does it affect bone? Calcif Tissue Int 73:515–519.  https://doi.org/10.1007/s00223-003-0023-7 CrossRefGoogle Scholar
  8. 8.
    Arkkila PET, Gautier J-F (2003) Musculoskeletal disorders in diabetes mellitus: an update. Best Pract Res Clin Rheumatol 17:945–970.  https://doi.org/10.1016/j.berh.2003.11.001 CrossRefGoogle Scholar
  9. 9.
    Alberti KGMM, Zimmet P (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus. Provisional report of a WHO consultation. Diabet Med 15:539–553.  https://doi.org/10.1002/(SICI)1096-9136(199807)15:7<539::AID-DIA668>3.0.CO;2-S CrossRefGoogle Scholar
  10. 10.
    Brutsaert E (2017) Diabetes mellitus (DM), The Merck manual for health professionals [Internet]. Availablefrom: https://www.msdmanuals.com/professional/endocrine-and-metabolic-disorders/diabetes-mellitus-anddisorders-of-carbohydrate-metabolism/diabetes-mellitus-dm
  11. 11.
    Brutsaert E (2017) Complications of diabetes mellitus, The Merck manual for health professionals [Internet]. Available from: https://www.merckmanuals.com/professional/endocrine-and-metabolic-disorders/diabetesmellitus-and-disorders-of-carbohydrate-metabolism/complications-of-diabetes-mellitus
  12. 12.
    Fowler MJ (2008) Microvascular and macrovascular complications of diabetes. Clin Diabetes 26:77–82CrossRefGoogle Scholar
  13. 13.
    Crispin JC, Alcocer-Varela J (2003) Rheumatologic manifestations of diabetes mellitus. Am J Med 114:753–757.  https://doi.org/10.1016/S0002-9343(03)00140-2 CrossRefGoogle Scholar
  14. 14.
    Politi C, Ciccacci C, D’Amato C et al (2016) Recent advances in exploring the genetic susceptibility to diabetic neuropathy. Diabetes Res Clin Pract 120:198–208.  https://doi.org/10.1016/j.diabres.2016.08.006 CrossRefGoogle Scholar
  15. 15.
    Beckman JA, Creager MA, Libby P (2002) Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 287:2570–2581.  https://doi.org/10.1001/jama.287.19.2570 CrossRefGoogle Scholar
  16. 16.
    van Daele PL, Stolk RP, Burger H, Algra D, Grobbee DE, Hofman A, Birkenhäger JC, Pols HA (1995) Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam study. Ann Intern Med 122:409–414CrossRefGoogle Scholar
  17. 17.
    Burner TW, Rosenthal AK (2009) Diabetes and rheumatic diseases. Curr Opin Rheumatol 21:50–54.  https://doi.org/10.1097/BOR.0b013e32831bc0c4 CrossRefGoogle Scholar
  18. 18.
    Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporos Int 18:427–444.  https://doi.org/10.1007/s00198-006-0253-4 CrossRefGoogle Scholar
  19. 19.
    Husni ME, Kroop SF, Simon LS (2005) Joint and bone manifestations of diabetes mellitus. In: Kahn CR, King GL, Moses AC et al (eds) Joslin’s Diabetes Mellitus, 14th edn. Lippincott Williams & Wilkins, BostonGoogle Scholar
  20. 20.
    Waldron T (2008) Palaeopathology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  21. 21.
    Aufderheide AC, Rodríguez-Martín C (1998) The Cambridge encyclopedia of human paleopathology. Cambridge University Press, CambridgeGoogle Scholar
  22. 22.
    Giurato L, Uccioli L (2006) The diabetic foot: Charcot joint and osteomyelitis. Nucl Med Commun 27:745–749.  https://doi.org/10.1097/01.mnm.0000230066.23823.cc CrossRefGoogle Scholar
  23. 23.
    Hartemann-Heurtier A, Senneville E (2008) Diabetic foot osteomyelitis. Diabetes Metab 34:87–95CrossRefGoogle Scholar
  24. 24.
    Levy MJ, Valabhji J (2008) The diabetic foot. Surg 26:25–28.  https://doi.org/10.1016/j.mpsur.2007.10.013 Google Scholar
  25. 25.
    Gray RG, Gottlieb NL (1976) Rheumatic disorders associated with diabetes mellitus: literature review. Semin Arthritis Rheum 6:19–34.  https://doi.org/10.1016/S0049-0172(76)80003-0 CrossRefGoogle Scholar
  26. 26.
    Martin MM (1952) Charcot joints in diabetes mellitus. Proc R Soc Med 45:503–506Google Scholar
  27. 27.
    Chantelau E, Onvlee GJ (2006) Charcot foot in diabetes: farewell to the neurotrophic theory. Horm Metab Res 38:361–367.  https://doi.org/10.1055/s-2006-944525 CrossRefGoogle Scholar
  28. 28.
    Smith LL, Burnet SP, McNeil JD (2003) Musculoskeletal manifestations of diabetes mellitus. Br J Sports Med 37:30–35CrossRefGoogle Scholar
  29. 29.
    Papanas N, Maltezos E (2010) The diabetic hand: a forgotten complication? J Diabetes Complicat 24:154–162.  https://doi.org/10.1016/j.jdiacomp.2008.12.009 CrossRefGoogle Scholar
  30. 30.
    Belcastro MG, Mariotti V, Facchini F, Dutour O (2005) Leprosy in a skeleton from the 7th century necropolis of Vicenne-Campochiaro (Molise, Italy). Int J Osteoarchaeol 15:431–448.  https://doi.org/10.1002/oa.799 CrossRefGoogle Scholar
  31. 31.
    Mader R, Lavi I (2009) Diabetes mellitus and hypertension as risk factors for early diffuse idiopathic skeletal hyperostosis (DISH). Osteoarthr Cartil 17:825–828.  https://doi.org/10.1016/j.joca.2008.12.004 CrossRefGoogle Scholar
  32. 32.
    Sencan D, Elden H, Nacitarhan V, Sencan M, Kaptanoglu E (2005) The prevalence of diffuse idiopathic skeletal hyperostosis in patients with diabetes mellitus. Rheumatol Int 25:518–521.  https://doi.org/10.1007/s00296-004-0474-9 CrossRefGoogle Scholar
  33. 33.
    Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ (2004) Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol 159:1160–1167.  https://doi.org/10.1093/aje/kwh161 CrossRefGoogle Scholar
  34. 34.
    Marx M, D’Auria SH (1986) CT examination of eleven Egyptian mummies. RadioGraphics 6:321–330.  https://doi.org/10.1148/radiographics.6.2.3317542 CrossRefGoogle Scholar
  35. 35.
    Dupras TL, Williams LJ, de Meyer M et al (2010) Evidence of amputation as medical treatment in ancient Egypt. Int J Osteoarchaeol 20:405–423.  https://doi.org/10.1002/oa.1061 Google Scholar
  36. 36.
    Biehler-Gomez L, Cattaneo C (2018) The diagnostic implications of two cases of known rheumatoid arthritis from the CAL Milano Cemetery Skeletal Collection. J Forensic Sci.  https://doi.org/10.1111/1556-4029.13799
  37. 37.
    Biehler-Gomez L, Cabrini A, De Angelis D, Cattaneo C (2018) How do skeletons with HIV present? A study on the identified CAL Milano Cemetery Skeletal Collection. Leg Med 33:11–16.  https://doi.org/10.1016/j.legalmed.2018.04.007 CrossRefGoogle Scholar
  38. 38.
    White TD, Folkens AP (2005) The Human Bone Manual. Elesvier Academic Press, San DiegoGoogle Scholar
  39. 39.
    Rothschild BM, Behnam S (2005) The often overlooked digital tuft: clues to diagnosis and pathophysiology of neuropathic disease and spondyloarthropathy. Ann Rheum Dis 64:286–290CrossRefGoogle Scholar
  40. 40.
    Ortner DJ (2003) Identification of pathological conditions in human skeletal remains, 3rd edn. Smithsonian Institution Press, New YorkGoogle Scholar
  41. 41.
    Clouse ME, Gramm HF, Legg M, Flood T (1974) Diabetic Osteoarthropathy. Am J Roentgenol 121:22–34.  https://doi.org/10.2214/ajr.121.1.22 CrossRefGoogle Scholar
  42. 42.
    Weston DA (2008) Investigating the specificity of periosteal reactions in pathology museum specimens. Am J Phys Anthr 137:48–59.  https://doi.org/10.1002/ajpa.20839 CrossRefGoogle Scholar
  43. 43.
    Boel LWT, Ortner DJ (2013) Skeletal manifestations of skin ulcer in the lower leg. Int J Osteoarchaeol 23:303–309.  https://doi.org/10.1002/oa.1248 CrossRefGoogle Scholar
  44. 44.
    Newman JH (1980) Non-infective disease of the diabetic foot. J Bone Joint Surg Br 63–B:593Google Scholar
  45. 45.
    Baer AN, Zahr ZA, Khan S, Polydefkis M (2012) Acroosteolysis in diabetes mellitus. J Rheumatol 39:2364–2365CrossRefGoogle Scholar
  46. 46.
    Sakai M, Sakuma S, Ishigaki T (1986) Osseous lesions of the hand and foot in diabetes mellitus: correlation between magnification roentgenographic findings and clinical findings. Nagoya J Med Sci 48:55–65Google Scholar
  47. 47.
    Doherty TM, Asotra K, Fitzpatrick LA, Qiao JH, Wilkin DJ, Detrano RC, Dunstan CR, Shah PK, Rajavashisth TB (2003) Calcification in atherosclerosis: bone biology and chronic inflammation at the arterial crossroads. Proc Natl Acad Sci U S A 100:11201–11206.  https://doi.org/10.1073/pnas.1932554100 CrossRefGoogle Scholar
  48. 48.
    Wexler L, Brundage B, Crouse J, Detrano R, Fuster V, Maddahi J, Rumberger J, Stanford W, White R, Taubert K (1996) Coronary artery calcification: pathophysiology, epidemiology, imaging methods, and clinical implications. A statement for health professionals from the American Heart Association. Writing group. Circulation 94:1175–1192CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.LABANOF, Laboratorio Di Antropologia E Odontologia Forense, Sezione Di Medicina Legale, Dipartimento Di Scienze Biomediche per La SaluteUniversità Degli Studi Di MilanoMilanItaly

Personalised recommendations