The synergy between radiographic and macroscopic observation of skeletal lesions on dry bone

  • Lucie Biehler-GomezEmail author
  • Stefania Tritella
  • Federica Martino
  • Carlo Pietro Campobasso
  • Angélique Franchi
  • Riccardo Spairani
  • Francesco Sardanelli
  • Cristina Cattaneo
Original Article


The diagnosis of bone lesions is a fundamental part of the study of skeletal remains, both in the archeological and forensic context. On the one side, the literature proved the relevance of radiography for the detection of bone lesions; on the other side, the careful macroscopic observation of the morphology of bone lesions is often underestimated. For this study, we examined and performed plain radiography on 14 skeletons of the CAL Milano Cemetery Skeletal Collection diagnosed with rheumatoid arthritis, diabetes, multiple myeloma, metastatic cancer, and osteomalacia to compare the macroscopic morphology and radiographic visualization of bone lesions. At least 200 osteolytic lesions and 65 areas of proliferative bone reaction (either spongiosclerotic or periosteal) were studied. We realized “comparative sets” of macroscopic pictures and radiographic imaging of the same skeletal elements to allow comparisons of detection and recognition of bone lesions. As a result, while trabecular lesions may be lost through naked eye observation, many lesions can also be unperceived on radiographs due to contrast, including periosteal reactions, osteolytic lesions, and spongiosclerosis. The aim of this research was to investigate the strengths and pitfalls of digital radiography and macroscopic analysis and to demonstrate the synergy of a complementary approach between the two methods for lesion analysis in dry bone.


Forensic anthropology Bone pathology Radiographic imaging Rheumatoid arthritis Diabetes Metastatic carcinoma 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.


  1. 1.
    Cunha E (2006) Pathology as a factor of personal identity in forensic anthropology. In: Schmitt A, Cunha E, Pinheiro J (eds) . Springer, Forensic anthropology and medicine, pp 333–358Google Scholar
  2. 2.
    Ortner DJ (2003) Identification of pathological conditions in human skeletal remains, 3rd edn. Smithsonian Institution Press, New YorkGoogle Scholar
  3. 3.
    Aufderheide AC, Rodríguez-Martín C (1998) The Cambridge encyclopedia of human paleopathology. Cambridge University Press, CambridgeGoogle Scholar
  4. 4.
    Waldron T (2008) Palaeopathology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  5. 5.
    Steinbock RT (1976) Paleopathological diagnosis and interpretation: bone diseases in ancient human populations. Charles Thomas Publisher, SpringfieldGoogle Scholar
  6. 6.
    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 63:1880–1887. CrossRefGoogle Scholar
  7. 7.
    Biehler-Gomez L, Castoldi E, Baldini E, Cappella A, Cattaneo C (2018) Diabetic bone lesions: a study on 38 known modern skeletons and the implications for forensic scenarios. Int J Legal Med 133:1–15. Google Scholar
  8. 8.
    Biehler-Gomez L, Giordano G, Cattaneo C (2019) Multiple myeloma bone lesions in skeletal remains: report of two known cases from the 20th century CAL Milano Cemetery Skeletal Collection. Int J Osteoarchaeol 29:101–107. CrossRefGoogle Scholar
  9. 9.
    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. CrossRefGoogle Scholar
  10. 10.
    Biehler-Gomez L, Giordano G, Cattaneo C (2019) The appearance of breast cancer metastases on dry bone: implications for forensic anthropology. J Forensic Legal Med 61:5–12. CrossRefGoogle Scholar
  11. 11.
    Biehler-Gomez L, Giordano G, Cattaneo C (2019) The overlooked primary: bladder cancer metastases on dry bone. A study of the 20th century CAL Milano Cemetery Skeletal Collection. Int J Paleopathol 24:130–140. CrossRefGoogle Scholar
  12. 12.
    Ortner DJ, Aufderheide AC (1991) Human paleopathology: current syntheses and future options. Smithsonian Institution Press, Washington, DCGoogle Scholar
  13. 13.
    Kelley MA, Micozzi MS (1984) Rib lesions in chronic pulmonary tuberculosis. Am J Phys Anthropol 65:381–386. CrossRefGoogle Scholar
  14. 14.
    Roberts CA, Lucy D, Manchester K (1994) Inflammatory lesions of ribs: an analysis of the Terry Collection. Am J Phys Anthropol 95:169–182. CrossRefGoogle Scholar
  15. 15.
    Santos AL, Roberts CA (2006) Anatomy of a serial killer: differential diagnosis of tuberculosis based on rib lesions of adult individuals from the Coimbra identified skeletal collection, Portugal. Am J Phys Anthropol 130:38–49. CrossRefGoogle Scholar
  16. 16.
    Matos V, Santos AL (2006) On the trail of pulmonary tuberculosis based on rib lesions: results from the human identified skeletal collection from the Museu Bocage (Lisbon, Portugal). Am J Phys Anthropol 130:190–200. CrossRefGoogle Scholar
  17. 17.
    Mays S (2018) How should we diagnose disease in palaeopathology? Some epistemological considerations. Int J Paleopathol 20:12–19. CrossRefGoogle Scholar
  18. 18.
    Chhem RK, Brothwell DR (2008) Paleoradiology: imaging mummies and fossils. Springer, BerlinGoogle Scholar
  19. 19.
    Rogers J, Watt I, Dieppe P (1990) Comparison of visual and radiographic detection of bony changes at the knee joint. BMJ 300:367–368CrossRefGoogle Scholar
  20. 20.
    Cattaneo C, Mazzarelli D, Cappella A et al (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. CrossRefGoogle Scholar
  21. 21.
    Brickley M, Ives R (2010) The bioarchaeology of metabolic bone disease. Elsevier Academic Press, LondonGoogle Scholar
  22. 22.
    Brickley M, Mays S, Ives R (2005) Skeletal manifestations of vitamin D deficiency osteomalacia in documented historical collections. Int J Osteoarchaeol 15:389–403. CrossRefGoogle Scholar
  23. 23.
    Brickley M, Mays S, Ives R (2007) An investigation of skeletal indicators of vitamin D deficiency in adults: effective markers for interpreting past living conditions and pollution levels in 18th and 19th century Birmingham, England. Am J Phys Anthropol 132:67–79. CrossRefGoogle Scholar
  24. 24.
    Ives R, Brickley M (2014) New findings in the identification of adult vitamin D deficiency osteomalacia: results from a large-scale study. Int J Paleopathol 7:45–56. CrossRefGoogle Scholar
  25. 25.
    Mays S, Brickley MB (2018) Vitamin D deficiency in bioarchaeology and beyond: the study of rickets and osteomalacia in the past. Int J Paleopathol 23:1–5. CrossRefGoogle Scholar
  26. 26.
    Choy E (2012) Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology 51:v3–v11. CrossRefGoogle Scholar
  27. 27.
    Henrique da Mota LM, Afonso Cruz B, Viegas Brenol C et al (2013) Guidelines for the diagnosis of rheumatoid arthritis. Rev Bras Reumatol (English Ed) 53:141–157. CrossRefGoogle Scholar
  28. 28.
    Firestein GS (2000) Rheumatoid arthritis. In: Humes HD, HL DP, Gardner LB et al (eds) Kelley’s Textbook of Internal Medicine, 4th edn. Lippincott Williams & Wilkins, pp 1347–1359Google Scholar
  29. 29.
    Rogers J, Waldron T, Dieppe P, Watt I (1987) Arthropathies in palaeopathology: the basis of classification according to most probable cause. J Archaeol Sci 14:179–193. CrossRefGoogle Scholar
  30. 30.
    Brahee DD, Pierre-Jerome C, Kettner NW (2003) Clinical and radiological manifestations of the rheumatoid wrist, A comprehensive review. J Manip Physiol Ther 26:323–329. CrossRefGoogle Scholar
  31. 31.
    Fitzgerald RH, Kaufer H, Malkani AL (2002) Orthopaedics. Mosby, St LouisGoogle Scholar
  32. 32.
    Sommer OJ, Kladosek A, Weiler V, Czembirek H, Boeck M, Stiskal M (2005) Rheumatoid arthritis: a practical guide to state-of-the-art imaging, image interpretation, and clinical implications. RadioGraphics 25:381–398. CrossRefGoogle Scholar
  33. 33.
    Vigorita VJ, Ghelman B (2016) Arthritis. In: Vigorita VJ, Ghelman B (eds) Orthopaedic pathology. Third. Lippincott Williams & Wilkins, Philadelphia, pp 710–768Google Scholar
  34. 34.
    Veale DJ, Fearon U (2015) What makes psoriatic and rheumatoid arthritis so different? RMD Open 1:e000025. CrossRefGoogle Scholar
  35. 35.
    Rothschild BM, Woods RJ (1991) Spondyloarthropathy: erosive arthritis in representative defleshed bones. Am J Phys Anthropol 85:125–134. CrossRefGoogle Scholar
  36. 36.
    Erickson AR, Cannella AC, Mikuls TR (2017) Clinical features of rheumatoid arthritis. In: Firestein GS, Budd R, Gabriel SE et al (eds) Kelley and Firestein’s textbook of rheumatology, 10th edn. Elsevier Health Sciences, Philadelphia, pp 1167–1186CrossRefGoogle Scholar
  37. 37.
    Kim HJ, Nemani VM, Riew KD, Brasington R (2015) Cervical spine disease in rheumatoid arthritis: incidence, manifestations, and therapy. Curr Rheumatol Rep 17:9. CrossRefGoogle Scholar
  38. 38.
    Leden I, Forslind K, Svensson B (2012) Ankylosis of wrist and small joints of the hand occurs in rheumatoid arthritis: diagnostic implication in paleopathology. Int J Paleopathol 2:249–251. CrossRefGoogle Scholar
  39. 39.
    Zias J, Mitchell P (1996) Psoriatic arthritis in a fifth-century Judean Desert monastery. Am J Phys Anthr 101:491–502.<491::AID-AJPA4>3.0.CO;2-Z CrossRefGoogle Scholar
  40. 40.
    Brutsaert E (2017) Complications of diabetes mellitus—Merck Manual for Health Professionals. Accessed 26 Mar 2019
  41. 41.
    Fowler MJ (2008) Microvascular and macrovascular complications of diabetes. Clin Diabetes 26:77–82CrossRefGoogle Scholar
  42. 42.
    Beckman JA, Creager MA, Libby P (2002) Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 287:2570–2581. CrossRefGoogle Scholar
  43. 43.
    Crispin JC, Alcocer-Varela J (2003) Rheumatologic manifestations of diabetes mellitus. Am J Med 114:753–757. CrossRefGoogle Scholar
  44. 44.
    Coleman RE (1997) Skeletal complications of malignancy. Cancer 80:1588–1594.<1588::AID-CNCR9>3.0.CO;2-G CrossRefGoogle Scholar
  45. 45.
    Coleman RE (2001) Metastatic bone disease: clinical features, pathophysiology and treatment strategies. Cancer Treat Rev 27:165–176. CrossRefGoogle Scholar
  46. 46.
    Strouhal E (1991) Myeloma multiplex versus osteolytic metastatic carcinoma: differential diagnosis in dry bones. Int J Osteoarchaeol 1:219–224. CrossRefGoogle Scholar
  47. 47.
    Rothschild BM, Hershkovitz I, Dutour O (1998) Clues potentially distinguishing lytic lesions of multiple myeloma from those of metastatic carcinoma. Am J Phys Anthropol 105:241–250.<241::AID-AJPA10>3.0.CO;2-0 CrossRefGoogle Scholar
  48. 48.
    Roodman GD (2004) Mechanisms of bone metastasis. N Engl J Med 350:1655–1664. CrossRefGoogle Scholar
  49. 49.
    Randall RL (2015) Metastatic bone disease: an integrated approach to patient care. SpringerGoogle Scholar
  50. 50.
    Paget S (1889) The distribution of secondary growths in cancer of the breast. Lancet 133:571–573. CrossRefGoogle Scholar
  51. 51.
    Talmadge JE, Fidler IJ (2010) AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 70:5649–5669. CrossRefGoogle Scholar
  52. 52.
    Brothwell D (2008) Tumor and tumor-like processes. John Wiley & SonsGoogle Scholar
  53. 53.
    Marques C, Santos AL, Cunha E (2013) Better a broader diagnosis than a misdiagnosis: the study of a neoplastic condition in a male individual who died in early 20th century (Coimbra, Portugal). Int J Osteoarchaeol 23:664–675. CrossRefGoogle Scholar
  54. 54.
    Ragsdale BD, Campbell RA, Kirkpatrick CL (2018) Neoplasm or not? General principles of morphologic analysis of dry bone specimens. Int J Paleopathol 21:27–40. CrossRefGoogle Scholar
  55. 55.
    Andersen JG, Manchester K (1992) The rhinomaxillary syndrome in leprosy: a clinical, radiological and palaeopathological study. Int J Osteoarchaeol 2:121–129. CrossRefGoogle Scholar
  56. 56.
    Smith MO (2002) A probable case of metastatic carcinoma from the late prehistoric eastern Tennessee River Valley. Int J Osteoarchaeol 12:235–247. CrossRefGoogle Scholar
  57. 57.
    Vilar J, Lezana AH, Pedrosa CS (1979) Spiculated periosteal reaction in metastatic lesions of bone. Skelet Radiol 3:230–233. CrossRefGoogle Scholar
  58. 58.
    Bloom RA, Libson E, Husband JE, Stoker DJ (1987) The periosteal sunburst reaction to bone metastases. A literature review and report of 20 additional cases. Skelet Radiol 16:629–634CrossRefGoogle Scholar
  59. 59.
    Guise TA, Kozlow WM, Heras-Herzig A, Padalecki SS, Yin JJ, Chirgwin JM (2005) Molecular mechanisms of breast cancer metastases to bone. Clin Breast Cancer 5:S46–S53. CrossRefGoogle Scholar
  60. 60.
    Lipton JF, Vigorita VJ (2016) Metastatic bone disease. In: Vigorita VJ, Ghelman B, Mintz D (eds) Orthopaedic pathology, 3rd edn. Lippincott Williams & Wilkin, Philadelphia, pp 594–619Google Scholar
  61. 61.
    Ortner DJ (2011) Human skeletal paleopathology. Int J Paleopathol 1:4–11. CrossRefGoogle Scholar
  62. 62.
    Rothschild BM, Rothschild C (1995) Comparison of radiologic and gross examination for detection of cancer in defleshed skeletons. Am J Phys Anthr 96:357–363. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Lucie Biehler-Gomez
    • 1
    Email author
  • Stefania Tritella
    • 2
  • Federica Martino
    • 3
  • Carlo Pietro Campobasso
    • 3
  • Angélique Franchi
    • 4
  • Riccardo Spairani
    • 5
  • Francesco Sardanelli
    • 2
    • 6
  • Cristina Cattaneo
    • 1
  1. 1.Laboratorio Di Antropologia E Odontologia Forense (LABANOF), Sezione Di Medicina Legale, Dipartimento Di Scienze Biomediche per La SaluteUniversità Degli Studi Di MilanoMilanItaly
  2. 2.Unit of RadiologyIRCCS Policlinico San DonatoSan Donato MilaneseItaly
  3. 3.Dipartimento di Medicina SperimentaleUniversità degli Studi della Campania “Luigi Vanvitelli”NaplesItaly
  4. 4.Forensic Medicine DepartmentUniversity Hospital of LyonLyonFrance
  5. 5.Post-Graduate School in RadiodiagnosticsUniversità degli Studi di MilanoMilanItaly
  6. 6.Department of Biomedical Sciences for HealthUniversità degli Studi di MilanoMilanItaly

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