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Bone Diagenesis and its Implication for Disease Diagnosis: The Relevance of Bone Microstructure Analysis for the Study of Past Human Remains

  • Sandra Assis (a1), Anne Keenleyside (a2), Ana Luísa Santos (a1) and Francisca Alves Cardoso (a3)


When bone is exposed to the burial environment it may experience structural changes induced by multiple agents. The study of postmortem alterations is important to differentiate decomposition phenomena from normal physiological processes or pathological lesions, as well as to assess bone tissue quality. Microscopy is of great utility to evaluate the integrity of bone microstructure and it provides significant data on long-term bone decomposition. A total of 18 human bone sections (eight archeological and ten retrieved from an identified skeletal collection) were selected for analysis under plane light and polarized light. The aim of this exploratory study was to analyze the impact of diagenesis and taphonomy on the bone microstructure, as well as on the differential diagnosis of pathological conditions. The results showed that the microscopy approach to bone tissues contributed materially as an aid in the detailed description of the main diagenetic changes observed. It showed that gross inspection does not provide a realistic assessment of bone tissue preservation, which can impact in the characterization of lesions present and subsequent disease diagnosis. Therefore, researchers should continue to consider the application of histological techniques if the aim is to comprehend tissue integrity and its association with decomposition or disease.


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Abdel-Maksound, G. (2010). Comparison between the properties of “accelerated-aged” bones and archaeological bones. MAA 10, 89112.
Aufderheide, A. & Rodríguez-Martín, C. (1998). The Cambridge Encyclopedia of Human Paleopathology. Cambridge: Cambridge University Press.
Balzer, A., Gleixner, G., Grupe, G., Schmidt, H.-L., Schramm, S. & Turban-Just, S. (1997). In vitro decomposition of bone collagen by bacteria: The implications for stable isotope analysis in archaeometry. Archaeometry 39, 415429.
Bell, L. & Jones, S. (1991). Macroscopic and microscopic evaluation of archaeological pathological bone: Backscattered electron imaging o putative pagetic bone. Int J Osteoarch 1, 179184.
Bell, L. & Piper, K. (2000). An introduction to palaeohistopathology. In Human Osteology in Archaeology and Forensic Sciences, Cox, M. & Mays, S. (Eds.), pp. 255274. London: Greenwich Medical Media, Ltd.
Bianco, P. & Ascenzi, A. (1993). Palaeohistology of human bone remains: A critical evaluation and an example of its use. In Histology of Ancient Human Bone: Methods and Diagnosis, Grupe, G. & Garland, A.N. (Eds.), pp. 157170. Berlin: Springer-Verlag.
Bruzek, J. (2002). A method for visual determination of sex, using the human hip bone. Am J Phys Anthropol 117, 157168.
Buikstra, J.E. & Ubelaker, D. (1994). Standards for data collection from human skeletal remains. Proceedings of a Seminar at the Field Museum of Natural History, Arkansas: Archaeological Survey Research Series, 44.
Burgener, F., Kormano, M. & Pudas, T. (2006). Bone and Joint Disorders: Differential Diagnosis in Conventional Radiology. Stittgard: Georg Thieme Verlag.
Cardoso, H.F. (2006). Brief communication: The Collection of Identified Human Skeletons housed at the Bocage Museum (National Museum of Natural History), Lisbon, Portugal. Am J Phys Anthropol 129, 173176.
Cardoso, H.F.V. (2005). Patterns of growth and development of the human skeleton and dentition in relation to environmental quality. PhD Thesis in Anthropology. Hamilton, Ontario, McMaster University.
Cipollaro, M., Di Bernardo, G., Galano, G., Galderisi, U., Guarino, F., Angelini, F. & Cascino, A. (1998). Ancient DNA in human bone remains from Pompeii archaeological site. Biochem Biophys Res Commun 247, 901904.
Collins, M.J., Nielsen-Marsh, C.M., Hiller, J., Smith, C.I., Roberts, J.P., Prigodich, R.V., Wess, T.J., Csapò, J., millard, A.R. & Turner-Walker, G. (2002). The survival of organic matter in bone: A review. Archaeometry 44, 383394.
De La Rúa, C., Baraybar, J. & Etxeberria, F. (1995). Neolithic case of metastasizing carcinoma: Multiple approaches to differential diagnosis. Int J Osteoarch 5, 254264.
Efremov, I.A. (1940). Taphonomy: A new branch of paleontology. Pan-Am Geol 74, 8193.
Garland, A.N. (1987). A histological study of archaeological bone decomposition. In Death, Decay and Reconstruction: Approaches to Archaeology and Forensic Science, Boddington, A., Garland, A.N. & Janaway, R. (Eds.), pp. 109126. Manchester: Manchester University Press.
Grupe, G. (2007). Taphonomic and diagenetic processes. In Handbook of Paleoanthropology, Henke, W., Tattersall, I. & Hardt, T. (Eds.), pp. 241259. Berlin Heidelberg: Springer-Verlag.
Grupe, G. & Dreses-Werringloer, U. (1993). Decomposition phenomena in thin sections of excavated human bones. In Histology of Ancient Human Bone: Methods and Diagnosis, Grupe, G. & Garland, A.N. (Eds.), pp. 2736. Berlin: Springer-Verlag.
Guarino, F., Angelini, F., Vollono, C. & Orefice, C. (2006). Bone preservation in human remains from the Terme del Sarno at Pompeii using light microscopy and scanning electron microscopy. J Arch Sci 33, 513530.
Hackett, C.J. (1981). Microscopical focal destruction (tunnels in exhumed human bones). Med Sci Law 21, 243265.
Hagelberg, E., Bell, L., Allen, T., Boyde, A., Jones, S., Clegg, J.B., Hummel, S., Brown, T.A. & Ambler, R.P. (1991). Analysis of ancient bone DNA: Techniques and applications. Phil Trans R Soc Lond B 333, 399407.
Hedges, R.E.M. (2002). Bone diagenesis: An overview of processes. Archaeometry 44, 319328.
Hedges, R.E.M. & Millard, A.R. (1995). Bones and groundwater: Towards the modeling of diagenetic processes. J Arch Sci 22, 155164.
Hedges, R.E.M., Millard, A.R. & Pike, A.W.G. (1995). Measurements and relationships of diagenetic alteration of bone from three archaeological sites. J Arch Sci 22, 201211.
Hollund, H., Arts, N., Jans, M. & Kars, H. (2013). Are teeth better? Histological characterization of diagenesis in archaeological bone–tooth pairs and a discussion of the consequences for archaeometric sample selection and analyses. Int J Osteoarch, doi: 10.1002/oa.2376.
Hollund, H., Jans, M., Collins, M., Kars, H., Joosten, I. & Kars, S. (2012). What happened here? Bone histology as a tool in decoding the postmortem histories of archaeological bone from Castricum, The Netherlands. Int J Osteoarch 22, 537548.
Jackes, M. (2011). Representativeness and bias in archaeological skeletal samples. In Social Bioarchaeology, Agarwal, S. & Glencross, B. (Eds.), pp. 107146. Malden: Blackwell Publishing, Ltd.
Jackes, M., Sherburne, R., Lubell, D., Barker, C. & Wayman, M. (2001). Destruction of microstructure in archaeological bone: A case study from Portugal. Int J Osteoarch 11, 415432.
Jans, M. (2005). Histological Characterisation of Diagenetic Alteration of Archaeological Bone. Amsterdam: VU University, Institute for Geo and Bioarchaeology, Printpartners Ipskamp BV. Geoarchaeological and Bioarchaeological Studies 4.
Jans, M. (2008). Microbial bioerosion of bone—A review. In Current Developments in Bioerosion, Wisshak, M. & Tapanila, L. (Eds.), pp. 397413. Berlin: Springer-Verlag.
Jans, M., Nielsen-Marsh, C., Smith, C., Collins, M. & Kars, H. (2004). Characterization of microbial attack on archaeological bone. J Arch Sci 31, 8795.
Luna, L., Aranda, C., Bosio, L. & Beron, M. (2008). A case of multiple metastases in Late Holocene hunter-gatherers from the Argentine Pampean region. Int J Osteoarch 18, 492506.
Maat, G. (1993). Bone preservation, decay and its related conditions in ancient human bones from Kuwait. Int J Osteoarch 3, 7786.
Maurer, A.-F., Person, A., Tütken, T., Amblard-Pison, S. & Segalen, L. (2014). Bone diagenesis in arid environments: An intra-skeletal approach. Palaeogeogr Palaeoclimatol Palaeoecol 416, 1729.
Mays, S. (1998). The Archaeology of Human Bones. London, UK. Routledge.
Nielsen-Marsh, C.M. & Hedges, R.E.M. (1999). Bone porosity and the use of mercury intrusion porosimetry in bone diagenesis studies. Archaeometry 41, 165174.
Nielsen-Marsh, C.M., Gearney, A.M., Turner-Walker, G., Hedges, R.E.M., Pike, A.G.W. & Collins, M.J. (2000). The chemical degradation of bone. In Human Osteology in Archaeology and Forensic Science, Cox, M. & Mays, C. (Eds.), pp. 439452. London: Greenwich Medical Media.
Ortner, D. (2003). Identification of Pathological Conditions in Human Skeletal Remains. Amsterdam: Academic Press.
Pfeiffer, S. (2000). Paleohistology: Health and disease. In Biological Anthropology of the Human Skeleton, Katzenberg, A. & Saunders, S. (Eds.), pp. 287302. New York: Wiley-Liss.
Pfeiffer, S. & Varney, T. (2000). Quantifying histological and chemical preservation in archaeological bone. In Biogeochemical Approaches to Paleodietary Analysis, Ambrose, S. & Katzenberg, A. (Eds.), pp. 141158. New York: Kluwer Academic/Plenum Publishers.
Pinhasi, R. & Bourbou, C. (2008). How representative are human skeletal assemblages for population analysis?. In Advances in Human Paleopathology, Pinhasi, R. & Mays, S. (Eds.), pp. 3144. Chichester: John Wiley & Sons, Ltd.
Reiche, I., Favre-Quattropani, L., Vignaud, C., Bocherens, H., Charlet, L. & Menu, M. (2003). A multi-analytical study of bone diagenesis: The Neolithic site of Bercy (Paris, France). Meas Sci Technol 14, 16081619.
Schoeninger, M.J., Moore, K.M., Murray, M.L. & Kingston, J.D. (1989). Detection of bone preservation in archaeological and fossil samples. Appl Geochem 4, 281292.
Schultz, M. (1993). Initial stages of systemic bone disease. In Histology of Ancient Human Bone: Methods and Diagnosis, Grupe, G. & Garland, A.N. (Eds.), pp. 185203. Berlin: Springer-Verlag.
Schultz, M. (1997). Microscopic investigation of excavated skeletal remains: A contribution to paleopathology and forensic medicine. In Forensic Taphonomy: The Postmortem Fate of Human Remains, Haglund, W. & Sorg, M. (Eds.), pp. 201222. Boca Raton: CRC Press.
Schultz, M. (2001). Paleohistopathology of bone: A new approach to the study of ancient diseases. Year Phys Anthropol 116, 106147.
Schultz, M. (2003). Light microscopic analysis in skeletal paleopathology. In Identification of Pathological Conditions in Human Skeletal Remains, Ortner, D. (Ed.), pp. 73107. Amsterdam: Academic Press.
Schultz, M. (2012). Light microscopic analysis of macerated pathologically changed bones. In Bone Histology: An Anthropological Perspective, Crowder, C. & Stout, S. (Eds.), pp. 253296. Boca Raton: CRC Press.
Šefčáková, A., Strouhal, E., Nemecková, A., Thurzo, M. & Stassíková-Stukovská, D. (2001). Case of metastatic carcinoma from end of the 8th-Early 9th century Slovakia. Am J Phys Anthropol 116, 216229.
Steinbock, R.T. (1976). Paleopathological Diagnosis and Interpretation. Springfield: CC Thomas.
Stodder, A. (2008). Taphonomy and the nature of archaeological assemblages. In Biological Anthropology of the Human Skeleton, Katzenberg, A. & Saunders, S. (Eds.), pp. 71114. New Jersey: John Wiley & Sons Inc.
Stout, S. (1978). Histological structure and its preservation in ancient bone. Curr Anthropol 19, 601604.
Turner-Walker, G. (2008). The chemical and microbial degradation of bones and teeth. In Advances in Human Paleopathology, Pinhasi, R. & Mays, S. (Eds.), pp. 329. Chichester: John Wiley & Sons, Ltd.
Turner-Walker, G. (2012). Early bioerosion in skeletal tissues: persistence through deep time. N Jb Geol Paläony Abh 265, 165183.
Turner-Walker, G. & Parry, T.V. (1995). The tensile strength of archaeological bone. J Arch Sci 22, 185192.
Turner-Walker, G. & Jans, M.M.E. (2008). Reconstructing taphonomic histories using histological analysis. Palaeogeogr Palaeoclimatol Palaeoecol 266, 227235.
Turner-Walker, G. & Syversen, U. (2002). Quantifying histological changes in archaeological bones using BSE-SEM image analysis. Archaeometry 44, 461468.
Tütken, T. & Vennerman, T.W. (2011). Preface. Fossil bones and teeth: Preservation or alteration of biogenic compositions. Palaeogeogr Palaeoclimatol Palaeoecol 310, 18.
Uytterschaut, H. (1993). Human bone remodelling and aging. In Histology of Ancient Human Bone: Methods and Diagnosis, Grupe, G. & Garland, A.N. (Eds.), pp. 95109. Berlin: Springer-Verlag.
van der Merwe, A., Maat, G. & Steyn, M. (2010). Ossified haematomas and infectious bone changes on the anterior tibia: Histomorphological features as an aid for accurate diagnosis. Int J Osteoarch 20, 227239.
von Hunnius, T., Roberts, C., Boylston, A. & Saunders, S. (2006). Histological identification of syphilis in pre-Columbian England. Am J Phys Anthropol 129, 559566.
Wakely, J., Anderson, T. & Carter, A. (1995). A multidisciplinarian case study of prostatic (?) carcinoma from medieval Canterbury. J Arch Sci 22, 469477.
White, T. & Folkens, P. (2005). The Human Bone Manual. Burlington: Elsevier Academic Press.
Zink, A., Grabner, W. & Nerlich, A. (2005). Molecular identification of human tuberculosis in recent and historic bone tissue samples: The role of molecular techniques for the study of historic tuberculosis. Am J Phys Anthropol 126, 3247.



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