Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T09:01:17.722Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  14 July 2015

Sandra Assis*
Affiliation:
CIAS—Research Centre for Anthropology and Health, Department of Life Sciences, University of Coimbra, Calçada Martins de Freitas 3000-456 Coimbra, Portugal
Anne Keenleyside
Affiliation:
Department of Anthropology, DNA-C, Trent University, 2140 East Bank Drive, Peterborough, Ontario, K9J 7B8, Canada
Ana Luísa Santos
Affiliation:
CIAS—Research Centre for Anthropology and Health, Department of Life Sciences, University of Coimbra, Calçada Martins de Freitas 3000-456 Coimbra, Portugal
Francisca Alves Cardoso
Affiliation:
CRIA—Centro em Rede de Investigação em Antropologia, Faculdade de Ciências Socias e Humanas, Universidade Nova de Lisboa, Av. Berna 26-C, 1069-061 Lisboa, Portugal
*
*Corresponding author.sandraassis78@gmail.com
Get access

Abstract

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.

Type
Biological Applications and Techniques
Copyright
© Microscopy Society of America 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-Maksound, G. (2010). Comparison between the properties of “accelerated-aged” bones and archaeological bones. MAA 10, 89112.Google Scholar
Aufderheide, A. & Rodríguez-Martín, C. (1998). The Cambridge Encyclopedia of Human Paleopathology. Cambridge: Cambridge University Press.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Bruzek, J. (2002). A method for visual determination of sex, using the human hip bone. Am J Phys Anthropol 117, 157168.Google Scholar
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.Google Scholar
Burgener, F., Kormano, M. & Pudas, T. (2006). Bone and Joint Disorders: Differential Diagnosis in Conventional Radiology. Stittgard: Georg Thieme Verlag.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
De La Rúa, C., Baraybar, J. & Etxeberria, F. (1995). Neolithic case of metastasizing carcinoma: Multiple approaches to differential diagnosis. Int J Osteoarch 5, 254264.Google Scholar
Efremov, I.A. (1940). Taphonomy: A new branch of paleontology. Pan-Am Geol 74, 8193.Google Scholar
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.Google Scholar
Grupe, G. (2007). Taphonomic and diagenetic processes. In Handbook of Paleoanthropology, Henke, W., Tattersall, I. & Hardt, T. (Eds.), pp. 241259. Berlin Heidelberg: Springer-Verlag.Google Scholar
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.Google Scholar
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.Google Scholar
Hackett, C.J. (1981). Microscopical focal destruction (tunnels in exhumed human bones). Med Sci Law 21, 243265.Google Scholar
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.Google Scholar
Hedges, R.E.M. (2002). Bone diagenesis: An overview of processes. Archaeometry 44, 319328.Google Scholar
Hedges, R.E.M. & Millard, A.R. (1995). Bones and groundwater: Towards the modeling of diagenetic processes. J Arch Sci 22, 155164.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Jackes, M. (2011). Representativeness and bias in archaeological skeletal samples. In Social Bioarchaeology, Agarwal, S. & Glencross, B. (Eds.), pp. 107146. Malden: Blackwell Publishing, Ltd.Google Scholar
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.Google Scholar
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.Google Scholar
Jans, M. (2008). Microbial bioerosion of bone—A review. In Current Developments in Bioerosion, Wisshak, M. & Tapanila, L. (Eds.), pp. 397413. Berlin: Springer-Verlag.Google Scholar
Jans, M., Nielsen-Marsh, C., Smith, C., Collins, M. & Kars, H. (2004). Characterization of microbial attack on archaeological bone. J Arch Sci 31, 8795.CrossRefGoogle Scholar
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.Google Scholar
Maat, G. (1993). Bone preservation, decay and its related conditions in ancient human bones from Kuwait. Int J Osteoarch 3, 7786.Google Scholar
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.Google Scholar
Mays, S. (1998). The Archaeology of Human Bones. London, UK. Routledge.Google Scholar
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.Google Scholar
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.Google Scholar
Ortner, D. (2003). Identification of Pathological Conditions in Human Skeletal Remains. Amsterdam: Academic Press.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
Schultz, M. (2001). Paleohistopathology of bone: A new approach to the study of ancient diseases. Year Phys Anthropol 116, 106147.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Steinbock, R.T. (1976). Paleopathological Diagnosis and Interpretation. Springfield: CC Thomas.Google Scholar
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.Google Scholar
Stout, S. (1978). Histological structure and its preservation in ancient bone. Curr Anthropol 19, 601604.Google Scholar
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. Google Scholar
Turner-Walker, G. (2012). Early bioerosion in skeletal tissues: persistence through deep time. N Jb Geol Paläony Abh 265, 165183.Google Scholar
Turner-Walker, G. & Parry, T.V. (1995). The tensile strength of archaeological bone. J Arch Sci 22, 185192.Google Scholar
Turner-Walker, G. & Jans, M.M.E. (2008). Reconstructing taphonomic histories using histological analysis. Palaeogeogr Palaeoclimatol Palaeoecol 266, 227235.Google Scholar
Turner-Walker, G. & Syversen, U. (2002). Quantifying histological changes in archaeological bones using BSE-SEM image analysis. Archaeometry 44, 461468.Google Scholar
Tütken, T. & Vennerman, T.W. (2011). Preface. Fossil bones and teeth: Preservation or alteration of biogenic compositions. Palaeogeogr Palaeoclimatol Palaeoecol 310, 18.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
von Hunnius, T., Roberts, C., Boylston, A. & Saunders, S. (2006). Histological identification of syphilis in pre-Columbian England. Am J Phys Anthropol 129, 559566.Google Scholar
Wakely, J., Anderson, T. & Carter, A. (1995). A multidisciplinarian case study of prostatic (?) carcinoma from medieval Canterbury. J Arch Sci 22, 469477.Google Scholar
White, T. & Folkens, P. (2005). The Human Bone Manual. Burlington: Elsevier Academic Press.Google Scholar
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.Google Scholar