Cited by 615Archaeology and ancient environmental studiesCultural Heritage Materials AnalysisSoil and Environmental Studies

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The survival of organic matter in bone: a review

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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·Archaeometry

DOI 10.1111/1475-4754.t01-1-00071

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Abstract

If bone is considered as a composite of collagen (protein) and bioapatite (mineral), then three pathways of diagenesis are identified: (1) chemical deterioration of the organic phase; (2) chemical deterioration of the mineral phase; and (3) (micro) biological attack of the composite. The first of these three pathways is relatively unusual and will only occur in environments that are geochemically stable for bone mineral. However, because rates of biomolecular deterioration in the burial environment are slow, such bones would yield useful biomolecular information. In most environments, bones are not in thermodynamic equilibrium with the soil solution, and undergo chemical deterioration (path 2). Dissolution of the mineral exposes collagen to biodeterioration, and in most cases the initial phase of dissolution will be followed by microbial attack (path 3). Biological attack (3) also proceeds by initial demineralization; therefore paths 2 and 3 are functionally equivalent. However,in a bone that follows path 3 the damage is more localized than in path 2, and regions equivalent to path 1 may therefore exist outside these zones of destruction. Other biomolecules, such as blood proteins, cellular lipids and DNA, exist within the physiological spaces within bone.For these biomolecules, death history may be particularly important for their survival.

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Background
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Ultrafiltration of Bone Samples is Neither the Problem nor the Solution
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“In addition to all of the above-mentioned analytical variations, results on bone samples are also complicated by factors such as burial conditions, soil pH, moisture, and temperature, and the type of flora and microfauna that characterize the burial environment (Collins et al. 2002).”
BackgroundInfluential
Intra‐ and Inter‐Element Variability in Mitochondrial and Nuclear DNA from Fresh and Environmentally Exposed Skeletal Remains,
Antinick, T. C., & Foran, D. R. (2018) · Journal of Forensic Sciences · doi:10.1111/1556-4029.13843 · Cited by 36
Qualitative application based on IR spectroscopy for bone sample quality control in radiocarbon dating
Gianfrate, G., D’Elia, M., Quarta, G., Giotta, L., Valli, L., & Calcagnile, L. (2007) · Nuclear Instruments and Methods in Physics Research Section B Beam Interactions with Materials and Atoms · doi:10.1016/j.nimb.2007.01.309 · Cited by 32
Rather yield than break: assessing the influence of human bone collagen content on heat-induced warping through vibrational spectroscopy
Vassalo, A. R., Cunha, E. M., de Carvalho, L. A. E. B., & Gonçalves, D. (2016) · International Journal of Legal Medicine · doi:10.1007/s00414-016-1400-x · Cited by 32
“depositional phenomena result in increasing loss of the organic component [21, 22], so it was expected that the more ancient archeological bones had a smaller preservation of CC in”
Background
Identification of degraded bone and tooth splinters from arid environments using palaeoproteomics
Meillour, L. L., Zazzo, A., Lesur, J., Cersoy, S., Marie, A., Lebon, M., Pleurdeau, D., & Zirah, S. (2018) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2018.09.013 · Cited by 32
Environmental, trophic, and ecological factors influencing bone collagen δ2H
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“Collins M. J., Nielsen-Mar sh C. M., Hiller J., Smith C. I., Roberts J. P., Prigodich R. V., Weiss T. J., Csapo ` J., Millard A. R. and K. Topalov et al. / Geochimica et Cosmoch imica Acta 111 (2013) 88–104 103 Turner-Wa lker (2002) The survival of organic matter in bone: a review.”
Background
Patterns of soft tissue and cellular preservation in relation to fossil bone tissue structure and overburden depth at the standing rock hadrosaur site, maastrichtian hell creek formation, South Dakota, USA
Ullmann, P. V., Pandya, S. H., & Nellermoe, R. (2019) · Cretaceous Research · doi:10.1016/j.cretres.2019.02.012 · Cited by 31
Raman hyperspectral imaging as an effective and highly informative tool to study the diagenetic alteration of fossil bones
Sasso, G. D., Angelini, I., Maritan, L., & Artioli, G. (2017) · Talanta · doi:10.1016/j.talanta.2017.10.059 · Cited by 31
“Collagen loss is mainly due to chemical hydrolysis, alteration of the mineral fraction and microbial degradation of bone [8,50,51]: these processes are”
Estimation of the post-mortem interval in human bones by infrared spectroscopy
Baptista, A., Pedrosa, M., Curate, F., Ferreira, M. T., & Marques, M. P. M. (2021) · Zeitschrift für Rechtsmedizin · doi:10.1007/s00414-021-02641-9 · Cited by 27
Microbes and the Fossil Record: Selected Topics in Paleomicrobiology
Tomescu, A., Klymiuk, A., Matsunaga, K., Bippus, A., & Shelton, G. W. K. (2016) · Advances in environmental microbiology · doi:10.1007/978-3-319-28071-4_3 · Cited by 26
Microscopic Post‐Mortem Changes: the Chemistry of Decomposition
Forbes, S. L., Perrault, K. A., & Comstock, J. L. (2017) · doi:10.1002/9781118953358.ch2 · Cited by 30
The effect of grain size on carbonate contaminant removal from tooth enamel: Towards an improved pretreatment for radiocarbon dating
Wood, R. E., Duval, M., Hương, N. T. M., Tuan, N. A., Bacon, A., Demeter, F., Duringer, P., Oxenham, M. F., & Piper, P. J. (2016) · Quaternary Geochronology · doi:10.1016/j.quageo.2016.08.010 · Cited by 30
“4.3 Implications for enamel diagenesis In contrast with the extensive study of bone diagenesis (Collins et al., 2002; Hedges, 2002), relatively little work has examined how enamel degrades in the burial environment.”
BackgroundInfluential
ATR-FTIR spectroscopy combined with data manipulation as a pre-screening method to assess DNA preservation in skeletal remains
Leskovar, T., Pajnič, I. Z., Geršak, Ž. M., Jerman, I., & Črešnar, M. (2019) · Forensic Science International Genetics · doi:10.1016/j.fsigen.2019.102196 · Cited by 29
Postmortem Skeletal Microbial Community Composition and Function in Buried Human Remains
Emmons, A. L., Mundorff, A. Z., Hoeland, K. M., Davoren, J., Keenan, S. W., Carter, D. O., Campagna, S. R., & DeBruyn, J. M. (2022) · mSystems · doi:10.1128/msystems.00041-22 · Cited by 29
“bone diagenetic processes, including chemical and/or biological modification (3).”
Background
An FTIR-based model for the diagenetic alteration of archaeological bones
Scaggion, C., Sasso, G. D., Nodari, L., Pagani, L., Carrara, N., Zotti, A., Banzato, T., Usai, D., Pasqualetto, L., Gadioli, G., et al. (2023) · Journal of Archaeological Science · doi:10.1016/j.jas.2023.105900 · Cited by 29
Residue Analysis
Craig, O. E., Saul, H., & Spiteri, C. D. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139013826.004 · Cited by 28
Autofluorescence of experimentally heated bone: Potential archaeological applications and relevance for estimating degree of burning
Lambrecht, G., & Mallol, C. (2020) · Journal of Archaeological Science Reports · doi:10.1016/j.jasrep.2020.102333 · Cited by 28
Bone diagenesis in archaeological and contemporary human remains: an investigation of bone 3D microstructure and minero-chemical assessment
Caruso, V., Marinoni, N., Diella, V., Berna, F., Cantaluppi, M., Mancini, L., Trombino, L., Cattaneo, C., Pastero, L., & Pavese, A. (2020) · Archaeological and Anthropological Sciences · doi:10.1007/s12520-020-01090-6 · Cited by 28
THE ROLE OF BACTERIALLY MEDIATED PRECIPITATION IN THE PERMINERALIZATION OF BONE
Daniel, J. C., & Chin, K. (2010) · Palaios · doi:10.2110/palo.2009.p09-120r · Cited by 28
“…of bone has been recognized since at least 1864 (Wedl, 1864) and has been generally thought to represent the dominant role of microbes in bone diagenesis (Tucker, 1991; Child, 1995a; Collins et al., 2002; Hedges, 2002, Trueman et al., 2003; Blumenschine et al., 2007; Lee-Thorp and Sealy, 2008).”
Background
Validation of a Non-Targeted LC-MS Approach for Identifying Ancient Proteins: Method Development on Bone to Improve Artifact Residue Analysis
Barker, A., Dombrosky, J., Chaput, D., Venbles, B., Wolverton, S., & Stevens, S. M. (2015) · Ethnobiology Letters · doi:10.14237/ebl.6.1.2015.294 · Cited by 27
“…their hydrophobicity, which promotes preservation, as well as collagens' documented resistance to several sources of degradation (see Child 1995; Collins et al. 2002; Dobberstein et al. 2009), and the number of previous studies that have successfully identified ancient bone collagens (e.g.,…”
Background
Genomic Correlates of Atherosclerosis in Ancient Humans
Zink, A., Wann, L. S., Thompson, R. C., Keller, A., Maixner, F., Allam, A. H., Finch, C. E., Frøhlich, B., Kaplan, H. S., Lombardi, G. P., et al. (2014) · Global Heart · doi:10.1016/j.gheart.2014.03.2453 · Cited by 29
“Several parameters such as high temperature, ultraviolet radiation, humidity, and a low pH value significantly accelerate the DNA decay [16,17].”
Background
Nitrogen content variation in archaeological bone and its implications for stable isotope analysis and radiocarbon dating
Jacob, E., Querci, D., y Caparrós, M. Á. C., Ruíz, C. B., Higham, T., & Devièse, T. (2018) · Journal of Archaeological Science · doi:10.1016/j.jas.2018.02.019 · Cited by 27
Acidic Monosaccharides become Incorporated into Calcite Single Crystals**
Lang, A., Mijowska, S., Polishchuk, I., Fermani, S., Falini, G., Katsman, A. V., Marin, F., & Pokroy, B. (2020) · Chemistry - A European Journal · doi:10.1002/chem.202003344 · Cited by 26
Bone need not remain an elephant in the room for radiocarbon dating
Herrando‐Pérez, S. (2021) · Royal Society Open Science · doi:10.1098/rsos.201351 · Cited by 27
Compressive marks from gravel substrate on vertebrate remains: a preliminary experimental study
Marin‐Monfort, M. D., Pesquero, M. D., & Fernández–Jalvo, Y. (2013) · Quaternary International · doi:10.1016/j.quaint.2013.10.028 · Cited by 27
“In contrast, when bones are soaked in strong alkaline fluids, deproteinization occurs, and the bone becomes more brittle as only the mineral component remains (Collins et al., 2002; White and Folkens, 2005).”
Background
Protein Molecular Data from Ancient (>1 million years old) Fossil Material: Pitfalls, Possibilities and Grand Challenges
Schweitzer, M. H., Schroeter, E. R., & Goshe, M. B. (2014) · Analytical Chemistry · doi:10.1021/ac500803w · Cited by 28
Diagenetiforms: A new term to explain protein changes as a result of diagenesis in paleoproteomics
Cleland, T. P., Schroeter, E. R., & Colleary, C. (2020) · Journal of Proteomics · doi:10.1016/j.jprot.2020.103992 · Cited by 29
Cadaver‐detection dogs: A review of their capabilities and the volatile organic compound profile of their associated training aids
Dargan, R., & Forbes, S. L. (2020) · Wiley Interdisciplinary Reviews Forensic Science · doi:10.1002/wfs2.1409 · Cited by 26
Use of thermogravimetric analysis to estimate collagen and hydroxyapatite contents in archaeological bone
Durga, R., Jiménez, N., Ramanathan, S., Suraneni, P., & Pestle, W. J. (2022) · Journal of Archaeological Science · doi:10.1016/j.jas.2022.105644 · Cited by 26
Last Glacial Maximum glacier fluctuations on the northern Alpine foreland: Geomorphological and chronological reconstructions from the Rhine and Reuss glacier systems
Kamleitner, S., Ivy-Ochs, S. D., Manatschal, L., Akçar, N., Christl, M., Vockenhuber, C., Hajdas, I., & Synal, H. (2022) · Geomorphology · doi:10.1016/j.geomorph.2022.108548 · Cited by 26
Ancient human genomics: the methodology behind reconstructing evolutionary pathways
Marciniak, S., Klunk, J., Devault, A. M., Enk, J. M., & Poinar, H. N. (2015) · Journal of Human Evolution · doi:10.1016/j.jhevol.2014.11.003 · Cited by 30
A novel method to measure steroid hormone concentrations in walrus bone from archaeological, historical, and modern time periods using liquid chromatography/tandem mass spectrometry
Charapata, P., Horstmann, L. A., Jannasch, A., & Misarti, N. (2018) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.8272 · Cited by 26
“Walrus bones from different archaeological, historical, and modern time periods potentially have different lipid compositions, as lipid in cortical bone is already low,(19,42) and taphonomic processes could affect the lipid composition of archaeological bones buried for thousands of years.(15,43) In addition, there ha…”
Background
Beyond documenting diagenesis: The fifth international bone diagenesis workshop
Lee‐Thorp, J. A., & Sealy, J. C. (2008) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2008.03.025 · Cited by 26
Sustainable phosphorus management in soil using bone apatite
Biswas, P. P., Turner‐Walker, G., Rathod, J., Liang, B., Wang, C., Lee, Y.-C., & Sheu, H. (2021) · Journal of Environmental Management · doi:10.1016/j.jenvman.2021.114344 · Cited by 25
Self-citation
Comparison of ultrashort echo time sequences for MRI of an ancient mummified human hand
Özen, A. Ç., Ludwig, U., Öhrström, L. M., Rühli, F. J., & Bock, M. (2015) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25651 · Cited by 25
DNA Profiling Success Rates from Degraded Skeletal Remains in Guatemala
Johnston, E., & Stephenson, M. (2016) · Journal of Forensic Sciences · doi:10.1111/1556-4029.13087 · Cited by 25
“It appears that skeletal material and DNA do not degrade through the same process or in parallel (4,5).”
Background
Use of micro-computed tomography imaging and porosity measurements as indicators of collagen preservation in archaeological bone
Tripp, J. A., Squire, M. E., Hedges, R. E. M., & Stevens, R. E. (2018) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2018.09.012 · Cited by 26

Authors: 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.
Affiliations: Newcastle University (GB)
Trinity College (US)
University of Stirling (GB)
Durham University (GB)
ORCID: Collins, M. J.
Smith, C. I.
Millard, A. R.
Venue: Archaeometry
Publisher: Wiley
Published: 2002-08
Volume: 44
Issue: 3
Pages: 383-394
ISSN: 0003-813X (ISSN-L)
1475-4754
DOI: 10.1111/1475-4754.t01-1-00071
OpenAlex: W1980807649
Semantic Scholar: 4c01539cadd487be926e662eff3dc1e017160333
Cited by: 615
References: 113
Citations by year: 2026: 28 · 2025: 28 · 2024: 27 · 2023: 31 · 2022: 43 · 2021: 60 · 2020: 43 · 2019: 34 · 2018: 32 · 2017: 36 · 2016: 30 · 2015: 29 · 2014: 35 · 2013: 25 · 2012: 23
FWCI: 4.25
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 137 d)
Locations: Archaeometry (publishedVersion)
Durham Research Online (Durham University) (acceptedVersion)
Durham Research Online (Durham University) (submittedVersion)
White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
Durham Research Online (Durham University) (submittedVersion, cc-by)
Newcastle University ePrints (Newcastle Univesity)
Funders: Durham University
Topics: Social Sciences › Archeology › Archaeology and ancient environmental studies
Social Sciences › Arts and Humanities › Archeology (arts and humanities) › Cultural Heritage Materials Analysis
Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil and Environmental Studies
Keywords: bone diagenesis, organic matter preservation, collagen degradation, demineralization, bone DNA, plasma proteins, cellular lipids

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The survival of organic matter in bone: a review

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