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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Effects of lipid extraction and different collagen extraction methods on archaeological fish bones and its implications for fish bone diagenesis
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Time-domain THz spectroscopy of the characteristics of hydroxyapatite provides a signature of heating in bone tissue
Plazanet, M., Tasseva, J., Bartolini, P., Taschin, A., Torre, R., Combes, C., Rey, C. C., Michele, A. D., Verezhak, M., & Gourrier, A. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201745 · Cited by 8
7 Taphonomic and Diagenetic Processes
Grupe, G. (2007) · Springer eBooks · doi:10.1007/978-3-540-33761-4_7 · Cited by 8
Studies on the degradation of horn, antler and ivory at archaeological sites
Simpson, P. B. (2011) · UPT. Syiah Kuala University Library (Syiah Kuala University) · Cited by 8
Comparing biological and pathological factors affecting osteocalcin concentrations in archaeological skeletal remains
Scott, A. B., Taurozzi, A. J., Hughes, N., Pedersen, D. D., Kontopoulos, I., Mackie, M., & Collins, M. J. (2020) · Journal of Archaeological Science Reports · doi:10.1016/j.jasrep.2020.102573 · Cited by 7
Self-citation
Experimental taphonomy of fish bone from warm and cold water species: Testing the effects of amino acid composition on collagen breakdown in modern fish bone using thermal maturation experiments
Harvey, V. L., Wogelius, R. A., Manning, P. L., & Buckley, M. (2021) · Journal of Archaeological Science · doi:10.1016/j.jas.2020.105318 · Cited by 7
The bottom line: Exploring analytical methods for assessing bioapatite preservation in archaeological bone using FTIR-ATR
Smith, D. R., Martin, E. K., Kaufman, B. L., Callaghan, M., Cardona, K., Kovacevich, B., & Toyne, J. M. (2023) · Journal of Archaeological Science Reports · doi:10.1016/j.jasrep.2023.104014 · Cited by 7
Preservation of proteins in the geosphere
Umamaheswaran, R., & Dutta, S. (2024) · Nature Ecology & Evolution · doi:10.1038/s41559-024-02366-z · Cited by 7
“…predicted the rapid defunctionalization of higher-order protein structures with an increase in temperature 17 , and studies into its early diagenesis have also emphasized the importance of local microbial activity and the chemical deterioration of the mineral phase associated with the protein 23 .”
Bone diagenesis in the medieval cemetery of Vratislavs’ Palace in Prague
Viani, A., Machová, D., Mácová, P., Mali, G., & Velemínský, P. (2021) · Archaeological and Anthropological Sciences · doi:10.1007/s12520-021-01286-4 · Cited by 7
Ancient DNA analysis of an archaeological assemblage of Chondrichthyes vertebrae from South Auckland, New Zealand
Shepherd, L. D., & Campbell, M. E. (2021) · Journal of Archaeological Science Reports · doi:10.1016/j.jasrep.2021.102830 · Cited by 7
Experimental Aqueous Alteration of Cortical Bone Microarchitecture Analyzed by Quantitative Micro-Computed Tomography
Kral, A. G., Ziegler, A., Tütken, T., & Geisler, T. (2021) · Frontiers in Earth Science · doi:10.3389/feart.2021.609496 · Cited by 9
“However, in particular during early stages of bone fossilization, the collagen-water interaction and the resulting degradation through chemical hydrolysis are of great importance (Collins et al., 2002; Pfretzschner, 2004; Dobberstein et al., 2009; Turner-Walker, 2011).”
Background
The Bodies in the ‘Bog’: A Multi-Isotope Investigation of Individual Life-Histories at an Unusual 6th/7th AD Century Group Burial from a Roman Latrine at Cramond, Scotland
Czére, O., Lawson, J. A., Müldner, G., Evans, J. E., Boyle, A., & Britton, K. (2022) · Archaeological and Anthropological Sciences · doi:10.1007/s12520-022-01509-2 · Cited by 7
Combining collagen extraction with mineral Zn isotope analyses from a single sample for robust palaeoecological investigations
McCormack, J., Bourgon, N., Sinet‐Mathiot, V., Režek, Ž., Smith, G. M., Hublin, J., Dabain, M., & Fewlass, H. (2022) · Archaeological and Anthropological Sciences · doi:10.1007/s12520-022-01601-7 · Cited by 7
“…alteration in more recent skeletal material compared to the Palaeolithic material examined herein; i.e. the likelihood of alteration increases with age, but the level of preservation will also strongly depend on the burial environment (van Klinken 1999; Collins et al. 2002; Clementz 2012).”
Background
The diagenetic fate of collagen as revealed by analytical pyrolysis of fossil fish scales from deep time
Umamaheswaran, R., Dutta, S., Prasad, G. V. R., Khan, M. A., Kumar, S., Bera, S., & Patnaik, R. (2022) · Geobiology · doi:10.1111/gbi.12537 · Cited by 7
Effect of Nucleotides on the Phase and Crystal Structure of Synthetic Calcium Carbonate
Lang, A., Polishchuk, I., Katsman, A. V., & Pokroy, B. (2023) · Crystal Growth & Design · doi:10.1021/acs.cgd.3c00367 · Cited by 7
Microstructural Changes of Bone after Soft Tissue Removal: ATR‐FTIR and XRD Spectroscopies
Alebrahim, M. A., Al-Akhras, M.-A. H., Al‐Hiyasat, A. S., Rajjash, A. S. B., Mousa, M. S., & Darayseh, A. A. (2023) · Journal of Spectroscopy · doi:10.1155/2023/6599002 · Cited by 7
The influence of taphonomy on histological and isotopic analyses of treated and untreated buried modern human bone
Reid, R. A. G., Jans, M. M. E., Chesson, L. A., Taylor, R. J., & Berg, G. E. (2023) · Journal of Archaeological Science · doi:10.1016/j.jas.2023.105901 · Cited by 7
A Nondestructive Prescreening Method for Bone Collagen Content Using Micro-Computed Tomography
Tripp, J. A., Squire, M. E., Hamilton, J., & Hedges, R. E. M. (2010) · Radiocarbon · doi:10.1017/s0033822200045641 · Cited by 7
“cooking or defleshing), temperature and hydration of the burial site, and time since death (Collins et al. 2002).”
Background
Paleogenomics: Genome-Scale Analysis of Ancient DNA and Population and Evolutionary Genomic Inferences
Lan, T., & Lindqvist, C. (2018) · Population genomics · doi:10.1007/13836_2017_7 · Cited by 7
Foraminifera—A new find in the microtaphonomical characterization of bones from marine archaeological excavations
Guareschi, E. E., Haig, D. W., Tobe, S. S., Nicholls, P. K., & Magni, P. A. (2021) · International Journal of Osteoarchaeology · doi:10.1002/oa.3013 · Cited by 7
Evaluation of techniques for human bone decalcification and amplification using sixteen STR markers
Balayan, A. P., Kapoor, A., Chaudhary, G., & Raina, A. (2014) · Egyptian Journal of Forensic Sciences · doi:10.1016/j.ejfs.2014.05.002 · Cited by 7
AMS 14C Dating of Bones from Archaeological Sites in Mexico
Solís, C., Pérez-Andrade, G., Rodríguez‐Ceja, M., Solis-Meza, E., Méndez, T., Chávez-Lomelí, E., Martínez‐Carrillo, M. Á., & Mondragón, M. A. (2017) · Radiocarbon · doi:10.1017/rdc.2017.136 · Cited by 7
“As a result, part of the original collagen associated with the bones is often lost or replaced by other compounds (Collins et al. 2002).”
Background
Taphonomic and Diagenetic Processes
Grupe, G., & Harbeck, M. (2014) · Springer eBooks · doi:10.1007/978-3-642-39979-4_7 · Cited by 7
Making vertebrate fossil radiocarbon dates more useful for global scientific research
Herrando‐Pérez, S., & Stafford, T. W. (2025) · Journal of Quaternary Science · doi:10.1002/jqs.70012 · Cited by 9
“After death, bones experience diagenesis that alters their chemical and physical properties, including changes in carbonate content, organic matter and the composition of collagen and DNA (Collins et al., 2002).”
Influential
Methodological advances in Neanderthal identification, phylogeny, chronology, mobility, climate, and diet
Bocherens, H., Jaouen, K., Rivals, F., Slon, V., Talamo, S., & Welker, F. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-821428-2.00002-0 · Cited by 6
Diagnosis of archaeological bones: Analyzing the state of conservation of lower Pleistocene bones through diagenesis methods
Díaz-Cortés, A., Valle, H. D., López‐Polín, L., Otero, J., Cáceres, I., Valtierra, N., Pineda, A., Saladié, P., & Vallverdú, J. (2024) · Microchemical Journal · doi:10.1016/j.microc.2024.111353 · Cited by 6
Establishing the volatile organic compound profile and detection capabilities of human remain detection dogs to human bones
Ouimet, F., Patel, D., Tsontakis, M., Samson, C., & Forbes, S. L. (2024) · Forensic Science International Synergy · doi:10.1016/j.fsisyn.2024.100566 · Cited by 6
Exploiting FTIR microspectroscopy and chemometric analysis in the discrimination between Egyptian ancient bones: a case study
El-Hussein, A., Yousef, I., & Kasem, M. (2020) · Journal of the Optical Society of America B · doi:10.1364/josab.397419 · Cited by 4
Proteomics and Integrated Techniques to Characterize Organic Residues in Funerary Findings from Italic Populations of the First Millennium BC
Siano, F., Picariello, G., Caruso, T., Esposito, S., Rescigno, C., Addeo, F., & Vasca, E. (2022) · Journal of Proteome Research · doi:10.1021/acs.jproteome.2c00093 · Cited by 6
Hydrogen isotope measurements of bone and dental tissues from archaeological human and animal samples and their use as climatic and diet proxies
Clauzel, T., Richardin, P., Ricard, J., Béchennec, Y. L., Amiot, R., Fourel, F., Joseph, D., Vinçon‐Laugier, A., Flandrois, J., & Lécuyer, C. (2022) · Journal of Archaeological Science · doi:10.1016/j.jas.2022.105676 · Cited by 6
Interpreting Stable Carbon and Nitrogen Isotope Ratios in Archaeological Remains: An Overview of the Processes Influencing the δ13C and δ15N Values of Type I Collagen
Leatherdale, A. (2013) · The University of Western Ontario Journal of Anthropology · doi:10.5206/uwoja.v21i1.8936 · Cited by 6
“Collins et al. (2002) and Hedges (2002) demonstrate that taphonomic degradation of remains can lead to structural changes, both macro- and micro-scopically, or even a complete loss of molecules.”
Background
Paleohistology and the study of human remains: past, present and future approaches
Assis, S., Santos, A. L., & Keenleyside, A. (2016) · Revista Argentina de Antropología Biológica · doi:10.17139/raab.2016.0018.02.02 · Cited by 6
A multi‐method approach to dating the burial and skeleton of Kiacatoo Man, New South Wales, Australia
Pietsch, T., Kemp, J., Pardoe, C., Grün, R., Olley, J. M., & Wood, R. E. (2019) · Journal of Quaternary Science · doi:10.1002/jqs.3165 · Cited by 6
“This is not an uncommon situation in bones preserved in hot environments, and although it suggests that the bone is not very recent, it does not in itself indicate a Pleistocene antiquity (Collins et al., 2002).”
Background
Perspectivas atuais sobre tecidos moles não mineralizados em fósseis de dinossauros não avianos
Alves, E. F., & Machado, M. F. (2020) · Terrae Didatica · doi:10.20396/td.v16i0.8659539 · Cited by 6
Twenty-Seven Y-Chromosome Short Tandem Repeats Analysis of Italian Mummies of the 16th and 18th Centuries: An Interdisciplinary Research
Bini, C., Cilli, E., Sarno, S., Traversari, M., Fontani, F., Boattini, A., Pelotti, S., & Luiselli, D. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.720640 · Cited by 9
Stored potential energy increases and elastic properties alterations are produced after restoring dentin with Zn-containing amalgams
Toledano, M., Osorio, E., Aguilera, F. S., Toledano‐Osorio, M., López‐López, M. T., & Osorio, R. (2018) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2018.12.002 · Cited by 6
The Assessment of Bone Deterioration with Nuclear Magnetic Resonance Spectroscopy in a Multidisciplinary Context: The Case of the UNESCO World Heritage Site of Sedlec, Czechia
Viani, A., Mácová, P., Machová, D., & Čendak, T. (2019) · Archaeometry · doi:10.1111/arcm.12475 · Cited by 6

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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