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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Ntasi, G., Palomo, I. R., Marino, G., Piaz, F. D., Cappellini, E., Birolo, L., & Petrone, P. (2022) · Scientific Reports · doi:10.1038/s41598-022-12042-6 · Cited by 16
Bone collagen from subtropical Australia is preserved for more than 50,000 years
Peters, C., Wang, Y. V., Vakil, V. N., Cramb, J., Dortch, J., Hocknull, S. A., Lawrence, R. A., Manne, T., Monks, C., Rössner, G. E., et al. (2023) · Communications Earth & Environment · doi:10.1038/s43247-023-01114-8 · Cited by 16
Self-citation
Bacterial bioerosion in human and animal bones from subtropical environments (Northern Pampa/Middle Paraná River Basin, República Argentina)
Galligani, P. E., Sartori, J. I., & Barrientos, G. (2019) · Journal of Archaeological Science Reports · doi:10.1016/j.jasrep.2019.05.015 · Cited by 15
Machine learning ATR-FTIR spectroscopy data for the screening of collagen for ZooMS analysis and mtDNA in archaeological bone
Chowdhury, M. P., Choudhury, K. D., Bouchard, G. P., Riel-Salvatore, J. G., Negrino, F., Benazzi, S., Slimak, L., Frasier, T. R., Szabo, V. E., Harrison, R., et al. (2021) · Journal of Archaeological Science · doi:10.1016/j.jas.2020.105311 · Cited by 15
A review of the current understanding of burned bone as a source of DNA for human identification
Mckinnon, M., Henneberg, M., & Higgins, D. (2021) · Science & Justice · doi:10.1016/j.scijus.2021.03.006 · Cited by 18
Soft Tissue and Biomolecular Preservation in Vertebrate Fossils from Glauconitic, Shallow Marine Sediments of the Hornerstown Formation, Edelman Fossil Park, New Jersey
Voegele, K. K., Boles, Z. M., Ullmann, P. V., Schroeter, E. R., Zheng, W., & Lacovara, K. J. (2022) · Biology · doi:10.3390/biology11081161 · Cited by 15
Raman Spectra and Ancient Life: Vibrational ID Profiles of Fossilized (Bone) Tissues
Jurašeková, Z., Fabriciová, G., Silveira, L. F., Lee, Y., Gutak, J. M., Ataabadi, M. M., & Kundrát, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810689 · Cited by 16
Examination of human osteoarchaeological remains as a feasible source of polar and apolar metabolites to study past conditions
Badillo-Sanchez, D. A., Ruber, M. S., Davies‐Barrett, A. M., Sandhu, J. K., Jones, D. J. L., Hansen, M. A., & Inskip, S. A. (2023) · Scientific Reports · doi:10.1038/s41598-023-27401-0 · Cited by 15
Analysis of fossil bone organic matrix by transmission electron microscopy
Zylberberg, L., & Laurin, M. (2011) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2011.04.004 · Cited by 15
Fluoridation of a lizard bone embedded in Dominican amber suggests open-system behavior
Barthel, H. J., Fougerouse, D., Geisler, T., & Rust, J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0228843 · Cited by 15
“In nature the chemical breakdown and loss of collagen may occur slowly in soil or groundwater via pH-dependent hydrolysis reactions (proteolysis), producing smaller peptides and amino acids, or later through conditions in a burial environment, where the degradation of collagen may increasingly be controlled by tempera…”
Background
Ancient DNA as a multidisciplinary experience
Cipollaro, M., Galderisi, U., & Bernardo, G. D. (2004) · Journal of Cellular Physiology · doi:10.1002/jcp.20116 · Cited by 16
“Collins et al. (2002) reviewed highlights on the biomolecular information retrievable from bones; Marota and Rollo (2002) reviewed some of the most important investigations based on molecular paleontology; Pusch et al. (2003) described the molecular phylogenetic approach used to tackle aDNA studies.”
Background
Bogs, Bodies and Burnt Mounds: Visits to the Soar Wetlands in the Neolithic and Bronze Age
Ripper, S., Beamish, M., Bayliss, A., Ramsey, C. B., Brown, A., Collins, M. J., Cooper, N. J., Cook, G., Cook, J., Gouldwell, A., et al. (2012) · Proceedings of the Prehistoric Society · doi:10.1017/s0079497x00027158 · Cited by 14
“These are attributed to putrefying collagenolytic bacteria (possibly Clostridium spp; Collins et al. 2002; Turner-Walker et al. 2002).”
BackgroundSelf-citation
Origin of archaeological black bones within a waterlogged context: A multidisciplinary approach
Stathopoulou, E., Phoca‐Cosmetatou, N., Théodoropoulou, T., Mallouchou, M. S., Margariti, E., & Psycharis, V. (2019) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2019.109334 · Cited by 14
Evaluation of rapid diagnostic tests and Enzyme Linked Immunoassay in the detection of malaria in ancient human remains
Mbouaka, A. L., Binder, M., Noedl, H., & Gamble, M. (2020) · Journal of Archaeological Science · doi:10.1016/j.jas.2020.105118 · Cited by 14
Conservation of Archaeological Bones: Assessment of Innovative Phosphate Consolidants in Comparison with Paraloid B72
Díaz-Cortés, A., Graziani, G., Boi, M., López‐Polín, L., & Sassoni, E. (2022) · Nanomaterials · doi:10.3390/nano12183163 · Cited by 14
The experimental degradation of archaeological human bone by anaerobic bacteria and the implications for recovery of ancient DNA
Dixon, R., Dawson, L., & Taylor, D. (2008) · Lincoln Repository (University of Lincoln) · Cited by 14
A unique late Eocene coleoid cephalopod Mississaepia from Mississippi, USA: New data on cuttlebone morphology, ultrastructure, chemical composition, and their phylogenetic implications
Doguzhaeva, L. A. (2012) · Acta Palaeontologica Polonica · doi:10.4202/app.2011.0208 · Cited by 14
“This mineral−organic interaction may have played a role in their preservation (Collins et al. 2002; Schmidt−Schultz and Schultz 2004).”
Background
Predicting sample success for large‐scale ancient DNA studies on marine mammals
Keighley, X., Bro‐Jørgensen, M. H., Ahlgren, H., Szpak, P., Ciucani, M. M., Sánchez-Barreiro, F., Howse, L. R., Gotfredsen, A. B., Glykou, A., Jordan, P. D., et al. (2021) · Molecular Ecology Resources · doi:10.1111/1755-0998.13331 · Cited by 13
“The lack of a clear relationship be - tween the atomic C:N ratio and DNA preservation may relate to the fact that all of the samples considered here were from geologically young contexts in environments that tend to be more favourable to collagen preservation (Collins et al., 2002).”
Background
Assessing the reliability of microbial bioerosion features in burnt bones: A novel approach using feature-labelling in histotaphonomical analysis
Végh, E. I., Czermak, A., Márquez‐Grant, N., & Schulting, R. (2021) · Journal of Archaeological Science Reports · doi:10.1016/j.jasrep.2021.102906 · Cited by 14
“…of the inorganic phase (bioapatite dissolution); and (3) microbial degradation of 94 both phases (Child, 1995; Hedges and Millard, 1995; Millard, 2001; Collins et al., 2002; 95 Nielsen-Marsh and Hedges, 2002; Huisman et al., 2017; Turner-Walker and Jans, 2008; 96 Kontopoulos et al., 2016).”
Background
Rapid alteration of cortical bone in fresh- and seawater solutions visualized and quantified from the millimeter down to the atomic scale
Kral, A. G., Lagos, M., Guagliardo, P. R., Tütken, T., & Geisler, T. (2022) · Chemical Geology · doi:10.1016/j.chemgeo.2022.121060 · Cited by 14
Age-related elemental change in bones
Wang, C., Eisa, M. H., Wei-fang, J., Shen, H. F., Mi, Y., Gao, J., Zhou, Y.-H., Yao, H., & Zhao, Y. B. (2008) · Nuclear Instruments and Methods in Physics Research Section B Beam Interactions with Materials and Atoms · doi:10.1016/j.nimb.2008.01.015 · Cited by 14
Bronze Age barrows at Longstone Edge: Taphonomy and site formation
Andrews, P., & Fernández–Jalvo, Y. (2011) · Quaternary International · doi:10.1016/j.quaint.2011.06.041 · Cited by 14
“providing patterns of bone diagenesis and preservation, as well as information on past environments (Weiner and Bar-Yosef, 1990; Hedges and Millard, 1995; Bell et al., 1996; Nielsen-Marsh and Hedges, 2000; Collins et al., 2002; Hedges, 2002; Lee-Thorp, 2002, 2008; Berna et al., 2004; Trueman et al., 2004; Pruvost et a…”
Background
An early Christian cemetery at Björned in northern Sweden : stable isotope analyses of skeletal material
Linderholm, A. E., Andersson, K., Mörth, C., Grundberg, L., Hårding, B., & Lidén, K. (2008) · Diva portal (Dalarna University Library) · Cited by 14
The biochemical signatures of stress: A preliminary analysis of osteocalcin concentrations and macroscopic skeletal changes associated with stress in the 13th ‐ 17th centuries black friars population
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Ca L2,3-edge XANES and Sr K-edge EXAFS study of hydroxyapatite and fossil bone apatite
Zougrou, I. M., Katsikini, M., Brzhezinskaya, M. M., Pinakidou, F., Papadopoulou, L., Tsoukala, E. S., & Paloura, E. C. (2016) · Die Naturwissenschaften · doi:10.1007/s00114-016-1383-y · Cited by 14
An Analysis of Systematic Elemental Changes in Decomposing Bone
Walden, S. J., Mulville, J., Rowlands, J., & Evans, S. L. (2017) · Journal of Forensic Sciences · doi:10.1111/1556-4029.13480 · Cited by 14
Sensitive detection of porcine DNA in processed animal proteins using a TaqMan real-time PCR assay
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“These observations are in line with other works that argue that survival of nucleic acids to drastic processes is particularly manifested in bones, where the adsorption of DNA to hydroxyapatite and the three-dimensional packaging of the macromolecule within the tissue could have a crucial role in DNA preservation (Col…”
BackgroundResult
Assessing the Utility of Soil DNA Extraction Kits for Increasing DNA Yields and Eliminating PCR Inhibitors from Buried Skeletal Remains
Hebda, L. M., & Foran, D. R. (2015) · Journal of Forensic Sciences · doi:10.1111/1556-4029.12878 · Cited by 13
“years old (43,44), although it does degrade over time, the rate of which is affected by heat, extremes in pH, and the microbial environment (45).”
Background
Nanoscale modifications in the early heating stages of bone are heterogeneous at the microstructural scale
Gourrier, A., Chadefaux, C., Lemaitre, E., Bellot‐Gurlet, L., Reynolds, M., Burghammer, M. C., Plazanet, M., Boivin, G., Farlay, D., Bunk, O., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0176179 · Cited by 13
How bone degradation, age, and collagen extraction methods affect stable isotope analysis
Hoke, N., Rott, A., Johler, S., Reul, A., Beck, A., Günther, A., Hochleitner, R., Kaliwoda, M., & Harbeck, M. (2018) · Archaeological and Anthropological Sciences · doi:10.1007/s12520-018-0765-9 · Cited by 13
Effect of a new modified polyamidoamine dendrimer biomimetic system on the mineralization of type I collagen fibrils: an in vitro study
Xie, F., Long, J., Yang, J., Qin, H., Lin, X., & Chen, W. (2021) · Journal of Biomaterials Science Polymer Edition · doi:10.1080/09205063.2021.1982642 · Cited by 13
“However, only the mineralized collagen fibrils can be retained for a long time, and they may remain unchanged even for millions of years [8].”
Background
Remineralization of human dentin type I collagen fibrils induced by carboxylated polyamidoamine dendrimer/amorphous calcium phosphate nanocomposite: an in vitro study
Yang, J., Huang, J., Qin, H., Long, J., Lin, X., & Xie, F. (2021) · Journal of Biomaterials Science Polymer Edition · doi:10.1080/09205063.2021.2008789 · Cited by 13
“Research indicates that only the mineralized collagen fibrils can be retained for a long time, and they may remain unchanged even for millions of years [11].”
Background
Taphonomic and Diagenetic Processes
Grupe, G., & Harbeck, M. (2013) · Springer eBooks · doi:10.1007/978-3-642-27800-6_7-5 · Cited by 13
An efficient DNA extraction method from bone and tooth samples by complete demineralization followed by the use of silica-based columns
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Why collagens best survived in fossils? Clues from amino acid thermal stability
Wang, S.-Y., Cappellini, E., & Zhang, H. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.04.122 · Cited by 13

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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